Opinion
Revisiting Adaptive Potential, Population Size, and Conservation

https://doi.org/10.1016/j.tree.2017.03.012Get rights and content

Trends

The importance of small population size in limiting adaptive potential is reinforced.

Estimates of genetic variance across populations tend to be imprecise.

Genomic data highlight linkage, load, and rare alleles in population size issues.

Long-term conservation maintaining adaptive potential requires large populations.

Additive genetic variance (VA) reflects the potential for evolutionary shifts and can be low for some traits or populations. High VA is critical for the conservation of threatened species under selection to facilitate adaptation. Theory predicts tight associations between population size and VA, but data from some experimental models, and managed and natural populations do not always support this prediction. However, VA comparisons often have low statistical power, are undertaken in highly controlled environments distinct from natural habitats, and focus on traits with limited ecological relevance. Moreover, investigations of VA typically fail to consider rare alleles, genetic load, or linkage disequilibrium, resulting in deleterious effects associated with favored alleles in small populations. Large population size remains essential for ensuring adaptation.

Section snippets

Population Size and Genetic Variation

Species and populations of conservation concern are threatened because of their inability to adapt to changes in environmental conditions as a consequence of natural processes or human activities, including habitat loss, urbanization, and invasive competing species and diseases. With ongoing climate change and expanding human populations generating stressful conditions for many species, threat levels are expected to increase and result in more populations and species being listed as threatened 1

Controlled Short-Term Studies Connect Population Size and Inbreeding to Selection Responses but Not necessarily VA

Larger populations are expected to respond relatively more rapidly per generation to selection because they contain more alleles favored by selection, carry a reduced risk of losing favored alleles as a consequence of genetic drift, and generate relatively more novel mutations. These expectations have been confirmed experimentally in Drosophila, Musca, Mus, and other model animals [8]. For example, using Drosophila melanogaster, Jones et al. [9] showed that populations of larger size responded

Theoretical Predictions of Loss of Quantitative Genetic Variation in Small Field Populations Are Not Well Supported

While natural populations of small size often have reduced levels of molecular genetic variation [26], there are numerous exceptions to this; and studies on fragmented and wild populations that are periodically small often reveal unexpectedly high levels of molecular genetic variation 27, 28. Furthermore, levels of quantitative genetic variation in wild populations as measured by VA and h2 are often not lower in small compared with larger populations [6] (Box 1). This may reflect the fact that

Comparing Quantitative Genetic Variation across Populations Is Challenging, Particularly for Low Heritability Traits

Heritability and evolvability estimates are prone to a high level of measurement error and, thus, low repeatability; this may be because some traits are inherently noisy and subject to the impact of minor environmental variability [39]. However, even where traits have high repeatabilities (e.g., many morphological and physiological traits) or are measured across entire life stages (e.g., many life-history traits), VA and h2 estimates still often have large standard errors (SEs) irrespective of

Environmental Effects Further Confound Population Comparisons of Heritable Variation

Effects of environmental conditions on heritability and evolvability can often be dramatic and lead to low estimates under some conditions. For instance, terrestrial isopods (Porcellio laevis) exposed to different diets and tested for size showed heritabilities of 0.61 ± 0.39 under high-protein conditions but this dropped to 0.08 ± 0.36 under high-carbohydrate conditions [46]. Similarly, in a recent study of two natural populations of D. melanogaster performed under seminatural conditions, h2 for

Adaptive Responses Not Captured by VA: Mutational Meltdown

Although much of the focus in conservation genetics remains on levels of genetic variation in populations, other factors linked to mutation and linkage disequilibrium (LD) influence the impact of population size on evolutionary adaptive capacity (Figure 1).

Perhaps the most well known of these relates to mutational meltdown 49, 50, 51, 52, where accumulating mutations interact with environmental effects to cause greater stochasticity in population size and further exacerbate the deleterious

Adaptive Responses Not Captured by VA: Deleterious Mutations and Linkage Disequilibrium

In addition to causing mutational meltdown, deleterious mutations coupled with LD can affect the adaptive capacity of small populations unrelated to VA. Selection responses in both natural and experimental populations can reach a plateau after several generations, even when substantial VA persists [57]. Under experimental evolution, where populations are maintained under different conditions, the expected directional response in a trait does not occur 58, 59 and, in natural populations, there

Adaptive Responses Not Captured by VA: Allelic Combinations and Low-Frequency Alleles

Heritability and VA estimates are dominated by the effects of alleles at intermediate frequencies, yet genomic analyses of selection responses in populations of model organisms highlight the complexity of genetic changes in adaptive responses 69, 70, 71. When Drosophila populations are exposed to new thermal conditions, the selection response involves not only some alleles that start at intermediate frequencies, but also many alleles that start at a low frequency and then sweep through

Concluding Remarks and Where to Next?

Wood et al. [6] highlighted that, while small population size is reflected in reduced molecular variation, it remains challenging to detect effects at the quantitative genetic level. We have outlined likely reasons for this, including a lack of power, particularly when it comes to low-heritability traits. Experimental studies emphasize that population size influences responses to directional selection and extinction probabilities. While rapid short-term decreases in population size might not

Acknowledgments

We thank Mads F. Schou, Kristian Trøjelsgaard, and Andrew R. Weeks for discussions on the topic and for providing comments on previous versions of this work.

Glossary

Additive genetic variance (VA)
variance due to additive allelic effects in a population.
Antagonistic interactions
indicates that the fitness effect of two factors (e.g., environments) is less than the sum of the effect of the individual factors.
Associate overdominance
a mechanism that can arise by an overdominant locus being linked to neutral loci or by the presence of multiple recessive deleterious alleles across different haplotypes resulting in a large cumulative advantage of a heterozygote

References (98)

  • J.A. Robinson

    Genomic flatlining in the endangered island fox

    Curr. Biol.

    (2016)
  • A.B. Shafer

    Genomics and the challenging translation into conservation practice

    Trends Ecol. Evol.

    (2015)
  • A.M. Bell

    The repeatability of behaviour: a meta-analysis

    Anim. Behav.

    (2009)
  • B.R. Scheffers

    The broad footprint of climate change from genes to biomes to people

    Science

    (2016)
  • M.C. Urban

    Accelerating extinction risk from climate change

    Science

    (2015)
  • D.T. Blumstein

    Heritability of anti-predatory traits: vigilance and locomotor performance in marmots

    J. Evol. Biol.

    (2010)
  • D.S. Falconer et al.

    Introduction to Quantitative Genetics

    (1996)
  • Y. Willi

    Limits to the adaptive potential of small populations

    Annu. Rev. Ecol. Evol. Syst.

    (2006)
  • J.L. Wood

    Are heritability and selection related to population size in nature? Meta-analysis and conservation implications

    Evol. Appl.

    (2016)
  • J.L.A. Wood

    Are heritability and selection related to population size in nature? Meta-analysis and conservation implications

    Evol. Appl.

    (2016)
  • J.P. Hanrahan

    Effects of small population size and selection intensity on short-term response to selection for postweaning gain in mice

    Genetics

    (1973)
  • L.P. Jones

    Correlation between bristle systems in Drosophila melanogaster

    Aust. J. Biol. Sci.

    (1969)
  • K.E. Weber

    Increased selection response in larger populations. 1. Selection for wing-tip height in Drosophila-melanogaster at 3 population sizes

    Genetics

    (1990)
  • K.E. Weber et al.

    Increased selection response in larger populations. 2. Selection for ethanol vapor resistance in Drosophila melanogaster at 2 population sizes

    Genetics

    (1990)
  • Y. Willi et al.

    Demographic factors and genetic variation influence population persistence under environmental change

    J. Evol. Biol.

    (2009)
  • C.J. Holmes

    Initial genetic diversity enhances population establishment and alters genetic structuring of a newly established Daphnia metapopulation

    Mol. Ecol.

    (2016)
  • J.A. Markert

    Population genetic diversity and fitness in multiple environments

    BMC Evol. Biol.

    (2010)
  • A. Dierks

    Response to selection on cold tolerance is constrained by inbreeding

    Evolution

    (2012)
  • T.N. Kristensen

    A test of quantitative genetic theory using Drosophila – effects of inbreeding and rate of inbreeding on heritabilities and variance components

    J. Evol. Biol.

    (2005)
  • I.J. Saccheri

    Effects of bottlenecks on quantitative genetic variation in the butterfly Bicyclus anynana

    Genet. Res.

    (2001)
  • I.M. Lerner

    Genetic Homeostasis

    (1954)
  • M.C. Whitlock et al.

    The changes in genetic and environmental variance with inbreeding in Drosophila melanogaster

    Genetics

    (1999)
  • H.R. Taft et al.

    Do bottlenecks increase additive genetic variance?

    Conserv. Genet.

    (2012)
  • P. Nietlisbach

    Genetic variance components and heritability of multiallelic heterozygosity under inbreeding

    Heredity

    (2016)
  • M. Turelli et al.

    Will population bottlenecks and multilocus epistasis increase additive genetic variance?

    Evolution

    (2006)
  • C. Lopez-Fanjul

    The role of epistasis in the increase in the additive genetic variance after population bottlenecks

    Genet. Res.

    (1999)
  • J.L. Wang

    Bottleneck effect on genetic variance: a theoretical investigation of the role of dominance

    Genetics

    (1998)
  • B. van Heerwaarden

    Population bottlenecks increase additive genetic variance but do not break a selection limit in rain forest Drosophila

    Genetics

    (2008)
  • R. Frankham

    Introduction to Conservation Genetics

    (2010)
  • C. Turchetto

    High levels of genetic diversity and population structure in an endemic and rare species: implications for conservation

    AoB Plants

    (2016)
  • J.M. Pemberton

    Inbreeding depression by environment interactions in a free-living mammal population

    Heredity

    (2017)
  • C. Berenos

    Estimating quantitative genetic parameters in wild populations: a comparison of pedigree and genomic approaches

    Mol. Ecol.

    (2014)
  • C. Drury

    Genomic variation among populations of threatened coral: Acropora cervicornis

    BMC Genom.

    (2016)
  • H.A. Lawrence

    High mitochondrial and nuclear genetic diversity in one of the world’s most endangered seabirds, the Chatham Island Taiko (Pterodroma magentae)

    Conserv. Genet.

    (2008)
  • J.P. Torres-Florez

    High genetic diversity in a small population: the case of Chilean blue whales

    Ecol. Evol.

    (2014)
  • P. Pamilo et al.

    Associate overdominance, heterozygosity and fitness

    Heredity

    (1998)
  • J.L. Williams

    Inbreeding and purging at the genomic Level: the Chillingham cattle reveal extensive, non-random SNP heterozygosity

    Anim. Genet.

    (2016)
  • C.E. Grueber

    The imprecision of heterozygosity-fitness correlations hinders the detection of inbreeding and inbreeding depression in a threatened species

    Mol. Ecol.

    (2011)
  • J. Huisman

    Inbreeding depression across the lifespan in a wild mammal population

    Proc. Natl. Acad. Sci. U. S. A.

    (2016)
  • M.B. Morrissey

    Bayesian approaches to the quantitative analysis of natural populations

  • T.F. Hansen

    Heritability is not evolvability

    Evol. Biol.

    (2011)
  • A.A. Hoffmann

    Heritability and evolvability of fitness and non-fitness traits: lessons from livestock

    Evolution

    (2016)
  • S.M. Carlson et al.

    A review of quantitative genetic components of fitness in salmonids: implications for adaptation to future change

    Evol. Appl.

    (2008)
  • A.A. Hoffmann

    Low potential for climatic stress adaptation in a rainforest Drosophila species

    Science

    (2003)
  • B. van Heerwaarden et al.

    Is adaptation to climate change really constrained in niche specialists?

    Proc. R. Soc. B Biol. Sci.

    (2014)
  • M.J. Carter

    Heritability of progeny size in a terrestrial isopod: transgenerational environmental effects on a life history trait

    Heredity

    (2004)
  • T.N. Kristensen

    Low evolutionary potential for egg-to-adult viability in Drosophila melanogaster at high temperatures

    Evolution

    (2015)
  • A.J. Wilson

    Environmental coupling of selection and heritability limits evolution

    PLoS Biol.

    (2006)
  • W. Gabriel et al.

    Extinction risk by mutational meltdown - synergistic effects between population regulation and genetic drift

    • Cited by (163)

    • A global synthesis of the patterns of genetic diversity in endangered and invasive plants

      2024, Biological Conservation

    • Landscape determinants of genetic structure for Schizopygopsis younghusbandi in the Yarlung Tsangpo River drainage, Tibetan Plateau

      2023, Ecological Indicators

    • Divergent gametic thermal performance and floral warming across an elevation gradient

      2024, Evolution

    • Population genomics of flat-tailed horned lizards (Phrynosoma mcallii) informs conservation and management across a fragmented Colorado Desert landscape

      2024, Molecular Ecology

    • Population genetics for insect conservation and control

      2024, Conservation Science and Practice

    • Topographic barriers drive the pronounced genetic subdivision of a range-limited fossorial rodent

      2024, Molecular Ecology
    View all citing articles on Scopus
    View full text
    © 2017 Elsevier Ltd. All rights reserved.