Conservation Genetics (2022) 23:865–870

https://doi.org/10.1007/s10592-022-01459-1

PERSPECTIVE

Evaluation of proposed genetic goals and targets for the Convention

on Biological Diversity
Richard Frankham1

Received: 22 April 2022 / Accepted: 2 June 2022 / Published online: 28 June 2022
© The Author(s) 2022

Abstract
In the current negotiations regarding revision of the Convention on Biological Diversity (CBD) proposals have been made
to strengthen the genetic goals, indicators, and targets for wild species in natural habitats by specifying “tolerable” losses
of genetic diversity. However, they have not been subjected to evaluations of their continued use over 100 years, a common
conservation time frame. I evaluated six scenarios (3, 5 or 10% loss of genetic diversity [heterozygosity] over 8 or 32 years)
proposed as targets for revision of genetic indicators in CBD by predicting their consequences on genetic diversity, inbreed-
ing, fitness, and evolutionary potential when applied at the same rate for 100 years. All proposals lead to substantial genetic
harm to species when continued for 100 years that will compromise species persistence, especially in the context of environ-
mental change. Consequently, none of the proposals are suitable for inclusion in the CBD. However, alternative indicators
are proposed that would reflect improvements in the genetic status of populations and species, namely (1) the number of
species and their populations being maintained at sizes sufficient to retain evolutionary potential in perpetuity, and (2) the
number of species for which population genetic connectivity has been improved.

Keywords Connectivity · Convention on Biological Diversity · Evolutionary potential · Fitness · Genetic diversity ·
Inbreeding depression

Introduction strengthen the genetic content of the convention to include

wild animals, plants, and fungi (Hoban et al. 2020; Laikre
The Convention on Biological Diversity (CBD) is the first et al. 2020) and to set goals, indicators, and targets for 2030
global agreement to cover all aspects of biodiversity. It was and 2050, but there has been little agreement about them.
drafted in Rio de Janeiro, Brazil in 1992 and became effec- Consequently, an IUCN taskforce was set up in December
tive on 29th December 1993. This multilateral treaty has 2021 to evaluate the various proposals and to report back
three main goals: the conservation of biodiversity, the sus- to the wider committee and I joined it as a representative
tainable use of its components, and the equitable sharing of the Conservation Planning Specialist Group of IUCN.
of benefits arising from genetic resources. Here, I am con- This material was first prepared as a position paper for that
cerned with its role in biodiversity conservation, especially taskforce. As of May 2022 the genetic content of the revised
wild species of animals, plants, and fungi in natural habitats. CBD is still being negotiated.
While the original CBD mentioned genetics, its main
focus was on conserving genetic diversity for domestic Evaluation of proposed CBD targets for retaining
plants and animals, with wild animals and plants being genetic diversity
neglected. A new post-2020 Global Biodiversity Framework,
is being developed to guide action through 2030, albeit with The targets for retaining genetic diversity (GD) proposed
delays due to the covid pandemic. There is a strong push to for insertion into the revised CBD appear to have originated
from the goal for captive populations, namely, to retain
* Richard Frankham 90% of genetic diversity (heterozygosity) for 100 years
richard.frankham@mq.edu.au (Frankham et al. 2002): this target was devised as a compro-
mise to allow more species to be captive bred while accept-
1
School of Natural Sciences, Macquarie University, Sydney, ing some genetic deterioration in the captive populations.
NSW 2109, Australia

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It is a compromise on a compromise as it was originally Consequence of loss of genetic diversity scenarios

devised as retaining 90% of genetic diversity for 200 years on inbreeding
(Soulé et al. 1986). This is not an appropriate target for spe-
cies in the wild, especially in the context of their need to In random mating populations, the loss of GD in outbreed-
adapt to global climate change. ing species approximates the inbreeding coefficient (Wright
The targets of retaining 90, 95 and 97% of genetic diver- 1969). Most scenarios have reached worrying high levels of
sity in the CBD discussion material mostly did not specify inbreeding by year 100 (Table 1). The accumulated mean
the duration in years or generations being considered, but inbreeding at year 100, is substantially greater than that for
from the contexts they appeared to be 2022–2030 (8 years) the progeny of a full-sib mating in scenarios 3 and 4, near
or 2022–2050 (28 years). However, the impacts of threats the inbreeding in the progeny of selfing in scenario 2, and
to species are more typically evaluated over longer periods, near that for the progeny of 2 generations of selfing in sce-
such as the 100 years used in the IUCN Red List Categori- nario 1.
zation system criterion E for Vulnerable (IUCN 2012) and However, it is the consequences on total fitness of these
genetic diversity targets for captive populations of threatened levels of inbreeding that most concern us.
species (Frankham et al. 2010).
I undertook quantitative evaluations of these six scenar- Consequences of loss of genetic diversity scenarios
ios in terms of the loss of genetic diversity over 100 years on total fitness (inbreeding depression)
based on these rates of loss being continued for this duration
(Table 1). Other genetic impacts associated with this were The magnitudes of inbreeding depression (ID) were pre-
also evaluated as described below. The evaluations assume dicted using the method of Ralls et al. (1988), namely:
that we are dealing with random mating diploid species, as
are most such evaluations. ID = 1 − e−FB (3)
The means for deriving these extrapolations for genetic
where F is the inbreeding coefficient and B the number of
diversity are shown for scenario 1, the retention of 90% of
haploid lethal equivalents (Morton et al. 1956). This method
genetic diversity for 8 years, as follows:
has been widely used elsewhere, as for example in Frankham
As 100 years represent 12.5 time-frames of 8 years,
et al. (2014), Frankham et al. (2017)). The F values used
the proportion of genetic diversity retained for 100 years
come from column 5. The B value for total fitness (lifetime
(GD100) is:
reproductive output) of 7.5 lethal equivalents for vertebrates
GD100 = 0.912.5 = 0.268 (1) is the median based on the available estimates for verte-
brates, while the corresponding B values for outbreeding
and plants is 3.50 (Frankham et al. 2017, p. 54 and p. 61).
While there are biases in these estimates of inbreeding
Loss of GD = 1 − 0.268 = 0.732 (2)
depression, some are downward and some upwards, so
All of the scenarios represent worrying losses of genetic they approximately cancel out. These estimates are biased
diversity over 100 years (Table 1). However, we need to pre- upwards when inbreeding increases slowly across genera-
dict the consequences of these losses on total reproductive tions in random mating populations (as here) as natural
fitness and ability to evolve in response to environmental selection has the opportunity to purge harmful recessive
change to appreciate the true impacts on species of follow- alleles (Day et al. 2003; Reed et al. 2003). However, purg-
ing such scenarios. ing has little effect in small random mating populations

Table 1  Quantitative Scenario Loss GD (%) Duration Loss GD in F at year ID vertebrates ID plants
evaluations of the effects of (years) 100 years (%) 100 (%) (B = 7.5a) (%) (B = 3.5a)
different proposed scenarios for (%)
loss of genetic diversity from
2022 to 2030 or 2050 on genetic 1 10 8 73 73 99.6 92
diversity (GD, inbreeding (F),
2 5 8 47 47 97 81
and inbreeding depression (ID)
after 100 years 3 3 8 32 32 91 67
4 10 28 31 31 90 67
5 5 28 17 17 72 44
6 3 28 10 10 54 30
a
Frankham et al. (2017, p. 54)

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representative of many threatened animal populations to restore genetic diversity is not an option in conservation
(Glémin 2003). Conversely, the B values are underestimates contexts.
as about half of them do not include the effects on offspring What other options do we have for goals for genetic fac-
fitness of having an inbred versus non-inbred mothers tors in the CBD? Two credible options come to mind:
(Frankham et al. 2017).
For those who recall hearing of only 3.14 diploid lethal • Retaining evolutionary potential in perpetuity
equivalents for juvenile survival in captive vertebrates (Ralls • Improving population genetic connectivity among frag-
et al. 1988), the cumulative impacts of inbreeding across mented populations
reproduction and survival for the whole life cycle are vastly
greater than for any single fitness component, and are typi-
cally greater in wild than captive habitats (Crnokrak and Goal 1: retaining evolutionary potential
Roff 1999; O’Grady et al. 2006; Frankham 2015; Frankham in perpetuity
et al. 2017).
There are expected to be devastating reductions in total Franklin (1980) proposed that an effective size (Ne) of 500
fitness due to inbreeding depression for all six scenarios was required to preserve evolutionary potential in perpetu-
in vertebrates and plants (Table 1 columns 6 and 7) that ity, based on the equilibrium between neutral mutation and
will reduce population sizes and increase extinction risks. genetic drift for quantitative characters peripheral to fitness.
Even for the least harmful scenario 6, the fitness reductions Lande and Barrowclough (1987) reached a similar conclu-
are very large: the 10% inbreeding coefficient is expected to sion, based on a model of mutation, drift, and stabilizing
result in a 54% loss of total fitness in naturally outbreeding selection.
vertebrate populations and 30% loss in outbreeding plants. Consequently, Hoban et al. (2020) and Laikre et al.
In addition to inbreeding depression, these small pop- (2020) proposed “the number of populations (or breeds)
ulations are expected to have reduced ability to evolve in with an effective size > 500 compared to the number < 500”
response to environmental change, a crucial issue in the as a genetic indicator for CBD. They also specified a proxy
context of global climate change (Frankham et al. 2017). for Ne in the absence of genetic data as an adult census size
(Nc) of 5,000, based on an average Ne/Nc = 0.1 (Frankham
Consequences of loss of genetic diversity scenarios 1995; Palstra and Ruzzante 2008; see also Frankham 2021).
on ability to evolve Frankham et al. (2014) re-evaluated the Ne target, based
on the accumulated evidence since 1980. They concluded
In the short term, the major effects of the above scenarios on that the objective should be to maintain genetic variation for
evolutionary potential are due to reduction in heterozygosity, total reproductive fitness in perpetuity and that the required
plus inbreeding depression reducing offspring numbers per Ne is at least 1000, based on empirical and theoretical work.
female and progeny survival to breeding age, leading to a This is a credible indicator, but using effective population
decline in the selection differential (Frankham et al. 2017, size in a CBD indicator is problematical as:
pp. 73–80). The reductions in genetic variation for neutral
genetic markers and for fitness should be similar (Kardos • Ne is far too complex for non-geneticists, as the literature
et al. 2021, Fig. 1). Consequently, the above scenarios will is extraordinarily complex and confusing, such that even
result in proportionate losses of ability to evolve that are specialist evolutionary geneticists make mistakes (e.g.
greater than the proportionate losses of genetic diversity Frankham 1995; Hoban et al. 2020; see Frankham 2021).
(Frankham et al. 2017). For example, there are many different variables called
But can we just wait for genetic diversity to be regener- Ne and they differ in magnitude (Frankham 1995; Wang
ated by mutation? et al. 2016; Ryman et al. 2019).
• In practice, this indicator will revert to Nc in the vast
Recovery of genetic diversity from mutation is far majority of cases as appropriate estimates of Ne (mul-
too slow to be an option tigenerational ones) are available for few species
(Frankham 2021), while Nc estimates are available for
Mutation rates are very low so times for mutation to restore many species (e.g. IUCN 2022). Further, very few appro-
genetic diversity are very long. Lande and Barrowclough priate genetic estimates of Ne are now being undertaken
(1987) estimated them to be hundreds of thousands to mil- due to the need for samples separated by several genera-
lions of generations for single locus genetic diversity and tions.
100 to 1000 of generations for quantitative genetic varia-
tion. Empirical evidence accords with the latter prediction These issues can be largely overcome by using the median
(Amador et al. 2010). Consequently, waiting for mutation estimate of Ne/Nc of ~ 0.1 (Frankham 1995, 2021) to convert

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the indicator from an Ne of 1,000 to a census size of 10,000, clearing often creates habitat fragments in an inhospitable
following the approach of Hoban et al. (2020) and Laikre matrix, resulting in reduced rates of gene flow (Frankham
et al. (2020). However, Laikre et al (2021) argued for the et al. 2017). Further, habitat clearing typically reduces the
retention of Ne with a default Nc of ten times this value when carrying capacity for populations, such that they may not
Ne is not available. In part, this was based on the existence of be able to support increased population size unless habitat
variation in Ne/Nc ratios among species. By contrast, Hoban restoration is undertaken.
et al. (2021) concluded that “In the absence of such informa-
tion (on species specific Ne), the rule of thumb of Ne/Nc = 0.1 Removing barriers to gene flow
is an empirically justified, conservative threshold for many
if not most organisms.” I remain unconvinced of the desir- Humans have in many cases inserted barriers to gene flow,
ability of specifying Ne, as much of the influential audience such as dams/weirs, fences, and roads. Removing these can
for implementation of the CBD consists of non-geneticists, re-establish gene flow (Frankham et al. 2017). For example,
especially bureaucrats and politicians from counties around many dams and weirs have been removed from rivers, pre-
the world, and for whom Ne will represent unwarranted and sumably restoring gene flow.
unwelcome complexity. I suggest we follow the lead of econ-
omists who use simple, easily measured indicators such as Building habitat corridors
gross domestic product, unemployment rate, etc., and who
have achieved substantial political influence. Adding strips of suitable habitat between isolated popula-
tions is another means to restore gene flow (Frankham et al.
2017). This depends on the corridors being used by the tar-
Goal 2: improving population genetic get species.
connectivity
Building wildlife underpasses and overpasses
Most species have fragmented distributions, many with
small isolated populations that have low genetic diversity, In a similar manner building wildlife overpasses or under-
are inbred, and have reduced fitness and ability to evolve passes can improve gene flow where it is inadequate
(Frankham et al. 2017; Frankham et al. 2019). An esti- (Frankham et al. 2017).
mated ~ 1.4 million isolated populations of threatened spe-
cies are suffering genetic erosion, and for non-threatened Genetic rescue attempts
plus threatened species the number climbs to ~ 150 million
isolated populations with genetic problems (Frankham et al. If the four actions above are not feasible, as may frequently
2017). be the case, the remaining option is human assisted move-
Genetic management of fragmented populations has ment of individuals or gametes to re-establish gene flow. In
been described as one of the most important, largely unad- the past, genetic rescue attempts were impeded by concerns
dressed issues in all of conservation biology (Frankham that gene flow would lead to harmful effects (outbreeding
2010a, 2010b). A major component of this management is depression) (Edmands 2007). However, the causes of out-
to increase gene flow in cases where it has ceased or become breeding depression are known and means to predict its risks
inadequate so that genetic problems associated with small have been devised and validated (Frankham et al. 2011;
isolated populations are prevented or reversed (Frankham Frankham 2015).
et al. 2017). Gene flow can be increased by: Genetic rescue attempts have resulted in large and con-
sistently beneficial effects that persist over generations in
• Increasing population sizes where populations are suf- outbreeding species (Frankham 2015, 2016; Frankham et al.
ficiently close for this to increase gene flow 2019). Outcrossing of inbred populations resulted in ben-
• Removing barriers to gene flow eficial effects in 92.9% of 156 cases screened as having a
• Building habit corridors low risk of outbreeding depression. The median increase in
• Building wildlife underpasses and overpasses composite fitness (combined fecundity and survival) follow-
• Moving individuals or gametes between populations ing outcrossing was 148% in wild/stressful environments and
(genetic rescue attempts) 45% in captive/benign ones. Consequently, genetic rescues
are a highly effective genetic management tool.
Increasing population size

Increasing population size is expected to increase gene

flow if the rate of migration is unchanged. However, land

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Proposed indicators of improved population exchange, and active monitoring and management of genetic
genetic connectivity for the CBD diversity, as well as no loss of populations.

People discussing non-genetic aspects of the CBD often Acknowledgements I thank Craig Moritz for inviting me to contribute
to a meeting on genetic revisions to the CBD, Caroline Lees and Onnie
specify options to alleviate their threats and reverse declines Byers for inviting me to contribute to the IUCN taskforce on genetic
(Maron et al. 2021). This is not currently a part of the pro- targets and goals for the revised CBD as a representative of CPSG, to
posal to strengthen the indicators for genetic connectivity in other members of that task force for feedback on the position paper,
the CBD but is equally needed there. It also addresses the and to Sean Hoban for suggesting that I convert it into a Perspective for
Conservation Genetics. I am grateful to Sean Hoban, Joachim Mergeay,
issue of offering hope and good news stories. and two anonymous reviewers for their helpful comments.
Each of the five items above are potential CBD indicators
of improvements in genetic connectivity. However, for each Author contributions I conceived the ideas, prepared the Table based
to be credible it needs to be established by genetic moni- on my computations, and wrote the paper.
toring that the genetic connectivity was initially inadequate
and that the action resulted in improved genetic connectivity Funding Open Access funding enabled and organized by CAUL and
its Member Institutions. The author declares that no funds, grants, or
(Allendorf et al. 2022). other support were received during the preparation of this manuscript.
I recommend that the cumulative total of cases of credible
improvements in genetic connectivity from these five items Data availability I conceived the ideas, prepared the Table based on
be included as a genetic connectivity indicator in the CBD. my computations, and wrote the paper. All associated data are included
They are easily understood and measured. Baseline lists of in the paper.
number of prior global genetic rescue attempts already exist
in Frankham et al. (2011, Table S1), and Frankham et al. Declarations
(2017, Table 1.1), and a further update is projected to appear
Conflict of interest The author has no relevant financial or non-finan-
in a forthcoming textbook. The cumulative global numbers cial interest to disclose.
of genetic rescues rose from 19 to 29 between 2011 and
2017 and were approximately 34 by 2021 (Frankham et al. Open Access This article is licensed under a Creative Commons Attri-
unpublished). I am confident that there will be an increase bution 4.0 International License, which permits use, sharing, adapta-
in the number of these indicators that will lead to good news tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
stories in 2030 and 2050. provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article's Creative Commons licence, unless indicated
Conclusion otherwise in a credit line to the material. If material is not included in
the article's Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
All six percentage-based genetic diversity target scenar- need to obtain permission directly from the copyright holder. To view a
ios result in harmful losses of genetic diversity, increased copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/.
inbreeding, major losses of fitness, and reduced ability to
evolve. Consequently, none of these scenarios should be
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