Landscape genetics, which explicitly quantifies landscape effects on gene flow and adaptation, ha... more Landscape genetics, which explicitly quantifies landscape effects on gene flow and adaptation, has largely focused on macroorganisms, with little attention given to microorganisms. This is despite overwhelming evidence that microorganisms exhibit spatial genetic structuring in relation to environmental variables. The increasing accessibility of genomic data has opened up the opportunity for landscape genetics to embrace the world of microorganisms, which may be thought of as 'the invisible regulators' of the macroecological world. Recent developments in bioinformatics and increased data accessibility have accelerated our ability to identify microbial taxa and characterize their genetic diversity. However, the influence of the landscape matrix and dynamic environmental factors on microorganism genetic dispersal and adaptation has been little explored. Also, because many microorganisms co-inhabit or co-disperse with macroorganisms, landscape genomic approaches may improve insights into how micro- and macroorganisms reciprocally interact to create spatial genetic structure. Conducting landscape genetic analyses on microorganisms requires that we accommodate shifts in spatial and temporal scales, presenting new conceptual and methodological challenges not yet explored in 'macro' landscape genetics. We argue that there is much value to be gained for microbial ecologists from embracing landscape genetic approaches. We provide a case for integrating landscape genetic methods into micro-ecological studies, and discuss specific considerations associated with the novel challenges this brings. We anticipate that microorganism landscape genetic studies will provide new insights into both micro- and macroecological processes and expand our knowledge of species' distributions, adaptive mechanisms and species' interactions in changing environments. This article is protected by copyright. All rights reserved.
Many ectothermic species are currently expanding their distributions polewards due to anthropogen... more Many ectothermic species are currently expanding their distributions polewards due to anthropogenic global warming. Molecular genetic mechanisms facilitating range expansion under these conditions are largely unknown, but understanding these could help mitigate expanding pests and disease vectors, or help explain why some species fail to track changing climates. Here, using RNA-seq data, we examine genome-wide changes in gene expression under heat and cold stress in the range-expanding damselfly Ischnura elegans in northern Europe. We find that both the number of genes involved and levels of gene expression under heat stress have become attenuated during the expansion, consistent with a previously-reported release from selection on heat tolerances as species move polewards. Genes upregulated under cold stress differed between core and edge populations, corroborating previously-reported rapid adaptation to cooler climates at the expansion front. Expression of sixty-nine genes exhibit...
Landscape genetics lacks explicit methods for dealing with the uncertainty in landscape resistanc... more Landscape genetics lacks explicit methods for dealing with the uncertainty in landscape resistance estimation, which is particularly problematic when sample sizes of individuals are small. Unless uncertainty can be quantified, valuable but small datasets may be rendered unusable for conservation purposes. We offer a method to quantify uncertainty in landscape resistance estimates using multi-model inference as an improvement over single-model based inference. We illustrate the approach empirically using co-occurring, woodland-preferring Australian marsupials within a common study area: two arboreal gliders (Petaurus breviceps, and Petaurus norfolcensis) and one ground-dwelling Antechinus (Antechinus flavipes). First, we use maximum-likelihood and a bootstrap procedure to identify the best-supported isolation by resistance (IBR) model out of 56 models defined by linear and non-linear resistance functions. We then quantify uncertainty in resistance estimates by examining parameter sel...
The conservation behavior framework is useful to identify key linkages between behavior and conse... more The conservation behavior framework is useful to identify key linkages between behavior and conservation practice.
We apply this framework to a novel host-parasite system on the Galapagos Islands and ask if there have been changes in parasite
oviposition behavior and host mortality patterns across the first decade (2004-2013) of its known association. The Dipteran parasite
Philornis downsi was first discovered in Darwin’s finch nests in 1997 and is the biggest threat to the survival of Galapagos
land birds. Host mortality has increased over the past decade. In Dipterans, pupation and pupae size are determined by access to
host resources. Here, we test the hypothesis that P. downsi flies are laying eggs in finch nests earlier in the nestling phase to
maximize larval feeding time and therefore chance of pupation success before host death. The results show fewer 1st instar larvae
later in the host nesting cycle in support of earlier egg laying behavior by female flies. Between 2004 and 2013, parasite intensity
increased from ~28 to ~48 parasites per nest, host mortality increased from ~50% to ~90%, and host age at death decreased from
~11 to ~5 days. The earlier age at host death was correlated with fewer pupae (from ~50% to ~20%) and smaller pupae size (~10%
decrease). Changes in parasite behavior reveal new fitness costs to both the parasite and Darwin’s finches. These findings underscore
the need for urgent conservation action to save Darwin’s finches from extinction due to a novel, lethal and introduced
parasite
Species hybridization can lead to fitness costs, species
collapse, and novel evolutionary trajec... more Species hybridization can lead to fitness costs, species
collapse, and novel evolutionary trajectories in changing environments. Hybridization is predicted to be more common when environmental conditions change rapidly. Here, we test patterns of hybridization in three sympatric tree finch species (small tree finch
Camarhynchus parvulus, medium tree finch Camarhynchus pauper,
and large tree finch: Camarhynchus psittacula) that are currently recognized on Floreana Island, Gala´pagos Archipelago. Genetic analysis of microsatellite data from contemporary samples showed two genetic populations and one hybrid cluster in both 2005 and 2010; hybrid individuals were derived from genetic population 1 (small
morph) and genetic population 2 (large morph). Females of the large
and rare species were more likely to pair with males of the small
common species. Finch populations differed in morphology in 1852–
1906 compared with 2005/2010. An unsupervised clustering method
showed (a) support for three morphological clusters in the historical
tree finch sample (1852–1906), which is consistent with current species recognition; (b) support for two or three morphological clusters in 2005 with some (19%) hybridization; and (c) support for just two morphological clusters in 2010 with frequent (41%) hybridization. We discuss these findings in relation to species demarcations of Camarhynchus tree finches on Floreana Island.
"Landscape genetics offers a powerful approach to understanding species’ dispersal patterns. Howe... more "Landscape genetics offers a powerful approach to understanding species’ dispersal patterns. However, a central obstacle is to account for ecological processes operating at multiple spatial scales, while keeping research outcomes applicable to conservation management. We address this challenge by applying a novel multilevel regression approach to model landscape drivers of genetic structure at both the resolution of individuals and at a spatial resolution relevant to management (i.e. local government management areas: LGAs) for the koala (Phascolartos cinereus) in Australia. Our approach allows for the simultaneous incorporation of drivers of landscape-genetic relationships operating at multiple spatial resolutions. Using microsatellite data for 1106 koalas, we show that, at the individual resolution, foliage projective cover (FPC) facilitates high gene flow (i.e. low resistance) until it falls below approximately 30%. Out of six additional land-cover variables, only highways and freeways further explained genetic
distance after accounting for the effect of FPC. At the LGA resolution, there was significant variation in isolation-by-resistance (IBR) relationships in terms of their slopes and intercepts. This was predominantly explained by the average resistance distance among LGAs, with a weaker effect of historical forest cover. Rates of recent landscape change did not further explain variation in IBR relationships among LGAs. By using a novel multilevel model, we disentangle the effect of landscape resistance on gene flow at the fine resolution (i.e. among individuals) from effects occurring at coarser resolutions (i.e. among LGAs). This has important implications for our ability to identify appropriate scale-dependent management actions."
Evolutionary processes can complicate conservation efforts for species with uncertain taxonomic c... more Evolutionary processes can complicate conservation efforts for species with uncertain taxonomic classifications and discrete geographic populations. Discordant morphological and genetic patterns across the geographic range of species further calls for the identification of evolutionary significant units for conservation. Using island and mainland populations of a small Australian passerine (the superb fairy-wren, Malurus cyaneus), we examine the relationship between morphological and genetic divergence among two subspecies, M. c. ashbyi (Kangaroo Island, South Australia) and M. c. leggei (South Australia, mainland), using eight microsatellite markers. Island birds showed clear evidence for morphological divergence, with a larger body size and thinner bill compared to mainland birds. Two genetic clusters were found using Bayesian methods, comprising mainland and island regions. Estimates of recent migration rates between all sites were very low (<2%). Morphological and genetic differentiation between island and mainland sites correlated significantly, but not when controlling for isolation by distance. Genetic and morphological substructure was evident with three distinct genetic clusters in each region. Males, the highly sedentary sex, appeared to drive correlations between morphological and genetic differentiation. Our study provides evidence that the subspecies classification of M. cyaneus in island and mainland regions encapsulates two independently diverging populations that can be recognised in conservation planning.► Molecular and phenotypic data are rarely combined to verify subspecies classification. ► Island and mainland birds show genetic and morphological divergence across subspecies. ► Both subspecies show evolutionary divergence without phylogenetic independence. ► Subspecies classification and independent conservation management is warranted.
An enrichment technique was used to isolate 11 di-, tri-, and tetra microsatellites for the paras... more An enrichment technique was used to isolate 11 di-, tri-, and tetra microsatellites for the parasitic fly Philornis downsi (Diptera: Muscidae). These loci were polymerase chain reaction amplified in singleplexes or two-plexes for P. downsi. The loci showed low to moderate polymorphism, exhibited between three and four alleles, and observed heterozygosity ranged from 0.05 to 0.86. These new markers will be useful for population-level and paternity analyses and will provide valuable information about the ecology of this high-impact parasite of vulnerable bird species.
Landscape genetics, which explicitly quantifies landscape effects on gene flow and adaptation, ha... more Landscape genetics, which explicitly quantifies landscape effects on gene flow and adaptation, has largely focused on macroorganisms, with little attention given to microorganisms. This is despite overwhelming evidence that microorganisms exhibit spatial genetic structuring in relation to environmental variables. The increasing accessibility of genomic data has opened up the opportunity for landscape genetics to embrace the world of microorganisms, which may be thought of as &#39;the invisible regulators&#39; of the macroecological world. Recent developments in bioinformatics and increased data accessibility have accelerated our ability to identify microbial taxa and characterize their genetic diversity. However, the influence of the landscape matrix and dynamic environmental factors on microorganism genetic dispersal and adaptation has been little explored. Also, because many microorganisms co-inhabit or co-disperse with macroorganisms, landscape genomic approaches may improve insights into how micro- and macroorganisms reciprocally interact to create spatial genetic structure. Conducting landscape genetic analyses on microorganisms requires that we accommodate shifts in spatial and temporal scales, presenting new conceptual and methodological challenges not yet explored in &#39;macro&#39; landscape genetics. We argue that there is much value to be gained for microbial ecologists from embracing landscape genetic approaches. We provide a case for integrating landscape genetic methods into micro-ecological studies, and discuss specific considerations associated with the novel challenges this brings. We anticipate that microorganism landscape genetic studies will provide new insights into both micro- and macroecological processes and expand our knowledge of species&#39; distributions, adaptive mechanisms and species&#39; interactions in changing environments. This article is protected by copyright. All rights reserved.
Many ectothermic species are currently expanding their distributions polewards due to anthropogen... more Many ectothermic species are currently expanding their distributions polewards due to anthropogenic global warming. Molecular genetic mechanisms facilitating range expansion under these conditions are largely unknown, but understanding these could help mitigate expanding pests and disease vectors, or help explain why some species fail to track changing climates. Here, using RNA-seq data, we examine genome-wide changes in gene expression under heat and cold stress in the range-expanding damselfly Ischnura elegans in northern Europe. We find that both the number of genes involved and levels of gene expression under heat stress have become attenuated during the expansion, consistent with a previously-reported release from selection on heat tolerances as species move polewards. Genes upregulated under cold stress differed between core and edge populations, corroborating previously-reported rapid adaptation to cooler climates at the expansion front. Expression of sixty-nine genes exhibit...
Landscape genetics lacks explicit methods for dealing with the uncertainty in landscape resistanc... more Landscape genetics lacks explicit methods for dealing with the uncertainty in landscape resistance estimation, which is particularly problematic when sample sizes of individuals are small. Unless uncertainty can be quantified, valuable but small datasets may be rendered unusable for conservation purposes. We offer a method to quantify uncertainty in landscape resistance estimates using multi-model inference as an improvement over single-model based inference. We illustrate the approach empirically using co-occurring, woodland-preferring Australian marsupials within a common study area: two arboreal gliders (Petaurus breviceps, and Petaurus norfolcensis) and one ground-dwelling Antechinus (Antechinus flavipes). First, we use maximum-likelihood and a bootstrap procedure to identify the best-supported isolation by resistance (IBR) model out of 56 models defined by linear and non-linear resistance functions. We then quantify uncertainty in resistance estimates by examining parameter sel...
The conservation behavior framework is useful to identify key linkages between behavior and conse... more The conservation behavior framework is useful to identify key linkages between behavior and conservation practice.
We apply this framework to a novel host-parasite system on the Galapagos Islands and ask if there have been changes in parasite
oviposition behavior and host mortality patterns across the first decade (2004-2013) of its known association. The Dipteran parasite
Philornis downsi was first discovered in Darwin’s finch nests in 1997 and is the biggest threat to the survival of Galapagos
land birds. Host mortality has increased over the past decade. In Dipterans, pupation and pupae size are determined by access to
host resources. Here, we test the hypothesis that P. downsi flies are laying eggs in finch nests earlier in the nestling phase to
maximize larval feeding time and therefore chance of pupation success before host death. The results show fewer 1st instar larvae
later in the host nesting cycle in support of earlier egg laying behavior by female flies. Between 2004 and 2013, parasite intensity
increased from ~28 to ~48 parasites per nest, host mortality increased from ~50% to ~90%, and host age at death decreased from
~11 to ~5 days. The earlier age at host death was correlated with fewer pupae (from ~50% to ~20%) and smaller pupae size (~10%
decrease). Changes in parasite behavior reveal new fitness costs to both the parasite and Darwin’s finches. These findings underscore
the need for urgent conservation action to save Darwin’s finches from extinction due to a novel, lethal and introduced
parasite
Species hybridization can lead to fitness costs, species
collapse, and novel evolutionary trajec... more Species hybridization can lead to fitness costs, species
collapse, and novel evolutionary trajectories in changing environments. Hybridization is predicted to be more common when environmental conditions change rapidly. Here, we test patterns of hybridization in three sympatric tree finch species (small tree finch
Camarhynchus parvulus, medium tree finch Camarhynchus pauper,
and large tree finch: Camarhynchus psittacula) that are currently recognized on Floreana Island, Gala´pagos Archipelago. Genetic analysis of microsatellite data from contemporary samples showed two genetic populations and one hybrid cluster in both 2005 and 2010; hybrid individuals were derived from genetic population 1 (small
morph) and genetic population 2 (large morph). Females of the large
and rare species were more likely to pair with males of the small
common species. Finch populations differed in morphology in 1852–
1906 compared with 2005/2010. An unsupervised clustering method
showed (a) support for three morphological clusters in the historical
tree finch sample (1852–1906), which is consistent with current species recognition; (b) support for two or three morphological clusters in 2005 with some (19%) hybridization; and (c) support for just two morphological clusters in 2010 with frequent (41%) hybridization. We discuss these findings in relation to species demarcations of Camarhynchus tree finches on Floreana Island.
"Landscape genetics offers a powerful approach to understanding species’ dispersal patterns. Howe... more "Landscape genetics offers a powerful approach to understanding species’ dispersal patterns. However, a central obstacle is to account for ecological processes operating at multiple spatial scales, while keeping research outcomes applicable to conservation management. We address this challenge by applying a novel multilevel regression approach to model landscape drivers of genetic structure at both the resolution of individuals and at a spatial resolution relevant to management (i.e. local government management areas: LGAs) for the koala (Phascolartos cinereus) in Australia. Our approach allows for the simultaneous incorporation of drivers of landscape-genetic relationships operating at multiple spatial resolutions. Using microsatellite data for 1106 koalas, we show that, at the individual resolution, foliage projective cover (FPC) facilitates high gene flow (i.e. low resistance) until it falls below approximately 30%. Out of six additional land-cover variables, only highways and freeways further explained genetic
distance after accounting for the effect of FPC. At the LGA resolution, there was significant variation in isolation-by-resistance (IBR) relationships in terms of their slopes and intercepts. This was predominantly explained by the average resistance distance among LGAs, with a weaker effect of historical forest cover. Rates of recent landscape change did not further explain variation in IBR relationships among LGAs. By using a novel multilevel model, we disentangle the effect of landscape resistance on gene flow at the fine resolution (i.e. among individuals) from effects occurring at coarser resolutions (i.e. among LGAs). This has important implications for our ability to identify appropriate scale-dependent management actions."
Evolutionary processes can complicate conservation efforts for species with uncertain taxonomic c... more Evolutionary processes can complicate conservation efforts for species with uncertain taxonomic classifications and discrete geographic populations. Discordant morphological and genetic patterns across the geographic range of species further calls for the identification of evolutionary significant units for conservation. Using island and mainland populations of a small Australian passerine (the superb fairy-wren, Malurus cyaneus), we examine the relationship between morphological and genetic divergence among two subspecies, M. c. ashbyi (Kangaroo Island, South Australia) and M. c. leggei (South Australia, mainland), using eight microsatellite markers. Island birds showed clear evidence for morphological divergence, with a larger body size and thinner bill compared to mainland birds. Two genetic clusters were found using Bayesian methods, comprising mainland and island regions. Estimates of recent migration rates between all sites were very low (<2%). Morphological and genetic differentiation between island and mainland sites correlated significantly, but not when controlling for isolation by distance. Genetic and morphological substructure was evident with three distinct genetic clusters in each region. Males, the highly sedentary sex, appeared to drive correlations between morphological and genetic differentiation. Our study provides evidence that the subspecies classification of M. cyaneus in island and mainland regions encapsulates two independently diverging populations that can be recognised in conservation planning.► Molecular and phenotypic data are rarely combined to verify subspecies classification. ► Island and mainland birds show genetic and morphological divergence across subspecies. ► Both subspecies show evolutionary divergence without phylogenetic independence. ► Subspecies classification and independent conservation management is warranted.
An enrichment technique was used to isolate 11 di-, tri-, and tetra microsatellites for the paras... more An enrichment technique was used to isolate 11 di-, tri-, and tetra microsatellites for the parasitic fly Philornis downsi (Diptera: Muscidae). These loci were polymerase chain reaction amplified in singleplexes or two-plexes for P. downsi. The loci showed low to moderate polymorphism, exhibited between three and four alleles, and observed heterozygosity ranged from 0.05 to 0.86. These new markers will be useful for population-level and paternity analyses and will provide valuable information about the ecology of this high-impact parasite of vulnerable bird species.
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We apply this framework to a novel host-parasite system on the Galapagos Islands and ask if there have been changes in parasite
oviposition behavior and host mortality patterns across the first decade (2004-2013) of its known association. The Dipteran parasite
Philornis downsi was first discovered in Darwin’s finch nests in 1997 and is the biggest threat to the survival of Galapagos
land birds. Host mortality has increased over the past decade. In Dipterans, pupation and pupae size are determined by access to
host resources. Here, we test the hypothesis that P. downsi flies are laying eggs in finch nests earlier in the nestling phase to
maximize larval feeding time and therefore chance of pupation success before host death. The results show fewer 1st instar larvae
later in the host nesting cycle in support of earlier egg laying behavior by female flies. Between 2004 and 2013, parasite intensity
increased from ~28 to ~48 parasites per nest, host mortality increased from ~50% to ~90%, and host age at death decreased from
~11 to ~5 days. The earlier age at host death was correlated with fewer pupae (from ~50% to ~20%) and smaller pupae size (~10%
decrease). Changes in parasite behavior reveal new fitness costs to both the parasite and Darwin’s finches. These findings underscore
the need for urgent conservation action to save Darwin’s finches from extinction due to a novel, lethal and introduced
parasite
collapse, and novel evolutionary trajectories in changing environments. Hybridization is predicted to be more common when environmental conditions change rapidly. Here, we test patterns of hybridization in three sympatric tree finch species (small tree finch
Camarhynchus parvulus, medium tree finch Camarhynchus pauper,
and large tree finch: Camarhynchus psittacula) that are currently recognized on Floreana Island, Gala´pagos Archipelago. Genetic analysis of microsatellite data from contemporary samples showed two genetic populations and one hybrid cluster in both 2005 and 2010; hybrid individuals were derived from genetic population 1 (small
morph) and genetic population 2 (large morph). Females of the large
and rare species were more likely to pair with males of the small
common species. Finch populations differed in morphology in 1852–
1906 compared with 2005/2010. An unsupervised clustering method
showed (a) support for three morphological clusters in the historical
tree finch sample (1852–1906), which is consistent with current species recognition; (b) support for two or three morphological clusters in 2005 with some (19%) hybridization; and (c) support for just two morphological clusters in 2010 with frequent (41%) hybridization. We discuss these findings in relation to species demarcations of Camarhynchus tree finches on Floreana Island.
distance after accounting for the effect of FPC. At the LGA resolution, there was significant variation in isolation-by-resistance (IBR) relationships in terms of their slopes and intercepts. This was predominantly explained by the average resistance distance among LGAs, with a weaker effect of historical forest cover. Rates of recent landscape change did not further explain variation in IBR relationships among LGAs. By using a novel multilevel model, we disentangle the effect of landscape resistance on gene flow at the fine resolution (i.e. among individuals) from effects occurring at coarser resolutions (i.e. among LGAs). This has important implications for our ability to identify appropriate scale-dependent management actions."
We apply this framework to a novel host-parasite system on the Galapagos Islands and ask if there have been changes in parasite
oviposition behavior and host mortality patterns across the first decade (2004-2013) of its known association. The Dipteran parasite
Philornis downsi was first discovered in Darwin’s finch nests in 1997 and is the biggest threat to the survival of Galapagos
land birds. Host mortality has increased over the past decade. In Dipterans, pupation and pupae size are determined by access to
host resources. Here, we test the hypothesis that P. downsi flies are laying eggs in finch nests earlier in the nestling phase to
maximize larval feeding time and therefore chance of pupation success before host death. The results show fewer 1st instar larvae
later in the host nesting cycle in support of earlier egg laying behavior by female flies. Between 2004 and 2013, parasite intensity
increased from ~28 to ~48 parasites per nest, host mortality increased from ~50% to ~90%, and host age at death decreased from
~11 to ~5 days. The earlier age at host death was correlated with fewer pupae (from ~50% to ~20%) and smaller pupae size (~10%
decrease). Changes in parasite behavior reveal new fitness costs to both the parasite and Darwin’s finches. These findings underscore
the need for urgent conservation action to save Darwin’s finches from extinction due to a novel, lethal and introduced
parasite
collapse, and novel evolutionary trajectories in changing environments. Hybridization is predicted to be more common when environmental conditions change rapidly. Here, we test patterns of hybridization in three sympatric tree finch species (small tree finch
Camarhynchus parvulus, medium tree finch Camarhynchus pauper,
and large tree finch: Camarhynchus psittacula) that are currently recognized on Floreana Island, Gala´pagos Archipelago. Genetic analysis of microsatellite data from contemporary samples showed two genetic populations and one hybrid cluster in both 2005 and 2010; hybrid individuals were derived from genetic population 1 (small
morph) and genetic population 2 (large morph). Females of the large
and rare species were more likely to pair with males of the small
common species. Finch populations differed in morphology in 1852–
1906 compared with 2005/2010. An unsupervised clustering method
showed (a) support for three morphological clusters in the historical
tree finch sample (1852–1906), which is consistent with current species recognition; (b) support for two or three morphological clusters in 2005 with some (19%) hybridization; and (c) support for just two morphological clusters in 2010 with frequent (41%) hybridization. We discuss these findings in relation to species demarcations of Camarhynchus tree finches on Floreana Island.
distance after accounting for the effect of FPC. At the LGA resolution, there was significant variation in isolation-by-resistance (IBR) relationships in terms of their slopes and intercepts. This was predominantly explained by the average resistance distance among LGAs, with a weaker effect of historical forest cover. Rates of recent landscape change did not further explain variation in IBR relationships among LGAs. By using a novel multilevel model, we disentangle the effect of landscape resistance on gene flow at the fine resolution (i.e. among individuals) from effects occurring at coarser resolutions (i.e. among LGAs). This has important implications for our ability to identify appropriate scale-dependent management actions."