Inbreeding Depression and Genetic Rescue in a Plant Metapopulation

2000 ◽  
Vol 155 (3) ◽  
pp. 383 ◽  
Author(s):  
Richards
2000 ◽  
Vol 155 (3) ◽  
pp. 383-394 ◽  
Author(s):  
Christopher M. Richards

Author(s):  
Donald M. Waller ◽  
Lukas F. Keller

Inbreeding (also referred to as “consanguinity”) occurs when mates are related to each other due to incest, assortative mating, small population size, or population sub-structuring. Inbreeding results in an excess of homozygotes and hence a deficiency of heterozygotes. This, in turn, exposes recessive genetic variation otherwise hidden by heterozygosity with dominant alleles relative to random mating. Interest in inbreeding arose from its use in animal and plant breeding programs to expose such variation and to fix variants in genetically homogenous lines. Starting with Gregor Mendel’s experiments with peas, geneticists have widely exploited inbreeding as a research tool, leading R. C. Lewontin to conclude that “Every discovery in classical and population genetics has depended on some sort of inbreeding experiment” (see Lewontin’s 1965 article “The Theory of Inbreeding.” Science 150:1800–1801). Charles Darwin wrote an entire book on the effects of inbreeding as measured in fifty-two taxa of plants. He and others noted that most plants and animals go to great length to avoid inbreeding, suggesting that inbreeding has high costs that often outweigh the benefits of inbreeding. Benefits of inbreeding include increased genetic transmission while the costs of inbreeding manifest as inbreeding depression when deleterious, mostly recessive alleles otherwise hidden as heterozygotes emerge in homozygote form upon inbreeding. Inbreeding also reduces fitness when heterozygotes are more fit than both homozygotes, but such overdominance is rare. Recurrent mutation continuously generates deleterious recessive alleles that create a genetic “load” of deleterious mutations mostly hidden within heterozygotes in outcrossing populations. Upon inbreeding, the load is expressed when deleterious alleles segregate as homozygotes, causing often substantial inbreeding depression. Although inbreeding alone does not change allele frequencies, it does redistribute genetic variation, reducing it within families or populations while increasing it among families or populations. Inbreeding also increases selection by exposing deleterious recessive mutations, a process called purging that can deplete genetic variation. For all these reasons, inbreeding is a central concept in evolutionary biology. Inbreeding is also central to conservation biology as small and isolated populations become prone to inbreeding and thus suffer inbreeding depression. Inbreeding can reduce population viability and increase extinction risk by reducing individual survival and/or reproduction. Such effects can often be reversed, however, by introducing new genetic material that re-establishes heterozygosity (“genetic rescue”). The current availability of DNA sequence and expression data is now allowing more detailed analyses of the causes and evolutionary consequences of inbreeding.


2007 ◽  
Vol 274 (1623) ◽  
pp. 2365-2371 ◽  
Author(s):  
Richard J Fredrickson ◽  
Peter Siminski ◽  
Melissa Woolf ◽  
Philip W Hedrick

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.


2019 ◽  
Author(s):  
Rebecca M Gooley ◽  
Carolyn J Hogg ◽  
Samantha Fox ◽  
David Pemberton ◽  
Katherine Belov ◽  
...  

Background. Vulnerable species experiencing inbreeding depression are prone to localised extinctions because of their reduced fitness. For Tasmanian devils, the rapid spread of devil facial tumour disease (DFTD) has led to population declines and fragmentation across the species’ range. Here we show that one of the few remaining DFTD-free populations of Tasmanian devils is experiencing inbreeding depression. Moreover, this population has experienced a significant reduction in reproductive success over recent years. Methods. We used 32 microsatellite loci to examine changes in genetic diversity and inbreeding in the wild population at Woolnorth, alongside field data on breeding success from females to test for inbreeding depression. Results. We found that maternal internal relatedness has a negative impact on litter sizes. The results of this study imply that this population has entered an extinction vortex and that to protect the population, genetic rescue may be required. This study provides conservation managers with useful information for managing wild devils and provides support for the “Wild Devil Recovery Program” which is currently augmenting small, isolated populations.


2021 ◽  
Vol 118 (49) ◽  
pp. e2023018118
Author(s):  
Anubhab Khan ◽  
Kaushalkumar Patel ◽  
Harsh Shukla ◽  
Ashwin Viswanathan ◽  
Tom van der Valk ◽  
...  

Increasing habitat fragmentation leads to wild populations becoming small, isolated, and threatened by inbreeding depression. However, small populations may be able to purge recessive deleterious alleles as they become expressed in homozygotes, thus reducing inbreeding depression and increasing population viability. We used whole-genome sequences from 57 tigers to estimate individual inbreeding and mutation load in a small–isolated and two large–connected populations in India. As expected, the small–isolated population had substantially higher average genomic inbreeding (FROH = 0.57) than the large–connected (FROH = 0.35 and FROH = 0.46) populations. The small–isolated population had the lowest loss-of-function mutation load, likely due to purging of highly deleterious recessive mutations. The large populations had lower missense mutation loads than the small–isolated population, but were not identical, possibly due to different demographic histories. While the number of the loss-of-function alleles in the small–isolated population was lower, these alleles were at higher frequencies and homozygosity than in the large populations. Together, our data and analyses provide evidence of 1) high mutation load, 2) purging, and 3) the highest predicted inbreeding depression, despite purging, in the small–isolated population. Frequency distributions of damaging and neutral alleles uncover genomic evidence that purifying selection has removed part of the mutation load across Indian tiger populations. These results provide genomic evidence for purifying selection in both small and large populations, but also suggest that the remaining deleterious alleles may have inbreeding-associated fitness costs. We suggest that genetic rescue from sources selected based on genome-wide differentiation could offset any possible impacts of inbreeding depression.


2021 ◽  
Author(s):  
Anubhab Khan ◽  
Kaushalkumar Patel ◽  
Harsh Shukla ◽  
Ashwin Viswanathan ◽  
Tom van der Valk ◽  
...  

Increasing habitat fragmentation leads to wild populations becoming small, isolated, and threatened by inbreeding depression. However, small populations may be able to purge recessive deleterious alleles as they become expressed in homozygotes, thus reducing inbreeding depression and increasing population viability. We used genome sequencing of 57 tigers to estimate individual inbreeding and mutation loads in a small-isolated, and two large-connected populations in India. As expected, the small-isolated population had substantially higher average genomic inbreeding (FROH=0.57) than the large-connected (FROH=0.35 and FROH=0.46) populations. The small-isolated population had the lowest loss-of-function mutation load, likely due to purging of highly deleterious recessive mutations. The large populations had lower missense mutation loads than the small-isolated population, but were not identical, possibly due to different demographic histories. While the number of the loss-of-function alleles in the small-isolated population was lower, these alleles were at high frequencies and homozygosity than in the large populations. Together, our data and analyses provide evidence of (a) high mutation load; (b) purging and (c) the highest predicted inbreeding depression, despite purging, in the small-isolated population. Frequency distributions of damaging and neutral alleles uncover genomic evidence that purifying selection has removed part of the mutation load across Indian tiger populations. These results provide genomic evidence for purifying selection in both small and large populations, but also suggest that the remaining deleterious alleles may have inbreeding associated fitness costs. We suggest that genetic rescue from sources selected based on genome-wide differentiation should offset any possible impacts of inbreeding depression.


2015 ◽  
Vol 112 (33) ◽  
pp. 10557-10562 ◽  
Author(s):  
Ruth A. Hufbauer ◽  
Marianna Szűcs ◽  
Emily Kasyon ◽  
Courtney Youngberg ◽  
Michael J. Koontz ◽  
...  

Setting aside high-quality large areas of habitat to protect threatened populations is becoming increasingly difficult as humans fragment and degrade the environment. Biologists and managers therefore must determine the best way to shepherd small populations through the dual challenges of reductions in both the number of individuals and genetic variability. By bringing in additional individuals, threatened populations can be increased in size (demographic rescue) or provided with variation to facilitate adaptation and reduce inbreeding (genetic rescue). The relative strengths of demographic and genetic rescue for reducing extinction and increasing growth of threatened populations are untested, and which type of rescue is effective may vary with population size. Using the flour beetle (Tribolium castaneum) in a microcosm experiment, we disentangled the genetic and demographic components of rescue, and compared them with adaptation from standing genetic variation (evolutionary rescue in the strictest sense) using 244 experimental populations founded at either a smaller (50 individuals) or larger (150 individuals) size. Both types of rescue reduced extinction, and those effects were additive. Over the course of six generations, genetic rescue increased population sizes and intrinsic fitness substantially. Both large and small populations showed evidence of being able to adapt from standing genetic variation. Our results support the practice of genetic rescue in facilitating adaptation and reducing inbreeding depression, and suggest that demographic rescue alone may suffice in larger populations even if only moderately inbred individuals are available for addition.


2016 ◽  
Vol 31 (12) ◽  
pp. 940-952 ◽  
Author(s):  
Philip W. Hedrick ◽  
Aurora Garcia-Dorado

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