Reduced genetic diversity and significant genetic differentiation after translocation: Comparison of the remnant and translocated populations of bridled nailtail wallabies (Onychogalea fraenata)

Loss of genetic diversity and increased population differentiation from source populations are common problems associated with translocation programmes established from captive-bred stock or a small number of founders. The bridled nailtail wallaby is one of the most endangered macropods in Australia, having been reduced to a single remnant population in the last 100 years. A translocated population of bridled nailtail wallabies was established using animals sourced directly from the remnant population (wild-released) as well as the progeny of animals collected for a captive breeding programme (captive-bred). The aims of this study were to compare genetic diversity among released animals and their wild-born progeny to genetic diversity observed in the remnant population, and to monitor changes in genetic diversity over time as more animals were released into the population. Heterozygosity did not differ between the translocated and remnant population; however, allelic diversity was significantly reduced across all released animals and their wild-born progeny. Animals bred in captivity and their wild-born progeny were also significantly differentiated from the source population after just four generations. Wild-released animals, however, were representative of the source population and several alleles were unique to this group. Both heterozygosity and allelic diversity among translocated animals decreased over time with the additional release of captive-bred animals, as no new genetic stock was added to the population. Captive breeding programmes can provide large numbers of animals for release, but this study highlights the importance of sourcing animals directly from remnant populations in order to maintain genetic diversity and minimise genetic drift.     

Multi-generational evaluation of genetic diversity and parentage in captive southern pygmy perch (<Emphasis Type="Italic">Nannoperca australis</Emphasis>)

Maintaining genetic diversity within captive breeding populations is a key challenge for conservation managers. We applied a multi-generational genetic approach to the captive breeding program of an endangered Australian freshwater fish, the southern pygmy perch (Nannoperca australis). During previous work, fish from the lower Murray-Darling Basin were rescued before drought exacerbated by irrigation resulted in local extinction. This endemic lineage of the species was captive-bred in genetically designed groups, and equal numbers of F1 individuals were reintroduced to the wild with the return of favourable habitat. Here, we implemented a contingency plan by continuing the genetic-based captive breeding in the event that a self-sustaining wild population was not established. F1 individuals were available as putative breeders from the subset of groups that produced an excess of fish in the original restoration program. We used microsatellite-based parentage analyses of these F1 fish to form breeding groups that minimized inbreeding. We assessed their subsequent parental contribution to F2 individuals and the maintenance of genetic diversity. We found skewed parental contribution to F2 individuals, yet minimal loss of genetic diversity from their parents. However, the diversity was substantially less than that of the original rescued population. We attribute this to the unavoidable use of F1 individuals from a limited number of the original breeding groups. Alternative genetic sources for supplementation or reintroduction should be assessed to determine their suitability. The genetic fate of the captive-bred population highlights the strong need to integrate DNA-based tools for monitoring and adaptive management of captive breeding programs.     

Characteristics of reproductive biology and proximate factors regulating seasonal breeding in captive golden-headed lion tamarins (Leontopithecus chrysomelas)

Reproduction is highly demanding in terms of energy expenditure, and the costs and benefits associated with postponing or investing in a reproductive effort are crucial determinants of an individual's fitness. Understanding the reproductive potential of a species under varying ecological conditions offers important insights into the dynamics of its social system. This study provides the first detailed analysis of the reproductive potential of wild- and captive-born golden-headed lion tamarins (Leontopithecus chrysomelas) under captive conditions, based on studbook data compiled during 1984-2000. Litters produced by wild-born females breeding in captivity are similar in size to litters observed in the wild, but smaller than litters of captive-born females. The more stringent ecological conditions experienced by wild-born females during maturation may result in a lifelong effect on litter size. However, interbirth intervals are shorter for wild-born than captive-born females. The relatively smaller burden of infant care that results from having smaller litters may allow wild-born females to sustain the next pregnancy sooner. Reproduction in the Brazilian captive population is highly seasonal for both wild-born females and females born in captivity in Brazil. Changes in photoperiod over a year provide a proximate explanation for changes in the proportion of conceptions and births per month. Outside Brazil, breeding occurs year-round, and no clear birth peak is apparent. Information from field reports that could be used to relate this finding to ecological factors, such as resource availability, is unavailable.     

Effective size of a wild salmonid population is greatly reduced by hatchery supplementation

Many declining and commercially important populations are supplemented with captive-born individuals that are intentionally released into the wild. These supplementation programs often create large numbers of offspring from relatively few breeding adults, which can have substantial population-level effects. We examined the genetic effects of supplementation on a wild population of steelhead (Oncorhynchus mykiss) from the Hood River, Oregon, by matching 12 run-years of hatchery steelhead back to their broodstock parents. We show that the effective number of breeders producing the hatchery fish (broodstock parents; N(b)) was quite small (harmonic mean N(b)=25 fish per brood-year vs 373 for wild fish), and was exacerbated by a high variance in broodstock reproductive success among individuals within years. The low N(b) caused hatchery fish to have decreased allelic richness, increased average relatedness, more loci in linkage disequilibrium and substantial levels of genetic drift in comparison with their wild-born counterparts. We also documented a substantial Ryman-Laikre effect whereby the additional hatchery fish doubled the total number of adult fish on the spawning grounds each year, but cut the effective population size of the total population (wild and hatchery fish combined) by nearly two-thirds. We further demonstrate that the Ryman-Laikre effect is most severe in this population when (1) >10% of fish allowed onto spawning grounds are from hatcheries and (2) the hatchery fish have high reproductive success in the wild. These results emphasize the trade-offs that arise when supplementation programs attempt to balance disparate goals (increasing production while maintaining genetic diversity and fitness).     

Reassessing the relationship between juvenile mortality and genetic monomorphism in captive cheetahs

Low levels of genetic heterozygosity are commonly considered a major threat to the survival of wild and captive populations. However, intense focus on genetic issues may obscure the importance of extrinsic factors influencing species' survival in wild and captive environments. A key example for this is the cheetah (Acinonyx jubatus), which is frequently cited as suffering from unusually high juvenile mortality and decreased fecundity in captivity due to genetic monomorphism at the species level. It has also been suggested that as a consequence of such extreme homozygosity, juvenile mortality rates of young from related vs. unrelated parents would not be expected to differ significantly. However, examination of current studbook data and breeding records of the North American captive population showed that juvenile mortality of young from related parents was significantly higher than that of young from unrelated parents, largely as a result of intrinsic causes, such as stillbirths and congenital defects, that may have a genetic basis. This indicates that in spite of the cheetah's homozygosity, effects of further inbreeding depression may still occur in the captive population, and deleterious recessive alleles are being segregated. Furthermore, juvenile mortality has declined over time and differs significantly among facilities, even when only young from unrelated parents are considered, suggesting that differences in management practices may be largely responsible for observed changes in mortality rate. Contrary to previous reports, cheetah juvenile mortality is not unusually high when compared to other captive-bred felids. In addition, cheetahs were found to have consistently higher litter sizes and the highest average number of surviving cubs per litter when compared to other captive-bred felid species. These findings cast doubt on the significance of overall homozygosity in this species for its juvenile survival and breeding performance and emphasize the key role of management practice in promoting breeding of endangered species. © 1996 Wiley-Liss. Inc.     

The efficiency of close inbreeding to reduce genetic adaptation to captivity

Although ex situ conservation is indispensable for thousands of species, captive breeding is associated with negative genetic changes: loss of genetic variance and genetic adaptation to captivity that is deleterious in the wild. We used quantitative genetic individual-based simulations to model the effect of genetic management on the evolution of a quantitative trait and the associated fitness of wild-born individuals that are brought to captivity. We also examined the feasibility of the breeding strategies under a scenario of a large number of loci subject to deleterious mutations. We compared two breeding strategies: repeated half-sib mating and a method of minimizing mean coancestry (referred to as gc/mc). Our major finding was that half-sib mating is more effective in reducing genetic adaptation to captivity than the gc/mc method. Moreover, half-sib mating retains larger allelic and adaptive genetic variance. Relative to initial standing variation, the additive variance of the quantitative trait increased under half-sib mating during the sojourn in captivity. Although fragmentation into smaller populations improves the efficiency of the gc/mc method, half-sib mating still performs better in the scenarios tested. Half-sib mating shows two caveats that could mitigate its beneficial effects: low heterozygosity and high risk of extinction when populations are of low fecundity and size and one of the following conditions are met: (i) the strength of selection in captivity is comparable with that in the wild, (ii) deleterious mutations are numerous and only slightly deleterious. Experimental validation of half-sib mating is therefore needed for the advancement of captive breeding programs.     

A species in decline: genetic diversity and conservation of the Victorian eastern barred bandicoot, Perameles gunnii

The eastern barred bandicoot, Perameles gunnii, has undergone a dramatic decline in distribution and abundance on the mainland of Australia during the twentieth century. In 1988 a captive breeding program was initiated to reduce the chance of extinction. With the extinction of the last wild mainland population in the early 1990s, reintroductions from captive-bred P. gunnii have met limited success, and currently only two extant populations persist in predator proof enclosures in the State of Victoria. With ~20 years of breeding, there are concerns that the genetic diversity within the breeding program has declined and may inhibit current and future success of the program. We have used ten nuclear microsatellite loci and sequencing of two partial mitochondrial genes (cytochrome oxidase I and ATPase 6) to determine genetic diversity within current Victorian P. gunnii. These diversity estimates are compared with historic samples from the captive breeding program dating back to 1995, historic samples from the last wild mainland population found at Hamilton in 1992 and contemporary Tasmanian wild populations. Results indicate that the captive P. gunnii population in the State of Victoria has lost significant genetic diversity through time. Genetic diversity is also reduced in populations at Hamilton Community Parklands and Mount Rothwell. Samples from the last wild population at Hamilton collected in 1992, along with samples from Tasmanian P. gunnii, had significantly greater genetic diversity than contemporary mainland populations. The results are discussed with reference to management options for maintaining genetic diversity within Victorian P. gunnii, including crossing Victorian and Tasmanian P. gunnii to increase genetic diversity, adaptability and evolutionary potential.     

Modeling problems in conservation genetics using captive Drosophila populations: Rapid genetic adaptation to captivity

Long-term captive breeding programs for endangered species generally aim to preserve the option of release back into the wild. However, the success of re-release programs will be jeopardized if there is significant genetic adaptation to the captive environment. Since it is difficult to study this problem in rare and endangered species, a convenient laboratory animal model is required. The reproductive fitness of a large population of Drosophila melanogaster maintained in captivity for 12 months was compared with that of a recently caught wild population from the same locality. The competitive index measure of reproductive fitness for the captive population was twice that of the recently caught wild population, the difference being highly significant. Natural selection over approximately eight generations in captivity has caused rapid genetic adaptation. Captive breeding strategies for endangered species should minimize adaptation to captivity in populations destined for reintroduction into the wild. A framework for predicting the impact of factors on the rate of genetic adaptation to captivity is suggested. Equalization of family sizes is predicted to approximately halve the rate of genetic adaptation. Introduction of genes from the wild, increasing the generation interval, using captive environments close to those in the wild and achieving low mortality rates are all expected to slow genetic adaptation to captivity. Many of these procedures are already recommended for other reasons. © 1992 Wiley-Liss, Inc.     

Rapid genetic deterioration in captive populations: Causes and conservation implications

Many species require captive breeding to ensuretheir survival. The eventual aim of suchprograms is usually to reintroduce the speciesinto the wild. Populations in captivitydeteriorate due to inbreeding depression, lossof genetic diversity, accumulation of newdeleterious mutations and genetic adaptationsto captivity that are deleterious in the wild.However, there is little evidence on themagnitude of these problems. We evaluatedchanges in reproductive fitness in populationsof Drosophila maintained under benigncaptive conditions for 50 generations witheffective population sizes of 500 (2replicates), 250 (3), 100 (4), 50 (6) and 25(8). At generation 50, fitness in the benigncaptive conditions was reduced in smallpopulations due to inbreeding depression andincreased in some of the large populations dueto modest genetic adaptation. When thepopulations were moved to `wild' conditions,all 23 populations showed a marked decline(64–86%percnt;) in reproductive fitness compared tocontrols. Reproductive fitness showed acurvilinear relationship with population size,the largest and smallest population sizetreatments being the worst. Genetic analysesindicated that inbreeding depression andgenetic adaptation were responsible for thegenetic deterioration in `wild' fitness.Consequently, genetic deterioration incaptivity is likely to be a major problem whenlong-term captive bred populations ofendangered species are returned to the wild. Aregime involving fragmentation of captivepopulations of endangered species is suggestedto minimize the problems.     

Assortative mating among animals of captive and wild origin following experimental conservation releases

Captive breeding is a high profile management tool used for conserving threatened species. However, the inevitable consequence of generations in captivity is broad scale and often-rapid phenotypic divergence between captive and wild individuals, through environmental differences and genetic processes. Although poorly understood, mate choice preference is one of the changes that may occur in captivity that could have important implications for the reintroduction success of captive-bred animals. We bred wild-caught house mice for three generations to examine mating patterns and reproductive outcomes when these animals were simultaneously released into multiple outdoor enclosures with wild conspecifics. At release, there were significant differences in phenotypic (e.g. body mass) and genetic measures (e.g. G_st and F) between captive-bred and wild adult mice. Furthermore, 83% of offspring produced post-release were of same source parentage, inferring pronounced assortative mating. Our findings suggest that captive breeding may affect mating preferences, with potentially adverse implications for the success of threatened species reintroduction programmes.     

Patterns of genetic diversity of mitochondrial DNA within captive populations of the endangered itasenpara bitterling: implications for a reintroduction program

In this study, the level of genetic diversity of captive populations of the itasenpara bitterling (Acheilognathus longipinnis) was assessed to obtain information useful for successful captive breeding and reintroduction; this analysis was performed using mitochondrial DNA (mtDNA) sequence data. Comparison of the captive and wild populations showed low levels of genetic diversity within the captive population and significant genetic differentiation among the captive populations and also between the wild and captive populations, suggesting at chance effect during the founding process for the captive population and a subsequent genetic drift. Therefore, for successful reintroduction, it is important that the reintroduced population reflects all the genetic diversity available from the captive populations, and that releasing a large number of individuals that consist of all captive populations.     

Very Low Population Structure in a Highly Mobile and Wide-Ranging Endangered Bird Species

The loss of biodiversity following fragmentation and degradation of habitat is a major issue in conservation biology. As competition for resources increases following habitat loss and fragmentation, severe population declines may occur even in common, highly mobile species; such demographic decline may cause changes within the population structure of the species. The regent honeyeater, Anthochaera phrygia, is a highly nomadic woodland bird once common in its native southeast Australia. It has experienced a sharp decline in abundance since the late 1970s, following clearing of large areas of its preferred habitat, box-ironbark woodland, within the last 200 years. A captive breeding program has been established as part of efforts to restore this species. This study used genetic data to examine the range-wide population structure of regent honeyeaters, including spatial structure, its change through time, sex differences in philopatry and mobility, and genetic differences between the captive and wild populations. There was low genetic differentiation between birds captured in different geographic areas. Despite the recent demographic decline, low spatial structure appears to have some temporal consistency. Both sexes appear to be highly mobile, and there does not seem to be significant genetic differentiation between the captive and wild populations. We conclude that management efforts for survival of this species, including habitat protection, restoration, and release of captive-bred birds into the wild, can treat the species as effectively a single genetic population.     

The Genetic Integrity of the Ex Situ Population of the European Wildcat (Felis silvestris silvestris) Is Seriously Threatened by Introgression from Domestic Cats (Felis silvestris catus)

Studies on the genetic diversity and relatedness of zoo populations are crucial for implementing successful breeding programmes. The European wildcat, Felis s. silvestris, is subject to intensive conservation measures, including captive breeding and reintroduction. We here present the first systematic genetic analysis of the captive population of Felis s. silvestris in comparison with a natural wild population. We used microsatellites and mtDNA sequencing to assess genetic diversity, structure and integrity of the ex situ population. Our results show that the ex situ population of the European wildcat is highly structured and that it has a higher genetic diversity than the studied wild population. Some genetic clusters matched the breeding lines of certain zoos or groups of zoos that often exchanged individuals. Two mitochondrial haplotype groups were detected in the in situ populations, one of which was closely related to the most common haplotype found in domestic cats, suggesting past introgression in the wild. Although native haplotypes were also found in the captive population, the majority (68%) of captive individuals shared a common mtDNA haplotype with the domestic cat (Felis s. catus). Only six captive individuals (7.7%) were assigned as wildcats in the STRUCTURE analysis (at K = 2), two of which had domestic cat mtDNA haplotypes and only two captive individuals were assigned as purebred wildcats by NewHybrids. These results suggest that the high genetic diversity of the captive population has been caused by admixture with domestic cats. Therefore, the captive population cannot be recommended for further breeding and reintroduction.     

Amphibians: suitable candidates for breeding-release programmes

Zoological parks are playing an increasingly important role in the management of threatened species through education, the maintenance of captive gene banks and the reintroduction of captive-bred animals into the wild. This paper discusses the suitability of amphibian species for reintroduction. The important features of amphibians for these programmes are highlighted, i.e., their high fecundity to allow rapid build-up of captive populations coupled with few behavioural problems with captive-bred animals, as well as the low cost of maintenance. The potential problems of inbreeding, poor retention of innate behavioural repertoires after multiple generation captive breeding, and the introduction of alien pathogens into wild populations are considered. Release programmes for two species, the Mallorcan midwife toad Alytes muletensis and the Puerto Rican crested toad Peltophryne lemur, are reviewed.     

Genetic diversity in wild and reared populations of the Japanese bitterling <Emphasis Type="Italic">Tanakia tanago</Emphasis> (Cyprinidae)

 The Japanese bitterling Tanakia tanago is an endangered cyprinid species; thus, captive breeding programs are being conducted in various facilities as ex situ conservation. To examine the genetic diversity in one wild and three reared populations, and its changes during the process of captive breeding, sequences of the mitochondrial cytochrome b gene and control region were determined. The wild population, collected in 1993, was monomorphic. Although the reared population that originated from the wild population was almost monomorphic, a rare haplotype, distinct from all others by a relatively large sequence divergence, was also observed. In the other reared populations, some degree of genetic diversity had been maintained. A reared hybrid population, which originated from a mixture of three distinct populations, showed the greatest genetic diversity. These results suggest considerable genetic diversity within and among populations of T. tanago in the past. Although a loss of genetic diversity was observed in some year-classes of reared populations, there was no tendency for genetic diversity to decrease as a result of captive breeding, probably because offspring were obtained from multi-year-class parents in the captive breeding program. Accordingly, this breeding method should be appropriate for conserving the genetic diversity of T. tanago. Received: June 12, 2002 / Revised: December 3, 2002 / Accepted: December 16, 2002     

Population Genetics and the Effects of a Severe Bottleneck in an Ex Situ Population of Critically Endangered Hawaiian Tree Snails

As wild populations decline, ex situ propagation provides a potential bank of genetic diversity and a hedge against extinction. These programs are unlikely to succeed if captive populations do not recover from the severe bottleneck imposed when they are founded with a limited number of individuals from remnant populations. In small captive populations allelic richness may be lost due to genetic drift, leading to a decline in fitness. Wild populations of the Hawaiian tree snail Achatinella lila, a hermaphroditic snail with a long life history, have declined precipitously due to introduced predators and other human impacts. A captive population initially thrived after its founding with seven snails, exceeding 600 captive individuals in 2009, but drastically declined in the last five years. Measures of fitness were examined from 2,018 captive snails that died between 1998 and 2012, and compared with genotypic data for six microsatellite loci from a subset of these deceased snails (N = 335), as well as live captive snails (N = 198) and wild snails (N = 92). Surprisingly, the inbreeding coefficient (F_is) declined over time in the captive population, and is now approaching values observed in the 2013 wild population, despite a significant decrease in allelic richness. However, adult annual survival and fecundity significantly declined in the second generation. These measures of fitness were positively correlated with heterozygosity. Snails with higher measures of heterozygosity had more offspring, and third generation offspring with higher measures of heterozygosity were more likely to reach maturity. These results highlight the importance of maintaining genetic diversity in captive populations, particularly those initiated with a small number of individuals from wild remnant populations. Genetic rescue may allow for an increase in genetic diversity in the captive population, as measures of heterozygosity and rarified allelic richness were higher in wild tree snails.     

Evidence for African origins of founders of the asiatic lion species survival plan

The Asiatic lion (Panthera leo persica) exists in the wild as a single relict population of approximately 250 individuals in the protected Gir Forest Sanctuary in western India. In 1981, a species survival plan (SSP) for the Asiatic lion was established by the American Association of Zoological Parks and Aquariums to manage the 200 + descendants of Asiatic lions in captivity in western zoological facilities. This captive population was derived from seven founders. In order to compare the genetic structure of the Gir Forest population with that of the captive SSP population, a genetic survey of 46 electrophoretic allozyme systems resolved from extracts of lion blood was undertaken by using 29 SSP Asiatic lions and 28 wild-caught or captive-bred lions maintained at the Sakkarbaug Zoo in India but originally derived from the Gir Forest. The Gir lion population was found to be genetically monomorphic at each of 46 allozyme loci. This was in contrast to several African lion (Panthera leo leo) populations, which show moderate levels of allozyme variation at the same loci. The SSP lion population was polymorphic at three allozyme loci (IDHI, TF, and PTI) for alleles that were previously found only in African lion populations. Pedigree analysis of the genetic transmission of these three biochemical loci demonstrated that two of the five primary founder animals of the SSP Asiatic lion population (a breeding pair originally imported from the Trivandrum Zoo in southern India) were descendants of the African subspecies. Three other founder animals were pure Asian. A retrospective SSP pedigree analysis of two morphologic characters (prominent abdominal fold and pairing of infraorbital foramen) that are partially diagnostic for persica vs leo was consistent with this conclusion as well. The implications for the management of small captive populations of threatened species and of the Asiatic lion SSP population are discussed.     

Genetic characterization of wild and captive rhesus macaques in China

The genetic structures of wild and captive rhesus macaque populations within China were compared by analyzing the mtDNA sequences of 203 captive-bred Chinese rhesus macaques with 77 GenBank sequences from wild-caught animals trapped throughout China. The genotypes of 22 microsatellites of captive Chinese rhesus macaques were also compared with those of captive Indian animals. The Chinese population is significantly differentiated from the Indian population and is more heterogeneous. Thus, compared with Indian rhesus macaques the phenotypic variance of traits with high heritability will be inflated in Chinese animals. Our data suggest that the western Chinese provinces have more subdivided populations than the eastern and southern Chinese provinces. The southern Chinese populations are the least structured and might have been more recently established. Human-mediated interbreeding among captive Chinese populations has occurred, implying that Chinese breeding strategies can influence the interpretation of biomedical research in the USA.     

Genetic admixture between captive-bred and wild individuals affects patterns of dispersal in a brown trout (<Emphasis Type="Italic">Salmo trutta</Emphasis>) population

Genetic admixture between captive-bred and wild individuals has been demonstrated to affect many individual traits, although little is known about its potential influence on dispersal, an important trait governing the eco-evolutionary dynamics of populations. Here, we quantified and described the spatial distribution of genetic admixture in a brown trout (Salmo trutta) population from a small watershed that was stocked until 1999, and then tested whether or not individual dispersal parameters were related to admixture between wild and captive-bred fish. We genotyped 715 fish at 17 microsatellite loci sampled from both the mainstream and all populated tributaries, as well as 48 fish from the hatchery used to stock the study area. First, we used Bayesian clustering to infer local genetic structure and to quantify genetic admixture. We inferred first generation migrants to identify dispersal events and test which features (genetic admixture, sex and body length) affected dispersal parameters (i.e. probability to disperse, distance of dispersal and direction of the dispersal event). We identified two genetic clusters in the river basin, corresponding to wild fish on the one hand and to fish derived from the captive strain on the other hand, allowing us to define an individual gradient of admixture. Individuals with a strong assignment to the captive strain occurred almost exclusively in some tributaries, and were more likely to disperse towards a tributary than towards a site of the mainstream. Furthermore, dispersal probability increased as the probability of assignment to the captive strain increased, and individuals with an intermediate level of admixture exhibited the lowest dispersal distances. These findings show that various dispersal parameters may be biased by admixture with captive-bred genotypes, and that management policies should take into account the differential spread of captive-bred individuals in wild populations.