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

Wood, Jacquelyn L. A.; Yates, Matthew C.; Fraser, Dylan J.

doi:10.1111/eva.12375

Cited by 95 publications

(111 citation statements)

References 83 publications

(184 reference statements)

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“…Our results thus support the view that, even in small populations, the random loss of variation does not affect all sites in the same way, and we further contribute to the general debate about the relative role of drift and selection when the effective population size is very small (9)(10)(11)58).…”

Section: Adaptation and Maladaptationsupporting

confidence: 85%

“…This conservation paradigm, strictly related to the extinction vortex metaphor (5), is supported by empirical evidence (6)(7)(8), but it is challenged by studies showing that selection can be powerful also at small population sizes (9,10) and that survival and even demographic expansion can occur with almost no genomic variation (11). Interestingly, if extinction does not occur, drift in small isolated groups can produce, or contribute to, genetic and phenotypic divergence, possibly leading to speciation (12,13).…”

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confidence: 99%

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Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

Benazzo

Trucchi

Cahill

et al. 2017

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

159

132

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Survival and divergence in a small group: the extraordinary genomic history of the endangered Apennine brown bear stragglers 2 AbstractAbout 100 km east of Rome, in the Central Apennine mountains, a critically endangered population of approximately fifty brown bears live in complete isolation. Mating outside this population is prevented by several hundred kilometers of bear-free territories. We exploited this natural experiment to better understand the gene and genomic consequences of surviving at extremely small population size. First, we found that brown bear populations in Europe lost connectivity since Neolithic times, when farming communities expanded and forest burning was used for land clearance. In Central Italy, this resulted in a 40-fold population decline. The overall genomic impact of this decline included the complete loss of variation in the mitochondrial genome and along long stretches of the nuclear genome. Several private and deleterious amino acid changes were fixed by random drift; predicted effects include energy deficit, muscle weakness, anomalies in cranial and skeletal development, and reduced aggressiveness. Despite this extreme loss of diversity, Apennine bear genomes show non-random peaks of high variation, possibly maintained by balancing selection, at genomic regions significantly enriched for genes associated with immune and olfactory systems. Challenging the paradigm of increased extinction risk in small populations, we suggest that random fixation of deleterious alleles a) can be an important driver of divergence in isolation, b) can be tolerated when balancing selection prevents random loss of variation at important genes and c) is followed by or results directly in favorable behavioral changes. SignificanceA small and relict population of brown bears lives in complete isolation in the Italian Apennine mountains, providing a unique opportunity to study the impact of drift and selection on the genomes of a large endangered mammal and to reconstruct the phenotypic consequences and the conservation implications of such evolutionary processes. The Apennine bear is highly inbred and harbors very low genomic variation. Several deleterious mutations have been accumulated by drift. We found evidence that this is a consequence of habitat fragmentation in the Neolithic, when human expansion and land clearance shrank its habitat, and that retention of variation at immune system and olfactory receptor genes, as well as changes in diet and behavior, prevented the extinction of the Apennine bear.

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Section: Adaptation and Maladaptationsupporting

confidence: 85%

mentioning

confidence: 99%

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

Benazzo

Trucchi

Cahill

et al. 2017

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

159

132

View full text Add to dashboard Cite

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“…; Wood et al. ). In addition, we did a bibliographic search using Google Scholar, looking for articles including the keywords “heritability,” “quantitative genetic parameters,” “ F ST ‐ Q ST comparison,” “natural population,” and “plant.” We limited our search to data from natural populations, and we removed any heritability estimates that were obtained by averaging over results from multiple populations; each heritability estimate we used is from data from a single population.…”

Section: Methodsmentioning

confidence: 97%

How does selfing affect the genetic variance of quantitative traits? An updated meta‐analysis on empirical results in angiosperm species

2019

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Most theoretical works predict that selfing should reduce the level of additive genetic variance available for quantitative traits within natural populations. Despite a growing number of quantitative genetic studies undertaken during the last two decades, this prediction is still not well supported empirically. To resolve this issue and confirm or reject theoretical predictions, we reviewed quantitative trait heritability estimates from natural plant populations with different rates of self‐fertilization and carried out a meta‐analysis. In accordance with models of polygenic traits under stabilizing selection, we found that the fraction of additive genetic variance is negatively correlated with the selfing rate. Although the mating system explains a moderate fraction of the variance, the mean reduction of narrow‐sense heritability values between strictly allogamous and predominantly selfing populations is strong, around 60%. Because some nonadditive components of genetic variance become selectable under inbreeding, we determine whether self‐fertilization affects the relative contribution of these components to genetic variance by comparing narrow‐sense heritability estimates from outcrossing populations with broad‐sense heritability estimated in autogamous populations. Results suggest that these nonadditive components of variance may restore some genetic variance in predominantly selfing populations; it remains, however, uncertain how these nonadditive components will contribute to adaptation.

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“…Admittedly, the number of empirical studies supporting the view that wild populations of very small effective sizes can retain adaptive potential is too small to draw generalities about the ubiquity of this phenomenon. Indeed, Wood et al () admitted that their meta‐analysis had some important limitations, partly imposed by the current lack of data for very small and isolated populations. Consequently, until more empirical population genomics studies from different biogeographic contexts ( e .…”

Section: Adaptive Potential In Small Populations: Is There a Role Formentioning

confidence: 99%

On the maintenance of genetic variation and adaptation to environmental change: considerations from population genomics in fishes

Bernatchez

2016

Journal of Fish Biology

208

216

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The first goal of this paper was to overview modern approaches to local adaptation, with a focus on the use of population genomics data to detect signals of natural selection in fishes. Several mechanisms are discussed that may enhance the maintenance of genetic variation and evolutionary potential, which have been overlooked and should be considered in future theoretical development and predictive models: the prevalence of soft sweeps, polygenic basis of adaptation, balancing selection and transient polymorphisms, parallel evolution, as well as epigenetic variation. Research on fish population genomics has provided ample evidence for local adaptation at the genome level. Pervasive adaptive evolution, however, seems to almost never involve the fixation of beneficial alleles. Instead, adaptation apparently proceeds most commonly by soft sweeps entailing shifts in frequencies of alleles being shared between differentially adapted populations. One obvious factor contributing to the maintenance of standing genetic variation in the face of selective pressures is that adaptive phenotypic traits are most often highly polygenic, and consequently the response to selection should derive mostly from allelic co-variances among causative loci rather than pronounced allele frequency changes. Balancing selection in its various forms may also play an important role in maintaining adaptive genetic variation and the evolutionary potential of species to cope with environmental change. A large body of literature on fishes also shows that repeated evolution of adaptive phenotypes is a ubiquitous evolutionary phenomenon that seems to occur most often via different genetic solutions, further adding to the potential options of species to cope with a changing environment. Moreover, a paradox is emerging from recent fish studies whereby populations of highly reduced effective population sizes and impoverished genetic diversity can apparently retain their adaptive potential in some circumstances. Although more empirical support is needed, several recent studies suggest that epigenetic variation could account for this apparent paradox. Therefore, epigenetic variation should be fully integrated with considerations pertaining to role of soft sweeps, polygenic and balancing selection, as well as repeated adaptation involving different genetic basis towards improving models predicting the evolutionary potential of species to cope with a changing world.

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

Cited by 95 publications

References 83 publications

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

How does selfing affect the genetic variance of quantitative traits? An updated meta‐analysis on empirical results in angiosperm species

On the maintenance of genetic variation and adaptation to environmental change: considerations from population genomics in fishes

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