scholarly journals Genetic Allee effects and their interaction with ecological Allee effects

2016 ◽  
Author(s):  
Meike J. Wittmann ◽  
Hanna Stuis ◽  
Dirk Metzler

SummaryIt is now widely accepted that genetic processes such as inbreeding depression and loss of genetic variation can increase the extinction risk of small populations. However, it is generally unclear whether extinction risk from genetic causes gradually increases with decreasing population size or whether there is a sharp transition around a specific threshold population size. In the ecological literature, such threshold phenomena are called “strong Allee effects” and they can arise for example from mate limitation in small populations.In this study, we aim to a) develop a meaningful notion of a “strong genetic Allee effect”, b) explore whether and under what conditions such an effect can arise from inbreeding depression due to recessive deleterious mutations, and c) quantify the interaction of potential genetic Allee effects with the well-known mate-finding Allee effect.We define a strong genetic Allee effect as a genetic process that causes a population’s survival probability to be a sigmoid function of its initial size. The inflection point of this function defines the critical population size. To characterize survival-probability curves, we develop and analyze simple stochastic models for the ecology and genetics of small populations.Our results indicate that inbreeding depression can indeed cause a strong genetic Allee effect, but only if individuals carry sufficiently many deleterious mutations (lethal equivalents) on average and if these mutations are spread across sufficiently many loci. Populations suffering from a genetic Allee effect often first grow, then decline as inbreeding depression sets in, and then potentially recover as deleterious mutations are purged. Critical population sizes of ecological and genetic Allee effects appear to be often additive, but even superadditive interactions are possible.Many published estimates for the number of lethal equivalents in birds and mammals fall in the parameter range where strong genetic Allee effects are expected. Unfortunately, extinction risk due to genetic Allee effects can easily be underestimated as populations with genetic problems often grow initially, but then crash later. Also interactions between ecological and genetic Allee effects can be strong and should not be neglected when assessing the viability of endangered or introduced populations.

2019 ◽  
Author(s):  
Christopher C. Kyriazis ◽  
Robert K. Wayne ◽  
Kirk E. Lohmueller

AbstractHuman-driven habitat fragmentation and loss have led to a proliferation of small and isolated plant and animal populations with high risk of extinction. One of the main threats to extinction in these populations is inbreeding depression, which is primarily caused by the exposure of recessive deleterious mutations as homozygous by inbreeding. The typical approach for managing these populations is to maintain high genetic diversity, often by translocating individuals from large populations to initiate a ‘genetic rescue.’ However, the limitations of this approach have recently been highlighted by the demise of the gray wolf population on Isle Royale, which was driven to the brink of extinction soon after the arrival of a migrant from the large mainland wolf population. Here, we use a novel population genetic simulation framework to investigate the role of genetic diversity, deleterious variation, and demographic history in mediating extinction risk due to inbreeding depression in small populations. We show that, under realistic models of dominance, large populations harbor high levels of recessive strongly deleterious variation due to these mutations being hidden from selection in the heterozygous state. As a result, when large populations contract, they experience a substantially elevated risk of extinction after these strongly deleterious mutations are exposed by inbreeding. Moreover, we demonstrate that although translocating individuals to small populations is broadly effective as a means to reduce extinction risk, using small or moderate-sized source populations rather than large source populations can greatly increase the effectiveness of genetic rescue due to greater purging in these smaller populations. Our findings challenge the traditional conservation paradigm that focuses on maximizing genetic diversity to reduce extinction risk in favor of a view that emphasizes minimizing strongly deleterious variation. These insights have important implications for managing small and isolated populations in the increasingly fragmented landscape of the Anthropocene.Impact SummaryNumerous threats to extinction exist for small populations, including the detrimental effects of inbreeding. Although much of the focus in reducing these harmful effects in small populations has been on maintaining high genetic diversity, here we use simulations to demonstrate that emphasis should instead be placed on minimizing strongly deleterious variation. More specifically, we show that historically-large populations with high levels of genetic diversity also harbor elevated levels of recessive strongly deleterious mutations hidden in the heterozygous state. Thus, when these populations contract, inbreeding can expose these strongly deleterious mutations as homozygous and lead to severe inbreeding depression and rapid extinction. Moreover, we demonstrate that, although translocating individuals to these small populations to perform a ‘genetic rescue’ is broadly beneficial, the effectiveness of this strategy can be greatly increased by targeting historically-smaller source populations where recessive strongly deleterious mutations have been purged. These results challenge long-standing views on how to best conserve small and isolated populations facing the threat of inbreeding depression, and have immediate implications for preserving biodiversity in the increasingly fragmented landscape of the Anthropocene.


2016 ◽  
Author(s):  
Gloria M. Lucque ◽  
Chloé Vayssade ◽  
Benoît Facon ◽  
Thomas Guillemaud ◽  
Franck Courchamp ◽  
...  

AbstractThe Allee effect is a theoretical model predicting low growth rates and the possible extinction of small populations. Historically, studies of the Allee effect have focused on demography. As a result, underlying processes other than the direct effect of population density on fitness components are not generally taken into account. There has been heated debate about the potential of genetic processes to drive small populations to extinction, but recent studies have shown that such processes clearly impact small populations over short time scales, and some may generate Allee effects. However, as opposed to the ecological Allee effect, which is underpinned by cooperative interactions between individuals, genetically driven Allee effects require a change in genetic structure to link the decline in population size with a decrease in fitness components. We therefore define the genetic Allee effect as a two-step process whereby a decrease in population size leads to a change in population genetic structure, and in turn, to a decrease in individual fitness. We describe potential underlying mechanisms, and review the evidence for this original type of component Allee effect, using published examples from both plants and animals. The possibility of considering demogenetic feedback in light of genetic Allee effects clarifies the analysis and interpretation of demographic and genetic processes, and the interplay between them, in small populations.


2005 ◽  
Vol 86 (1) ◽  
pp. 41-51 ◽  
Author(s):  
SYLVAIN GLÉMIN

The fate of lethal alleles in populations is of interest in evolutionary and conservation biology for several reasons. For instance, lethals may contribute substantially to inbreeding depression. The frequency of lethal alleles depends on population size, but it is not clear how it is affected by population structure. By analysing the case of the infinite island model by numerical approaches and analytical approximations it is shown that, like population size, population structure affects the fate of lethal alleles if dominance levels are low. Inbreeding depression caused by such alleles is also affected by the population structure, whereas the mutation load is only weakly affected. Heterosis also depends on population structure, but it always remains low, of the order of the mutation rate or less. These patterns are compared with those caused by mildly deleterious mutations to give a general picture of the effect of population structure on inbreeding depression, heterosis, and the mutation load.


2000 ◽  
Vol 75 (1) ◽  
pp. 75-81 ◽  
Author(s):  
THOMAS BATAILLON ◽  
MARK KIRKPATRICK

We studied the effects of population size on the inbreeding depression and genetic load caused by deleterious mutations at a single locus. Analysis shows how the inbreeding depression decreases as population size becomes smaller and/or the rate of inbreeding increases. This pattern contrasts with that for the load, which increases as population size becomes smaller but decreases as inbreeding rate goes up. The depression and load both approach asymptotic limits when the population size becomes very large or very small. Numerical results show that the transition between the small and the large population regimes is quite rapid, and occurs largely over a range of population sizes that vary by a factor of 10. The effects of drift on inbreeding depression may bias some estimates of the genomic rate of deleterious mutation. These effects could also be important in the evolution of breeding systems in hermaphroditic organisms and in the conservation of endangered populations.


2019 ◽  
Author(s):  
Paula E. Adams ◽  
Anna L. Crist ◽  
Ellen M. Young ◽  
John H. Willis ◽  
Patrick C. Phillips ◽  
...  

AbstractThe deleterious effects of inbreeding have been of extreme importance to evolutionary biology, but it has been difficult to characterize the complex interactions between genetic constraints and selection that lead to fitness loss and recovery after inbreeding. Viruses, bacteria, and the selfing nematode Caenorhabditis elegans have been shown to be capable of rapid recovery from the fixation of novel deleterious mutation, however the potential for fitness recovery from fixation of segregating variation under inbreeding in outcrossing organisms is poorly understood. C. remanei is an outcrossing relative of C. elegans with high polymorphic variation and extreme inbreeding depression. Here we sought to characterize changes C. remanei in patterns of genomic diversity after ∼30 generations of inbreeding via brother-sister mating followed by several hundred generations of recovery at large population size. As expected, inbreeding led to a large decline in reproductive fitness, but unlike results from mutation accumulation experiments, recovery from inbreeding at large populations sizes generated only very moderate recovery in fitness after 300 generations. At the genomic level, we found that while 66% of ancestral segregating SNPs were fixed in the inbred population, this was far fewer than expected under neutral processes. Under recovery, 36 SNPs across 30 genes involved in alimentary, muscular, nervous and reproductive systems changed reproducibly across all replicates, indicating that strong selection for fitness recovery does exist but is likely mutationally limited due to the large number of potential targets. Our results indicate that recovery from inbreeding depression via new compensatory mutations is likely to be constrained by the large number of segregating deleterious variants present in natural populations, limiting the capacity for rapid evolutionary rescue of small populations.Impact SummaryInbreeding is defined as mating between close relatives and can have a large effect on the genetic diversity and fitness of populations. This has been recognized for over 100 years of study in evolutionary biology, but the specific genomic changes that accompany inbreeding and the loss of fitness are still not known. Evolutionary theory predicts that inbred populations lose fitness through the fixation of many deleterious alleles and it is not known if populations can recover fitness after prolonged periods of inbreeding and deleterious fixations, or how long recovery may take. These questions are particularly important for wild populations experiencing declines. In this study we use laboratory populations of the nematode worm Caenorhabditis remanei to analyze the loss of fitness and genomic changes that accompany inbreeding via brother-sister mating, and to track the populations as they recover from inbreeding at large population size over 300 generations. We find that: Total progeny decreased by 65% after inbreedingThere were many nucleotides in the genome that remained heterozygous after inbreedingThere was an excess of inbreeding-resistant nucleotides on the X chromosomeThe number of progeny remained low after 300 generations of recovery from inbreeding30 genes changed significant in allele frequency during recovery, including genes involved in the alimentary, muscular, nervous and reproductive systemsTogether, our results demonstrate that recovery from inbreeding is difficult, likely due to the fixation of numerous deleterious alleles throughout the genome.


2017 ◽  
Vol 284 (1857) ◽  
pp. 20170878 ◽  
Author(s):  
Kyle H. Elliott ◽  
Gustavo S. Betini ◽  
D. Ryan Norris

Allee effects driven by predation can play a strong role in the decline of small populations but are conventionally thought to occur when generalist predators target specific prey (i.e. type II functional response). However, aside from direct consumption, fear of predators could also increase vigilance and reduce time spent foraging as population size decreases, as has been observed in wild mammals living in social groups. To investigate the role of fear on fitness in relation to population density in a species with limited sociality, we exposed varying densities of Drosophila melanogaster to mantid predators either during an experimental breeding season or non-breeding season. The presence of mantids in either season decreased the reproductive performance of individuals but only at low breeding densities, providing evidence for an Allee effect. We then used our experimental results to parametrize a mathematical model to examine the population consequences of fear at low densities. Fear tended to destabilize population dynamics and increase the risk of extinction up to sevenfold. Our study provides unique experimental evidence that the indirect effects of the presence of predators can cause an Allee effect and has important consequences for our understanding of the dynamics of small populations.


2011 ◽  
Vol 68 (1) ◽  
pp. 62-73 ◽  
Author(s):  
Amy M. Schueller ◽  
Daniel B. Hayes

Population viability analysis is a useful tool to explore the relationship between extinction risk and population size, but often does not include genetic factors. Our objectives were to determine minimum viable population size (MVP) for lake sturgeon ( Acipenser fulvescens ) and examine how inbreeding depression may affect MVP. Our individual-based model incorporated inbreeding depression in two ways: individuals with inbreeding coefficients above a threshold experienced inbreeding depression (threshold), and individuals experienced inbreeding depression at a rate related to their inbreeding coefficient (gradual). Three mechanisms relating inbreeding to fitness were explored (young-of-the-year (YOY) viability, post-YOY viability, number of progeny). The criterion we used to determine MVP was a 5% chance of extinction over 250 years. The estimated MVP without inbreeding effects was 80 individuals. For some scenarios incorporating inbreeding, MVP did not change, but for others, MVP was substantially higher, reaching values up to 1800. Results demonstrate that extinction risk and MVP can be influenced by both demographic stochasticity and inbreeding depression. This research should inform management by determining MVP and how inbreeding, which is expected to accrue in remnant populations because of generations of low abundance, may affect MVP.


Genetics ◽  
2003 ◽  
Vol 165 (4) ◽  
pp. 2193-2212 ◽  
Author(s):  
Sylvain Glémin ◽  
Joëlle Ronfort ◽  
Thomas Bataillon

AbstractInbreeding depression is a general phenomenon that is due mainly to recessive deleterious mutations, the so-called mutation load. It has been much studied theoretically. However, until very recently, population structure has not been taken into account, even though it can be an important factor in the evolution of populations. Population subdivision modifies the dynamics of deleterious mutations because the outcome of selection depends on processes both within populations (selection and drift) and between populations (migration). Here, we present a general model that permits us to gain insight into patterns of inbreeding depression, heterosis, and the load in subdivided populations. We show that they can be interpreted with reference to single-population theory, using an appropriate local effective population size that integrates the effects of drift, selection, and migration. We term this the “effective population size of selection” (NeS). For the infinite island model, for example, it is equal to NeS=N(1+m∕hs), where N is the local population size, m the migration rate, and h and s the dominance and selection coefficients of deleterious mutation. Our results have implications for the estimation and interpretation of inbreeding depression in subdivided populations, especially regarding conservation issues. We also discuss the possible effects of migration and subdivision on the evolution of mating systems.


2019 ◽  
Author(s):  
Hugo Cayuela ◽  
Jérôme G. Prunier ◽  
Martin Laporte ◽  
Jérôme Gippet ◽  
Laurent Boualit ◽  
...  

AbstractUnderstanding the mechanisms underlying biological extinctions is a critical challenge for conservation biologists. Both deterministic (e.g. habitat loss, fragmentation) and stochastic (i.e. demographic stochasticity, Allee effect) demographic processes are involved in population decline. Simultaneously, a decrease of population size has far-reaching consequences for genetics of populations by increasing the risk of inbreeding and the effects of genetic drift, which together inevitably results in a loss of genetic diversity and a reduced effective population size (Ne). These genetic factors may retroactively affect vital rates (a phenomenon coined ‘inbreeding depression’), and therefore reduce population growth and accelerate the extinction process of small populations. To date, few studies have simultaneously examined the demographic and genetic mechanisms driving the extinction of wild populations, and have most of the time neglected the spatial structure of populations. In this study, we examined demographic and genetic factors involved in the extinction process of a spatially structured population of a lekking bird, the western capercaillie (Tetrao urogallus). To address this issue, we collected capture-recapture and genetic data over a 6-years period in Vosges mountains, France. Our study showed that the population of T. urogallus experienced a severe decline between 2010 and 2015. We did not detect any Allee effect on survival and recruitment. By contrast, individuals of both sexes dispersed to avoid small leks, suggesting a behavioral response to a mate finding Allee effect. In parallel to this demographic decline, the population showed a low genetic diversity and high inbreeding. In addition, the effective population sizes at both lek and population levels was low. Despite this, we did not detected evidence of inbreeding depression: neither survival nor recruitment were affected by individual inbreeding level. Our study underlines the benefit from combining demographic and genetic approaches to investigate processes that are involved in biological extinctions.


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