Received: 5 August 2020 | Revised: 3 February 2021 | Accepted: 21 February 2021

DOI: 10.1111/eva.13212

REVIEWS

Phenotypic plasticity under rapid global changes: The intrinsic

force for future seagrasses survival

Jessica Pazzaglia1,2 | Thorsten B. H. Reusch3 | Antonio Terlizzi2,4 |

Lázaro Marín-­Guirao1,5 | Gabriele Procaccini1

1
Department of Integrative Marine Ecology,
Stazione Zoologica Anton Dohrn, Naples, Abstract
Italy Coastal oceans are particularly affected by rapid and extreme environmental changes
2
Department of Life Sciences, University of
with dramatic consequences for the entire ecosystem. Seagrasses are key ecosystem
Trieste, Trieste, Italy
3
Marine Evolutionary Ecology, GEOMAR
engineering or foundation species supporting diverse and productive ecosystems
Helmholtz Centre for Ocean Research Kiel, along the coastline that are particularly susceptible to fast environmental changes. In
Kiel, Germany
4
this context, the analysis of phenotypic plasticity could reveal important insights into
Department of Biology and Evolution of
Marine Organisms, Stazione Zoologica seagrasses persistence, as it represents an individual property that allows species’
Anton Dohrn, Naples, Italy phenotypes to accommodate and react to fast environmental changes and stress.
5
Seagrass Ecology Group, Oceanographic
Many studies have provided different definitions of plasticity and related processes
Center of Murcia, Spanish Institute of
Oceanography, Murcia, Spain (acclimation and adaptation) resulting in a variety of associated terminology. Here,
we review different ways to define phenotypic plasticity with particular reference
Correspondence
Gabriele Procaccini and Lázaro Marín-­ to seagrass responses to single and multiple stressors. We relate plasticity to the
Guirao, Department of Integrative Marine
shape of reaction norms, resulting from genotype by environment interactions, and
Ecology, Stazione Zoologica Anton Dohrn,
Naples, Italy. examine its role in the presence of environmental shifts. The potential role of genetic
Emails: gpro@szn.it; maringuirao@gmail.com
and epigenetic changes in underlying seagrasses plasticity in face of environmental
Funding information changes is also discussed. Different approaches aimed to assess local acclimation and
Horizon 2020 Framework Programme,
adaptation in seagrasses are explored, explaining strengths and weaknesses based
Grant/Award Number: ASSEMBLE+;
Ministero dell'Istruzione, dell'Università e on the main results obtained from the most recent literature. We conclude that the
della Ricerca, Grant/Award Number: Marine
implemented experimental approaches, whether performed with controlled or field
Hazard PON03PE_00203_1
experiments, provide new insights to explore the basis of plasticity in seagrasses.
However, an improvement of molecular analysis and the application of multi-­factorial
experiments are required to better explore genetic and epigenetic adjustments to
rapid environmental shifts. These considerations revealed the potential for selecting
the best phenotypes to promote assisted evolution with fundamental implications on
restoration and preservation efforts.

KEYWORDS

acclimation, adaptation, genetic diversity, global changes, phenotypic plasticity, reaction

norm, seagrasses

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2021 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd

Evolutionary Applications. 2021;14:1181–1201.  wileyonlinelibrary.com/journal/eva | 1181

1182 | PAZZAGLIA et al.

1 | I NTRO D U C TI O N important ecosystem services worldwide, including oxygen produc-

tion and CO2 sequestration (Champenois & Borges, 2019; Duarte
In the context of global environmental changes, studying the & Krause-­Jensen, 2017). Although they occupy only 0.1% of the
ability of species to cope with environmental shifts is fundamen- ocean surface, it is estimated that seagrasses can store 27–­4 4 Tg
tal for predicting their fate. The possibility to rapidly respond organic carbon (Corg) year−1 globally, corresponding to the 10–­18%
to environmental changes is exacerbated by the occurrences of the total carbon stock in the oceans (Fourqurean et al., 2012).
of different human pressures, which can have critical effects at As in terrestrial plants, where clonal species are the most abundant
the ecosystem level, forcing ecological systems into an alterna- members among perennial grasslands (Klimeš et al., 1997), sea-
tive stable state (Beisner et al., 2003; Harley et al., 2006). The grasses are also mostly herbaceous even if stiff and hard stems and
marine coastline is particularly vulnerable to environmental dis- rhizomes occur in some families (e.g., Posidoniaceae). A huge vari-
turbances, such as sea level rise, acidification, increase of tem- ability exists among seagrasses, ranging from species characterized
perature, and intensity of heat waves events and storms (IPCC, by short-­lived shoots, with a quicker cycle of growth and death of
2019). Additionally, climate-­d erived environmental changes and shoots (i.e., Cymodoceaceae), to slow-­growing and long-­lived plants
their consequences on habitats can potentially be intensified by (i.e., Posidoniaceae) (Larkum et al., 2006). Seagrasses often exhibit a
regional anthropogenic pressures, including overfishing and nu- mix of sexual and clonal reproduction that has been a crucial aspect
trient pollution among others (Chaturvedi et al., 2017; Zaneveld of their evolutionary history. Seagrass meadows show high-­genetic
et al., 2016). The resulted exposure to multiple stressors forces variability depending on the interplay between sexual reproduc-
coastal marine environments to drastic changes as a consequence tion and clonal growth and by latitudinal and geographical regions
of the alteration of species biodiversity, distribution, and ecosys- (Bricker et al., 2011; Jahnke et al., 2016). As for terrestrial plants,
tem functioning (Gunderson et al., 2016). Importantly, rapid and seed dispersal is critical for population distribution, contributing to
extreme environmental changes strongly affect the performance the maintenance of genetic diversity and the shaping of spatial ge-
of foundation species (i.e., species with a structural role within netic structure (Kendrick et al., 2012). Theory predicts that the lack
an ecosystem) altering the resilience capacity (i.e., the ability to of genetic variation leads to the accumulation of deleterious muta-
recover and continue functioning after a disturbance) of the en- tions that negatively affect plants’ persistence under environmental
tire ecosystem (Thrush et al., 2009). The degree of the ecosystem shifts (Silvertown, 2008). However, sexual reproduction has a draw-
transition into different states strongly depends upon the founda- back, since it is a costly energetic process that requires resource al-
tion species’ tolerance and resistance to environmental variability location and depends on surrounding conditions (Diaz-­Almela et al.,
or disturbances (Scheffer & Carpenter, 2003). These abilities, in 2006).
turn, rely on different physiological and molecular mechanisms In seagrasses, vegetative (= clonal) reproduction occurs through
that drive individual or population responses in the presence of rhizome extension and branching in space, leading to the formation
relatively rapid environmental changes (Sih et al., 2011; Summers of extensive underwater meadows (Larkum et al., 2006). The success
et al., 2012; York et al., 2013). One of the main concerns of rapid of clonal propagation is related to different and unique ecological
shifts is that these changes do not allow species to react swiftly advantages, such as resource and risk sharing, and economies of
enough in order to cope with and survive in the new more stressful scale among ramets within a genotype (Dodd & Douhovnikoff, 2016;
environment. Analyzing how species traits change with the envi- Ruocco et al., 2020). Thus, clonal plants appear to be more resistant
ronment becomes thus of crucial importance. than plants lacking clonal reproduction and are likely more buffered
Among higher plants, seagrasses are the only group that has against habitat deterioration (Pennings & Callaway, 2000). This ca-
returned to a completely submerged marine life (Shepherd et al., pacity has allowed clonal plants to colonize diverse terrestrial and
1989). Although fossil evidence for marine plants is limited, some marine ecosystems, and include many of the most important crops
records indicate that seagrass’ ancestors likely evolved more than and invasive plants, and some of the earth's largest and oldest plant
100 Ma ago in the Cretaceous Period, whereas modern seagrass species (Honnay & Bossuyt, 2005; Pan & Price, 2002).
families beginning to diverge more than 70 Ma ago (Hedges & Seagrass meadows are particularly susceptible to environmen-
Kumar, 2009). Seagrasses are a polyphyletic group of monocot- tal changes. They are exposed to the effects of single and multiple
yledons, belonging to the order of Alismatales which includes 11 stressors, due to local and global threats, including changes of en-
families of aquatic–­freshwater species and four families that are vironmental parameters (i.e., light and salinity levels) and nutrient
fully marine (Posidoniaceae, Zosteraceae, Hydrocharitaceae, and condition of the water column (Moreno-­Marín et al., 2018; Pereda-­
Cymodoceaceae; Les et al., 1997). Among the hundreds of thousand Briones et al., 2019; Salo & Pedersen, 2014). The intensifying de-
species of angiosperms today, there are currently only 12 genera struction of the marine environment is promoting a huge decline
and ca. 65 species of seagrasses (Chase et al., 2016). Seagrasses of seagrass meadows with knock-­on effects for the entire coastal
are widely recognized as key ecosystem engineering or foundation benthic ecosystem (Boudouresque et al., 2009; Gacia et al., 1999). A
species, supporting diverse and productive ecosystems in the pho- complete analysis performed by Waycott et al. (2009) revealed that
tic zone of the marine coastline around all the continents except seagrass loss rates have increased to 7% year−1 since 1990, placing
Antarctica (Bos et al., 2007). These marine plants fulfill a series of seagrasses among the most threatened ecosystems on earth.
PAZZAGLIA et al. | 1183

How marine clonal plants with low-­genetic recombination have suggest the most suitable approaches to analyze the role of plastic
been able to survive to past environmental changes and which are responses in seagrasses under global climate changes and local envi-
the main implications for current and future environmental shifts are ronmental stressors. A glossary of more specific terms utilized in this
still to be clarified and becomes mandatory for assessing their fate review is given in Table S1.
and adopting proactive management actions. An aspect that has to
be considered is the longevity that characterizes genets in some spe-
cies (Arnaud-­Haond et al., 2012; Ruggiero et al., 2002). This points 2 | TH E CO N C E P T O F PH EN OT Y PI C
to an intrinsic ability of single genotypes, including mostly clonal PL A S TI CIT Y
populations, to survive and persist across environmental changes
(Arnaud-­Haond et al., 2012; Ruggiero et al., 2002). Plastic responses The concept of “phenotypic plasticity” was applied for the first time
represent an individual property that allow genotypes to accommo- by Nilsson-­Ehle (1914) in a case study of plant’ phenotypic changes
date and react to fast environmental changes (Donelson et al., 2019). resulting from different environments. Since then, the term itself
According to the climate variability hypothesis, seagrass populations evolved according to the development of new studies that docu-
living in more dynamic environments and/or at their tolerance lim- ment changes in environmental conditions, moving the scientific
its (e.g., lagoons characterized by unstable salinity or temperature interest on organismal responses to environmental shifts. Not sur-
conditions) may better perform in face of environmental changes prisingly, a broad literature defined concepts related to plasticity in
(Ashander et al., 2016; Botero et al., 2015; Chevin & Hoffmann, plants during recent years. Different ways to define plasticity have
2017; Tomasello et al., 2009). Thus, organisms growing in highly vari- been utilized, along with a variety of associated terms and more spe-
able environments are more plastic (tolerant) than organisms from cific terminology (Kelly et al., 2012). Plasticity was also described
more stable environments (Tuya et al., 2019). with philosophical significance, as the ‘plastic nature’ of organisms
Although environmental cues trigger phenotypic differences, or ‘plastic properties’ inherent to life. According to West-­Eberhard
the ability to respond is genetically based. Recent evidence sug- (1989), phenotypic plasticity can be defined as the ability of an or-
gests that part of this capacity is also due to epigenetic variations ganism to produce different phenotypes when it is exposed to dif-
(Douhovnikoff & Dodd, 2015) or to somatic mutations that have ferent biotic and abiotic environmental conditions. In other words, a
been shown to segregate among ramets (Yu et al., 2020; see Box single genotype has the possibility to adjust its response to environ-
1; Figure 1). If the latter is true, plasticity may interact with “hard-­ mental changes, modifying its phenotypic state in terms of chem-
wired” genetic changes that thus far have been neglected. istry, physiology, morphology, and gene expression. The exposure
Here, we focus on marine angiosperms (aka seagrasses) and de- to environmental variations enhances the development of different
scribe the concept of phenotypic plasticity and its role in the face phenotypes (i.e. phenotypic plasticity) within and among individuals
of rapid environmental changes as a potential way to overcome fu- of the same population. The window of phenotype changes of a gen-
ture environmental shifts. To do that, we focussed in particular on otype along environmental variations defines its “phenotypic curve”
the most recent literature on seagrass responses to environmental or “reaction norm”, a basic and highly useful concept to understand
stressors that has been critically analyzed also underlining the pros the interrelations among phenotype, genome, and environment
and cons of the technical approaches utilized. As an outlook, we (Woltereck & Woltereck, 1909). Importantly, the reaction norm it-
self is under genetic control (Schlichting & Pigliucci, 1998) and can
be defined as a function that relates the environment with the
phenotype resulting from a particular genotype across an environ-
mental gradient. This function can take any shape, and for continu-
ously distributed traits, such as many physiological, morphological,
and life-­history traits, it is typically visualized as a line or curve on
a plot of the environment vs the phenotype (Gabriel & Lynch, 1992;
Schlichting & Pigliucci, 1998). Evidently, deciphering more complex
threshold/saturation type responses requires more than two meas-
urements of the environment. Being a property of the reaction norm
of single genotypes, plasticity is described by comparing the slope
of the phenotype curve with the mean phenotypic value resulting
from the external conditions. Consequently, the greater the slope of
the curve, the more it deviates from the mean phenotypic value and
F I G U R E 1 Schematic representation of plasticity resulting from the more the phenotype is plastic (Figure 1). Assessing the genetic
the interaction of linear reaction norms and environments (line
basis of the reaction norm slope (i.e., phenotypic plasticity) is funda-
slopes). Black and green solid lines refer to different genotypes
mental to explore the genotype–­environment relation. In this regard,
characterized by genetic variation (line heights); dashed lines refer
to the mean phenotypic value across environments (A and B) (from the genetic variation of a genotype is displayed by the “height” of
Schlichting & Pigliucci, 1998, modified) the reaction norm plot. Thus, genotypes differing in terms of heights
1184 | PAZZAGLIA et al.

BOX 1 Linking genetics to epigenetics

The term epigenetics refers to all DNA and chromatin changes that can be inherited by the next generations and that do not involve
changes in the DNA sequence (Bossdorf et al., 2008). These intrinsic mechanisms include methylation of cytosine residues, chroma-
tin structure changes through chemical modifications of histone proteins, and a possible “crosstalk” between modifications at differ-
ent levels (Holliday, 2006; Kouzarides, 2007). Overall, these modifications can be environmentally induced, promoting phenotypic
plasticity through gene regulation and its heritability (epigenetic plasticity) (Feil & Fraga, 2012; Verhoeven et al., 2016). Since epige-
netic marks can promote down-­ and up-­regulation of genes that can also be inherited to next generations, epigenetic alterations
could be referred to as a regulatory machine, firstly for the acclimation response, and then through the fixation of that “epigenetic
acclimation”, for a rapid adaptation (Dodd & Douhovnikoff, 2016; Richards et al., 2017). In this context, epigenetics could be the
link between genetic diversity, phenotypic plasticity and the environment (Zhang et al., 2013). Another relevant issue in epigenetic
mechanisms is related to the inheritance of histone modifications, as the possibility in plants to “remember” past stress events. This
is already demonstrated for terrestrial clonal plants (Latzel et al., 2016; Verhoeven et al., 2016). Therefore, one of the most important
epigenetic contributions in individual plasticity is the possibility to pass specific environmental information to the next generations
and to regulate fast responses to ongoing environmental perturbations. This “learning process” could contribute to the accumula-
tion of memory mechanisms, altering plant–­environmental interactions in future generations. The epigenetic memory as plastic
behavior seems to be partially responsible also for rapid phenotypic adjustments following fast environmental changes (Dodd &
Douhovnikoff, 2016). For instance, Arabidopsis thaliana showed that a single genotype can display different epigenetic states, mean-
ing that probably a widely epigenetic variation takes place between different ramets as a result not only of environmental conditions
but also of the connection that exists among phenotypes, environment, and progenitors (Johannes et al., 2009). Recently, evidence
about epigenetic mosaics within a genotype has been also shown in marine clonal plants, where epigenetics has been suggested
as a key molecular mechanism enhancing phenotypic plasticity conferring thermal tolerance and the evolution of (pre-­) adaptive
strategies (Marín-­Guirao et al., 2017, 2019). In particular, a case study performed on a clonal meadow of Zostera marina described
epigenetics as the potential advantage to enhance beneficial phenotypic variations under environmental stressors without costs of
clonal reproduction (Jueterbock et al., 2020). In seagrasses, new evidence pointed out the appearance of more tolerant phenotypes
to contrast fast environmental shifts as a mechanism regulated by epigenetic rearrangement that occurs through genetic regulation
(Jueterbock et al., 2020). Thus, the activation/inactivation of this regulatory machinery is strongly dependent on the environment
triggering the existence of a stress memory with important implications for seagrasses exposed to future factors of stress (Nguyen
et al., 2020). In Posidonia oceanica, differences in global DNA methylation has also been found among leaf tissue of different age in
the same shoot, highlighting its role in the response to changes in environmental conditions (i.e., light availability and water tempera-
ture; Ruocco, De Luca et al., 2019; Ruocco, Marín-­Guirao et al., 2019). Additionally, an in silico gene–­body–­methylation approach
showed that house-­keeping genes are hyper-­methylated, while genes with more inducible expression are widely hypo-­methylated
(Entrambasaguas et al., under review).

(genetic variation) and slopes (degree of plasticity) of their reaction standardized. Long-­life cycles and slow growth, which characterize
norms are more likely to evolve (see next paragraph, Pigliucci, 2001; most of the seagrass species, impede manipulative experiments and
Schlichting & Pigliucci, 1998). Another important issue is that the trans-­generation assessments. Additionally, advanced genetic tools,
shape of the reaction norm can be the result of a different organis- such as recombinant technologies (e.g., CRISP), are currently un-
mal response along the biological hierarchy. Responses at the gene available for all seagrass species and a complete sequenced genome
expression level, for example, may be plastic, that is, exhibit a strong is only available for two species, that is, Zostera marina (Olsen et al.,
slope when stress genes (HSPs) are activated (e.g., in seagrasses: 2016) and Z. muelleri (Lee et al., 2016).
Bergmann et al., 2010; Traboni et al., 2018). At the higher organiza-
tional level, however, this results in the maintenance or resilience of
organismal function, for example photosynthesis, so essentially in a 3 | TH E G E N E TI C CO M P O N E NT O F
flat reaction norm with increasing stress (as in a generalist response) PH E N OT Y PI C PL A S TI C IT Y
(Reusch, 2014).
In general, the analysis of processes involved in phenotypic Seagrass populations can be more resilient or resistant to environ-
plasticity and the possibility that such plastic responses might or mental changes as the expression of individual or population plastic-
might not be adaptive is complex. Currently, phenotypic plasticity ity. In general, the process can be addressed at two different but
is not unequivocally defined in seagrasses, and the approaches to interconnected levels: genetic diversity displayed among genets, and
assess the adaptive potential of phenotypic plasticity have not been number and distribution of genets at a particular location that can
PAZZAGLIA et al. | 1185

be summarized as genotypic diversity. Genetic diversity depends on diverse (e.g., P. oceanica: Arnaud-­Haond et al., 2012; Z. marina;
the allelic variation and heterozygosity resulting from the sexual re- Ferber et al., 2008; Figure 2).
production and the immigration of new genetic variants from other Despite the importance of population size, low-­genetic variation
populations, whereas the genotypic diversity depends on the size has been found as a winner strategy in different plant species (e.g.,
structure and persistence of clones (or genets, consisting of many clonal invasive species; Lambertini et al., 2010; Li et al., 2006), partic-
ramets) at a location, through vegetative propagation (i.e., clonal ularly in long-­lived ones (e.g., P. oceanica; Arnaud-­Haond et al., 2012;
diversity) (Procaccini et al., 2007). Experimental studies have dem- Ruggiero et al., 2002; Z. marina: Reusch et al., 1999). Population size
onstrated that genetic and genotypic diversity of populations are a (the level of genetic variation within populations) is considered a
good proxy of population resilience and plasticity to changes (Ehlers major constrain for the adaptation of natural populations to environ-
et al., 2008; Hughes et al., 2008; Jahnke et al., 2015) since popula- mental changes, as the higher is the number of genotypes, the higher
tion reaction norm results in a broad sense from the amplitude of the is the possibility that some of them can be positively selected (Bell &
reaction norms of single genotypes. Gonzalez, 2009; Matesanz & Valladares, 2014). Effective population
Since seagrass genotypes can persist for a long time size can be decreased by the selection of plastic genotypes (adaptive
(>>100 years) as in long-­living species such as P. oceanica (Arnaud-­ phenotypes), in presence of rapid environmental changes, through
Haond et al., 2012) and Z. marina (Olsen et al., 2016), the genetic changes of allele frequencies of specific loci and globally on the ge-
diversity among the genet level is maintained by the interplay be- nome (Grenier et al., 2016).
tween sexual reproduction and clonal growth (Arnaud-­Haond et al., Any adaptation to a new environment at population level is a pro-
2020; Kendrick et al., 2012). This results in the formation of sub- cess resulting from the natural selection of better-­suited genotypes
merged meadows ranging from almost monoclonal to highly genetic across generations, changing the genetic composition of populations.

F I G U R E 2 The role of genetic diversity

and its effect on phenotypic plasticity in
face of prompt environmental changes
(see the text for more details)
1186 | PAZZAGLIA et al.

This process can be slow, inducing an initial decline in population fit- times that are not achieved against fast environmental changes as
ness and size and experiencing a subsequent increase once adaptive we are facing nowadays.
genotypes exhibit appropriate phenotypes (Hamilton & Miller, 2016;
Valladares et al., 2014). The selection of these genotypes leads to
changes in the frequency of alleles that confer greater fitness under 3.1 | Genotype by environment interactions
the new altered conditions, promoting adaptive evolution (Grether,
2005). For this reason, the slope or shape of reaction norms is con- Being a characteristic of individual genotypes, the amount of phe-
tinuously evolving in most cases, rendering the mutually exclusive notypic variation across the environment describes the degree of
distinction of plasticity vs. adaptation meaningless (Schlichting & genotype plasticity (genotypes by environment interactions –­ GxE;
Pigliucci, 1998). The occurrence of somatic DNA mutations in single ­Li et al., 2018). Different reaction norms arise according to the de-
individuals can provide a readily available extra source of variation gree of the interaction between individual genotypes and the envi-
that was previously not considered and that can be maintained via ronment (which is represented by the slope of each reaction norms
clonal growth in long-­living genotypes (Whitham & Slobodchikoff, in Figure 2). When environmental conditions change, populations
1981). The role of somatic mutations in seagrasses was initially as- with low genotypic diversity (Figure 2a,b) can react in different ways:
sessed by Reusch and Boström (2011) (Reusch & Boström, 2011). (i) genotypes are stable and show no plastic behaviors (the reac-
Recently, high somatic genetic variation was detected among ramets tion norms are parallel with the same shape, Figure 2d). Phenotypic
of a single genet of Z. marina plants (Yu et al., 2020). changes do not occur, meaning that the mean of the phenotypic
Similar to genotypes within a population, populations from con- value of genotypes is enough to support environmental changes;
trasting environmental conditions also showed different plasticity (ii) genotypes re-­shape their phenotypes to the new environmental
which is indicative of local adaptation (Sánchez-­Gómez et al., 2011). condition exhibiting positive phenotypic plasticity (Figure 2e). This
Thus, the existence of populations locally adapted to natural envi- results in different positive plastic responses depending on the in-
ronments showing more adaptive genotype curves (i.e., reaction dividual genotype interaction with the new environmental factor;
norms) results in population divergence in plasticity patterns rep- (iii) genotypes interact with the new environment showing pheno-
resenting an evolutionary potential for the species. In this sense, typic changes that are maladaptive or not able to accommodate new
plasticity has the potential to drive population divergence as the conditions (Figure 2f). Negative phenotypic plasticity could result in
environment changes (Pfennig et al., 2010). The capability of an indi- population extinction. Contrary, more diverse populations have the
vidual to adapt and the timing of evolutionary adaptation is intrinsi- potential to exhibit more plasticity if most plastic genotypes bring
cally related to its plasticity. phenotypes closest to the new optimum conditions (Figure 2e). Then,
Even in species with high clonal persistence, such as P. oce- if the plastic response is positively correlated with plant fitness, phe-
anica, stochastic events of sexual reproduction and migration of notypic plasticity can evolve by natural selection (Valladares et al.,
genetic variants through populations via sexual propagules seem 2014) leading to genotype plasticity evolution (Figure 2g).
to suffice to promote genetic rearrangements and enhance se-
lectively advantageous genetic variations (Arnaud-­Haond et al.,
2014; Jahnke et al., 2015; Kendrick et al., 2012; Procaccini et al., 4 | PL A S TI C R E S P O N S E S TO
2007). The connectivity among populations depends on the exis- R A PI D E N V I RO N M E NTA L C H A N G E S :
tence of geographic or oceanographic barriers and the different ACC LI M ATI O N A N D M I G R ATI O N
features of dispersal vectors, that is, sexual or clonal propagules
(e.g., Jahnke et al., 2016; McMahon et al., 2014; Serra et al., 2010). Currently, global environmental changes may be too fast to allow for
High-­resolution genetic data for the seagrass Thalassia testudinum selection and evolutionary changes to occur in long living species,
along the western tropical Atlantic coasts revealed high-­genetic di- resulting in mean decline in population fitness. Thus, the persistence
versity as the result of high connectivity between subpopulations of species in the age of global climate changes will mainly depend on
(i.e., gene flow) which in turn favored the appearance of different their intrinsic abilities that facilitate their persistence under environ-
phenotypes (Bricker et al., 2011). Isolated meadows, instead, can mental shifts adjusting to new conditions (i.e., acclimation capacity)
progress toward genetic drift lowering allelic diversity and making or increase their dispersal capacity to find a more suitable environ-
populations even more fragile against changes in environmental ment to which they are adapted (i.e., movement capacity, Figure 3).
conditions (Figure 2a). When environmental conditions change Here, we refer to acclimation capacity as the most relevant short-­
only more diverse populations could harbor genotypes able to term response derived from pre-­existing phenotypic plasticity, which
face the new extreme conditions, while monoclonal or less diverse allows organisms to adjust to rapidly changing environments extend-
populations could disappear (Figure 2b–­d). This is the reason for ing their tolerance ranges (De Los Santos et al., 2009; Sharon et al.,
the higher sensitivity to environmental changes of marginal popu- 2009). Phenotypic responses to environmental changes occur at
lations concerning central populations of the species distribution different organizational levels that may include highly specific devel-
(e.g., Billingham et al., 2003). The alternative would be to move opmental, morphological, and physiological adjustments enhancing
toward conditions that are more favorable or to adapt, requiring survival and persistence in the novel environment (Bercovich et al.,
PAZZAGLIA et al. | 1187

ensure the processing of information and the development of the

best phenotype–­environment match (Gibbin et al., 2017). This is
especially true for fast environmental changes and highly variable
environments that force continuous prompt adjustment. The cost
of switching the phenotype related to individuals and populations
could be determinant for the ability of organisms to withstand envi-
ronmental changes and to sustain the provision of ecological func-
tions (Auld et al., 2010; Forsman, 2015; Murren et al., 2015). The
high energetic costs involved in producing the optimum phenotype
and the presence of a trade-­off diverting energetic costs to support
other traits and/or functions (DeWitt et al., 1998) can also result in
the appearance of phenotypes that are less fit to the new environ-
ment (non-­adaptive or maladaptive phenotypes) and hence not posi-
tively selected by evolutionary processes (see Figure 2 and previous
paragraph; Palacio-­López et al., 2015). Non-­adaptive phenotypes
would induce the decline of many species, including seagrasses, as
fast global changes are currently increasing environmental stochas-
ticity. However, costs related to phenotypic plasticity are currently
under-­studied in seagrasses.
Short-­term responses occur through acclimatory mechanisms.
In seagrasses, it has been described that these involve the modu-
lation of gene expression profiles, which in turn depend on stress
intensity, time of exposure to stressful conditions (Pernice et al.,
2016; Ruocco et al., 2018), and morphometric plasticity in relation
to geographical distributions and nutrient status (De los Santos et al.,
F I G U R E 3 Representation of seagrass reactions to 2016; Soissons et al., 2018). At the individual level, plasticity can
environmental changes. In the presence of environmental buffer environmental changes throughout the plant's lifetime, fur-
perturbations as global changes, seagrass survival is compromised,
ther increasing its tolerance to stress (e.g., short-­term acclimation to
through habitat fragmentation and structural and functional
light conditions; Olesen et al., 2002). It has been shown that plants
ecosystem loss with consequent species extinction. Alternatively,
intrinsic forces can increase their dispersal capacity to find more of the Mediterranean species Posidonia oceanica have plastic re-
suitable environments (i.e., migration) or facilitate their persistence sponses to different light conditions as a consequence of regulatory
in the new environment through phenotypic plasticity. This mechanisms that allow them to acclimate to low-­light environments
adjustment to external conditions can be enhanced by epigenetic (Dattolo et al., 2014; Mazzuca et al., 2009; Procaccini et al., 2017).
modifications or somatic DNA mutations, which increase epigenetic
Plasticity at lower levels of the biological organization needs
and genetic diversity, respectively. The resulting phenotype will
favor the acclimation to the new environment and can be naturally to be integrated at the level of individual and/or population fitness
selected. Thus, acclimation and adaptation are interrelated to evaluate how this influences the fitness and therefore alters the
strategies of the seagrass plasticity representing intrinsic forces for structure and the functioning of seagrass ecosystems. As an exam-
their survival to future environmental changes ple, the stenohaline P. oceanica is able to thrive in environments with
highly fluctuant salinity regimes thanks to high plasticity at the phys-
2019; Zhang et al., 2014). The degree of plasticity, as stated above, is iological (e.g., photosynthesis, carbohydrates metabolism) and mor-
related to the slopes of reaction norms that are variable among indi- phological (e.g., plant size) levels (Marín-­Guirao et al., 2017). These
viduals, populations, and species. Thus, the steeper is the slope of the adjustments permit the species to keep unaltered plant density and
reaction norm, the more an organism is able to acclimate to different population growth rates, as a plastic response to maintain popula-
environmental conditions, and the more it is plastic. The process of tion fitness. Nevertheless, the reduced size of plants weakens the
acclimation resulting from phenotypic adjustments to environmen- physical structure of the leaf canopy and thus, its functionality, af-
tal cues can occur during the early development of an organism that fecting the provision of ecological services.
persists also on the adult stage, or as reversibly acclimation occur- At the population—­and ultimately species—­level, plasticity can
ring during the lifetime (Beaman et al., 2016). The continuous align- allow colonization and establishment in diverse habitats and there-
ment of phenotypes to the environment involves associated costs fore influences the species’ ecological breadth (Gimeno et al., 2009;
to perform strategies for sensing and responding without affecting Pigliucci, 2001; Sultan, 2003). In the presence of environmental
individual performances (Vialet-­Chabrand et al., 2017; Zimmerman, stressors, plasticity could increase the dispersal capacity favoring
2017). In fact, phenotypic plasticity is constrained by the energetic the migration to more comfortable conditions or increase the reac-
costs required for the sensory and regulatory mechanisms that tion norm slope of a particular trait to cope with new environmental
1188 | PAZZAGLIA et al.

conditions. In this sense, organisms could adopt an escape mecha- phenotypic changes, such as changing sex ratio (Nguyen et al., 2018;
nism to avoid unfavorable conditions due to environmental changes. Winters et al., 2020). The rapid establishment and spread of this spe-
Thus, the migration capacity can be described as an alternative cies in cooler regions are mediated by its great plasticity for shifting
strategy to local acclimation, which allows organisms to track more the thermal tolerance during the Mediterranean invasion (Georgiou
favorable conditions (Bulleri et al., 2018). It is important to empha- et al., 2016; Nguyen et al., 2020; Wesselmann et al., 2020). Despite
size that the movement capacity can be a consequence of trait plas- the migration being a valuable strategy to avoid species extinction,
ticity when its reaction norm is defined by the interaction with the losers can be the native species that are potentially outcompeted by
environment. colonizing species (e.g., H. stipulacea; Winters et al., 2020).
The migration capacity of seagrasses is related to clonal growth, It is noteworthy to mention that plasticity is an underlying at-
sexual reproduction and dispersal of sexual propagules, and vege- tribute to these processes, which in turn are not mutually exclusive
tative fragments (McMahon et al., 2014). This means that the mo- since acclimation, adaptation, and distributional changes are interre-
tion capacity is very different among species and even within the lated to some extend (Donelson et al., 2019; Kelly, 2019).
same seagrass species given that the frequency of sexual reproduc-
tion, the dispersion of seeds (floating vs buried seeds), the rates of
clonal elongation, and the persistence of plant fragments greatly 5 | A S S E S S I N G PH E N OT Y PI C PL A S TI C IT Y
vary among populations, let alone species (Orth et al., 2007). For in- I N S E AG R A S S E S
stance, settling velocities of fragments are important for successful
seagrass movements, which allow plants to disperse spatially. Thus, The analysis of plasticity and the discrimination between adaptive
rapid settling capacities can be the result of an adaptive process that or acclimation processes in plants has been mostly approached in
reduces the risks for plants of being away from theirs optimal habi- model species, where the appropriate molecular and manipulative
tats (Weatherall et al., 2016). tools have been developed (Bossdorf et al., 2010; Matesanz et al.,
Overall, large and long-­lived species mainly rely on slow vegeta- 2020). Seagrasses are a polyphyletic and unique group of plants,
tive growth and have infrequent sexual reproduction events, which with convergent morphology due to constraining imposed by the
may potentially result in a reduced migratory success since they adaptation to a fully submerged life in the marine environment (Les
spread extremely slowly over large distances and seldom produce et al., 1997; Olsen et al., 2016). Sexual reproduction is adapted to the
sexual propagules (McMahon et al., 2014). However, some species marine environment and its experimental manipulation has not been
have shown high plasticity in reproductive phenology in response developed for most of the species. Hence, the dissection of the dif-
to environmental changes that increase their movement capacity. ferent drivers of plasticity can mostly be assessed based on indirect
For instance, in terrestrial plants, it has been observed that differ- evidence. The complex and multidisciplinary information needed
ent natural populations grown in common environments showed for disentangling plasticity components can be obtained through
different flowering time in response to wet and dry conditions (e.g., field observations, experimental manipulations, and laboratory ap-
Brassica rapa; Franks, 2011), a way to produce dispersal vectors proaches that are described in detail in the following paragraphs.
(i.e., sexual propagules) and escape from the existing environment. The most recent seagrass literature has been reviewed to present
B. rapa genotypes growing from seeds that experienced drought the strength and weaknesses of each approach (Table 1; Table S2).
anticipate flowering in further dry conditions, in respect to seeds
collected before the stressing event (Franks et al., 2007). This ev-
idence suggests that the escape strategy adopted by these plants 5.1 | Field observations
could be an indication of a rapid evolutionary shift to early flow-
ering rather than the modification of the phenotypic state through Phenotypic plasticity, and in particular whether it is adaptive and
trait adjustments (i.e., phenotypic plasticity). Thus, the potential to which are the energetic costs involved, can be first approached by
adopt plastic strategies is mostly the result of a trade-­off between comparing performances between populations subjected to differ-
avoidance (through phenotypic plasticity) and escape (through early ent environmental conditions (Forsman, 2015). Variation in single
flowering). Similar evidence was recently described for seagrasses, or multivariate trait plasticity along environmental gradients can in-
where flowering phenotypes resulted in response to warming (i.e., form about factors and conditions potentially promoting the evolu-
Z. marina, Blok et al., 2018; P. oceanica, Ruiz et al., 2018). Collecting tion of phenotypic variation and give insights into how plasticity can
and storing seeds from seagrass populations growing in different contribute to evolutionary differentiation within species (Donelson
conditions would allow testing evolutionary processes in face of fu- et al., 2019).
ture environmental scenarios. Analysis of functional traits selected for plants combined
Small and more ruderal species, such as Halophila stipulacea, are with genetic data is a helpful approach to investigate genotype–­
able to migrate fast into new environments adjusting their disper- environment interactions (Haseneyer et al., 2009). For instance,
sal ability through phenotypic plasticity. This species, a native from Maxwell et al. (2014) observed that physiological and morphological
the Red Sea, rapidly spread and colonized new environments, as characteristics of Zostera muelleri varied along a gradient of water
the Mediterranean and Caribbean seas, locally adapting through quality according to well-­known light acclimation responses. They
PAZZAGLIA et al. | 1189

TA B L E 1 Summary of pros and cons

Approaches Pros Cons
of approaches used to assess phenotypic
plasticity in seagrasses (see the main text Field observations Inform about factors that potentially promote Limited to observations
for more detail) the evolution of phenotypic variation and
how plasticity can contribute to evolutionary
differentiation within species
Field experiments Quantify the degree of plastic responses, Natural environmental
analyzing phenotypic changes in relation to variation leads
the environment to misleading
interpretations
Mesocosm Simulate the effect of the stress factor of Require sophisticated
experiments interest for analyzing intraspecific and systems. Results
interspecific responses and the genetic basis cannot be
of phenotypic plasticity automatically
transferred to natural
conditions
Reciprocal Identify the genetic component of plastic Sensitive to
transplant responses environmental forces
experiments and regional stressors
Common garden Allow discriminating the contribution of Require long
experiments genetic and plastic effects comparing acclimation phases
genetically distinct families or populations and an accurate
experimental design

also observed a consistent response in all meadows to a severe species (Buyantuyev et al., 2012). The analysis of samples along a
flooding event increasing freshwater run-­off along the gradient. wide spatial range allows to assess relationships between pheno-
Plants maintained population productivity unaltered (i.e., biomass, typic variations and the environmental gradient without the con-
shoot, or leaf density alterations) through physiological adjustments, straints of time (Banet & Trexler, 2013). As showed by Bricker et al.
suggesting high phenotypic plasticity and a reaction norm with a (2011), T. testudinum individuals from different populations across
large positive slope. In another example, the congeneric seagrass north–­south physiochemical environmental gradients in the Florida
species Z. noltii showed the capacity to acclimate to local environ- Bay was an effective method to discriminate plasticity as the main
mental conditions exhibiting different phenotypes in terms of me- driver for phenotypic variations across sites. The space-­for-­time
chanical and morphological traits during one growing season and substitution approach is helpful not only to analyze populations’
across the latitudinal range of the species. The presence of stronger plasticity through natural gradients and thus to assess long-­term
and stiffer leaves under oligotrophic as compared to more eutrophic consequences of human impacts, but also to infer temporal dynam-
conditions suggested that the species suffers in nutrient-­enriched ics by comparing multiple sites with different disturbance gradients
environments without evolving a potentially adaptive phenotype (Fukami & Wardle, 2005). For instance, Yang et al. (2018) showed,
(Soissons et al., 2017). under different stress regimes, different degree of plasticity for
Phylogeny-­based comparative analyses can be used to infer the physiological and morphological traits in Z. marina plants collected
role of plasticity for evolutionary diversification among species and across regions that displayed diverse eutrophic gradients. New po-
for speciation (Coyer et al., 2013; Olsen et al., 2004). Candidate tential bio-­monitoring metrics, which may help the management of
genes that are indirectly related to environmental gradients, provid- seagrass meadows in monitoring and predicting phenotypic varia-
ing evidence of local adaptation, can be identified through genome-­ tions, can derive from this kind of study.
wide transcriptomic analysis performed on wild populations (Jahnke
et al., 2019), though the identification of real causation among genes
and the environment is not trivial. This could be approached by com- 5.2 | Experimental manipulation of
bining genome-­wide analysis with manipulative stress experiments selected parameters
(e.g., Anderson et al., 2014).
The analysis of spatial variation across environments by compar- Observational studies can offer important insights in order to gener-
ing ecosystems and populations along gradients is a useful approach ate further hypotheses and testable predictions. However, demon-
to extrapolate temporal dynamics and to infer about future ecosys- strating causal relationships and mechanisms, linking either variation
tem responses (i.e., space for time substitution; Fukami & Wardle, in the capacity for plasticity itself or plasticity induced phenotypic
2005). This is a valid approach, which states that environmental variation to aspects of the individual or population fitness, is com-
factors vary over time in the same way as they vary in space pro- plex, as it requires experimental manipulation, replication, and con-
viding new opportunities to explore the potential success of plastic trolled comparisons (Forsman, 2015).
1190 | PAZZAGLIA et al.

The experimental manipulation of one or more environmental acidification by exposing them to in situ nutrient enrichment. The
factors can be performed directly in the field or in the laboratory field experiment revealed that the increased CO2 benefits plants fa-
under controlled conditions. The last option requires a deep analysis cilitating the absorption and assimilation of nutrients.
of the relevant environmental factor to establish the correct exper- Although experimentation in the field is helpful for quantifying
imental design, which in turn reflects the environmental variation the plasticity in the response to environmental stressors, the natural
that occurs under natural conditions. This is not an easy task, since environmental variability can lead to misleading interpretations of
many environmental factors act and interact with each other in nat- the specific drivers responsible for the resulted phenotypic changes.
ural conditions. Additionally, these experiments provide results that are difficult to
replicate and compare with similar studies because regional stress-
ors and biotic interactions may modify the final outcome (e.g.,
5.2.1 | Field experiments Garrote-­Moreno et al., 2016).

Field experiments allow quantifying the degree of plastic responses,

analyzing phenotypic changes in relation to the environment (Merilä 5.2.2 | Mesocosm experiments
& Hendry, 2014), and predicting shifts in species compositions under
environmental changes (La Nafie et al., 2013). This can be realized One of the main advantages of performing experimental manipula-
through the artificial modulation of one or more factors, to compare tions under controlled conditions is the possibility to simulate the
control and treatment under natural environmental conditions, in effect of the stress factor of interest, isolating it from all the other
order to investigate the potential drivers for the observed pheno- variables that are naturally occurring, and to analyze intraspecific
typic changes. One of the major strengths of this approach is the and interspecific responses. Additionally, controlled experiments
inclusion of natural variability and processes that are difficult to re- offer the opportunity to evaluate the degree of phenotypic plastic-
produce under controlled conditions. In this respect, individual re- ity in the form of a genetically determined reaction norm. An exam-
sponses measured in situ provide more reliable results than those ple from terrestrial plants refers to the manipulation of temperature,
performed in the laboratory. Different studies have been carried out utilized for assessing thermal tolerance variability across latitudes
in the field, exploring phenotypic responses of seagrass species to (Molina-­Montenegro & Naya, 2012). In this case, the authors meas-
single (e.g., Bité et al., 2007; Collier et al., 2012; Cox et al., 2015; ured the phenotypic plasticity of an invasive species (Taraxacum of-
Darnell & Dunton, 2017; Silva et al., 2013; Table S2) or to multiple ficinale) to different environmental temperatures, confirming that
environmental factors (e.g., Ceccherelli et al., 2018; La Nafie et al., higher thermal tolerance at higher latitudes is related to an improved
2013; Ravaglioli et al., 2017). For instance, Ruocco et al. (2018) phenotypic expression. Different studies performed under labora-
showed that in P. oceanica plants, herbivory increases under nutri- tory conditions assessed phenotypic plasticity of seagrass species,
ents addition, with a clear effect on seagrass productivity. In such such as the mesocosm experiments performed on the most abundant
environmental conditions, the species can enhance growth to com- Mediterranean species, Posidonia oceanica and Cymodocea nodosa.
pensate for the increase of herbivory, or can increase the accumu- These studies have confirmed that these two species have different
lation of deterrent substances and the translocation of nutrients tolerance to hypersaline stress (i.e., C. nodosa > P. oceanica), consist-
to underground tissues to protect them against external pressures ent with their physiological and morphological plasticity (Piro et al.,
(Alcoverro & Mariani, 2005; Ruocco et al., 2018; Sánchez-­Sánchez & 2015; Sandoval-­Gil et al., 2012, 2014). Furthermore, C. nodosa also
Morquecho-­Contreras, 2017). showed higher tolerance and higher plasticity to warming, possi-
Tuya et al. (2019) assessed the tolerance of C. nodosa to low-­light bly related to the tropical affinity of the genus (Marín-­Guirao et al.,
levels across different populations located in the Canary Islands and 2018; Olsen et al., 2012; Tutar et al., 2017). Controlled experiments
the Mediterranean Sea by manipulating the light intensity directly also allow the manipulation of multiple stressors simulating realis-
in the field. Results demonstrated biogeographical variability among tic environmental changes affecting coastal marine habitats (Artika
populations in the degree of shading tolerance, with Canary Island et al., 2020; Egea et al., 2018; Pazzaglia et al., 2020; Viana et al.,
populations being less tolerant in respect to the others. As sug- 2020). Through the manipulation of temperature and nutrients con-
gested by authors, the lower plasticity of Canary Island populations centration, Ontoria et al. (2019) investigated individual and popu-
can be related to the lower genetic diversity of these populations, lation responses in C. nodosa plants. Different phenotypes arose
living at the range edges of species’ distribution. Salo et al. (2015) depending on the interaction among temperature-­ammonium and
also found different gene expression and physiological performance temperature-­organic carbon suggesting that the exposure to mul-
of Z. marina genotypes to light reduction. The experimental ma- tiple stressors triggers phenotypic responses in relation to stress-­
nipulation in the field offers also the opportunity to study plastic specific thresholds. The analysis of the recovery after stressing
responses of plants locally adapted to particular environmental conditions, allowed to point out contrasting resilience abilities of
conditions. In order to model the response to eutrophication in a seagrass populations living in different environments, as a result
future ocean acidification scenario, Ravaglioli et al. (2017) evalu- of their adaptation to local climatic conditions (e.g., Franssen et al.,
ated the performances of P. oceanica plants adapted to long-­term 2011; Winters et al., 2011; Table S2). This represents an important
PAZZAGLIA et al. | 1191

advantage of experimental manipulations, as offers the possibility 2015; Procaccini & Piazzi, 2001; Reusch et al., 2005; Reynolds et al.,
to understand if plants are able to turn back to their original natural 2012; Williams & Davis, 1996; Williams, 2001).
state after extreme events providing new insights into the long-­term A reciprocal transplantation approach has also been used to eval-
survival of seagrasses to environmental changes. uate seagrass short-­term acclimation along environmental gradients.
Sharon et al. (2009) transplanted shoots of H. stipulacea between the
depth extremes of its distribution, to evaluate the plastic response
5.3 | Transplantation experiments to different irradiance regimes (Table S2). After 2 weeks of exposure
to reciprocal environments, they found fast changes in photosyn-
Transplantation experiments fall into two distinct approaches. A thetic performance supporting the high plasticity of the species.
reciprocal transplant experiment entails the movement of pheno- The long-­term maintenance of field experiments can be jeop-
types between contrasting natural environments along with on-­site ardized by environmental forces (storms, salinity, and temperature
transplantation controls. In common garden experiments, genotypes fluctuations), regional stressors (anchoring boats and anthropic in-
coming from different environments are planted into the common puts), or other technical problems (van Katwijk et al., 2009). As an al-
environmental conditions of a single site. ternative, reciprocal transplant experiments in controlled conditions
are a valid tool to overcome logistical issues with transplantation in
the field that also includes the risk of introducing as yet unknown
5.3.1 | Reciprocal transplant experiments pathogens over longer distances. In P. oceanica, plants from shal-
low and deep environments were transplanted in individual pots
This experimental approach allows for a direct test of local adapta- and exposed to their reciprocal light regimes in a controlled meso-
tion by comparing two sites with each other (Kawecki & Ebert, 2004). cosm approach (Dattolo et al., 2017). P. oceanica genotypes showed
Thus, provided proper acclimation and control for carry-­over effects some degree of photo-­physiological and morphological plasticity.
(see below), a potential genetic component of the plastic response Nevertheless, after several weeks under reciprocal light environ-
(as reaction norm) can be quantified by comparing the phenotypic ments, genotypes showed performances that were similar to those
performances of transplants in native vs. foreign environments. shown by plants from their original depth, suggesting local adapta-
Local adaptation and plastic abilities of different populations can be tion to their home environment.
addressed using two different comparisons. First, local populations
can be compared within habitats, that is, “local” vs “immigrant” de-
sign; second, plants can be compared across habitats, that is, “home” 5.3.2 | Common garden experiments
vs “away” design (Svensson et al., 2019). The final expectation of
such experimental conditions is that plants perform better in their Common garden experiments are particularly relevant to investigate
“home” environment in respect to the “away” ones, showing direct the nature of plastic responses and to discriminate the contribution
indications of a local adaptation. In this case, the degree of plasticity of genetic and plastic effects on phenotypic variation. In fact, these
of genotypes locally adapted to their home site and transplanted to experiments allow comparing distinct genotypes or populations
reciprocal environments within their environmental tolerance range from different environments by growing them under identical envi-
can be assessed. A recent review summarizing 75 years of plant ronmental conditions (De Villemereuil et al., 2016; Merilä & Hendry,
experiments on local adaptation revealed that indeed, local popu- 2014). This approach is commonly used to test for local adaptation,
lations almost always showed higher performance than non-­local as it enables to unravel the genetic basis of phenotypes from differ-
ones, especially in traits related to reproductive output, suggesting a ent populations excluding the effects of the corresponding environ-
notably local adaptation in terrestrial plants (Baughman et al., 2019). ments (Cruz et al., 2019; De Villemereuil et al., 2016; Lepais & Bacles,
Factors other than local adaptation can affect transplants per- 2014; Vermaat et al., 2000).
formance. Evans et al. (2018) designed a reciprocal transplantation In seagrasses, Franssen et al. (2011) performed a common garden
experiment of two genetically and geographically distinct popula- stress experiment to assess transcriptomic profiles of Z. marina pop-
tions of P. australis in southeastern Australia. They assessed local ulations from two contrasting thermal environments (Venice Bay,
adaptation by comparing plant productivity of low-­and high-­genetic Italy, vs. Limfjord, Denmark) to a simulated heat wave. They found
diversity meadows using the “home” vs “away” approach. After a strong divergence in terms of gene expression profiles between
6 months, they found higher survival rates and productivity for high-­ populations only in the recovery phase, while the immediate stress
genetic diversity plots, which outperformed less genetically diverse response was similar and showed the typical heat shock protein-­
plants both at home and away sites. This means that more genet- encoding genes with overexpression. This was consistent with local
ically diverse plots included also more plastic genotypes that per- adaptation to the local natural thermal environment. One caveat of
formed better than less diverse plots, allowing them to survive after such studies is that even under a long acclimation phase of about
transplantation. This high genetic demonstrated that both high-­ 1 month, this may not be sufficient to overcome long-­term acclima-
genetic diversity and local adaptation play a crucial role in enhancing tization to the home environment. We can thus not fully conclude
transplant success (Hämmerli & Reusch, 2002; Jahnke, Serra, et al., that observed stress responses resulted from a genetically based
1192 | PAZZAGLIA et al.

adaptation (as stated by Bergmann et al., 2010; Winters et al., 2011; Mediterranean populations, favoring adaptive differentiation (Olsen
Table S2). One way forward to overcome such limitations is raising et al., 2004; Procaccini et al., 2007).
the experimental plants from seeds. This was done in seagrasses,
for the first time to our knowledge, in eight populations across
the distribution range of the seagrass C. nodosa. Seeds were ger- 6 | FU T U R E PE R S PEC TI V E S : E N H A N C I N G
minated and subsequently grown for sixteen months in a common PL A S TI C IT Y FO R B O OS TI N G S E AG R A S S
garden before being exposed to two marine heat waves of different A DA P TATI O N
intensity (Pereda-­Briones et al., under review). The positive relation-
ship observed between the resilience and local thermal regimes of Ascertained the importance of phenotypic plasticity and its role in
the studied populations strongly evidenced local adaptation of the driving short-­term responses and evolution, it is now necessary to
populations to their thermal regime. Such studies provide strong explain how all this information can be integrated into seagrasses
evidence for the existence of underlying genetic variation resulting research. In the framework of conservation and restoration manage-
from divergent selection, representing the evolutionary potential of ment, understanding the phenotypic plasticity of selected meadows
the species within the frame of global warming, although the attain- to restore a disrupted habitat strongly boosts the success of resto-
able rates of change remain obscure (Reusch & Wood, 2007). This ration plans (Falk et al., 2001; Paulo et al., 2019). In fact, the selec-
“adaptive transgenerational plasticity” is not only the result of the tion of highly plastic and tolerant/resilient genotypes of foundation
development of specific traits in response to environmental stresses species could be a valid approach to restore marine ecosystems
passed from parental individuals to the progeny, but also the in- (Abelson et al., 2020; Coleman et al., 2020; Kettenring et al., 2014;
heritance of regulatory epigenetic machinery enhancing offspring van Katwijk et al., 2009). Selected genotypes should present a set
to activate regulatory mechanisms under the same stresses (King of positive traits in order to increase their plasticity for successfully
et al., 2018). Despite the relative long acclimation imposed on plants facing coming fast environmental changes.
under common conditions, it remains still difficult to conclude on In order to support the restoration, better performing genotypes
the genetic and/or epigenetic basis of the observed plasticity. Long can not only be identified and selected but can also be experimen-
acclimation phases and phenotypic responses of individuals under tally manipulated. A possible way is to use gene-­editing approaches,
common conditions over one or more generations are necessary to though their ethical implications are currently under debate
test for adaptive traits in order to reset plants’ experiences of their (Rodriguez, 2016). After the identification of genes that directly af-
place of origin (as in terrestrial model species; Raabová et al., 2007; fect seagrass ability to thrive in a changing climate, genetic engineer-
Watson-­L azowski et al., 2016). However, as stated above, the repro- ing techniques, such as CRISPR (Clustered Regularly Interspaced
duction of seagrasses under controlled conditions is challenging, and Short Palindromic Repeats), can be used to produce genotypes with
life cycles are often too long to allow experimentation over multiple higher plasticity and the ability to acclimate and adapt to strong and
generations. stochastic environmental changes (Scheben et al., 2016).
Common garden experiments can also be designed based on a Another way, which does not involve genetic manipulation, is the
space-­for-­time substitution approach. A case in point is the study experimental hardening. The terms “hardening” or “priming” define
by Winters et al. (2011) that compared plant responses to a heat phenomena that induce temporally limited environmental stimulus
wave originating from three populations of Z. marina across a latitu- in order to prepare and modify the response to future stress (Hilker
dinal thermal gradient. The differential thermal response in terms of et al., 2016). This is a well-­known concept among botanists, which
growth and photo-­physiology was consistent with local adaptation used to harden plants taking advantage of their ability to “remem-
and could be integrated into seagrass models to predict the future ber” their ancestral environments via phenotypic plasticity, reveal-
persistence of this species in different regions affected by climate ing a mechanism by which past experience affects future evolution
changes. (Gibbin et al., 2017; Ho et al., 2020). The capability of genotypes
Some common garden experimental designs are a merger of to save memory of past stress events and to better perform when
all approaches described above (Jueterbock et al., 2016; Marín-­ the stress re-­occurs has recently been observed in seagrasses (i.e.,
Guirao et al., 2018). Jueterbock and colleagues tested temperature P. australis and Z. muelleri, Nguyen et al., 2020). This process is one
adaptation of Z. marina populations collected from contrasting and element of “assisted evolution” strategies to promote individual
phylogenetically independent thermal clines (North vs South in and population resilience against environmental changes without
Mediterranean and Atlantic areas), using a common garden exper- genetic manipulation constraints (Filbee-­Dexter & Smajdor, 2019).
iment combined with a space-­for-­time substitution design in an- Genotypes with improved resistance (i.e., hardening response, Bruce
ticipation of rapid ocean warming predicted for the next decades. et al., 2007) can represent preferential material for the restoration of
Upon exposure of plants to a marine heat wave, full transcriptome endangered or disturbed populations. In terrestrial studies, the abil-
profiles were obtained and mapped onto the genome. Results re- ity to “remember” past stressful events is currently investigated for
vealed a stronger adaptive transcriptomic differentiation between model crop species, especially through the assessment of epigenetic
the Mediterranean and the Atlantic samples that is likely due to modifications induced by the exposure to stress (Liu et al., 2015).
the reduced gene flows that characterized the smaller and isolated Although the field of ecological epigenetics is gaining momentum, due
PAZZAGLIA et al. | 1193

to the application of increasingly specific and sophisticated molec- consideration of molecular elements that may have strongly regu-
ular techniques (Ay et al., 2014; Bossdorf et al., 2010; Popova et al., latory roles in stress responses, such as transposable elements and
2013; Rendina Gonzàlez et al., 2018; Richards et al., 2017), the study micro-­RNA (miRNAs) (e.g., Barghini et al., 2015). The improvement
of the epigenetic “stress memory” is still at the beginning, for both of molecular approaches in seagrasses could play a crucial role not
marine and terrestrial plants. only in studying their plasticity but also in digging on the basis of
stress memory and on its potential evolutionary role under global
climate changes (Chinnusamy & Zhu, 2009; Lämke & Bäurle, 2017).
7 | CO N C LU S I O N S In conclusion, we strongly suggest that the evaluation of plastic
adaptive responses should be moved from a local to a global scale.
Our main goal was to present an overview on the importance of The future implementation and evolution of seagrass observatories
plasticity in the face of rapid environmental changes for a group of will foster this process. Next-­generation marine observatories should
marine plants with long generation times owing to clonality that lives make it possible to collect multivariate time series synchronously
in an environment with very steep environmental gradients, subject in different sites or regions and to exploit the information by inte-
to alarming rates of global change. The rapid occurrence of global grating data through multivariate statistics and/or machine-­learning
changes forces marine plants to react in order to prevent popula- algorithms (Crise et al., 2018; Danovaro et al., 2016). Real-­time mul-
tion declines. Species react acclimating to new conditions, through tivariate monitoring in seagrass observatories will enable assessing
phenotypic plasticity, evolutionary adaptation, or migration (Bulleri environmental and seagrass trait changes and inferring adaptive po-
et al., 2018). The acclimation abilities as one major form of pheno- tential of the observed processes in seagrass populations.
typic plasticity are widely explored in seagrasses’ studies (Bité et al.,
2007; Dattolo et al., 2017; Duarte et al., 2018; Maxwell et al., 2014). AC K N OW L E D G E M E N T S
This acclimation process can be based on genetic and epigenetic JP was supported by University of Trieste Ph.D. fellowship shared
processes, the last fostering rapid adaptive evolution (Douhovnikoff with SZN, by the project Marine Hazard, PON03PE_00203_1, Italian
& Dodd, 2015), but it is so far unstudied in seagrasses. Equally, un- Ministry of Education, University and Research (MIUR), and by the
studied is the adaptive significance of a large degree of standing so- project Assemble Plus EU-­FP7.
matic genetic variation detected in seagrass clones that could be the
basis for adaptation within a genet or clone (Yu et al., 2020). The C O N FL I C T S O F I N T E R E S T
adaptation occurs through natural selection and requires too long There is no conflicts of interest to declare.
times to react in the face of rapid changes. Nevertheless, the selec-
tion of more plastic genotypes could prevent population declines, DATA AVA I L A B I L I T Y S TAT E M E N T
as they are more likely to contrast dynamic changes (Bricker et al., Data sharing not applicable to this article as no datasets were gener-
2011; Table S2). ated or analyzed during the current study.
We explored several main approaches that allow us to infer the
nature of plastic responses to global changes and discussed pros and ORCID
cons. The experimental approaches implemented in seagrass stud- Jessica Pazzaglia https://orcid.org/0000-0002-8677-7712
ies, whether performed with controlled or field experiments and Thorsten B. H. Reusch https://orcid.org/0000-0002-8961-4337
space for time designs, were instrumental for exploring the basis of Antonio Terlizzi https://orcid.org/0000-0001-5968-4548
plasticity. One future avenue is clearly more multi-­factorial exper- Lázaro Marín-­Guirao https://orcid.org/0000-0001-6240-8018
iments that would be required to understand seagrass responses Gabriele Procaccini https://orcid.org/0000-0002-6179-468X
under more realistic present and future scenarios. Another import-
ant way forward is the integration of different phenotypic and ge-
REFERENCES
nomic approaches to study the interaction among the genetic and
Abelson, A., Reed, D. C., Edgar, G. J., Smith, C. S., Kendrick, G. A., Orth,
plastic components of phenotypic variation, including the study
R. J., Airoldi, L., Silliman, B., Beck, M. W., Krause, G., Shashar, N.,
of epigenetic mechanisms. Considering the importance that plas- Stambler, N., & Nelson, P. (2020). Challenges for restoration of
ticity may have in response to rapid environmental changes, future coastal marine ecosystems in the anthropocene. Frontiers in Marine
promising research in seagrasses should involve the analysis of rela- Science, 7, 892. https://doi.org/10.3389/fmars.2020.544105
Alcoverro, T., & Mariani, S. (2005). Shoot growth and nitrogen responses
tionships between gene expression profiles resulting from environ-
to simulated herbivory in Kenyan seagrasses. Botanica Marina, 48(1),
mental stresses and epigenetic regulatory machinery. The majority 1–­7. https://doi.org/10.1515/BOT.2005.010
of seagrass studies employing molecular approaches involve gene Anderson, J. T., Lee, C. R., & Mitchell-­Olds, T. (2014). Strong selection
expression and transcriptomic analysis, while being limited to few genome-­wide enhances fitness trade-­offs across environments
and episodes of selection. Evolution, 68(1), 16–­31. https://doi.
species and mostly related to thermal and light responses (Davey
org/10.1111/evo.12259
et al., 2016; Gu et al., 2012; Marín-­Guirao et al., 2017; Procaccini Arnaud-­Haond, S., Duarte, C. M., Diaz-­Almela, E., Marbà, N., Sintes, T.,
et al., 2017; Tutar et al., 2017). We also observed that many recent & Serrão, E. A. (2012). Implications of extreme life span in clonal or-
transcriptomic studies in response to environmental stressors lack ganisms: Millenary clones in meadows of the threatened seagrass
1194 | PAZZAGLIA et al.

posidonia oceanica. PLoS One, 7(2), e30454. https://doi.org/10.1371/ Ecology, 265, 77–­83. https://doi.org/10.1007/978-­3-­319-­06419​
journ​al.pone.0030454 -­2_84
Arnaud-­Haond, S., Moalic, Y., Hernández-­García, E., Eguiluz, V. M., Bité, J. S., Campbell, S. J., McKenzie, L. J., & Coles, R. G. (2007).
Alberto, F., Serrão, E. A., & Duarte, C. M. (2014). Disentangling the Chlorophyll fluorescence measures of seagrasses Halophila ovalis
influence of mutation and migration in clonal seagrasses using the and Zostera capricorni reveal differences in response to experimental
genetic diversity spectrum for microsatellites. Journal of Heredity, shading. Marine Biology, 152(2), 405–­414. https://doi.org/10.1007/
105(4), 532–­541. https://doi.org/10.1093/jhere​d/esu015 s0022​7-­0 07-­0700-­6
Arnaud-­Haond, S., Stoeckel, S., & Bailleul, D. (2020). New insights into Blok, S., Olesen, B., & Krause-­Jensen, D. (2018). Life history events of
the population genetics of partially clonal organisms: When seagrass eelgrass Zostera marina L. populations across gradients of latitude
data meet theoretical expectations. Molecular Ecology, 29(17), 3248–­ and temperature. Marine Ecology Progress Series, 590, 79–­93. https://
3260. https://doi.org/10.1111/mec.15532 doi.org/10.3354/meps1​2479
Artika, S. R., Ambo-­Rappe, R., Teichberg, M., Moreira-­Saporiti, A., & Bos, A. R., Bouma, T. J., de Kort, G. L. J., & van Katwijk, M. M. (2007).
Viana, I. G. (2020). Morphological and physiological responses of Ecosystem engineering by annual intertidal seagrass beds: Sediment
Enhalus acoroides seedlings under varying temperature and nu- accretion and modification. Estuarine, Coastal and Shelf Science, 74(1–­
trient treatment. Frontiers in Marine Science, 7, 325. https://doi. 2), 344–­3 48. https://doi.org/10.1016/j.ecss.2007.04.006
org/10.3389/fpls.2020.571363 Bossdorf, O., Arcuri, D., Richards, C. L., & Pigliucci, M. (2010).
Ashander, J., Chevin, L. M., & Baskett, M. L. (2016). Predicting evolu- Experimental alteration of DNA methylation affects the pheno-
tionary rescue via evolving plasticity in stochastic environments. typic plasticity of ecologically relevant traits in Arabidopsis thaliana.
Proceedings of the Royal Society B: Biological Sciences, 283(1839), Evolutionary Ecology, 24(3), 541–­553. https://doi.org/10.1007/s1068​
20161690. https://doi.org/10.1098/rspb.2016.1690 2-­010-­9372-­7
Auld, J. R., Agrawal, A. A., & Relyea, R. A. (2010). Re-­evaluating the Bossdorf, O., Richards, C. L., & Pigliucci, M. (2008). Epigenetics
costs and limits of adaptive phenotypic plasticity. Proceedings of the for ecologists. Ecology Letters, 11(2), 106–­115. https://doi.
Royal Society B: Biological Sciences, 277(1681), 503–­511. https://doi. org/10.1111/j.1461-­0248.2007.01130.x
org/10.1098/rspb.2009.1355 Botero, C. A., Weissing, F. J., Wright, J., & Rubenstein, D. R. (2015).
Ay, N., Janack, B., & Humbeck, K. (2014). Epigenetic control of plant Evolutionary tipping points in the capacity to adapt to environmen-
senescence and linked processes. Journal of Experimental Botany, tal change. Proceedings of the National Academy of Sciences of the
65(14), 3875–­3887. https://doi.org/10.1093/jxb/eru132 United States of America, 112(1), 184–­189. https://doi.org/10.1073/
Banet, A. I., & Trexler, J. C. (2013). Space-­for-­time substitution works in pnas.14085​89111
everglades ecological forecasting models. PLoS One, 8(11), e81025. Boudouresque, C. F., Bernard, G., Pergent, G., Shili, A., & Verlaque, M.
https://doi.org/10.1371/journ​al.pone.0081025 (2009). Regression of Mediterranean seagrasses caused by natu-
Barghini, E., Mascagni, F., Natali, L., Giordani, T., & Cavallini, A. (2015). ral processes and anthropogenic disturbances and stress: A critical
Analysis of the repetitive component and retrotransposon popula- review. Botanica Marina, 52(5), 395–­418. https://doi.org/10.1515/
tion in the genome of a marine angiosperm, Posidonia oceanica (L.) BOT.2009.057
Delile. Marine Genomics, 24, 397–­4 04. https://doi.org/10.1016/j. Bricker, E., Waycott, M., Calladine, A., & Zieman, J. C. (2011). High con-
margen.2015.10.002 nectivity across environmental gradients and implications for pheno-
Baughman, O. W., Agneray, A. C., Forister, M. L., Kilkenny, F. F., Espeland, typic plasticity in a marine plant. Marine Ecology Progress Series, 423,
E. K., Fiegener, R., & Leger, E. A. (2019). Strong patterns of intra- 57–­67. https://doi.org/10.3354/meps0​8962
specific variation and local adaptation in Great Basin plants revealed Bruce, T. J. A., Matthes, M. C., Napier, J. A., & Pickett, J. A. (2007).
through a review of 75 years of experiments. Ecology and Evolution, Stressful “memories” of plants: Evidence and possible mechanisms.
9(11), 6259–­6275. https://doi.org/10.1002/ece3.5200 Plant Science, 173(6), 603–­608. https://doi.org/10.1016/j.plant​
Beaman, J. E., White, C. R., & Seebacher, F. (2016). Evolution of plas- sci.2007.09.002
ticity: Mechanistic link between development and reversible accli- Bulleri, F., Eriksson, B. K., Queirós, A., Airoldi, L., Arenas, F., Arvanitidis,
mation. Trends in Ecology and Evolution, 31(3), 237–­249. https://doi. C., Bouma, T. J., Crowe, T. P., Davoult, D., Guizien, K., Iveša, L.,
org/10.1016/j.tree.2016.01.004 Jenkins, S. R., Michalet, R., Olabarria, C., Procaccini, G., Serrão, E. A.,
Beisner, B. E., Haydon, D. T., & Cuddington, K. (2003). Alternative stable Wahl, M., & Benedetti-­Cecchi, L. (2018). Harnessing positive species
states in ecology. Frontiers in Ecology and the Environment, 1(7), 376. interactions as a tool against climate-­driven loss of coastal biodiver-
https://doi.org/10.2307/3868190 sity. PLoS Biology, 16(9), e2006852. https://doi.org/10.1371/journ​
Bell, G., & Gonzalez, A. (2009). Evolutionary rescue can prevent extinc- al.pbio.2006852
tion following environmental change. Ecology Letters, 12(9), 942–­948. Buyantuyev, A., Xu, P., Wu, J., Piao, S., & Wang, D. (2012). A space-­for-­
https://doi.org/10.1111/j.1461-­0248.2009.01350.x time (SFT) substitution approach to studying historical phenological
Bercovich, M. V., Schubert, N., Almeida Saá, A. C., Silva, J., & Horta, changes in urban environment. PLoS One, 7(12), e51260. https://doi.
P. A. (2019). Multi-­level phenotypic plasticity and the persistence org/10.1371/journ​al.pone.0051260
of seagrasses along environmental gradients in a subtropical la- Ceccherelli, G., Oliva, S., Pinna, S., Piazzi, L., Procaccini, G., Marin-­Guirao,
goon. Aquatic Botany, 157, 24–­32. https://doi.org/10.1016/j.aquab​ L., Dattolo, E., Gallia, R., La Manna, G., Gennaro, P., Costa, M. M.,
ot.2019.06.003 Barrote, I., Silva, J., & Bulleri, F. (2018). Seagrass collapse due to syner-
Bergmann, N., Winters, G., Rauch, G., Eizaguirre, C., Gu, J., Nelle, gistic stressors is not anticipated by phenological changes. Oecologia,
P., Fricke, B., & Reusch, T. B. H. (2010). Population-­s pecificity 186(4), 1137–­1152. https://doi.org/10.1007/s0044​2-­018-­4 075-­9
of heat stress gene induction in northern and southern eel- Champenois, W., & Borges, A. V. (2019). Inter-­annual variations over a
grass Zostera marina populations under simulated global decade of primary production of the seagrass Posidonia oceanica.
warming. Molecular Ecology, 19(14), 2870–­2883. https://doi. Limnology and Oceanography, 64(1), 32–­45. https://doi.org/10.1002/
org/10.1111/j.1365-­294X.2010.04731.x lno.11017
Billingham, M., Reusch, T., Alberto, F., & Serrão, E. (2003). Is asexual re- Chase, M. W., Christenhusz, M. J. M., Fay, M. F., Byng, J. W., Judd, W.
production more important at geographical limits? A genetic study S., Soltis, D. E., & Weber, A. (2016). An update of the Angiosperm
of the seagrass Zostera marina in the Ria Formosa, Portugal. Marine Phylogeny Group classification for the orders and families of
PAZZAGLIA et al. | 1195

flowering plants: APG IV. Botanical Journal of the Linnean Society, Davey, P. A., Pernice, M., Sablok, G., Larkum, A., Lee, H. T., Golicz,
181(1), 1–­20. https://doi.org/10.1111/boj.12385 A., Edwards, D., Dolferus, R., & Ralph, P. (2016). The emergence
Chaturvedi, A. K., Bahuguna, R. N., Pal, M., Shah, D., Maurya, S., & of molecular profiling and omics techniques in seagrass biol-
Jagadish, K. S. V. (2017). Elevated CO2 and heat stress interactions ogy; furthering our understanding of seagrasses. Functional and
affect grain yield, quality and mineral nutrient composition in rice Integrative Genomics, 16(5), 465–­4 80. https://doi.org/10.1007/
under field conditions. Field Crops Research, 206, 149–­157. https:// s1014​2-­016-­0501-­4
doi.org/10.1016/j.fcr.2017.02.018 De Los Santos, C. B., Brun, F. G., Bouma, T. J., Vergara, J. J., & Pérez-­
Chevin, L. M., & Hoffmann, A. A. (2017). Evolution of phenotypic plas- Lloréns, J. L. (2009). Acclimation of seagrass Zostera noltii to co-­
ticity in extreme environments. Philosophical Transactions of the occurring hydrodynamic and light stresses. Marine Ecology Progress
Royal Society B: Biological Sciences, 372(1723), 20160138. https://doi. Series, 398, 127–­135. https://doi.org/10.3354/meps0​8343
org/10.1098/rstb.2016.0138 De Los Santos, C. B., Onoda, Y., Vergara, J. J., Pérez-­Lloréns, J. L., Bouma,
Chinnusamy, V., & Zhu, J. K. (2009). Epigenetic regulation of stress re- T. J., La Nafie, Y. A., Cambridge, M. L., & Brun, F. G. (2016). A compre-
sponses in plants. Current Opinion in Plant Biology, 12(2), 133–­139. hensive analysis of mechanical and morphological traits in temperate
https://doi.org/10.1016/j.pbi.2008.12.006 and tropical seagrass species. Marine Ecology Progress Series, 551, 81–­
Coleman, M. A., Wood, G., Filbee-­D exter, K., Minne, A. J. P., Goold, 94. https://doi.org/10.3354/meps1​1717
H. D., Vergés, A., Marzinelli, E. M., Steinberg, P. D., & Wernberg, De Villemereuil, P., Gaggiotti, O. E., Mouterde, M., & Till-­Bottraud, I.
T. (2020). Restore or redefine: Future trajectories for resto- (2016). Common garden experiments in the genomic era: New per-
ration. Frontiers in Marine Science, 7, 237. https://doi.org/10.3389/ spectives and opportunities. Heredity, 116(3), 249–­254. https://doi.
fmars.2020.00237 org/10.1038/hdy.2015.93
Collier, C. J., Waycott, M., & Ospina, A. G. (2012). Responses of four Indo-­ DeWitt, T. J., Sih, A., & Wilson, D. S. (1998). Costs and limits of pheno-
West Pacific seagrass species to shading. Marine Pollution Bulletin, typic plasticity. Trends in Ecology and Evolution, 13(2), 77–­81. https://
65(4–­9), 342–­354. https://doi.org/10.1016/j.marpo​lbul.2011.06.017 doi.org/10.1016/S0169​-­5347(97)01274​-­3
Cox, T. E., Schenone, S., Delille, J., Díaz-­C astañeda, V., Alliouane, Diaz-­Almela, E., Marbà, N., Álvarez, E., Balestri, E., Ruiz-­Fernández, J.
S., Gattuso, J. P., & Gazeau, F. (2015). Effects of ocean acidifi- M., & Duarte, C. M. (2006). Patterns of seagrass (Posidonia ocean-
cation on Posidonia oceanica epiphytic community and shoot ica) flowering in the Western Mediterranean. Marine Biology, 148(4),
productivity. Journal of Ecology, 103(6), 1594–­1609. https://doi. 723–­742. https://doi.org/10.1007/s0022​7-­0 05-­0127-­x
org/10.1111/1365-­2745.12477 Dodd, R. S., & Douhovnikoff, V. (2016). Adjusting to global change
Coyer, J. A., Hoarau, G., Kuo, J., Tronholm, A., Veldsink, J., & Olsen, J. L. through clonal growth and epigenetic variation. Frontiers in Ecology
(2013). Phylogeny and temporal divergence of the seagrass family and Evolution, 4, 86. https://doi.org/10.3389/fevo.2016.00086
Zosteraceae using one nuclear and three chloroplast loci. Systematics Donelson, J. M., Sunday, J. M., Figueira, W. F., Gaitán-­Espitia, J. D.,
and Biodiversity, 11(3), 271–­284. https://doi.org/10.1080/14772​ Hobday, A. J., Johnson, C. R., Leis, J. M., Ling, S. D., Marshall, D.,
000.2013.821187 Pandolfi, J. M., Pecl, G., Rodgers, G. G., Booth, D. J., & Munday, P.
Crise, A., Ribera d’Alcalà, M., Mariani, P., Petihakis, G., Robidart, J., L. (2019). Understanding interactions between plasticity, adapta-
Iudicone, D., Bachmayer, R., & Malfatti, F. (2018). A conceptual tion and range shifts in response to marine environmental change.
framework for developing the next generation of marine observa- Philosophical Transactions of the Royal Society B: Biological Sciences,
tories (MOBs) for science and society. Frontiers in Marine Science, 5, 374(1768), 20180186. https://doi.org/10.1098/rstb.2018.0186
318. https://doi.org/10.3389/fmars.2018.00318 Douhovnikoff, V., & Dodd, R. S. (2015). Epigenetics: A potential mecha-
Cruz, M. V., Mori, G. M., Signori-­Müller, C., da Silva, C. C., Oh, D.-­H., nism for clonal plant success. Plant Ecology, 216(2), 227–­233. https://
Dassanayake, M., Zucchi, M. I., Oliveira, R. S., & de Souza, A. P. (2019). doi.org/10.1007/s1125​8-­014-­0 430-­z
Local adaptation of a dominant coastal tree to freshwater availabil- Duarte, B., Martins, I., Rosa, R., Matos, A. R., Roleda, M. Y., Reusch, T.
ity and solar radiation suggested by genomic and ecophysiological B. H., Engelen, A. H., Serrão, E. A., Pearson, G. A., Marques, J. C.,
approaches. Scientific Reports, 9(1), 1–­15. https://doi.org/10.1038/ Caçador, I., Duarte, C. M., & Jueterbock, A. (2018). Climate change
s4159​8-­019-­56469​-­w impacts on seagrass meadows and macroalgal forests: An integra-
Danovaro, R., Carugati, L., Berzano, M., Cahill, A. E., Carvalho, S., Chenuil, tive perspective on acclimation and adaptation potential. Frontiers
A., Corinaldesi, C., Cristina, S., David, R., Dell'Anno, A., Dzhembekova, in Marine Science, 5, 190. https://doi.org/10.3389/fmars.2018.00190
N., Garcés, E., Gasol, J. M., Goela, P., Féral, J.-­P., Ferrera, I., Forster, Duarte, C. M., & Krause-­Jensen, D. (2017). Export from seagrass mead-
R. M., Kurekin, A. A., Rastelli, E., … Borja, A. (2016). Implementing ows contributes to marine carbon sequestration. Frontiers in Marine
and innovating marine monitoring approaches for assessing marine Science, 4, 1–­7. https://doi.org/10.3389/fmars.2017.00013
environmental status. Frontiers in Marine Science, 3, 213. https://doi. Egea, L. G., Jiménez-­Ramos, R., Vergara, J. J., Hernández, I., & Brun, F.
org/10.3389/fmars.2016.00213 G. (2018). Interactive effect of temperature, acidification and am-
Darnell, K. M., & Dunton, K. H. (2017). Plasticity in turtle grass (Thalassia monium enrichment on the seagrass Cymodocea nodosa. Marine
testudinum) flower production as a response to porewater nitrogen Pollution Bulletin, 134, 14–­26. https://doi.org/10.1016/j.marpo​
availability. Aquatic Botany, 138, 100–­106. https://doi.org/10.1016/j. lbul.2018.02.029
aquab​ot.2017.01.007 Ehlers, A., Worm, B., & Reusch, T. B. H. (2008). Importance of genetic
Dattolo, E., Marín-­Guirao, L., Ruiz, J. M., & Procaccini, G. (2017). Long-­ diversity in eelgrass Zostera marina for its resilience to global warm-
term acclimation to reciprocal light conditions suggests depth-­ ing. Marine Ecology Progress Series, 355, 1–­7. https://doi.org/10.3354/
related selection in the marine foundation species Posidonia ocean- meps0​7369
ica. Ecology and Evolution, 7(4), 1148–­1164. https://doi.org/10.1002/ Evans, S. M., Sinclair, E. A., Poore, A. G. B., Bain, K. F., & Vergés, A. (2018).
ece3.2731 Assessing the effect of genetic diversity on the early establishment
Dattolo, E., Ruocco, M., Brunet, C., Lorenti, M., Lauritano, C., D'Esposito, of the threatened seagrass Posidonia australis using a reciprocal-­
D., De Luca, P., Sanges, R., Mazzuca, S., & Procaccini, G. (2014). transplant experiment. Restoration Ecology, 26(3), 570–­580. https://
Response of the seagrass Posidonia oceanica to different light doi.org/10.1111/rec.12595
environments: Insights from a combined molecular and photo-­ Falk, D. A., Knapp, E. E., & Guerrant, E. O. (2001). An introduction to res-
physiological study. Marine Environmental Research, 101(1), 225–­236. toration genetics, (12–­21). Washington, DC: Society for Ecological
https://doi.org/10.1016/j.maren​vres.2014.07.010 Restoration.
1196 | PAZZAGLIA et al.

Feil, R., & Fraga, M. F. (2012). Epigenetics and the environment: Emerging Gu, J., Weber, K., Klemp, E., Winters, G., Franssen, S. U., Wienpahl, I.,
patterns and implications. Nature Reviews Genetics, 13(2), 97–­109. Huylmans, A.-­K ., Zecher, K., Reusch, T. B. H., Bornberg-­Bauer, E., &
https://doi.org/10.1038/nrg3142 Weber, A. P. M. (2012). Identifying core features of adaptive met-
Ferber, S., Stam, W. T., & Olsen, J. L. (2008). Genetic diversity and con- abolic mechanisms for chronic heat stress attenuation contributing
nectivity remain high in eelgrass Zostera marina populations in the to systems robustness. Integrative Biology, 4(5), 480–­493. https://doi.
Wadden Sea, despite major impacts. Marine Ecology Progress Series, org/10.1039/c2ib0​0109h
372, 87–­96. https://doi.org/10.3354/meps0​7705 Gunderson, A. R., Armstrong, E. J., & Stillman, J. H. (2016). Multiple
Filbee-­Dexter, K., & Smajdor, A. (2019). Ethics of assisted evolution in stressors in a changing world: The need for an improved perspec-
marine conservation. Frontiers in Marine Science, 6, 1–­6. https://doi. tive on physiological responses to the dynamic marine environ-
org/10.3389/fmars.2019.00020 ment. Annual Review of Marine Science, 8(1), 357–­378. https://doi.
Forsman, A. (2015). Rethinking phenotypic plasticity and its conse- org/10.1146/annur​ev-­marin​e-­12241​4-­033953
quences for individuals, populations and species. Heredity, 115(4), Hamilton, J. A., & Miller, J. M. (2016). Adaptive introgression as a re-
276–­284. https://doi.org/10.1038/hdy.2014.92 source for management and genetic conservation in a changing cli-
Fourqurean, J. W., Duarte, C. M., Kennedy, H., Marbà, N., Holmer, M., mate. Conservation Biology, 30(1), 33–­41. https://doi.org/10.1111/
Mateo, M. A., Apostolaki, E. T., Kendrick, G. A., Krause-­Jensen, D., cobi.12574
McGlathery, K. J., & Serrano, O. (2012). Seagrass ecosystems as a Harley, C. D. G., Randall Hughes, A., Hultgren, K. M., Miner, B. G.,
globally significant carbon stock. Nature Geoscience, 5(7), 505–­509. Sorte, C. J. B., Thornber, C. S., Rodriguez, L. F., Tomanek, L., &
https://doi.org/10.1038/ngeo1477 Williams, S. L. (2006). The impacts of climate change in coastal
Franks, S. J. (2011). Plasticity and evolution in drought avoidance and es- marine systems. Ecology Letters, 9(2), 228–­241. https://doi.
cape in the annual plant Brassica rapa. New Phytologist, 190(1), 249–­ org/10.1111/j.1461-­0248.2005.00871.x
257. https://doi.org/10.1111/j.1469-­8137.2010.03603.x Haseneyer, G., Stracke, S., Paul, C., Einfeldt, C., Broda, A., Piepho, H.-­
Franks, S. J., Sim, S., & Weis, A. E. (2007). Rapid evolution of flowering time P., Graner, A., & Geiger, H. H. (2009). Population structure and
by an annual plant in response to a climate fluctuation. Proceedings of phenotypic variation of a spring barley world collection set up for
the National Academy of Sciences of the United States of America, 104(4), association studies. Plant Breeding, 129(3), 271–­279. https://doi.
1278–­1282. https://doi.org/10.1073/pnas.06083​79104 org/10.1111/j.1439-­0523.2009.01725.x
Franssen, S. U., Gu, J., Bergmann, N., Winters, G., Klostermeier, U. Hämmerli, A., & Reusch, T. B. H. (2002). Local adaptation and trans-
C., Rosenstiel, P., Bornberg-­Bauer, E., & Reusch, T. B. H. (2011). plant dominance in genets of the marine clonal plant Zostera ma-
Transcriptomic resilience to global warming in the seagrass rina. Marine Ecology Progress Series, 242, 111–­118. https://doi.
Zostera marina, a marine foundation species. Proceedings of the org/10.3354/meps2​42111
National Academy of Sciences, 108(48), 19276–­19281. https://doi. Hedges, S. B., & Kumar, S. (Eds.), (2009). The Timetree of Life. OUP
org/10.1073/pnas.11076​8 0108 Oxford.
Fukami, T., & Wardle, D. A. (2005). Long-­term ecological dynamics: Hilker, M., Schwachtje, J., Baier, M., Balazadeh, S., Bäurle, I., Geiselhardt,
Reciprocal insights from natural and anthropogenic gradients. S., Hincha, D. K., Kunze, R., Mueller-­Roeber, B., Rillig, M. C., Rolff, J.,
Proceedings of the Royal Society B: Biological Sciences, 272(1577), Romeis, T., Schmülling, T., Steppuhn, A., van Dongen, J., Whitcomb,
2105–­2115. https://doi.org/10.1098/rspb.2005.3277 S. J., Wurst, S., Zuther, E., & Kopka, J. (2016). Priming and memory
Gabriel, W., & Lynch, M. (1992). The selective advantage of reaction of stress responses in organisms lacking a nervous system. Biological
norms for environmental tolerance. Journal of Evolutionary Biology, Reviews, 91(4), 1118–­1133. https://doi.org/10.1111/brv.12215
5(1), 41–­59. https://doi.org/10.1046/j.1420-­9101.1992.50100​41.x Ho, W. C., Li, D., Zhu, Q., Zhang, J., & Zhang, J. (2020). Phenotypic plas-
Gacia, E., Littler, M. M., & Littler, D. S. (1999). An experimental test of ticity as a long-­term memory easing readaptations to ancestral en-
the capacity of food web interactions (fish–­epiphytes–­seagrasses) vironments. Science Advances, 6(21), 1–­9. https://doi.org/10.1126/
to offset the negative consequences of eutrophication on seagrass sciadv.aba3388
communities. Estuarine, Coastal and Shelf Science, 48(6), 757–­766. Holliday, R. (2006). Epigenetics: A historical overview. Epigenetics, 1(2),
https://doi.org/10.1006/ecss.1999.0477 76–­8 0. https://doi.org/10.4161/epi.1.2.2762
Garrote-­Moreno, A., Cambridge, M., & Sánchez-­Lizaso, J. L. (2016). Ion Honnay, O., & Bossuyt, B. (2005). Prolonged clonal growth: Escape
concentrations in seagrass: A comparison of results from field and route or route to extinction? Oikos, 108(2), 427–­432. https://doi.
controlled-­environment studies. Estuarine, Coastal and Shelf Science, org/10.1111/j.0030-­1299.2005.13569.x
181, 209–­217. https://doi.org/10.1016/j.ecss.2016.08.034 Hughes, A. R., Inouye, B. D., Johnson, M. T. J., Underwood, N., & Vellend, M.
Georgiou, D., Alexandre, A., Luis, J., & Santos, R. (2016). Temperature (2008). Ecological consequences of genetic diversity. Ecology Letters,
is not a limiting factor for the expansion of Halophila stipulacea 11, 609–­623. https://doi.org/10.1111/j.1461-­0248.2008.01179.x
throughout the Mediterranean Sea. Marine Ecology Progress Series, IPCC (2019). Technical summary. In H.-­O. Pörtner, D. C. Roberts, V.
544, 159–­167. https://doi.org/10.3354/meps1​1582 Masson-­Delmotte, P. Zhai, E. Poloczanska, K. Mintenbeck, et al.
Gibbin, E. M., Massamba N’Siala, G., Chakravarti, L. J., Jarrold, M. D., & (Eds.), IPCC special report on the ocean and cryosphere in a changing
Calosi, P. (2017). The evolution of phenotypic plasticity under global climate (37–­74). IPCC.
change. Scientific Reports, 7(1), 1–­8. https://doi.org/10.1038/s4159​ Jahnke, M., Christensen, A., Micu, D., Milchakova, N., Sezgin, M.,
8-­017-­17554​- ­0 Todorova, V., Strungaru, S., & Procaccini, G. (2016). Patterns and
Gimeno, T. E., Pías, B., Lemos-­Filho, J. P., & Valladares, F. (2009). Plasticity mechanisms of dispersal in a keystone seagrass species. Marine
and stress tolerance override local adaptation in the responses Environmental Research, 117, 54–­62. https://doi.org/10.1016/j.maren​
of Mediterranean holm oak seedlings to drought and cold. Tree vres.2016.04.004
Physiology, 29(1), 87–­98. https://doi.org/10.1093/treep​hys/tpn007 Jahnke, M., D’Esposito, D., Orrù, L., Lamontanara, A., Dattolo, E.,
Grenier, S., Barre, P., & Litrico, I. (2016). Phenotypic plasticity and selec- Badalamenti, F., Mazzuca, S., Procaccini, G., & Orsini, L. (2019).
tion: Nonexclusive mechanisms of adaptation. Scientifica, 2016, 1–­9. Adaptive responses along a depth and a latitudinal gradient in the
https://doi.org/10.1155/2016/7021701 endemic seagrass Posidonia oceanica. Heredity, 122(2), 233–­243.
Grether, G. F. (2005). Environmental change, phenotypic plasticity, and https://doi.org/10.1038/s4143​7-­018-­0103-­0
genetic compensation. The American Naturalist, 166(4), E115–­E123. Jahnke, M., Olsen, J. L., & Procaccini, G. (2015). A meta-­analysis re-
https://doi.org/10.1086/432023 veals a positive correlation between genetic diversity metrics and
PAZZAGLIA et al. | 1197

environmental status in the long-­lived seagrass Posidonia oceanica. plants. Genome Biology, 18(1), 1–­11. https://doi.org/10.1186/s1305​
Molecular Ecology, 24(10), 2336–­2348. https://doi.org/10.1111/ 9-­017-­1263-­6
mec.13174 Larkum, A. W. D., Orth, R. J., & Duarte, C. M. (2006). Seagrasses: Biology,
Jahnke, M., Serra, I., Bernard, G., & Procaccini, G. (2015). The impor- ecology and conservation (Vol. 53). Netherlands: Springer.
tance of genetic make-­up in seagrass restoration: A case study of the Latzel, V., Rendina González, A. P., & Rosenthal, J. (2016). Epigenetic
seagrass Zostera noltei. Marine Ecology Progress Series, 532, 111–­122. memory as a basis for intelligent behavior in clonal plants. Frontiers in
https://doi.org/10.3354/meps1​1355 Plant Science, 7, 1–­7. https://doi.org/10.3389/fpls.2016.01354
Johannes, F., Porcher, E., Teixeira, F. K., Saliba-­Colombani, V., Simon, M., Lee, H., Golicz, A. A., Bayer, P. E., Jiao, Y., Tang, H., Paterson, A. H., &
Agier, N., Bulski, A., Albuisson, J., Heredia, F., Audigier, P., Bouchez, Edwards, D. (2016). The genome of a southern hemisphere seagrass
D., Dillmann, C., Guerche, P., Hospital, F., & Colot, V. (2009). Assessing species (Zostera muelleri). Plant Physiology, 172(1), 272–­283. https://
the impact of transgenerational epigenetic variation on complex doi.org/10.1104/pp.16.00868
traits. PLoS Genetics, 5(6), e1000530. https://doi.org/10.1371/journ​ Lepais, O., & Bacles, C. F. E. (2014). Two are better than one: Combining
al.pgen.1000530 landscape genomics and common gardens for detecting local adap-
Jueterbock, A., Boström, C., Coyer, J. A., Olsen, J. L., Kopp, M., Dhanasiri, tation in forest trees. Molecular Ecology, 23, 4671–­4673. https://doi.
A. K. S., Smolina, I., Arnaud-­Haond, S., Van de Peer, Y., & Hoarau, org/10.1111/mec.12906
G. (2020). The seagrass methylome is associated with variation in Les, D. H., Cleland, M. A., & Waycott, M. (1997). Phylogenetic stud-
photosynthetic performance among clonal shoots. Frontiers in Plant ies in alismatidae, II: Evolution of marine angiosperms (sea-
Science, 11, 1. https://doi.org/10.3389/fpls.2020.571646 grasses) and hydrophily. Systematic Botany, 22(3), 443. https://doi.
Jueterbock, A., Franssen, S. U., Bergmann, N., Gu, J., Coyer, J. A., Reusch, org/10.2307/2419820
T. B. H., & Olsen, J. L. (2016). Phylogeographic differentiation versus Li, W., Wang, B., & Wang, J. (2006). Lack of genetic variation of an in-
transcriptomic adaptation to warm temperatures in Zostera marina, a vasive clonal plant Eichhornia crassipes in China revealed by RAPD
globally important seagrass. Molecular Ecology, 25(21), 5396–­5411. and ISSR markers. Aquatic Botany, 84(2), 176–­180. https://doi.
https://doi.org/10.1111/mec.13829 org/10.1016/j.aquab​ot.2005.09.008
Kawecki, T. J., & Ebert, D. (2004). Conceptual issues in local ad- Li, X., Guo, T., Mu, Q., Li, X., & Yu, J. (2018). Genomic and environmental
aptation. Ecology Letters, 7(12), 1225–­1241. https://doi. determinants and their interplay underlying phenotypic plasticity.
org/10.1111/j.1461-­0248.2004.00684.x Proceedings of the National Academy of Sciences, 115(26), 6679–­6684.
Kelly, M. (2019). Adaptation to climate change through genetic ac- https://doi.org/10.1073/pnas.17183​26115
commodation and assimilation of plastic phenotypes. Philosophical Liu, J., Feng, L., Li, J., & He, Z. (2015). Genetic and epigenetic control of
Transactions of the Royal Society B: Biological Sciences, 374(1768), plant heat responses. Frontiers in Plant Science, 06, 1–­21. https://doi.
20180176. https://doi.org/10.1098/rstb.2018.0176 org/10.3389/fpls.2015.00267
Kelly, S. A., Panhuis, T. M., & Stoehr, A. M. (2012). Phenotypic plasticity: Marín-­Guirao, L., Bernardeau-­Esteller, J., García-­Muñoz, R., Ramos,
Molecular mechanisms and adaptive significance. Comprehensive A., Ontoria, Y., Romero, J., Pérez, M., Ruiz, J. M., & Procaccini, G.
Physiology, 2(2), 1417–­1439. https://doi.org/10.1002/cphy. (2018). Carbon economy of Mediterranean seagrasses in response
c110008 to thermal stress. Marine Pollution Bulletin, 135, 617–­629. https://doi.
Kendrick, G. A., Waycott, M., Carruthers, T. J. B., Cambridge, M. L., org/10.1016/j.marpo​lbul.2018.07.050
Hovey, R., Krauss, S. L., Lavery, P. S., Les, D. H., Lowe, R. J., Vidal, Marín-­Guirao, L., Entrambasaguas, L., Dattolo, E., Ruiz, J. M., & Procaccini,
O. M. I., Ooi, J. L. S., Orth, R. J., Rivers, D. O., Ruiz-­Montoya, L., G. (2017). Molecular mechanisms behind the physiological resistance
Sinclair, E. A., Statton, J., van Dijk, J. K., & Verduin, J. J. (2012). The to intense transient warming in an iconic marine plant. Frontiers in
central role of dispersal in the maintenance and persistence of sea- Plant Science, 8, 8–­1142. https://doi.org/10.3389/fpls.2017.01142
grass populations. BioScience, 62(1), 56–­65. https://doi.org/10.1525/ Marín-­Guirao, L., Entrambasaguas, L., Ruiz, J. M., & Procaccini, G. (2019).
bio.2012.62.1.10 Heat-­stress induced flowering can be a potential adaptive response to
Kettenring, K. M., Mercer, K. L., Reinhardt Adams, C., & Hines, J. (2014). ocean warming for the iconic seagrass Posidonia oceanica. Molecular
Application of genetic diversity-­ecosystem function research to Ecology, 28(10), 2486–­2501. https://doi.org/10.1111/mec.15089
ecological restoration. Journal of Applied Ecology, 51(2), 339–­3 48. Matesanz, S., Ramos-­Muñoz, M., Moncalvillo, B., Rubio Teso, M. L.,
https://doi.org/10.1111/1365-­2664.12202 García de Dionisio, S. L., Romero, J., & Iriondo, J. M. (2020). Plasticity
King, N. G., McKeown, N. J., Smale, D. A., & Moore, P. J. (2018). The to drought and ecotypic differentiation in populations of a crop wild
importance of phenotypic plasticity and local adaptation in driving relative. AoB PLANTS, 12(2), plaa006. https://doi.org/10.1093/aobpl​
intraspecific variability in thermal niches of marine macrophytes. a/plaa006
Ecography, 41(9), 1469–­1484. https://doi.org/10.1111/ecog.03186 Matesanz, S., & Valladares, F. (2014). Ecological and evolutionary re-
Klimeš, L., Klimešová, J., Hendriks, R., & van Groenendael, J. (1997). sponses of Mediterranean plants to global change. Environmental and
Clonal plant architecture: A comparative analysis of form and func- Experimental Botany, 103, 53–­67. https://doi.org/10.1016/j.envex​
tion. The Ecology and Evolution of Clonal Plants, 2017, 1–­29. pbot.2013.09.004
Kouzarides, T. (2007). Chromatin modifications and their function. Cell, Maxwell, P. S., Pitt, K. A., Burfeind, D. D., Olds, A. D., Babcock, R. C., &
128(4), 693–­705. https://doi.org/10.1016/j.Cell.2007.02.005 Connolly, R. M. (2014). Phenotypic plasticity promotes persistence
La Nafie, Y. A., de los Santos, C. B., Brun, F. G., Mashoreng, S., van following severe events: Physiological and morphological responses
Katwijk, M. M., & Bouma, T. J. (2013). Biomechanical response of two of seagrass to flooding. Journal of Ecology, 102(1), 54–­6 4. https://doi.
fast-­growing tropical seagrass species subjected to in situ shading org/10.1111/1365-­2745.12167
and sediment fertilization. Journal of Experimental Marine Biology and Mazzuca, S., Spadafora, A., Filadoro, D., Vannini, C., Marsoni, M., Cozza,
Ecology, 446, 186–­193. https://doi.org/10.1016/j.jembe.2013.05.020 R., Bracale, M., Pangaro, T., & Innocenti, A. M. (2009). Seagrass
Lambertini, C., Riis, T., Olesen, B., Clayton, J. S., Sorrell, B. K., & Brix, light acclimation: 2-­DE protein analysis in Posidonia leaves grown
H. (2010). Genetic diversity in three invasive clonal aquatic spe- in chronic low light conditions. Journal of Experimental Marine
cies in New Zealand. BMC Genetics, 11(1), 1–­18. https://doi. Biology and Ecology, 374(2), 113–­122. https://doi.org/10.1016/j.
org/10.1186/1471-­2156-­11-­52 jembe.2009.04.010
Lämke, J., & Bäurle, I. (2017). Epigenetic and chromatin-­based mech- McMahon, K., van Dijk, K.-­J., Ruiz-­Montoya, L., Kendrick, G. A., Krauss, S.
anisms in environmental stress adaptation and stress memory in L., Waycott, M., Verduin, J., Lowe, R., Statton, J., Brown, E., & Duarte,
1198 | PAZZAGLIA et al.

C. (2014). The movement ecology of seagrasses. Proceedings of the Palacio-­López, K., Beckage, B., Scheiner, S., & Molofsky, J. (2015). The
Royal Society B: Biological Sciences, 281(1795), 20140878. https://doi. ubiquity of phenotypic plasticity in plants: A synthesis. Ecology and
org/10.1098/rspb.2014.0878 Evolution, 5(16), 3389–­3 400. https://doi.org/10.1002/ece3.1603
Merilä, J., & Hendry, A. P. (2014). Climate change, adaptation, and phe- Pan, J. J., & Price, R. (2002). Fitness and evolution in clonal plants: The
notypic plasticity: The problem and the evidence. Evolutionary impact of clonal growth. Evolutionary Ecology, 15, 583–­600. https://
Applications, 7(1), 1–­14. https://doi.org/10.1111/eva.12137 doi.org/10.1007/978-­94-­017-­1345-­0_20
Molina-­M ontenegro, M. A., & Naya, D. E. (2012). Latitudinal patterns Paulo, D., Cunha, A. H., Boavida, J., Serrão, E. A., Gonçalves, E. J., &
in phenotypic plasticity and fitness-­related traits: Assessing the Fonseca, M. (2019). Open coast seagrass restoration. Can we do it?
climatic variability hypothesis (CVH) with an invasive plant spe- Large scale seagrass transplants. Frontiers in Marine Science, 6, 52.
cies. PLoS One, 7(10), e47620. https://doi.org/10.1371/journ​ https://doi.org/10.3389/fmars.2019.00052
al.pone.0047620 Pazzaglia, J., Santillán-­sarmiento, A., Helber, S. B., Ruocco, M., Terlizzi,
Moreno-­Marín, F., Brun, F. G., & Pedersen, M. F. (2018). Additive re- A., Marín-­guirao, L., & Procaccini, G. (2020). Does warming likely
sponse to multiple environmental stressors in the seagrass Zostera enhance the effects of eutrophication in the seagrass Posidonia oce-
marina L. Limnology and Oceanography, 63(4), 1528–­1544. https://doi. anica? Frontiers in Marine Science, 7, 1–­15. https://doi.org/10.3389/
org/10.1002/lno.10789 fmars.2020.564805
Murren, C. J., Auld, J. R., Callahan, H., Ghalambor, C. K., Handelsman, C. Pennings, S. C., & Callaway, R. M. (2000). The advantages of clonal in-
A., Heskel, M. A., Kingsolver, J. G., Maclean, H. J., Masel, J., Maughan, tegration under different ecological conditions: A community-­wide
H., Pfennig, D. W., Relyea, R. A., Seiter, S., Snell-­Rood, E., Steiner, test. Ecology, 81(3), 709. https://doi.org/10.2307/177371
U. K., & Schlichting, C. D. (2015). Constraints on the evolution of Pereda-­Briones, L., Terrados, J., & Tomas, F. (2019). Negative effects of
phenotypic plasticity: Limits and costs of phenotype and plasticity. warming on seagrass seedlings are not exacerbated by invasive algae.
Heredity, 115(4), 293–­3 01. https://doi.org/10.1038/hdy.2015.8 Marine Pollution Bulletin, 141, 36–­45. https://doi.org/10.1016/j.
Nguyen, H. M., Kim, M., Ralph, P. J., Marín-­Guirao, L., Pernice, M., & marpo​lbul.2019.01.049
Procaccini, G. (2020). Stress memory in seagrasses: First insight into Pernice, M., Sinutok, S., Sablok, G., Commault, A. S., Schliep, M.,
the effects of thermal priming and the role of epigenetic modifica- Macreadie, P. I., Rasheed, M. A., & Ralph, P. J. (2016). Molecular phys-
tions. Frontiers in Plant Science, 11, 494. https://doi.org/10.3389/ iology reveals ammonium uptake and related gene expression in the
FPLS.2020.00494 seagrass Zostera muelleri. Marine Environmental Research, 122, 126–­
Nguyen, H. M., Kleitou, P., Kletou, D., Sapir, Y., & Winters, G. (2018). 134. https://doi.org/10.1016/j.maren​vres.2016.10.003
Differences in flowering sex ratios between native and invasive pop- Pfennig, D. W., Wund, M. A., Snell-­Rood, E. C., Cruickshank, T., Schlichting,
ulations of the seagrass Halophila stipulacea. Botanica Marina, 61(4), C. D., & Moczek, A. P. (2010). Phenotypic plasticity’s impacts on di-
337–­3 42. https://doi.org/10.1515/bot-­2018-­0 015 versification and speciation. Trends in Ecology and Evolution, 25(8),
Nilsson-­Ehle, H. (1914). Vilka erfarenheter hava hittills vunnits rörande 459–­467. https://doi.org/10.1016/j.tree.2010.05.006
möjligheten av växters acklimatisering? Kunglig Landtbruksakadamiens Pigliucci, M. (2001). Phenotypic plasticity: Beyond nature and nurture.
Handlingar och Tidskrift, 53, 537–­572. Baltimore (Md.): Johns Hopkins University Press.
Olesen, B., Enríquez, S., Duarte, C. M., & Sand-­Jensen, K. (2002). Piro, A., Marín-­Guirao, L., Serra, I. A., Spadafora, A., Sandoval-­Gil, J.
Depth-­acclimation of photosynthesis, morphology and demogra- M., Bernardeau-­Esteller, J., Fernandez, J. M. R., & Mazzuca, S.
phy of Posidonia oceanica and Cymodocea nodosa in the Spanish (2015). The modulation of leaf metabolism plays a role in salt tol-
Mediterranean Sea. Marine Ecology Progress Series, 236, 89–­97. erance of Cymodocea nodosa exposed to hypersaline stress in me-
https://doi.org/10.3354/meps2​36089 socosms. Frontiers in Plant Science, 6, 1–­12. https://doi.org/10.3389/
Olsen, J. L., Rouzé, P., Verhelst, B., Lin, Y.-­C ., Bayer, T., Collen, J., fpls.2015.00464
Dattolo, E., De Paoli, E., Dittami, S., Maumus, F., Michel, G., Kersting, Popova, O. V., Dinh, H. Q., Aufsatz, W., & Jonak, C. (2013). The RdDM
A., Lauritano, C., Lohaus, R., Töpel, M., Tonon, T., Vanneste, K., pathway is required for basal heat tolerance in arabidopsis. Molecular
Amirebrahimi, M., Brakel, J., … Van de Peer, Y. (2016). The genome Plant, 6(2), 396–­410. https://doi.org/10.1093/mp/sst023
of the seagrass Zostera marina reveals angiosperm adaptation to the Procaccini, G., Olsen, J. L., & Reusch, T. B. H. (2007). Contribution of ge-
sea. Nature, 530(7590), 331–­335. https://doi.org/10.1038/natur​ netics and genomics to seagrass biology and conservation. Journal of
e16548 Experimental Marine Biology and Ecology, 350(1–­2), 234–­259. https://
Olsen, J. L., Stam, W. T., Coyer, J. A., Reusch, T. B. H., Billingham, doi.org/10.1016/j.jembe.2007.05.035
M., Boström, C., Calvert, E., Christie, H., Granger, S., Lumière, Procaccini, G., & Piazzi, L. (2001). Genetic polymorphism and transplan-
R. L., Milchakova, N., Oudot-­le secq, M.-­P., Procaccini, G., tation success in the Mediterranean seagrass posidonia oceanica.
Sanjabi, B., Serrão, E., Veldsink, J., Widdicombe, S., & Wyllie-­ Restoration Ecology, 9(3), 332–­338. https://doi.org/10.1046/j.1526-­
echeverria, S. (2004). North Atlantic phylogeography and 100X.2001.00900​3332.x
large-­s cale population differentiation of the seagrass Zostera Procaccini, G., Ruocco, M., Marín-­Guirao, L., Dattolo, E., Brunet, C.,
marina L. Molecular Ecology, 13(7), 1923–­1941. https://doi. D’Esposito, D., Lauritano, C., Mazzuca, S., Serra, I. A., Bernardo, L.,
org/10.1111/j.1365-­294X.2004.02205.x Piro, A., Beer, S., Björk, M., Gullström, M., Buapet, P., Rasmusson,
Olsen, Y. S., Sánchez-­C amacho, M., Marbà, N., & Duarte, C. M. (2012). L. M., Felisberto, P., Gobert, S., Runcie, J. W., … Santos, R. (2017).
Mediterranean seagrass growth and demography responses to ex- Depth-­specific fluctuations of gene expression and protein abun-
perimental warming. Estuaries and Coasts, 35(5), 1205–­1213. https:// dance modulate the photophysiology in the seagrass Posidonia oce-
doi.org/10.1007/s1223​7-­012-­9521-­z anica. Scientific Reports, 7(1), 1–­15. https://doi.org/10.1038/srep4​
Ontoria, Y., González-­Guedes, E., Sanmartí, N., Bernardeau-­Esteller, 2890
J., Ruiz, J. M., Romero, J., & Pérez, M. (2019). Interactive effects of Raabová, J., Münzbergová, Z., & Fischer, M. (2007). Ecological rather
global warming and eutrophication on a fast-­growing Mediterranean than geographic or genetic distance affects local adaptation of the
seagrass. Marine Environmental Research, 145, 27–­38. https://doi. rare perennial herb, Aster amellus. Biological Conservation, 139(3–­4),
org/10.1016/j.maren​vres.2019.02.002 348–­357. https://doi.org/10.1016/j.biocon.2007.07.007
Orth, R. J., Harwell, M. C., & Inglis, G. J. (2007). Ecology of seagrass seeds Ravaglioli, C., Lauritano, C., Buia, M. C., Balestri, E., Capocchi, A.,
and seagrass dispersal processes. In Seagrasses: Biology, ecology and Fontanini, D., Pardi, G., Tamburello, L., Procaccini, G., & Bulleri, F.
conservation (pp. 111–­133). Dordrecht, Netherlands: Springer. (2017). Nutrient loading fosters seagrass productivity under ocean
PAZZAGLIA et al. | 1199

acidification. Scientific Reports, 7(1), 1–­14. https://doi.org/10.1038/ loading in the seagrass Posidonia oceanica undergoing herbivore
s4159​8-­017-­14075​-­8 pressure. Oecologia, 188(1), 23–­39. https://doi.org/10.1007/s0044​
Rendina González, A. P., Preite, V., Verhoeven, K. J., & Latzel, V. (2018). 2-­018-­4172-­9
Transgenerational effects and epigenetic memory in the clonal Salo, T., & Pedersen, M. F. (2014). Synergistic effects of altered salinity
plant Trifolium repens. Frontiers in Plant Science, 9, 1677. https://doi. and temperature on estuarine eelgrass (Zostera marina) seedlings and
org/10.3389/fpls.2018.01677 clonal shoots. Journal of Experimental Marine Biology and Ecology, 457,
Reusch, T. B. H. (2014). Climate change in the oceans: Evolutionary ver- 143–­150. https://doi.org/10.1016/j.jembe.2014.04.008
sus phenotypically plastic responses of marine animals and plants. Salo, T., Reusch, T. B. H., & Boström, C. (2015). Genotype-­specific re-
Evolutionary Applications, 7(1), 104–­122. https://doi.org/10.1111/ sponses to light stress in eelgrass Zostera marina, a marine founda-
eva.12109 tion plant. Marine Ecology Progress Series, 519, 129–­140. https://doi.
Reusch, T. B. H., & Boström, C. (2011). Widespread genetic mosaicism org/10.3354/meps1​1083
in the marine angiosperm Zostera marina is correlated with clonal Sánchez-­Gómez, D., Velasco-­Conde, T., Cano-­Martín, F. J., Ángeles
reproduction. Evolutionary Ecology, 25(4), 899–­913. https://doi. Guevara, M., Teresa Cervera, M., & Aranda, I. (2011). Inter-­clonal
org/10.1007/s1068​2-­010-­9436-­8 variation in functional traits in response to drought for a genet-
Reusch, T. B. H., Boström, C., Stam, W. T., & Olsen, J. L. (1999). An ancient ically homogeneous Mediterranean conifer. Environmental and
eelgrass clone in the Baltic. Marine Ecology Progress Series, 183, 301–­ Experimental Botany, 70(2–­3), 104–­109. https://doi.org/10.1016/j.
304. https://doi.org/10.3354/meps1​83301 envex​pbot.2010.08.007
Reusch, T. B. H., Ehlers, A., Hämmerli, A., & Worm, B. (2005). Ecosystem Sánchez-­Sánchez, H., & Morquecho-­Contreras, A. (2017). Chemical plant
recovery after climatic extremes enhanced by genotypic diversity. defense against herbivores. In Shields Vonnie D. C. (Ed.), Herbivores.
Proceedings of the National Academy of Sciences of the United States (4–­18). InTechOpen. https://doi.org/10.5772/67346
of America, 102(8), 2826–­2831. https://doi.org/10.1073/pnas.05000​ Sandoval-­Gil, J. M., Marín-­Guirao, L., & Ruiz, J. M. (2012). Tolerance of
08102 Mediterranean seagrasses (Posidonia oceanica and Cymodocea no-
Reusch, T. B. H., & Wood, T. E. (2007). Molecular ecology of global dosa) to hypersaline stress: Water relations and osmolyte concen-
change. Molecular Ecology, 16(19), 3973–­3992. https://doi. trations. Marine Biology, 159(5), 1129–­1141. https://doi.org/10.1007/
org/10.1111/j.1365-­294X.2007.03454.x s0022​7-­012-­1892-­y
Reynolds, L. K., McGlathery, K. J., & Waycott, M. (2012). Genetic di- Sandoval-­Gil, J. M., Ruiz, J. M., Marín-­Guirao, L., Bernardeau-­Esteller, J.,
versity enhances restoration success by augmenting ecosystem & Sánchez-­Lizaso, J. L. (2014). Ecophysiological plasticity of shallow
services. PLoS One, 7(6), e38397. https://doi.org/10.1371/journ​ and deep populations of the Mediterranean seagrasses Posidonia
al.pone.0038397 oceanica and Cymodocea nodosa in response to hypersaline stress.
Richards, C. L., Alonso, C., Becker, C., Bossdorf, O., Bucher, E., Colomé-­ Marine Environmental Research, 95, 39–­61. https://doi.org/10.1016/j.
Tatché, M., Durka, W., Engelhardt, J., Gaspar, B., Gogol-­Döring, A., maren​vres.2013.12.011
Grosse, I., van Gurp, T. P., Heer, K., Kronholm, I., Lampei, C., Latzel, V., Scheben, A., Yuan, Y., & Edwards, D. (2016). Advances in genomics for
Mirouze, M., Opgenoorth, L., Paun, O., … Verhoeven, K. J. F. (2017). adapting crops to climate change. Current Plant Biology, 6, 2–­10.
Ecological plant epigenetics: Evidence from model and non-­model https://doi.org/10.1016/j.cpb.2016.09.001
species, and the way forward. Ecology Letters, 20(12), 1576–­1590. Scheffer, M., & Carpenter, S. R. (2003). Catastrophic regime shifts in eco-
https://doi.org/10.1111/ele.12858 systems: Linking theory to observation. Trends in Ecology and Evolution,
Rodriguez, E. (2016). Ethical issues in genome editing using Crispr/Cas9 18(12), 648–­656. https://doi.org/10.1016/j.tree.2003.09.002
system. Journal of Clinical Research & Bioethics, 7(2), 1–­4. https://doi. Schlichting, C. D., & Pigliucci, M. (1998). In Sinauer Associates
org/10.4172/2155-­9627.1000266 Incorporated. (Ed.), Phenotypic evolution –­A reaction norm perspec-
Ruggiero, M. V., Turk, R., & Procaccini, G. (2002). Genetic identity and tive. Heredity (Vol. 82). Sunderland, MA: Sinauer Associates.
homozygosity in North-­Adriatic populations of Posidonia oceanica: Serra, I. A., Innocenti, A. M., Di Maida, G., Calvo, S., Migliaccio,
An ancient, post-­glacial clone? Zoologica, 3(1), 71–­74. https://doi. M., Zambianchi, E., & Procaccini, G. (2010). Genetic struc-
org/10.1023/A ture in the Mediterranean seagrass Posidonia oceanica:
Ruiz, J. M., Marín-­Guirao, L., García-­Muñoz, R., Ramos-­Segura, A., Disentangling past vicariance events from contemporary pat-
Bernardeau-­Esteller, J., Pérez, M., Sanmartí, N., Ontoria, Y., Romero, terns of gene flow. Molecular Ecology, 19(3), 557–­568. https://doi.
J., Arthur, R., Alcoverro, T., & Procaccini, G. (2018). Experimental ev- org/10.1111/j.1365-­294X.2009.04462.x
idence of warming-­induced flowering in the Mediterranean seagrass Sharon, Y., Silva, J., Santos, R., Runcie, J. W., Chernihovsky, M., & Beer,
Posidonia oceanica. Marine Pollution Bulletin, 134, 49–­54. https://doi. S. (2009). Photosynthetic responses of Halophila stipulacea to a light
org/10.1016/j.marpo​lbul.2017.10.037 gradient. II. Acclimations following transplantation. Aquatic Biology,
Ruocco, M., De Luca, P., Marín-­Guirao, L., & Procaccini, G. (2019). 7(1–­2), 153–­157. https://doi.org/10.3354/ab00148
Differential leaf age-­dependent thermal plasticity in the keystone Shepherd, S. A., McComb, A. J., & Larkum, A. W. D. (1989). Biology of
seagrass Posidonia oceanica. Frontiers in Plant Science, 10, 1556. seagrasses: A treatise on the biology of seagrasses with special reference
https://doi.org/10.3389/fpls.2019.01556 to the Australian region, vol. 1, (2nd edn, pp. 105–­112). Dordrecht,
Ruocco, M., Entrambasaguas, L., Dattolo, E., Milito, A., Marín-­Guirao, Amsterdam, New York: Elsevier. Retrieved from https://resea​rchre​
L., & Procaccini, G. (2020). A king and vassals’ tale: Molecular sig- posit​ory.murdo​ch.edu.au/id/eprin​t/23985/
natures of clonal integration in Posidonia oceanica under chronic Sih, A., Ferrari, M. C. O., & Harris, D. J. (2011). Evolution and be-
light shortage. Journal of Ecology, 109, 1365–­2745. https://doi. havioural responses to human-­induced rapid environmental
org/10.1111/1365-­2745.13479 change. Evolutionary Applications, 4(2), 367–­387. https://doi.
Ruocco, M., Marín-­Guirao, L., & Procaccini, G. (2019). Within-­and among-­ org/10.1111/j.1752-­4571.2010.00166.x
leaf variations in photo-­physiological functions, gene expression Silva, J., Barrote, I., Costa, M. M., Albano, S., & Santos, R. (2013).
and DNA methylation patterns in the large-­sized seagrass Posidonia Physiological responses of Zostera marina and Cymodocea nodosa
oceanica. Marine Biology, 166(3), 24. https://doi.org/10.1007/s0022​ to light-­limitation stress. PLoS One, 8(11), e81058. https://doi.
7-­019-­3 482-­8 org/10.1371/journ​al.pone.0081058
Ruocco, M., Marín-­Guirao, L., Ravaglioli, C., Bulleri, F., & Procaccini, G. Silvertown, J. (2008). The evolutionary maintenance of sexual re-
(2018). Molecular level responses to chronic versus pulse nutrient production: Evidence from the ecological distribution of asexual
1200 | PAZZAGLIA et al.

reproduction in clonal plants. International Journal of Plant Sciences, spreading of risks, and ecosystem engineering effects. Marine
169(1), 157–­168. https://doi.org/10.1086/523357 Pollution Bulletin, 58(2), 179–­188. https://doi.org/10.1016/j.marpo​
Soissons, L. M., van Katwijk, M. M., Peralta, G., Brun, F. G., Cardoso, lbul.2008.09.028
P. G., Grilo, T. F., Ondiviela, B., Recio, M., Valle, M., Garmendia, J. Verhoeven, K. J. F., VonHoldt, B. M., & Sork, V. L. (2016). Epigenetics
M., Ganthy, F., Auby, I., Rigouin, L., Godet, L., Fournier, J., Desroy, in ecology and evolution: What we know and what we need to
N., Barillé, L., Kadel, P., Asmus, R., … Bouma, T. J. (2017). Seasonal know. Molecular Ecology, 25(8), 1631–­1638. https://doi.org/10.1111/
and latitudinal variation in seagrass mechanical traits across Europe: mec.13617
The influence of local nutrient status and morphometric plasticity. Vermaat, J. E., Verhagen, F. C. A., & Lindenburg, D. (2000). Contrasting
Limnology and Oceanography, 63(1), 37–­46. https://doi.org/10.1002/ responses in two populations of Zostera noltii Hornem. to experimen-
lno.10611 tal photoperiod manipulation at two salinities. Aquatic Botany, 67(3),
Soissons, L. M., Haanstra, E. P., van Katwijk, M. M., Asmus, R., Auby, I., 179–­189. https://doi.org/10.1016/S0304​-­3770(00)00090​-­5
Barillé, L., Brun, F. G., Cardoso, P. G., Desroy, N., Fournier, J., Ganthy, Vialet-­Chabrand, S., Matthews, J. S. A., Simkin, A. J., Raines, C. A., &
F., Garmendia, J.-­M., Godet, L., Grilo, T. F., Kadel, P., Ondiviela, B., Lawson, T. (2017). Importance of fluctuations in light on plant pho-
Peralta, G, Puente, A., Recio, M., … Bouma, T. J. (2018). Latitudinal tosynthetic acclimation. Plant Physiology, 173(4), 2163–­2179. https://
Patterns in European Seagrass Carbon Reserves: Influence of doi.org/10.1104/pp.16.01767
Seasonal Fluctuations versus Short-­Term Stress and Disturbance Viana, I. G., Moreira-­Saporiti, A., & Teichberg, M. (2020). Species-­specific
Events. Frontiers in Plant Science, 9, 88. https://doi.org/10.3389/ trait responses of three tropical seagrasses to multiple stressors: The
fpls.2018.00088 case of increasing temperature and nutrient enrichment. Frontiers in
Sultan, S. E. (2003). Phenotypic plasticity in plants: A case study in eco- Plant Science, 11, 571363. https://doi.org/10.3389/fpls.2020.571363
logical development. Evolution & Development, 5(1), 25–­33. https:// Watson-­Lazowski, A., Lin, Y., Miglietta, F., Edwards, R. J., Chapman, M. A., &
doi.org/10.1046/j.1525-­142x.2003.03005.x Taylor, G. (2016). Plant adaptation or acclimation to rising CO2? Insight
Summers, D. M., Bryan, B. A., Crossman, N. D., & Meyer, W. from first multigenerational RNA-­Seq transcriptome. Global Change
S. (2012). Species vulnerability to climate change: Impacts Biology, 22(11), 3760–­3773. https://doi.org/10.1111/gcb.13322
on spatial conservation priorities and species representa- Waycott, M., Duarte, C. M., Carruthers, T. J. B., Orth, R. J., Dennison, W.
tion. Global Change Biology, 18(7), 2335–­2348. https://doi. C., Olyarnik, S., Calladine, A., Fourqurean, J. W., Heck, K. L., Hughes,
org/10.1111/j.1365-­2486.2012.02700.x A. R., Kendrick, G. A., Kenworthy, W. J., Short, F. T., & Williams, S. L.
Svensson, E. I., Goedert, D., Gómez-­Llano, M. A., Spagopoulou, F., Nava-­ (2009). Accelerating loss of seagrasses across the globe threatens
Bolaños, A., & Booksmythe, I. (2019). Sex differences in local adap- coastal ecosystems. Proceedings of the National Academy of Sciences,
tation: What can we learn from reciprocal transplant experiments? 106(30), 12377–­12381. https://doi.org/10.1073/pnas.09056​20106
Philosophical Transactions of the Royal Society B: Biological Sciences, Weatherall, E. J., Jackson, E. L., Hendry, R. A., & Campbell, M. L. (2016).
373(1757), 20170420. https://doi.org/10.1098/rstb.2017.0420 Quantifying the dispersal potential of seagrass vegetative fragments: A
Thrush, S. F., Hewitt, J. E., Dayton, P. K., Coco, G., Lohrer, A. M., Norkko, comparison of multiple subtropical species. Estuarine, Coastal and Shelf
A., Norkko, J., & Chiantore, M. (2009). Forecasting the limits of resil- Science, 169, 207–­215. https://doi.org/10.1016/j.ecss.2015.11.026
ience: Integrating empirical research with theory. Proceedings of the Wesselmann, M., Anton, A., Duarte, C. M., Hendriks, I. E., Agustí, S.,
Royal Society B: Biological Sciences, 276(1671), 3209–­3217. https:// Savva, I., & Marbà, N. (2020). Tropical seagrass Halophila stipulacea
doi.org/10.1098/rspb.2009.0661 shifts thermal tolerance during Mediterranean invasion. Proceedings
Tomasello, A., Di Maida, G., Calvo, S., Pirrotta, M., Borra, M., & of the Royal Society B, 287(1922), 20193001. https://doi.org/10.1098/
Procaccini, G. (2009). Seagrass meadows at the extreme of en- rspb.2019.3001
vironmental tolerance: The case of Posidonia oceanica in a semi-­ West-­Eberhard, M. J. (1989). Phenotypic plasticity and the origins of
enclosed coastal lagoon. Marine Ecology, 30(3), 288–­3 00. https://doi. diversity. Annual Review of Ecology and Systematics, 20(1), 249–­278.
org/10.1111/j.1439-­0 485.2009.00285.x https://doi.org/10.1146/annur​ev.es.20.110189.001341
Traboni, C., Mammola, S. D., Ruocco, M., Ontoria, Y., Ruiz, J. M., Whitham, T. G., & Slobodchikoff, C. N. (1981). Evolution by individuals,
Procaccini, G., & Marín-­Guirao, L. (2018). Investigating cellular stress plant-­herbivore interactions, and mosaics of genetic variability: The
response to heat stress in the seagrass Posidonia oceanica in a global adaptive significance of somatic mutations in plants. Oecologia, 49(3),
change scenario. Marine Environmental Research, 141, 12–­23. https:// 287–­292. https://doi.org/10.1007/BF003​47587
doi.org/10.1016/j.maren​vres.2018.07.007 Williams, S. L. (2001). Reduced genetic diversity in eelgrass transplanta-
Tutar, O., Marín-­Guirao, L., Ruiz, J. M., & Procaccini, G. (2017). tions affects both population growth and individual fitness. Ecological
Antioxidant response to heat stress in seagrasses. A gene expres- Applications, 11(5), 1472. https://doi.org/10.2307/3060933
sion study. Marine Environmental Research, 132, 94–­102. https://doi. Williams, S. L., & Davis, C. A. (1996). Population genetic analyses of
org/10.1016/j.maren​vres.2017.10.011 transplanted eelgrass (Zostera marina) beds reveal reduced genetic
Tuya, F., Fernández-­Torquemada, Y., Zarcero, J., del Pilar-­Ruso, Y., diversity in southern California. Restoration Ecology, 4(2), 163–­180.
Csenteri, I., Espino, F., Manent, P., Curbelo, L., Antich, A., de la Ossa, https://doi.org/10.1111/j.1526-­100X.1996.tb001​17.x
J. A., Royo, L., Castejón, I., Procaccini, G., Terrados, J., & Tomas, F. Winters, G., Beer, S., Willette, D. A., Viana, I. G., Chiquillo, K. L., Beca-­
(2019). Biogeographical scenarios modulate seagrass resistance to Carretero, P., Villamayor, B., Azcárate-­García, T., Shem-­Tov, R.,
small-­scale perturbations. Journal of Ecology, 107(3), 1263–­1275. Mwabvu, B., Migliore, L., Rotini, A., Oscar, M. A., Belmaker, J.,
https://doi.org/10.1111/1365-­2745.13114 Gamliel, I., Alexandre, A., Engelen, A. H., Procaccini, G., & Rilov, G.
Valladares, F., Matesanz, S., Guilhaumon, F., Araújo, M. B., Balaguer, L., (2020). The tropical seagrass Halophila stipulacea: Reviewing what
Benito-­Garzón, M., Cornwell, W., Gianoli, E., Kleunen, M., Naya, D. we know from its native and invasive habitats, alongside identify-
E., Nicotra, A. B., Poorter, H., & Zavala, M. A. (2014). The effects ing knowledge gaps. Frontiers in Marine Science, 7, 300. https://doi.
of phenotypic plasticity and local adaptation on forecasts of species org/10.3389/fmars.2020.00300
range shifts under climate change. Ecology Letters, 17(11), 1351–­ Winters, G., Nelle, P., Fricke, B., Rauch, G., & Reusch, T. B. H. (2011).
1364. https://doi.org/10.1111/ele.12348 Effects of a simulated heat wave on photophysiology and gene ex-
van Katwijk, M. M., Bos, A. R., de Jonge, V. N., Hanssen, L. S. A. M., pression of high-­ and low-­latitude populations of Zostera marina.
Hermus, D. C. R., & de Jong, D. J. (2009). Guidelines for seagrass Marine Ecology Progress Series, 435, 83–­95. https://doi.org/10.3354/
restoration: Importance of habitat selection and donor population, meps0​9213
PAZZAGLIA et al. | 1201

Woltereck, R., & Woltereck, R. (1909). Weitere experimentelle nutrient loading. Marine Pollution Bulletin, 83(2), 508–­515. https://
Untersuchungen über Artveränderung, speziell über das Wesen doi.org/10.1016/j.marpo​lbul.2013.12.056
quantitativer Artunterschiede bei Daphniden. Verhandlungen der Zhang, Y. Y., Fischer, M., Colot, V., & Bossdorf, O. (2013). Epigenetic
Deutschen Zoologischen Gesellschaft, 19, 110–­173. variation creates potential for evolution of plant phenotypic plas-
Yang, X., Zhang, P., Li, W., Hu, C., Zhang, X., & He, P. (2018). Evaluation of ticity. New Phytologist, 197(1), 314–­322. https://doi.org/10.1111/
four seagrass species as early warning indicators for nitrogen over- nph.12010
loading: Implications for eutrophic evaluation and ecosystem man- Zimmerman, R. C. (2017). Systems biology and the seagrass paradox:
agement. Science of the Total Environment, 635, 1132–­1143. https:// Adaptation, acclimation, and survival of marine angiosperms in a
doi.org/10.1016/j.scito​tenv.2018.04.227 changing ocean climate. In M. Kumar & P. Ralph (Eds.), Systems bi-
York, P. H., Gruber, R. K., Hill, R., Ralph, P. J., Booth, D. J., & Macreadie, P. ology of marine ecosystems (pp. 1–­351). Springer, Cham. https://doi.
I. (2013). Physiological and morphological responses of the temper- org/10.1007/978-­3-­319-­62094​-­7_8
ate seagrass Zostera muelleri to multiple stressors: Investigating the
interactive effects of light and temperature. PLoS One, 8(10), e76377.
S U P P O R T I N G I N FO R M AT I O N
https://doi.org/10.1371/journ​al.pone.0076377
Yu, L., Boström, C., Franzenburg, S., Bayer, T., Dagan, T., & Reusch, T. Additional supporting information may be found online in the
B. H. (2020). Somatic genetic drift and multi-­level selection in mod- Supporting Information section.
ular species. Nature Ecology & Evolution, 4(952), 962. https://doi.
org/10.1101/833335
Zaneveld, J. R., Burkepile, D. E., Shantz, A. A., Pritchard, C. E., McMinds,
How to cite this article: Pazzaglia J, Reusch TBH, Terlizzi A,
R., Payet, J. P., Welsh, R., Correa, A. M. S., Lemoine, N. P., Rosales, S.,
Fuchs, C., Maynard, J. A., & Thurber, R. V. (2016). Overfishing and nu-
Marín-Guirao L, Procaccini G. Phenotypic plasticity under
trient pollution interact with temperature to disrupt coral reefs down rapid global changes: The intrinsic force for future seagrasses
to microbial scales. Nature Communications, 7(1), 1–­12. https://doi. survival. Evol Appl. 2021;14:1181–­1201. https://doi.
org/10.1038/ncomm​s11833 org/10.1111/eva.13212
Zhang, J., Huang, X., & Jiang, Z. (2014). Physiological responses of the
seagrass Thalassia hemprichii (Ehrenb.) Aschers as indicators of