Evaluation of the genetic management of the endangered black‐footed ferret (Mustela nigripes)

Empirical support for the genetic management strategies employed by captive breeding and reintroduction programs is scarce. We evaluated the genetic management plan for the highly endangered black‐footed ferret (Mustela nigripes) developed by the American Zoo and Aquarium Associations (AZA) as a part of the species survival plan (SSP). We contrasted data collected from five microsatellite loci to predictions from a pedigree‐based kinship matrix analysis of the captive black‐footed ferret population. We compared genetic diversity among captive populations managed for continued captive breeding or reintroduction, and among wild‐born individuals from two reintroduced populations. Microsatellite data gave an accurate but only moderately precise estimate of heterozygosity. Genetic diversity was similar in captive populations maintained for breeding and release, and it appears that the recovery program will achieve its goal of maintaining 80% of the genetic diversity of the founder population over 25 years. Wild‐born individuals from reintroduced populations maintained genetic diversity and avoided close inbreeding. We detected small but measurable genetic differentiation between the reintroduced populations. The model of random mating predicted only slightly lower levels of heterozygosity retention compared to the SSP strategy. The random mating strategy may be a viable alternative for managing large, stable, captive populations such as that of the black‐footed ferret. Zoo Biol 22:287–298, 2003. © 2003 Wiley‐Liss, Inc.     

Estimating the prevalence of inbreeding from incomplete pedigrees

A previous review of inbreeding in natural populations suggested that close inbreeding (inbreeding coefficient f = 0.25) is generally rare in wild birds and mammals. However, the review did not assess rates of moderate inbreeding (f = 0.125), which may make a rather larger contribution to overall inbreeding in a population. Furthermore, previous studies may have underestimated the prevalence of inbreeding in wild populations with incomplete pedigrees. By categorizing inbreeding events by the relationship of the parental pair, we suggest a simple method for estimating rates of close and moderate inbreeding from incomplete pedigree data. We applied this method to three wild populations of ruminants: red deer on Rum, Scotland, Soay sheep on Hirta, Scotland and reintroduced Arabian oryx on the Jiddat-al-Harasis, Oman. Although paternal half-sib pairs were the most common category of inbreeding in all three populations, there was considerable variation among populations in the frequencies of the various categories of inbreeding. This variation may be largely explained by differences in population size and dynamics, in maternal and paternal sibship size and in the overlap of reproductive lifespan of consecutive generations. Close and moderate inbreeding appear to be a routine part of breeding behaviour in these ruminant populations.     

Conservation genetic management of a critically endangered New Zealand endemic bird: minimizing inbreeding in the Black Stilt Himantopus novaezelandiae

For threatened species with small captive populations, it is advisable to incorporate conservation management strategies that minimize inbreeding in an effort to avoid inbreeding depression. Using multilocus microsatellite genotype data, we found a significant negative relationship between genetic relatedness (inbreeding) and reproductive success (fitness) in a captive population of the critically endangered Black Stilt or KakīHimantopus novaezelandiae. In an effort to avoid inbreeding depression in this iconic New Zealand endemic, we recommend re‐pairing closely related captive birds with less related individuals and pairing new captive birds with distantly related individuals.     

Quantitative genetics in conservation biology

Most of the major genetic concerns in conservation biology, including inbreeding depression, loss of evolutionary potential, genetic adaptation to captivity and outbreeding depression, involve quantitative genetics. Small population size leads to inbreeding and loss of genetic diversity and so increases extinction risk. Captive populations of endangered species are managed to maximize the retention of genetic diversity by minimizing kinship, with subsidiary efforts to minimize inbreeding. There is growing evidence that genetic adaptation to captivity is a major issue in the genetic management of captive populations of endangered species as it reduces reproductive fitness when captive populations are reintroduced into the wild. This problem is not currently addressed, but it can be alleviated by deliberately fragmenting captive populations, with occasional exchange of immigrants to avoid excessive inbreeding. The extent and importance of outbreeding depression is a matter of controversy. Currently, an extremely cautious approach is taken to mixing populations. However, this cannot continue if fragmented populations are to be adequately managed to minimize extinctions. Most genetic management recommendations for endangered species arise directly, or indirectly, from quantitative genetic considerations.     

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.     

Inbreeding avoidance influences the viability of reintroduced populations of African wild dogs (Lycaon pictus)

The conservation of many fragmented and small populations of endangered African wild dogs (Lycaon pictus) relies on understanding the natural processes affecting genetic diversity, demographics, and future viability. We used extensive behavioural, life-history, and genetic data from reintroduced African wild dogs in South Africa to (1) test for inbreeding avoidance via mate selection and (2) model the potential consequences of avoidance on population persistence. Results suggested that wild dogs avoided mating with kin. Inbreeding was rare in natal packs, after reproductive vacancies, and between sibling cohorts (observed on 0.8%, 12.5%, and 3.8% of occasions, respectively). Only one of the six (16.7%) breeding pairs confirmed as third-order (or closer) kin consisted of animals that were familiar with each other, while no other paired individuals had any prior association. Computer-simulated populations allowed to experience inbreeding had only a 1.6% probability of extinction within 100 years, whereas all populations avoiding incestuous matings became extinct due to the absence of unrelated mates. Populations that avoided mating with first-order relatives became extinct after 63 years compared with persistence of 37 and 19 years for those also prevented from second-order and third-order matings, respectively. Although stronger inbreeding avoidance maintains significantly more genetic variation, our results demonstrate the potentially severe demographic impacts of reduced numbers of suitable mates on the future viability of small, isolated wild dog populations. The rapid rate of population decline suggests that extinction may occur before inbreeding depression is observed.     

Implications of social dominance and multiple paternity for the genetic diversity of a captive-bred reptile population (tuatara)

Captive breeding is an integral part of many species recovery plans. Knowledge of the genetic mating system is essential for effective management of captive stocks and release groups, and can help to predict patterns of genetic diversity in reintroduced populations. Here we investigate the poorly understood mating system of a threatened, ancient reptile (tuatara) on Little Barrier Island, New Zealand and discuss its impact on the genetic diversity. This biologically significant population was thought to be extinct, due to introduced predators, until 8 adults (4 males, 4 females) were rediscovered in 1991/92. We genotyped these adults and their 121 captively-bred offspring, hatched between 1994 to 2005, at five microsatellite loci. Multiple paternity was found in 18.8% of clutches. Male variance in reproductive success was high with one male dominating mating (77.5% of offspring sired) and one male completely restricted from mating. Little Barrier Island tuatara, although clearly having undergone a demographic bottleneck, are retaining relatively high levels of remnant genetic diversity which may be complemented by the presence of multiple paternity. High variance in reproductive success has decreased the effective size of this population to approximately 4 individuals. Manipulation to equalize founder representation was not successful, and the mating system has thus had a large impact on the genetic diversity of this recovering population. Although population growth has been successful, in the absence of migrants this population is likely at risk of future inbreeding and genetic bottleneck.     

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.     

Genetic diversity and conservation units in wild and captive populations of endangered freshwater fishes: a case of <Emphasis Type="Italic">Hemigrammocypris rasborella</Emphasis> in Shizuoka,Japan

Population structure and genetic diversity were examined using partial mitochondrial cytochrome b gene sequences of four wild, one reintroduced, and five captive populations of the endangered cyprinid Hemigrammocypris rasborella from three river systems in the easternmost region of the species’ range in Shizuoka Prefecture, central Honshu, Japan. We detected loss of genetic diversity from portions of the wild and captive populations, as well as suspected nonindigenous haplotypes in some captive, reintroduced, and even wild populations. Given the population structure revealed, we suggest that the populations should be managed with consideration for both the endemism and viability (avoidance of inbreeding depression) of the local populations.     

Genetic rescue and inbreeding depression in Mexican wolves

Although inbreeding can reduce individual fitness and contribute to population extinction, gene flow between inbred but unrelated populations may overcome these effects. Among extant Mexican wolves (Canis lupus baileyi), inbreeding had reduced genetic diversity and potentially lowered fitness, and as a result, three unrelated captive wolf lineages were merged beginning in 1995. We examined the effect of inbreeding and the merging of the founding lineages on three fitness traits in the captive population and on litter size in the reintroduced population. We found little evidence of inbreeding depression among captive wolves of the founding lineages, but large fitness increases, genetic rescue, for all traits examined among F1 offspring of the founding lineages. In addition, we observed strong inbreeding depression among wolves descended from F1 wolves. These results suggest a high load of deleterious alleles in the McBride lineage, the largest of the founding lineages. In the wild, reintroduced population, there were large fitness differences between McBride wolves and wolves with ancestry from two or more lineages, again indicating a genetic rescue. The low litter and pack sizes observed in the wild population are consistent with this genetic load, but it appears that there is still potential to establish vigorous wild populations.     

Molecular paternity determination in captive bonobos and the impact of inbreeding on infant mortality

Inbreeding and the loss of genetic diversity may lower fitness and reduce the potential for a population to adapt to changing environments. In small populations, for example in captive populations or populations of endangered species, this can have considerable consequences for their survival. We investigated the effects of inbreeding on infant mortality in the world captive population of bonobos Pan paniscus . Using a combination of studbook data and high-quality pedigree data from genotyped individuals, inbreeding information was available for 142 captive-born individuals. For the determination of paternities that were unresolved in the studbook, nuclear microsatellite DNA was amplified from hair and blood samples using the Great Ape Kit and PowerPlex^® 16 System. In total, 54 bonobos (17 offspring and their putative parents) were genotyped at eight tetranucleotide repeat microsatellite loci. Inbreeding coefficients were calculated for each individual for whom paternity was confirmed by either studbook data or DNA analysis. We found significantly higher infant mortality in inbred offspring compared with non-inbred offspring, suggesting that inbreeding reduces infant survival in captive bonobos. In addition, we argue that the total magnitude of inbreeding depression is probably underestimated in this captive population. In conclusion, even though the breeding programme of captive bonobos is aimed at avoiding inbreeding, closely related individuals do occasionally produce offspring that do show inbreeding depression. There is, however, no indication that this currently threatens the long-time survival of the captive population of bonobos.     

Pedigrees, MHC and microsatellites: an integrated approach for genetic management of captive African wild dogs (Lycaon pictus)

Captive breeding programmes aim to provide an insurance against extinction in the wild and a source for re-introductions making it essential to minimise genetic threats, and maximise representation of wild adaptive genetic diversity. As such, genetic assessments of captive breeding programmes are increasingly common. However, these rarely include comprehensive comparisons with wild populations and typically neutral, rather than adaptive, genetic diversity is assayed. Moreover, genetic data are rarely integrated with studbook information, which enables the most robust assessments. Here we use the European captive African wild dog (Lycaon pictus) population to demonstrate the utility of this combined approach. Specifically, we combined studbook pedigree information with genetic assessments of captive and wild samples at both neutral markers and a locus thought to be important for adaptation (a gene at the Major Histocompatibility Complex, MHC). With these data we were able to evaluate founder origin and representation, as well as the distribution and origin of genetic variation within the captive population. We found discrepancies between diversity metrics derived from neutral and adaptive markers and pedigree versus genetic derived inbreeding estimates. Overall, however, we found a large proportion of genetic diversity from wild populations to be conserved in the captive population, much of which can be attributed to recent imports from outside of the European breeding programme. Nonetheless, we also found a high incidence of inbreeding and very skewed founder contributions. Based on these results, we proposed and implemented a genetic management plan to prevent further losses of diversity and reduce inbreeding.     

Moderate inbreeding depression in a reintroduced population of North Island robins

Reintroductions of threatened species are increasingly common in conservation. The translocation of a small subset of individuals from a genetically diverse source population could potentially lead to substantial inbreeding depression due to the high genetic load of the parent population. We analysed 12 years of data from the reintroduced population of North Island robins Petroica longipes on Tiritiri Matangi Island, New Zealand, to determine the frequency of inbreeding and magnitude of inbreeding depression. The initial breeding population consisted of 12 females and 21 males, which came from a large mainland population of robins. The frequency of mating between relatives ( f >0; 39%, n =82 pairs) and close relatives ( f =0.25; 6.1%) and the average level of inbreeding ( f =0.027) were within the range reported for other small island populations of birds. The average level of inbreeding fluctuated from year to year depending on the frequency of close inbreeding (e.g. sib–sib pairs). We found evidence for inbreeding depression in juvenile survival, with survival probability estimated to decline from 31% among non-inbred birds ( f =0) to 11% in highly inbred juveniles ( f =0.25). The estimated number of lethal equivalents based on this relationship (4.14) was moderate compared with values reported for other island populations of passerines. Given that significant loss of fitness was only evident in highly inbred individuals, and such individuals were relatively rare once the population expanded above 30 pairs, we conclude that inbreeding depression should have little influence on this robin population. Although the future fitness consequences of any loss of genetic variation due to inbreeding are uncertain, the immediate impact of inbreeding depression is likely to be low in any reintroduced population that expands relatively quickly after establishment.     

DNA fingerprinting of captive breeding pairs of lesser white-fronted geese (Anser erythropus) with unknown pedigrees

For a number of decades, the lesser white-fronted goose (Anser erythropus) has been almost-absent from the Fennoscandian fauna and has a current population size of only about 60 breeding pairs, with fewer than 10 pairs in Sweden. During the period 1981–1991 more than 200 young have been reintroduced in northern Sweden. However, the origin and possible relatedness of lesser white-fronted individuals were unknown when the breeding program started. We have used DNA fingerprinting to assess the similarity of 18 individuals, i.e., the entire captive population used for breeding in 1991 and about 60% of the captive population used in 1981–1991. Minisatellite probe 33.15 provided an index for an average similarity of 0.39 between the mates of the 12 breeding pairs used for producing offspring for reintroduction. This is a higher similarity than in natural populations of birds in general but lower than in populations that have passed through serious population bottlenecks. Individuals originating from different breeders are more dissimilar than those from the same breeder. However, the close relationships (similarity, 0.5–0.6) found in a group of five individuals from different breeders show that selecting individuals from different breeding groups is not sufficient to prevent mating between closely related individuals.     

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.     

Evidence of inbreeding depression but not inbreeding avoidance in a natural house sparrow population

Inbreeding is common in small and threatened populations and often has a negative effect on individual fitness and genetic diversity. Thus, inbreeding can be an important factor affecting the persistence of small populations. In this study, we investigated the effects of inbreeding on fitness in a small, wild population of house sparrows (Passer domesticus) on the island of Aldra, Norway. The population was founded in 1998 by four individuals (one female and three males). After the founder event, the adult population rapidly increased to about 30 individuals in 2001. At the same time, the mean inbreeding coefficient among adults increased from 0 to 0.04 by 2001 and thereafter fluctuated between 0.06 and 0.10, indicating a highly inbred population. We found a negative effect of inbreeding on lifetime reproductive success, which seemed to be mainly due to an effect of inbreeding on annual reproductive success. This resulted in selection against inbred females. However, the negative effect of inbreeding was less strong in males, suggesting that selection against inbred individuals is at least partly sex specific. To examine whether individuals avoided breeding with close relatives, we compared observed inbreeding and kinship coefficients in the population with those obtained from simulations of random mating. We found no significant differences between the two, indicating weak or absent inbreeding avoidance. We conclude that there was inbreeding depression in our population. Despite this, birds did not seem to actively avoid mating with close relatives, perhaps as a consequence of constraints on mating possibilities in such a small population.     

Evidence of multiple paternity and mate selection for inbreeding avoidance in wild eastern chipmunks

Mate selection for inbreeding avoidance is documented in several taxa. In mammals, most conclusive evidence comes from captive experiments that control for the availability of mates and for the level of genetic relatedness between mating partners. However, the importance of mate selection for inbreeding avoidance as a determinant of siring success in the wild has rarely been addressed. We followed the reproduction of a wild population of eastern chipmunks (Tamias striatus) during five breeding seasons between 2006 and 2009. Using molecular tools and parentage assignment methods, we found that multiple paternity (among polytocous litters) varied from 25% in an early-spring breeding season when less than a quarter of females in the population were reproductively active to 100% across three summer breeding seasons and one spring breeding season when more than 85% of females were reproductively active. Genetically related parents were common in this population and produced less heterozygous offspring. Furthermore, litters with multiple sires showed a higher average relatedness among partners than litters with only a single sire. In multiply sired litters, however, males that were more closely related to their partners sired fewer offspring. Our results corroborate findings from captive experiments and suggest that selection for inbreeding avoidance can be an important determinant of reproductive success in wild mammals.     

陕西省林麝mtDNA D-loop区序列结构和种群遗传多样性

林麝(Moschus berezovskii)曾广泛分布于中国,由于盗猎和栖息地缩小,秦岭地区野生种群数量迅速下降,圈养繁殖种群已成立了几十年,但大多数圈养种群的遗传背景不清,种群规模增长非常缓慢。为了给这一物种的保护和管理提供有用的信息,调查了陕西省林麝1个圈养种群3个野生种群线粒体DNA(mt DNA)D-Loop 632 bp片段的遗传多样性和种群结构。在69个个体中其碱基组成为A+T的平均含量63.2%高于G+C含量36.8%,共检测到变异位点171个(约占总位点数的27.05%)。核苷酸多样性(Pi)为0.04424,平均核苷酸差异数(K)为19.908。69个个体分属32个单倍型,单倍型间的平均遗传距离(P)为0.070。32个单倍型构建的NJ系统树聚为3个分支,4个林麝群体中的单倍型是随机分布的。4个群体的平均遗传距离为0.043(标准误SE为0.005),凤县养殖场群体与留坝和陇县群体的亲缘关系较远。单倍型间的平均遗传距离为0.043,可见其遗传分化尚未达到种群分化的水平。结果表明,陕西省林麝群体mt DNA D-loop区序列存在着较丰富的变异和遗传多样性,凤县野生群体和凤县养殖场群体的核苷酸多样性和单倍型多样较高,养殖场种群没有出现近亲繁殖及遗传多样性下降的情况。凤县野生群体和凤县养殖场群体两者遗传分化较小,存在着较高的基因流水平。     

The impact of founder events and introductions on genetic variation in the muskox <Emphasis Type="Italic">Ovibos moschatus</Emphasis> in Sweden

The muskox Ovibos moschatus (Zimmerman 1780) is a specialised arctic mammal with a highly fragmented circumpolar distribution, with native populations in Canada and east Greenland and introduced populations in west Greenland, Alaska, Siberia and Eurasia. In 1971, five O. moschatus individuals from an introduced population in Norway migrated to Sweden. After a peak population of 36 individuals in the mid-1980s, the Swedish population now numbers seven individuals, making it vulnerable to both demographic and genetic stochasticity (i.e. inbreeding). Here, we analyse genetic variation among native and introduced populations of O. moschatus to evaluate the genetic effect of sequential founder events in this species. Our results show that genetic variation among native and introduced O. moschatus populations do not conform entirely to the expectations from sequential founder events, most likely because of random processes associated with introduction. In the Swedish population, a calf resulting from the mating of a wild cow and a captive Greenlandic bull contributes significantly to the current genetic variation. Thus, even a single outbreeding event may, at least momentarily, increase the genetic variation and potentially prevent inbreeding depression. Our results should aid the long-term preservation of O. moschatus in Sweden and Europe.     

圈养小熊猫遗传多样性与种群遗传结构分析

小熊猫是亚洲特有的珍稀濒危动物,目前受到栖息地减少、片断化和人类活动干扰等威胁。中国圈养小熊猫已经有60 多年历史,约55 个机构曾经饲养过小熊猫,现今圈养数量有400 多只,评估小熊猫圈养种群的遗传多样性和遗传结构对科学维持圈养种群和保存遗传种质资源意义重大。本研究利用19 个微卫星座位,对中国境内11 个小熊猫圈养种群的116 只个体进行了遗传多样性评估及遗传结构分析。结果显示11 个种群都具有较高的遗传多样性,平均基因丰富度3.505 ± 1.033 (北京)至4.026 ± 1.219 (冕宁),期望杂合度0.631 ± 0.225(黄山)至0.782 ±0.171 (温岭)。其中福州和无锡种群极显著偏离Hardy-Weinberg 平衡。整个圈养群体内各个种群遗传分化系数为0.055,呈显著分化,表明11 个种群遗传分化水平较高。Bayesian 遗传聚类分析将11 个种群聚为三个遗传簇,与野生种群的遗传聚类结果一致。结论:小熊猫圈养种群与野生种群相比,同样具有较高的遗传多样性。因此,圈养小熊猫遗传管理的重点不再是引进野生个体充实圈养种群,应制订科学的繁殖计划,避免近交,从而维持圈养种群的遗传多样性。