Is Mutation Accumulation a Threat to the Survival of Endangered Populations?

The accumulation of new deleterious mutations has been predicted to constitute a significant threat to the survival of finite sexually reproducing populations. Three measures of genetic load were made on populations of Drosophila melanogaster maintained at effective population sizes of 25, 50, 100, 250, and 500 for 45 or 50 generations and their outbred base population and a new sample from the same wild population. Genetic loads were measured as fitness differentials between inbred and non-inbred lines derived from each population under both benign ( productivity of single pairs) and competitive (competitive index) conditions. No trend of smaller populations exhibiting greater genetic loads than larger ones was observed under either benign or competitive conditions. Further, genetic loads were similar in captive and wild populations. Frequencies of deleterious and lethal alleles on chromosome II were measured by making the chromosome (approximately 40% of the genome) homozygous using a marked balancer stock. Neither deleterious nor lethal allele frequencies exhibited a relationship with population size. The accumulation of detrimental mutations does not appear to pose a significant threat to finite sexual populations with effective sizes of 25 or more over the 100–200 year time frames considered in most wildlife conservation programs.     

Linking Inbreeding Effects in Captive Populations with Fitness in the Wild: Release of Replicated Drosophila melanogaster Lines under Different Temperatures

Abstract:  Inbreeding effects have been detected in captive populations of threatened species, but the extent to which these effects translate into fitness under field conditions is mostly unknown. We address this issue by comparing the performance of replicated noninbred and inbred Drosophila lines under field and laboratory conditions. We asked whether environment-dependent effects of inbreeding can be demonstrated for a field-fitness component in Drosophila , the ability of flies to locate resources, and associated the results with results on effects of inbreeding investigated in the laboratory. Inbreeding effects were evident when releases were undertaken under warm conditions, but not under cold conditions, which illustrates the environment-dependent nature of inbreeding depression. Inbreeding effects were much stronger in the field at warm temperatures than in laboratory stress tests, particularly for females. Effects of inbreeding based on performance in traditional inbreeding assays (viability, productivity) or from laboratory stress tests poorly predicted performance in the field. Inbreeding effects on resource location in the field can be strongly deleterious under some thermal conditions and involve traits not easily measured under laboratory conditions. More generally, inbreeding effects measured in captive populations may not necessarily predict their field performance, and programs to purge captive populations of deleterious alleles may not necessarily lead to fitness benefits in the wild.     

Experimental Tests of Captive Breeding for Endangered Species

Abstract: Several captive breeding regimes were compared for their ability to maintain fitness ( larval viability) and genetic variation in small populations of the housefly ( Musca domestica L.). Populations were either maintained at constant sizes of 40, 200, or 2000 individuals or initiated with two pairs of flies and allowed to grow to 40 individuals ( low-founder-number populations). Low-founder-number populations without migration exhibited low larval viability (22%) after 24 generations, compared to larger populations maintained at either 200 (49%) or 2000 (69%) individuals, and suffered high extinction, with only 44% of the lines surviving 24 generations. Low-founder-number populations subjected to two additional founder ( bottleneck) episodes, reducing them to two pairs of flies, suffered little additional loss in fitness or extinction compared to the single-founder treatments. Migration as low as one individual per generation (2.5% migration) significantly offset both reduced fitness and rate of extinction. Conversely, fitness was not significantly increased for low-founder-number populations when founders were selected from the top performing 20% of pairs under full-sib mating. Populations maintained at 40 individuals were not sustainable, exhibiting low larval viability (35%) and a high extinction rate (40%) over 24 generations, similar to the extinction rates for populations initiated with only four founders. Although none of the populations maintained at 200 individuals went extinct, their fitness was reduced by 20% compared to a large control population maintained at 2000 individuals. Electrophoretic variation was significantly correlated with fitness across treatments, but the correlation of fitness to narrow-sense heritability of two morphometric traits was not significant.     

Evaluating Alternative Strategies for Minimizing Unintended Fitness Consequences of Cultured Individuals on Wild Populations

Artificial propagation strategies often incur selection in captivity that leads to traits that are maladaptive in the wild. For propagation programs focused on production rather than demographic contribution to wild populations, effects on wild populations can occur through unintentional escapement or the need to release individuals into natural environments for part of their life cycle. In this case, 2 alternative management strategies might reduce unintended fitness consequences on natural populations: (1) reduce selection in captivity as much as possible to reduce fitness load (keep them similar), or (2) breed a separate population to reduce captive‐wild interactions as much as possible (make them different). We quantitatively evaluate these 2 strategies with a coupled demographic–genetic model based on Pacific salmon hatcheries that incorporates a variety of relevant processes and dynamics: selection in the hatchery relative to the wild, assortative mating based on the trait under selection, and different life cycle arrangements in terms of hatchery release, density dependence, natural selection, and reproduction. Model results indicate that, if natural selection only occurs between reproduction and captive release, the similar strategy performs better. However, if natural selection occurs between captive release and reproduction, the different and similar strategies present viable alternatives to reducing unintended fitness consequences because of the greater opportunity to purge maladaptive individuals. In this case, the appropriate approach depends on the feasibility of each strategy and the demographic goal (e.g., increasing natural abundance, or ensuring that a high proportion of natural spawners are naturally produced). In addition, the fitness effects of hatchery release are much greater if hatchery release occurs before (vs. after) density‐dependent interactions. Given the logistical challenges to achieving both the similar and different strategies, evaluation of not just the preferred strategy but also the consequences of failing to achieve the desired target is critical. Evaluación de Estrategias Alternativas para Minimizar las Consecuencias No Inesperadas en la Adecuación de Individuos Criados en Cautiverio sobre Poblaciones Silvestres     

Effect of Migration or Inbreeding Followed by Selection on Low-Founder-Number Populations: Implications for Captive Breeding Programs

Using the housefly, Musca domestica (L), as a model system, we tested the ability of two extremes in the range of possible captive breeding protocols to yield sustainable populations following founding with low founder numbers. The protocols tested included two levels of migration as well as inbreeding followed by selection, each with appropriate controls. Each low-founder-number population was founded with two pairs of flies. The maximum migration scheme had 50% migration per generation, and the minimum migration populations experienced a migration rate of 2.5% per generation. The control level of migration was 0%. A fourth low-founder-number treatment was designed to test the effect of inbreeding followed by selection. Two sets of high-founder-number control groups were also derived from the stock population. Two fitness measures, viability and productivity of the populations, were recorded at the fifth generation. Populations in the minimum-migration and zero migration treatment groups had lower fitness than populations in any other treatment for both measures. Populations that experienced inbreeding and selection for high fitness levels, high levels of migration, or large high-founder-number populations were equally fit. These results demonstrate that a captive-breeding scheme that contains substantial levels of migration or inbreeding followed by selection can yield highly adapted populations.     

Selecting for Tolerance against Pathogens and Herbivores to Enhance Success of Reintroduction and Translocation

Abstract: Some species have insufficient defenses against climate change, emerging infectious diseases, and non‐native species because they have not been exposed to these factors over their evolutionary history, and this can decrease their likelihood of persistence. Captive breeding programs are sometimes used to reintroduce individuals back into the wild; however, successful captive breeding and reintroduction can be difficult because species or populations often cannot coexist with non‐native pathogens and herbivores without artificial selection. In captive breeding programs, breeders can select for host defenses that prevent or reduce pathogen or herbivore burden (i.e., resistance) or traits that limit the effects of parasitism or herbivory on host fitness (i.e., tolerance). We propose that selection for host tolerance may enhance the success of reintroduction or translocation because tolerant hosts generally have neutral effects on introduced pathogens and herbivores. The release of resistant hosts would have detrimental effects on their natural enemies, promoting rapid evolution to circumvent the host resistance that may reduce the long‐term probability of persistence of the reintroduced or translocated species. We examined 2 case studies, one on the pathogenic amphibian chytrid fungus ( Batrachochytrium dendrobatidis [Bd]) and the other on the herbivorous cactus moth ( Cactoblastis cactorum) in the United States, where it is not native. In each case study, we provide recommendations for how captive breeders and managers could go about selecting for host tolerance. Selecting for tolerance may offer a promising tool to rescue hosts species from invasive natural enemies as well as new natural enemies associated with climate change‐induced range shifts.     

Estimates of Natural Selection in a Salmon Population in Captive and Natural Environments

Abstract:  Captive breeding is a commonly used strategy for species conservation. One risk of captive breeding is domestication selection—selection for traits that are advantageous in captivity but deleterious in the wild. Domestication selection is of particular concern for species that are bred in captivity for many generations and that have a high potential to interbreed with wild populations. Domestication is understood conceptually at a broad level, but relatively little is known about how natural selection differs empirically between wild and captive environments. We used genetic parentage analysis to measure natural selection on time of migration, weight, and morphology for a coho salmon ( Oncorhynchus kisutch ) population that was subdivided into captive and natural components. Our goal was to determine whether natural selection acting on the traits we measured differed significantly between the captive and natural environments. For males, larger individuals were favored in both the captive and natural environments in all years of the study, indicating that selection on these traits in captivity was similar to that in the wild. For females, selection on weight was significantly stronger in the natural environment than in the captive environment in 1 year and similar in the 2 environments in 2 other years. In both environments, there was evidence of selection for later time of return for both males and females. Selection on measured traits other than weight and run timing was relatively weak. Our results are a concrete example of how estimates of natural selection during captivity can be used to evaluate this common risk of captive breeding programs.     

Linking Wild and Captive Populations to Maximize Species Persistence: Optimal Translocation Strategies

Abstract:  Captive breeding of animals is widely used to manage endangered species, frequently with the ambition of future reintroduction into the wild. Because this conservation measure is very expensive, we need to optimize decisions, such as when to capture wild animals or release captive-bred individuals into the wild. It is unlikely that one particular strategy will always work best; instead, we expect the best decision to depend on the number of individuals in the wild and in captivity. We constructed a first-order Markov-chain population model for two populations, one captive and one wild, and we used stochastic dynamic programming to identify optimal state-dependent strategies. The model recommends unique sequences of optimal management actions over several years. A robust rule of thumb for species that can increase faster in captivity than in the wild is to capture the entire wild population whenever the wild population is below a threshold size of 20 females. This rule applies even if the wild population is growing and under a broad range of different parameter values. Once a captive population is established, it should be maintained as a safety net and animals should be released only if the captive population is close to its carrying capacity. We illustrate the utility of this model by applying it to the Arabian oryx ( Oryx leucoryx ). The threshold for capturing the entire Arabian oryx population in the wild is 36 females, and captive-bred individuals should not be released before the captive facilities are at least 85% full.     

Relationship between Population Size and Fitness

Abstract:  Long-term effective population size, which determines rates of inbreeding, is correlated with population fitness. Fitness, in turn, influences population persistence. I synthesized data from the literature concerning the effects of population size on population fitness in natural populations of plants to determine how large populations must be to maintain levels of fitness that will provide adequate protection against environmental perturbations that can cause extinction. Integral to this comment on what has been done and what needs to be done, sThe evidence suggests that there is a linear relationship between log population size and population fitness over the range of population sizes examined. More importantly, populations will have to be maintained at sizes of >2000 individuals to maintain population fitness at levels compatible with the conservation goal of long-term persistence. This approach to estimating minimum viable population size provides estimates that are in general agreement with those from numerous other studies and strengthens the argument that conservation efforts should ultimately aim at maintaining populations of several thousand individuals to ensure long-term persistence.     

Phylogenetic Reanalysis of the Saudi Gazelle and Its Implications for Conservation

Abstract: The identification of taxonomically appropriate populations of endangered species for captive breeding and reintroduction programs is fundamental to the success of those programs. The Saudi gazelle (   Gazella saudiya ) was endemic to the Arabian peninsula but is now considered extinct in the wild and is potentially a candidate for captive breeding and reintroduction. Using 375 base pairs of mitochondrial DNA (mtDNA) cytochrome b gene derived from museum samples collected from the wild prior to the presumed extinction of this species, we show that G. saudiya is the sister taxon of the African dorcas gazelle (  G. dorcas ). Reciprocal monophyly of G. saudiya mtDNA haplotypes with G. dorcas , coupled with morphological distinctiveness, suggests that it is an evolutionarily significant unit. These data indicate that captive populations identified previously as potential sources of G. saudiya for captive breeding appear incorrectly designated and are irrelevant to the conservation of G. saudiya. The polymerase chain reaction–restriction fragment length polymorphism ( PCR-RFLP) analysis of several private collections of living gazelles in Saudi Arabia provides no evidence for the survival of G. saudiya. We recommend that field surveys be undertaken to establish whether G. saudiya is indeed extinct in the wild and that other private collections within the Arabian peninsula be screened genetically. We urge caution when captive animals of unknown provenance are used to investigate the phylogenetics of cryptic species groups.     

Longitudinal monitoring of neutral and adaptive genomic diversity in a reintroduction

Restoration programs in the form of ex-situ breeding combined with reintroductions are becoming critical to counteract demographic declines and species losses. Such programs are increasingly using genetic management to improve conservation outcomes. However, the lack of long-term monitoring of genetic indicators following reintroduction prevents assessments of the trajectory and persistence of reintroduced populations. We carried out an extensive monitoring program in the wild for a threatened small-bodied fish (southern pygmy perch, Nannoperca australis) to assess the long-term genomic effects of its captive breeding and reintroduction. The species was rescued prior to its extirpation from the terminal lakes of Australia's Murray-Darling Basin, and then used for genetically informed captive breeding and reintroductions. Subsequent annual or biannual monitoring of abundance, fitness, and occupancy over a period of 11 years, combined with postreintroduction genetic sampling, revealed survival and recruitment of reintroduced fish. Genomic analyses based on data from the original wild rescued, captive born, and reintroduced cohorts revealed low inbreeding and strong maintenance of neutral and candidate adaptive genomic diversity across multiple generations. An increasing trend in the effective population size of the reintroduced population was consistent with field monitoring data in demonstrating successful re-establishment of the species. This provides a rare empirical example that the adaptive potential of a locally extinct population can be maintained during genetically informed ex-situ conservation breeding and reintroduction into the wild. Strategies to improve biodiversity restoration via ex-situ conservation should include genetic-based captive breeding and longitudinal monitoring of standing genomic variation in reintroduced populations.     

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.     

Modeling Problems in Conservation Genetics Using Captive Drosophila Populations: Consequences of Equalization of Family Sizes

Equalization of family sizes is recommended for use in captive breeding programs, as it is predicted to double effective population sizes, reduce inbreeding, and slow the loss of genetic variation. The effects of maintaining small captive populations with equalization of family sizes versus random choice of parents on levels of inbreeding genetic variation, reproductive fitness, and effective population sizes ( N _e) were evaluated in 10 lines of each treatment maintained with four pairs of parents per generation. The mean inbreeding coefficient ( F ) increased at a significantly slower rate with equalization than with random choice (means of 0.35 and 0.44 at generation 10). Average heterozygosities at generation 10, based on six polymorphic enzyme loci, were significantly higher with equalization (0.149) than with random choice (0.085), compared to the generation 0 level of 0.188. The competitive index measure of reproductive fitness at generation 11 was more than twice as high with equalization as with random choice, both being much lower than in the outbred base population. There was considerable variation among replicate lines within treatments in all the above measures and considerable overlap between lines from the two treatments. Estimates of N _e for equalization were greater than those for random choice, whether estimated from changes in average heterozygosities or from changes in F. Equalization of family sizes can be unequivocally recommended for use in the genetic management of captive populations.     

Double Allee Effects and Extinction in the Island Fox

Abstract:  An Allee effect (AE) occurs in populations when individuals suffer a decrease in fitness at low densities. If a fitness component is reduced (component AE), per capita population growth rates may decline as a consequence (demographic AE) and extinction risk is increased. The island fox ( Urocyon littoralis ) is endemic to six of the eight California Channel Islands. Population crashes have coincided with an increase in predation by Golden Eagles ( Aquila chrysaetos ). We propose that AEs could render fox populations more sensitive and may be a likely explanation for their sharp decline. We analyzed demographic data collected between 1988 and 2000 to test whether fox density (1) influences survival and reproductive rates; (2) interacts with eagle presence and affects fox fitness parameters; and (3) influences per capita fox population trends. A double component AE simultaneously influenced survival (of adults and pups) and proportion of breeding adult females. The adult survival AE was driven by predation by eagles. These component AEs led to a demographic AE. Multiple-component AEs, a predation-driven AE, and the simultaneous occurrence of both component and demographic AEs in a mammal are all previously unreported processes. Populations below 7 foxes/km² could have suboptimal population growth rates due to the demographic AE, and AEs may have contributed to the dramatic declines in three fox populations. Because fox densities in critically endangered populations are well below this level, removing Golden Eagles appears necessary to prevent a predation-driven AE. Conservationists should also be aware of AEs when planning the release of captive foxes. More generally, our findings highlight the danger of overlooking AEs in the conservation of populations of rare or threatened species.     

Effective Population Size and Maintenance of Genetic Diversity in Captive-Bred Populations of a Lake Victoria Cichlid

Abstract: We used microsatellite DNA markers to investigate the maintenance of genetic diversity within and between samples of subpopulations (spanning five captive-bred generations) of the haplochromine cichlid Prognathochromis perrieri . The subpopulations are maintained as part of the Lake Victoria Cichlid species survival plan. Changes in the frequencies of 24 alleles, over four polymorphic loci, were used to estimate effective population size (   N _e   ). Point estimates of N _e ranged from 2.5 to 7.7 individuals and were significantly smaller than the actual census size (   N _obs  ) for all subpopulations (32–243 individuals per generation), with the corresponding conservative N _e   /  N _obs ratios ranging from 0.01 to 0.12. Approximately 19% of the initial alleles were lost within the first four generations of captive breeding. Between-generation comparisons of expected heterozygosity showed significant losses ranging from 6% to 12% per generation. Seven private alleles were observed in the last sampled generation of four subpopulations, and analysis of population structure by F _ST indicated that approximately 33% of the total genetic diversity is maintained between the subpopulations from different institutions. To reduce the loss of genetic variation, we recommend that offspring production be equalized by periodically removing dominant males, which will encourage reproduction by additional males. Consideration should also be given to encouraging more institutions to maintain populations, because a significant fraction of the genetic variation exists as among-population differences resulting from random differentiation among subpopulations.     

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.     

Rapid Loss of Genetic Variation in Large Captive Populations of Drosophila Flies: Implications for the Genetic Management of Captive Populations

Levels of variation in eight large captive populations of D. melanogaster (census sizes ∼ 5000) that had been in captivity for periods from 6 months to 23 years (8 to 365 generations) were estimated from allozyme heterozygosities, lethal frequencies, and inversion heterozygosities and phenotypic variances, additive genetic variances ( V _A), and heritabilities ( h ²) for sternopleural bristle numbers. Correlations between all measures of variation except lethal frequencies were high and significant. All measures of genetic variation declined with time in captivity, with those for average heterozygosities, V _A, and h ² being significant. The effective population size ( N _e) was estimated to be 185–253 in these populations, only 0.037–0.051 of census size (N). Levels of allozyme heterozygosities declined rapidly in two large captive populations founded from another wild stock, being reduced by 86% and 62% within 2.5 years in spite of being maintained at sizes of approximately 1000 and 3500. Estimates of N _e/ N for these populations were only 0.016 and 0.004. Two estimates of N _e/ N for captive populations of D. pseudoobscura from data in the literature were also low at 0.036 and 0.012. Consequently, the rate of loss of genetic variation in captive populations and endangered species may be more rapid than hitherto recognized. Merely maintaining captive populations at large census sizes may not be sufficient to maintain essential genetic variation.     

Long-term demographic and genetic effects of releasing captive-born individuals into the wild

Because of continued habitat destruction and species extirpations, the need to use captive breeding for conservation purposes has been increasing steadily. However, the long-term demographic and genetic effects associated with releasing captive-born individuals with varied life histories into the wild remain largely unknown. To address this question, we developed forward-time, agent-based models for 4 species with long-running captive-breeding and release programs: coho salmon (Oncorhynchus kisutch), golden lion tamarin (Leontopithecus rosalia), western toad (Anaxyrus boreas), and Whooping Crane (Grus americana). We measured the effects of supplementation by comparing population size and neutral genetic diversity in supplemented populations to the same characteristics in unaltered populations 100 years after supplementation ended. Releasing even slightly less fit captive-born individuals to supplement wild populations typically resulted in reductions in population sizes and genetic diversity over the long term when the fitness reductions were heritable (i.e., due to genetic adaptation to captivity) and populations continued to be regulated by density-dependent mechanisms over time. Negative effects for species with longer life spans and lower rates of population replacement were smaller than for species with shorter life spans and higher rates of population replacement. Programs that released captive-born individuals over fewer years or that avoided breeding individuals with captive ancestry had smaller reductions in population size and genetic diversity over the long term. Relying on selection in the wild to remove individuals with reduced fitness mitigated some negative demographic effects, but at a substantial cost to neutral genetic diversity. Our results suggest that conservation-focused captive-breeding programs should take measures to prevent even small amounts of genetic adaptation to captivity, quantitatively determine the minimum number of captive-born individuals to release each year, and fully account for the interactions among genetic adaptation to captivity, population regulation, and life-history variation.     

Risk Assessment of Inbreeding and Outbreeding Depression in a Captive‐Breeding Program

Captive‐breeding programs can be implemented to preserve the genetic diversity of endangered populations such that the controlled release of captive‐bred individuals into the wild may promote recovery. A common difficulty, however, is that programs are founded with limited wild broodstock, and inbreeding can become increasingly difficult to avoid with successive generations in captivity. Program managers must choose between maintaining the genetic purity of populations, at the risk of inbreeding depression, or interbreeding populations, at the risk of outbreeding depression. We evaluate these relative risks in a captive‐breeding program for 3 endangered populations of Atlantic salmon (Salmo salar). In each of 2 years, we released juvenile F₁ and F₂ interpopulation hybrids, backcrosses, as well as inbred and noninbred within‐population crosstypes into 9 wild streams. Juvenile size and survival was quantified in each year. Few crosstype effects were observed, but interestingly, the relative fitness consequences of inbreeding and outbreeding varied from year to year. Temporal variation in environmental quality might have driven some of these annual differences, by exacerbating the importance of maternal effects on juvenile fitness in a year of low environmental quality and by affecting the severity of inbreeding depression differently in different years. Nonetheless, inbreeding was more consistently associated with a negative effect on fitness, whereas the consequences of outbreeding were less predictable. Considering the challenges associated with a sound risk assessment in the wild and given that the effect of inbreeding on fitness is relatively predictable, we suggest that risk can be weighted more strongly in terms of the probable outcome of outbreeding. Factors such as genetic similarities between populations and the number of generations in isolation can sometimes be used to assess outbreeding risk, in lieu of experimentation. Evaluación del Riesgo de Depresión por Endogamia y Exogamia en un Programa de Reproducción en Cautiverio     

Increased Infectious Disease Susceptibility Resulting from Outbreeding Depression

Abstract:  The mechanisms by which outbreeding depression leads to reduced fitness are poorly understood. We considered the hypothesis that outbreeding can depress fitness by increasing the susceptibility of hybrid individuals and populations to infectious disease. Competitive breeding trials in experimental ponds indicated that outbred largemouth bass (  Micropterus salmoides ) crossed from two geographically and genetically distinct populations suffered a reduction in fitness of approximately 14% relative to parental stocks. We measured the comparative susceptibility of these same outbred stocks to a novel viral pathogen, largemouth bass virus. Following experimental inoculation, F2 generation hybrids suffered mortality at a rate 3.6 times higher than either F1 generation hybrids or wild-type parental fish. Analysis of viral loads indicated that viral replication was more rapid in F2 fish than in F1 hybrids or wild-type parental fish. We attribute these results to the disruption of coadapted gene complexes in the immune systems of outbred fish in the F2 generation. Increased susceptibility to infectious disease may be an important but underappreciated mechanism by which outbreeding reduces the fitness of individuals and populations and by which novel infectious diseases emerge in populations of hybrid organisms.