Inbreeding Depression in the Speke's Gazelle Captive Breeding Program

Abstract: The Speke's gazelle ( Gazella spekei ) captive breeding program has been presented as one of the few examples of selection reducing the genetic load of a population and as a potential model for the captive breeding of endangered species founded from a small number of individuals. In this breeding program, three generations of mate selection apparently increased the viability of inbred individuals. We reanalyzed the Speke's gazelle studbook and examined potential causes for the reduction of inbreeding depression. Our analysis indicates that the decrease in inbreeding depression is not consistent with any model of genetic improvement in the herd. Instead, we found that the effect of inbreeding decreased from severe to moderate during the first generation of inbreeding, and that this change is responsible for almost all of the decline in inbreeding depression observed during the breeding program. This eliminates selection as a potential explanation for the decrease in inbreeding depression and suggests that inbreeding depression may be more sensitive to environmental influences than is usually thought.     

Translating effects of inbreeding depression on component vital rates to overall population growth in endangered bighorn sheep

Evidence of inbreeding depression is commonly detected from the fitness traits of animals, yet its effects on population growth rates of endangered species are rarely assessed. We examined whether inbreeding depression was affecting Sierra Nevada bighorn sheep (Ovis canadensis sierrae), a subspecies listed as endangered under the U.S. Endangered Species Act. Our objectives were to characterize genetic variation in this subspecies; test whether inbreeding depression affects bighorn sheep vital rates (adult survival and female fecundity); evaluate whether inbreeding depression may limit subspecies recovery; and examine the potential for genetic management to increase population growth rates. Genetic variation in 4 populations of Sierra Nevada bighorn sheep was among the lowest reported for any wild bighorn sheep population, and our results suggest that inbreeding depression has reduced adult female fecundity. Despite this population sizes and growth rates predicted from matrix-based projection models demonstrated that inbreeding depression would not substantially inhibit the recovery of Sierra Nevada bighorn sheep populations in the next approximately 8 bighorn sheep generations (48 years). Furthermore, simulations of genetic rescue within the subspecies did not suggest that such activities would appreciably increase population sizes or growth rates during the period we modeled (10 bighorn sheep generations, 60 years). Only simulations that augmented the Mono Basin population with genetic variation from other subspecies, which is not currently a management option, predicted significant increases in population size. Although we recommend that recovery activities should minimize future losses of genetic variation, genetic effects within these endangered populations-either negative (inbreeding depression) or positive (within subspecies genetic rescue)-appear unlikely to dramatically compromise or stimulate short-term conservation efforts. The distinction between detecting the effects of inbreeding depression on a component vital rate (e.g., fecundity) and the effects of inbreeding depression on population growth underscores the importance of quantifying inbreeding costs relative to population dynamics to effectively manage endangered populations.     

Erosion of Heterozygosity in Fluctuating Populations

Abstract: Demographic, environmental, and genetic stochasticity threaten the persistence of isolated populations. The relative importance of these intertwining factors remains unresolved, but a common view is that random demographic and environmental events will usually drive small populations to the brink of extinction before genetic deterioration poses a serious threat. To evaluate the potential importance of genetic factors, we analyzed a model linking demographic and environmental conditions to the loss of genetic diversity in isolated populations undergoing natural levels of fluctuation. Nongenetic processes—environmental stochasticity and population demography—were modeled according to a bounded diffusion process. Genetic processes were modeled by quantifying the rate of drift according to the effective population size, which was predicted from the same parameters used to describe the nongenetic processes. We combined these models to predict the heterozygosity remaining at the time of extinction, as predicted by the nongenetic portion of the model. Our model predicts that many populations will lose most or all of their neutral genetic diversity before nongenetic random events lead to extinction. Given the abundant evidence for inbreeding depression and recent evidence for elevated extinction rates of inbred populations, our findings suggest that inbreeding may be a greater general threat to population persistence than is generally recognized. Therefore, conservation biologists should not ignore the genetic component of extinction risk when assessing species endangerment and developing recovery plans.     

Relative Contribution of Inbreeding Depression and Eroded Adaptive Diversity to Extinction Risk in Small Populations of Shore Campion

Abstract:  To study the relative importance of inbreeding depression and the loss of adaptive diversity in determining the extinction risk of small populations, we carried out an experiment in which we crossed and self-fertilized founder plants from a single, large population of shore campion ( Silene littorea Brot.). We used the seeds these plants produced to colonize 18 new locations within the distribution area of the species. The reintroduced populations were of three kinds: inbred and genetically homogeneous, each made up of selfed seed from a single plant; inbred and mixed, made up of a mixture of selfed seeds from all founder plants; and outbred and mixed, made up of a mixture of seeds obtained in outcrosses between the founders. We compared the inbred homogeneous populations with the inbred mixed to measure the effect of genetic diversity among individuals and the inbred mixed with the outbred mixed to measure the effect of inbreeding. Reintroduction success was seriously limited by inbreeding, whereas it was not affected by genetic diversity. This observation and the nonsignificant interaction between family and reintroduction location for individual plant characters suggest that the fixation of overall deleterious genes causing inbreeding depression posed a more serious threat to the short-term survival of the populations than the loss of genes involved in genotype and environment interactions. Thus, reintroduction success was related to adaptive diversity. Preventing such fixation might be the most important consideration in the genetic management and conservation of shore campion populations.     

Inbreeding and Loss of Genetic Variation in a Reintroduced Population of Mauritius Kestrel

Abstract:  Many populations have recovered from severe bottlenecks either naturally or through intensive conservation management. In the past, however, few conservation programs have monitored the genetic health of recovering populations. We conducted a conservation genetic assessment of a small, reintroduced population of Mauritius Kestrel ( Falco punctatus ) to determine whether genetic deterioration has occurred since its reintroduction. We used pedigree analysis that partially accounted for individuals of unknown origin to document that (1) inbreeding occurred frequently (2.6% increase per generation; N _eI= 18.9), (2) 25% of breeding pairs were composed of either closely or moderately related individuals, (3) genetic diversity has been lost from the population (1.6% loss per generation; N _eV= 32.1) less rapidly than the corresponding increase in inbreeding, and (4) ignoring the contribution of unknown individuals to a pedigree will bias the metrics derived from that pedigree, ultimately obscuring the prevailing genetic dynamics. The rates of inbreeding and loss of genetic variation in the subpopulation of Mauritius Kestrel we examined were extreme and among the highest yet documented in a wild vertebrate population. Thus, genetic deterioration may affect this population's long-term viability. Remedial conservation strategies are needed to reduce the impact of inbreeding and loss of genetic variation in this species. We suggest that schemes to monitor genetic variation after reintroduction should be an integral component of endangered species recovery programs.     

Low Genetic Variability in the Hawaiian Monk Seal

The Hawaiian monk seal (   Monachus schauinslandi) is a critically endangered species that has failed to recover from human exploitation despite decades of protection and ongoing management efforts designed to increase population growth. The seals breed at five principal locations in the northwestern Hawaiian islands, and inter-island migration is limited. Genetic variation in this species is expected to be low due to a recent population bottleneck and probable inbreeding within small subpopulations. To test the hypothesis that small population size and strong site fidelity has led to low within-island genetic variability and significant between-island differentiation, we used two independent approaches to quantify genetic variation both within and among the principal subpopulations. Mitochondrial control region and tRNA gene sequences (359 base pairs) were obtained from 50 seals and revealed very low genetic diversity (0.6% variable sites), with no evidence of subpopulation differentiation. Multilocus DNA fingerprints from 22 individuals also indicated low genetic variation in at least some subpopulations (band-sharing values for "unrelated" seals from the same island ranged from 49 to 73%). This method also provided preliminary evidence of population subdivision (  F'_st estimates of 0.20 and 0.13 for two adjacent island pairs). Translocations of seals among islands may therefore have the potential to relieve local inbreeding and possibly to reduce the total amount of variation preserved in the population. Genetic variation is only one of many factors that determine the ability of an endangered species to recover. Maintenance of existing genetic diversity, however, remains an important priority for conservation programs because of the possibility of increased disease resistance in more variable populations and the chance that inbreeding depression may only be manifest under adverse environmental conditions.     

Inbreeding avoidance or tolerance? Comparison of mating behavior between mass-reared and wild strains of the sweet potato weevil

Inadvertent selection is an important genetic process that frequently occurs during laboratory culture. The mass-reared strain of the sweet potato weevil Cylas formicarius exhibits stronger inbreeding depression than the wild strain does. When inbreeding depression occurs in a population, mating with a close relative is often considered maladaptive; however, in some contexts, the inclusive fitness benefits of inbreeding may outweigh the costs, favoring individuals that tolerate a low level of inbreeding depression. Theory predicts that mass-reared strain weevils will avoid inbreeding while wild strain weevils will tolerate inbreeding. To examine this prediction, we compared the effect of relatedness on the mating and insemination successes in mass-reared and wild strains of C. formicarius. While close relative pairs of the wild strain copulated less frequently than non-kin pairs, almost all mass-reared strain pairs copulated irrespective of relatedness. The results showed that the strain with weak inbreeding depression (wild strain) avoided inbreeding, whereas the strain with strong inbreeding depression (mass-reared strain) tolerated inbreeding. The contradiction between the theoretical prediction and our results is discussed from the perspective of laboratory adaptation, mating systems, and life history of C. formicarius.     

A Reassessment of Homozygosity and the Case for Inbreeding Depression in the Cheetah, Acinonyx jubatus: Implications for Conservation

Preservation of genetic diversity within declining populations of endangered species is a major concern in the discipline of conservation biology. The endangered cheetah, Acinonyx jubatus , exhibits relatively little genetic variability (polymorphism = 0.02–0.04, heterozygosity = 0.0004–0.014). Since the discovery of the cheetah's relative homozygosity, this species has been frequently cited as an example of one whose survival may be compromised by the loss of genetic diversity. The cheetah's genetic uniformity is generally believed to be the result of an historical population bottle-neck followed by a high level of inbreeding. Evidence offered in support of this hypothesis includes the cheetah's present low level of genetic variability and symptoms of inbreeding depression in captive populations. Using available data on fluctuating asymmetry and genetic variation in other carnivores, I question the assumption that the present level of genetic diversity in the cheetah is indicative of a loss of former variability. Carnivores exhibit significantly lower levels of genetic variation than other mammals, and several carnivores for which data are available exhibit lower levels of heterozygosity and polymorphism than the cheetah does. Measures of fluctuating asymmetry do not support the hypothesis that the cheetah is suffering an increased level of bomozygosity due to genetic stress. Many of the phenotypic effects attributed to inbreeding depression, such as infertility, reduced litter sizes, and increased susceptibility to disease, are limited to captive individuals and may be explained as physiological or behavioral artifacts of captivity. In sum, the genetic constitution of the cheetah does not appear to compromise the survival of the species. Conservation efforts may be more effectively aimed at a real, immediate threat to the cheetah's future: the loss of its natural habitat.     

Founder Effects,Inbreeding, and Loss of Genetic Diversity in Four Avian Reintroduction Programs

Abstract: The number of individuals translocated and released as part of a reintroduction is often small, as is the final established population, because the reintroduction site is typically small. Small founder and small resulting populations can result in population bottlenecks, which are associated with increased rates of inbreeding and loss of genetic diversity, both of which can affect the long‐term viability of reintroduced populations. I used information derived from pedigrees of four monogamous bird species reintroduced onto two different islands (220 and 259 ha) in New Zealand to compare the pattern of inbreeding and loss of genetic diversity among the reintroduced populations. Although reintroduced populations founded with few individuals had higher levels of inbreeding, as predicted, other factors, including biased sex ratio and skewed breeding success, contributed to high levels of inbreeding and loss of genetic diversity. Of the 10–58 individuals released, 4–25 genetic founders contributed at least one living descendent and yielded approximately 3–11 founder–genome equivalents (number of genetic founders assuming an equal contribution of offspring and no random loss of alleles across generations) after seven breeding seasons. This range is much lower than the 20 founder–genome equivalents recommended for captive‐bred populations. Although the level of inbreeding in one reintroduced population initially reached three times that of a closely related species, the long‐term estimated rate of inbreeding of this one population was approximately one‐third that of the other species due to differences in carrying capacities of the respective reintroduction sites. The increasing number of reintroductions to suitable areas that are smaller than those I examined here suggests that it might be useful to develop long‐term strategies and guidelines for reintroduction programs, which would minimize inbreeding and maintain genetic diversity.     

Genetic Structure of Fragmented Populations of the Endangered Daisy Rutidosis leptorrhynchoides

Abstract: The endangered grassland daisy Rutidosis leptorrhynchoides has been subject to severe habitat destruction and fragmentation over the past century. Using allozyme markers, we examined the genetic diversity and structure of 16 fragmented populations. The species had high genetic variation compared to other plant species, and both polymorphism and allelic richness showed strong positive relationships with log reproductive population size, reflecting a loss of rare alleles (frequency of q < 0.1) in smaller populations. Fixation coefficients were positively related to size, due either to a lack of rare homozygotes in small populations or to Wahlund effects (owing to spatial genetic structure) in large ones. Neither gene diversity nor heterozygosity was related to population size, and other population parameters such as density, spatial contagion, and isolation had no apparent effect on genetic variation. Genetic divergence among populations was low , despite a large north-to-south break in the species' current distribution. To preserve maximum genetic variation, conservation strategies should aim to maintain the five populations larger than 5000 reproductive plants, all of which occur in the north of the range, as well as the largest southern population of 626 plants at Truganina. Only one of these is currently under formal protection. High heterozygosity in smaller populations suggests that they are unlikely to be suffering from inbreeding depression and so are also valuable for conservation. Erosion of allelic richness at self-incompatibility loci, however, may limit the reproductive capacity of populations numbering less than 20 flowering plants.     

Environmental Dependency of Inbreeding Depression: Implications for Conservation Biology

Inbreeding depression is environmentally dependent, such that a population may suffer from inbreeding depression in one environment but not another. We examined the phenotypic responses of 35 inbred ( F = 0.672) lineages of the red flour beetle Tribolium castaneum in two different climatic environments. We found a significant environmental effect on males but not females. More important, we found that the rank fitness order of lineages differs between environments; lineages of high fitness in one environment may have low fitness in another environment. This change in rank is evident in a significant genotype-by-environment interaction for inbreeding depression for both females and males. These results suggest that even if we know the average environmental effect of inbreeding depression in a population, for any particular lineage measurements of inbreeding depression in one environment may not predict the level of inbreeding depression in another environment. Conservation biologists need to be aware of the environmental dependency of inbreeding depression when planning wildlife refuges or captive propagation programs for small populations. Ideally, captive propagation programs should maintain separate lineages for release efforts. Refuge design programs should consider maintaining a range of habitat types.     

Marine extinctions and conservation

In contrast to the large number of terrestrial extinctions that have taken place over the past 12,000 years, there have apparently been very few marine extinctions. But these small losses should not be reason for complacency. During the past 50 years, government supported, commercial fishing has resulted in the collapse of about a thousand populations that once supplied most of the world’s seafood. For the collapsed species, now existing as small remnants of their former population sizes, the future is bleak. They suffer from loss of genetic diversity, inbreeding depression, and depensation. Because marine species were eliminated by historic climatic changes, continued global warming is likely to result in the extinction of small populations that already have a precarious existence. They may be considered evidence of an extinction debt that must be paid as the climate change becomes more severe. For some of the remnant species, extinction can be avoided if there is a rapid management conversion to the use of more marine protected areas (MPAs) and extensive ocean zoning where fishing is prohibited.     

Inbreeding Depression Accumulation across Life‐History Stages of the Endangered Takahe

Abstract: Studies evaluating the impact of inbreeding depression on population viability of threatened species tend to focus on the effects of inbreeding at a single life‐history stage (e.g., juvenile survival). We examined the effects of inbreeding across the full life‐history continuum, from survival up to adulthood, to subsequent reproductive success, and to the recruitment of second‐generation offspring, in wild Takahe ( Porphyrio hochstetteri ) by analyzing pedigree and fitness data collected over 21 breeding seasons. Although the effect size of inbreeding at individual life‐history stages was small, inbreeding depression accumulated across multiple life‐history stages and ultimately reduced long‐term fitness (i.e., successful recruitment of second‐generation offspring). The estimated total lethal equivalents (2B) summed across all life‐history stages were substantial (16.05, 95% CI 0.08–90.8) and equivalent to an 88% reduction in recruitment of second‐generation offspring for closely related pairs (e.g., sib–sib pairings) relative to unrelated pairs (according to the pedigree). A history of small population size in the Takahe could have contributed to partial purging of the genetic load and the low level of inbreeding depression detected at each single life‐history stage. Nevertheless, our results indicate that such “purged” populations can still exhibit substantial inbreeding depression, especially when small but negative fitness effects accumulate across the species’ life history. Because inbreeding depression can ultimately affect population viability of small, isolated populations, our results illustrate the importance of measuring the effects of inbreeding across the full life‐history continuum.     

Mutation and Conservation

Mutation can critically affect the viability of small populations by causing inbreeding depression, by maintaining potentially adaptive genetic variation in quantitative characters, and through the erosion of fitness by accumulation of mildly detrimental mutations. I review and integrate recent empirical and theoretical work on spontaneous mutation and its role in population viability and conservation planning. I analyze both the maintenance of potentially adaptive genetic variation in quantitative characters and the role of detrimental mutations in increasing the extinction risk of small populations. Recent experiments indicate that the rate of production of quasineutral, potentially adaptive genetic variance in quantitative characters is an order of magnitude smaller than the total mutational variance because mutations with large phenotypic effects tend to be strongly detrimental. This implies that, to maintain normal adaptive potential in quantitative characters under a balance between mutation and random genetic drift (or among mutation, drift, and stabilizing natural selection), the effective population size should be about 5000 rather than 500 (the Franklin-Soulé number). Recent theoretical results suggest that the risk of extinction due to the fixation of mildly detrimental mutations may be comparable in importance to environmental stochasticity and could substantially decrease the long-term viability of populations with effective sizes as large as a few thousand. These findings suggest that current recovery goals for many threatened and endangered species are inadequate to ensure long-term population viability.     

Sex‐Biased Inbreeding Effects on Reproductive Success and Home Range Size of the Critically Endangered Black Rhinoceros

A central premise of conservation biology is that small populations suffer reduced viability through loss of genetic diversity and inbreeding. However, there is little evidence that variation in inbreeding impacts individual reproductive success within remnant populations of threatened taxa, largely due to problems associated with obtaining comprehensive pedigree information to estimate inbreeding. In the critically endangered black rhinoceros, a species that experienced severe demographic reductions, we used model selection to identify factors associated with variation in reproductive success (number of offspring). Factors examined as predictors of reproductive success were age, home range size, number of nearby mates, reserve location, and multilocus heterozygosity (a proxy for inbreeding). Multilocus heterozygosity predicted male reproductive success (p< 0.001, explained deviance >58%) and correlated with male home range size (p < 0.01, r² > 44%). Such effects were not apparent in females, where reproductive success was determined by age (p < 0.01, explained deviance 34%) as females raise calves alone and choose between, rather than compete for, mates. This first report of a 3‐way association between an individual male's heterozygosity, reproductive output, and territory size in a large vertebrate is consistent with an asymmetry in the level of intrasexual competition and highlights the relevance of sex‐biased inbreeding for the management of many conservation‐priority species. Our results contrast with the idea that wild populations of threatened taxa may possess some inherent difference from most nonthreatened populations that necessitates the use of detailed pedigrees to study inbreeding effects. Despite substantial variance in male reproductive success, the increased fitness of more heterozygous males limits the loss of heterozygosity. Understanding how individual differences in genetic diversity mediate the outcome of intrasexual competition will be essential for effective management, particularly in enclosed populations, where individuals have restricted choice about home range location and where the reproductive impact of translocated animals will depend upon the background distribution in individual heterozygosity. Efectos de la Endogamia Sesgada por el Sexo sobre el Éxito Reproductivo y el Rango del Tamaño de Hábitat del Rinoceronte Negro, Especie en Peligro Crítico     

The Paradox of Forest Fragmentation Genetics

Abstract:  Theory predicts widespread loss of genetic diversity from drift and inbreeding in trees subjected to habitat fragmentation, yet empirical support of this theory is scarce. We argue that population genetics theory may be misapplied in light of ecological realities that, when recognized, require scrutiny of underlying evolutionary assumptions. One ecological reality is that fragment boundaries often do not represent boundaries for mating populations of trees that benefit from long-distance pollination, sometimes abetted by long-distance seed dispersal. Where fragments do not delineate populations, genetic theory of small populations does not apply. Even in spatially isolated populations, where genetic theory may eventually apply, evolutionary arguments assume that samples from fragmented populations represent trees that have had sufficient time to experience drift, inbreeding, and ultimately inbreeding depression, an unwarranted assumption where stands in fragments are living relicts of largely unrelated predisturbance populations. Genetic degradation may not be as important as ecological degradation for many decades following habitat fragmentation.     

Guidelines for genetic monitoring of translocated plant populations

Plant translocation is a useful tool for implementing assisted gene flow in recovery plans of critically endangered plant species. Although it helps to restore genetically viable populations, it is not devoid of genetic risks, such as poor adaptation of transplants and outbreeding depression in the hybrid progeny, which may have negative consequences in terms of demographic growth and plant fitness. Hence, a follow-up genetic monitoring should evaluate whether the translocated populations are genetically viable and self-sustaining in the short and long term. The causes of failure to adjust management responses also need to be identified. Molecular markers and fitness-related quantitative traits can be used to determine whether a plant translocation enhanced genetic diversity, increased fitness, and improved the probability of long-term survival. We devised guidelines and illustrated them with studies from the literature to help practitioners determine the appropriate genetic survey methods so that management practices can better integrate evolutionary processes. These guidelines include methods for sampling and for assessing changes in genetic diversity and differentiation, contemporary gene flow, mode of local recruitment, admixture level, the effects of genetic rescue, inbreeding or outbreeding depression and local adaptation on plant fitness, and long-term genetic changes.     

Hereditary Blindness in a Captive Wolf (Canis lupus) Population: Frequency Reduction of a Deleterious Allele in Relation to Gene Conservation

Numerous cases of hereditary diseases and disorders have been reported in wild animals bred in captivity, but little attention has been paid to the particular genetic management problems that arise when such defects occur. These problems include the obstacle of eliminating the deleterious allele(s) without contemporary loss of genetic variability. In this paper we use the statistical methods of pedigree analysis to address questions regarding a previously presumed hereditary form of blindness observed in a captive wolf population bred for conservation purposes in Scandinavian zoos. The most likely mode of inheritance coincides with an autosomal recessive allele with either a full penetrance or a reduced penetrance of 0.6 (depending on the reliability of studbook records). Using these two models of inheritance, we calculate the probability of carrying the blindness allele for each living animal. Analysis of the effect of removing high-probability carriers on founder allele survival and level of inbreeding demonstrates that the frequency of the deleterious allele can be significantly reduced without seriously affecting founder allele survival or current degree of inbreeding in the wolf population.     

An experimental test of alternative population augmentation scenarios

Human land use is fragmenting habitats worldwide and inhibiting dispersal among previously connected populations of organisms, often leading to inbreeding depression and reduced evolutionary potential in the face of rapid environmental change. To combat this augmentation of isolated populations with immigrants is sometimes used to facilitate demographic and genetic rescue. Augmentation with immigrants that are genetically and adaptively similar to the target population effectively increases population fitness, but if immigrants are very genetically or adaptively divergent, augmentation can lead to outbreeding depression. Despite well‐cited guidelines for the best practice selection of immigrant sources, often only highly divergent populations remain, and experimental tests of these riskier augmentation scenarios are essentially nonexistent. We conducted a mesocosm experiment with Trinidadian guppies (Poecilia reticulata) to test the multigenerational demographic and genetic effects of augmenting 2 target populations with 3 types of divergent immigrants. We found no evidence of demographic rescue, but we did observe genetic rescue in one population. Divergent immigrant treatments tended to maintain greater genetic diversity, abundance, and hybrid fitness than controls that received immigrants from the source used to seed the mesocosms. In the second population, divergent immigrants had a slightly negative effect in one treatment, and the benefits of augmentation were less apparent overall, likely because this population started with higher genetic diversity and a lower reproductive rate that limited genetic admixture. Our results add to a growing consensus that gene flow can increase population fitness even when immigrants are more highly divergent and may help reduce uncertainty about the use of augmentation in conservation.