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.     

濒危植物居群恢复的遗传学考量

本文针对濒危植物居群的遗传多样性、生殖适合度、基因流、近交和远交衰退等遗传学问题在居群恢复过程中的应用进行了探讨。濒危植物居群的回归重建,既面临遗传多样性的迅速丧失、近交衰退等遗传风险,还因回归引种地存在较多近缘种而带来远交衰退的风险,最终导致遗传适应性降低,生境适应性变窄,繁殖和竞争能力减弱。为提高濒危物种保护的质量和效率,在构建回归居群时,应分批次从同一来源居群的不同母株采集材料,确保种源的遗传纯正性和遗传组成的多样性,还应使回归居群尽可能远离近缘广布种。另外,还需要对回归种群进行持续的监测和管理才能保证回归引种的成功。     

Use of microsatellite data and pedigree information in the genetic management of two long-term salmon conservation programs

In this paper, we describe the utility of microsatellite data and genetic pedigree information to guide the genetic management of two long-term conservation programs for endangered populations of salmon: Snake River Sockeye Salmon, Oncorhynchus nerka, and inner Bay of Fundy Atlantic Salmon, Salmo salar. Both programs are captive broodstock (live gene banking) programs for endangered populations of salmon. In order for these programs to be successful for recovery efforts, genetic change, including accumulation of inbreeding, loss of genetic variation, and adaptation to captivity, must be minimized. We provide an overview of each program, describe broodstock selection and pairing for spawning, and discuss how pedigree data are being used to evaluate different management practices. While there are inherent species and programmatic differences, both of these programs use widely accepted genetic conservation strategies (minimize mean kinship, reduce variance in family size, minimize inbreeding in the next generation, maintain large census and effective population size) to potentially mitigate some unintended side-effects associated with the rearing of small populations in captivity. These case studies highlight the benefits and practical limitations of applying these strategies in the genetic management of salmon, and may be used to inform other conservation programs.     

Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species

Captive breeding has become an important tool in species conservation programmes. Current management strategies for ex situ populations are based on theoretical models, which have mainly been tested in model species or assessed using studbook data. During recent years an increasing number of molecular genetic studies have been published on captive populations of several endangered species. However, a comprehensive analysis of these studies is still outstanding. Here, we present a review of the published literature on ex situ conservation genetics with a focus on molecular studies. We analysed 188 publications which either presented empirical studies using molecular markers (105), studbook analyses (26), theoretical work (38), or tested the genetic effects of management strategies using model species (19). The results show that inbreeding can be minimized by a thorough management of captive populations. There seems to be a minimum number of founders (15) and a minimum size of a captive population (100) necessary in order to minimize a loss of genetic diversity. Optimally, the founders should be unrelated and new founders should be integrated into the captive population successively. We recommend that genetic analyses should generally precede and accompany ex situ conservation projects in order to avoid inbreeding and outbreeding depression. Furthermore, many of the published studies do not provide all the relevant parameters (founder size, captive population size, H_o, H_e, inbreeding coefficients). We, therefore, propose that a general standard for the presentation of genetic studies should be established, which would allow integration of the data into a global database.     

Genetic assessment of the Arabian oryx founder population in the Emirate of Abu Dhabi, UAE: an example of evaluating unmanaged captive stocks for reintroduction

Since being declared extinct in the wild in 1972, the Arabian oryx has been the subject of intense and sustained effort to maintain a healthy captive population and to reintroduce the species to its ancestral range. Previous reintroductions and associated genetic assessments focused on the release of closely managed zoo animals into Oman and included observations of inbreeding and outbreeding depression. Here we describe the use of multiple unmanaged herds as source populations for a new reintroduction project in the United Arab Emirates, allowing a comparison between studbook management and uncontrolled semi-captive breeding approaches to the conservation of genetic diversity. Results of mitochondrial control region sequencing and 13-locus microsatellite profiling highlight a severe lack of diversity within individual source populations, but a level of differentiation among populations that supports the formation of a mixed founder herd. The combined release group contained a similar level of diversity to each of the intensively managed captive populations. The research includes the first genetic data for animals held on Sir Bani Yas Island, a former private reserve which until recently held over 50% of the world’s Arabian and scimitar-horned oryx and is recognized as having huge potential for re-establishing endangered antelope species in the wild. The genetic assessment provides the first stage of an ongoing genetic monitoring programme to support future supplemental releases, translocations and genetic management of reintroduced 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.     

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.     

Single large or several small? Population fragmentation in the captive management of endangered species

Captive populations of endangered species are typically maintained effectively as single random-mating populations by translocating individuals between institutions. Genetic, disease, and cost considerations, however, suggest that this may not be the optimal management strategy. Genetic theory predicts that a pooled population derived from several small isolated populations will have greater genetic diversity, less inbreeding, and less genetic adaptation to captivity than a single large population of equivalent total size, provided there are no population extinctions. These predictions were tested using populations of Drosophila with effective size comparisons of 50 vs. 2 × 25; 100 vs. 2 × 50 vs. 4 × 25, and 500 vs. 2 × 250 vs. 4 × 100 + 2 × 50 vs. 8 × 25 + 6 × 50. Populations were maintained at the indicated sizes as separate pedigreed populations for 50 generations. The several small treatments were subsequently pooled and maintained for eight to 10 generations prior to determination of fitness and evolutionary potential. Several small populations (pooled), when compared to single large populations of equivalent total size, were found to have lower average inbreeding coefficients, significantly higher reproductive fitness under competitive conditions, similar fitness under benign captive conditions, higher genetic diversity, and equivalent evolutionary potential. Trends favored the several small (pooled) populations in all comparisons at population sizes of 50 and 100. We recommend that endangered species in captivity be maintained as several small populations, with occasional exchange of genetic material. This has genetic benefits over current management both in captivity and especially for reintroductions, as well as reducing translocation costs and risks of disease transfer. Zoo Biol 17:467–480, 1998. © 1998 Wiley-Liss, Inc.     

Genetic adaptation to captivity in species conservation programs

As wild environments are often inhospitable, many species have to be captive-bred to save them from extinction. In captivity, species adapt genetically to the captive environment and these genetic adaptations are overwhelmingly deleterious when populations are returned to wild environments. I review empirical evidence on (i) the genetic basis of adaptive changes in captivity, (ii) factors affecting the extent of genetic adaptation to captivity, and (iii) means for minimizing its deleterious impacts. Genetic adaptation to captivity is primarily due to rare alleles that in the wild were deleterious and partially recessive. The extent of adaptation to captivity depends upon selection intensity, genetic diversity, effective population size and number of generation in captivity, as predicted by quantitative genetic theory. Minimizing generations in captivity provides a highly effective means for minimizing genetic adaptation to captivity, but is not a practical option for most animal species. Population fragmentation and crossing replicate captive populations provide practical means for minimizing the deleterious effects of genetic adaptation to captivity upon populations reintroduced into the wild. Surprisingly, equalization of family sizes reduces the rate of genetic adaptation, but not the deleterious impacts upon reintroduced populations. Genetic adaptation to captivity is expected to have major effects on reintroduction success for species that have spent many generations in captivity. This issue deserves a much higher priority than it is currently receiving.     

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.     

Looking back to go forward: genetics informs future management of captive and reintroduced populations of the black-footed rock-wallaby <Emphasis Type="Italic">Petrogale lateralis</Emphasis>

Active management is essential to the survival of many threatened species globally. Captive breeding programmes can play an important role in facilitating the supplementation, translocation and reintroduction of wild populations. However, understanding the genetic dynamics within and among wild and captive populations is crucial to the planning and implementation of ex situ management, as adaptive potential is, in part, driven by genetic diversity. Here, we use 14 microsatellite loci and mitochondrial Control Region sequence to examine the population genetics of both wild populations and captive colonies of the endangered warru (the MacDonnell Ranges race of the black-footed rock-wallaby Petrogale lateralis) in central Australia, to understand how historical evolutionary processes have shaped current diversity and ensure effective ex situ management. Whilst microsatellite data reveal significant contemporary differentiation amongst remnant warru populations, evidence of contemporary dispersal and relatively weak isolation by distance, as well as a lack of phylogeographic structure suggests historical connectivity. Genetic diversity within current captive populations is lower than in the wild source populations. Based on our genetic data and ecological observations, we predict outbreeding depression is unlikely and hence make the recommendation that captive populations be managed as one genetic group. This will increase genetic diversity within the captive population and as a result increase the adaptive potential of reintroduced populations. We also identify a new site in the Musgrave Ranges which contains unique alleles but also connectivity with a population 6 km away. This novel genetic diversity could be used as a future source for supplementation.     

Stress and adaptation in conservation genetics

Stress, adaptation and evolution are major concerns in conservation biology. Stresses from pollution, climatic changes, disease etc. may affect population persistence. Further, stress typically occurs when species are placed in captivity. Threatened species are usually managed to conserve their ability to adapt to environmental changes, whilst species in captivity undergo adaptations that are deleterious upon reintroduction into the wild. In model studies using Drosophila melanogaster, we have found that; (a) inbreeding and loss of genetic variation reduced resistance to the stress of disease, (b) extinction rates under inbreeding are elevated by stress, (c) adaptive evolutionary potential in an increasingly stressful environment is reduced in small population, (d) rates of inbreeding are elevated under stressful conditions, (e) genetic adaptation to captivity reduces fitness when populations are reintroduced into the 'wild', and (f) the deleterious effects of adaptation on reintroduction success can be reduced by population fragmentation.     

Impacts of early viability selection on management of inbreeding and genetic diversity in conservation

Maintaining genetic diversity is a crucial goal of intensive management of threatened species, particularly for those populations that act as sources for translocation or re‐introduction programmes. Most captive genetic management is based on pedigrees and a neutral theory of inheritance, an assumption that may be violated by selective forces operating in captivity. Here, we explore the conservation consequences of early viability selection: differential offspring survival that occurs prior to management or research observations, such as embryo deaths in utero. If early viability selection produces genotypic deviations from Mendelian predictions, it may undermine management strategies intended to minimize inbreeding and maintain genetic diversity. We use empirical examples to demonstrate that straightforward approaches, such as comparing litter sizes of inbred vs. noninbred breeding pairs, can be used to test whether early viability selection likely impacts estimates of inbreeding depression. We also show that comparing multilocus genotype data to pedigree predictions can reveal whether early viability selection drives systematic biases in genetic diversity, patterns that would not be detected using pedigree‐based statistics alone. More sophisticated analysis combining genomewide molecular data with pedigree information will enable conservation scientists to test whether early viability selection drives deviations from neutrality across wide stretches of the genome, revealing whether this form of selection biases the pedigree‐based statistics and inference upon which intensive management is based.     

Evolution of Peromyscus leucopus Mice in Response to a Captive Environment

Many wildlife species are propagated in captivity as models for behavioral, physiological, and genetic research or to provide assurance populations to protect threatened species. However, very little is known about how animals evolve in the novel environment of captivity. The histories of most laboratory strains are poorly documented, and protected populations of wildlife species are usually too small and too short-term to allow robust statistical analysis. To document the evolutionary change in captive breeding programs, we monitored reproduction and behavior across 18 generations in six experimental populations of Peromyscus leucopus mice started from a common set of 20 wild-caught founders. The mice were propagated under three breeding protocols: a strategy to retain maximal genetic diversity, artificial selection against stereotypic behaviors that were hypothesized to reflect poor adaptation to captivity, and random bred controls. Two replicates were maintained with each protocol, and inter-replicate crosses at generations 19 and 20 were used to reverse accumulated inbreeding. We found that one of the stereotypic behaviors (repetitive flipping) was positively associated with reproductive fitness, while the other (gnawing) was relatively invariant. Selection to reduce these stereotypic behaviors caused marked reduction in reproduction, and populations not under artificial selection to reduce these behaviors responded with large increases in flipping. In non-selected populations, there was rapid evolution toward much higher proportion of pairs breeding and more rapid conception. Litter size, pup survival, and weaning mass all declined slowly, to the extent that would be predicted based on inbreeding depression. Inter-crossing between replicate populations reversed these declines in fitness components but did not reverse the changes in behavior or the accelerated breeding. These findings indicate that adaptation to captivity can be rapid, affecting reproductive patterns and behaviors, even under breeding protocols designed to minimize the rate of genetic change due to random drift and inadvertent selection.     

注意植物迁地保护中的遗传风险

稀有濒危植物迁地保护的长期目标之一就是要保护物种的遗传多样性和进化潜力。介绍了稀有濒危植物在植物园迁地保护过程中存在的一系列遗传风险。由于引种或取样的不足,容易导致被保存的物种缺乏足够的遗传代表性;盲目的引种、不合理的定植以及材料的来源不清则会导致稀有濒危植物的遗传混杂、近交衰退或杂交衰退;人为选择和生长环境的改变也容易造成濒危物种对迁地保护的遗传适应。在实际的迁地保护工作中,这些遗传风险往往被忽视。植物迁地保护中遗传风险将严重影响稀有濒危物种的回归和恢复。植物园应当重视濒危植物的遗传管理,以降低或避免迁地保护中的遗传风险。Abstract: Conserving genetic diversity of rare and endangered species and their evolutionary potential is one of the long-term goals of ex-situ conservation. Some potential genetic risks in ex-situ conservation in botanical gardens are presented. The preserved species may lack genetic representativity because of poor sampling. Inappropriate plantations, inadequate records and unclear kinships jeopardize endangered species to genetic confusion, inbreeding depression or outbreeding depression. Artificial selection and habitat conversion also potentially result endangered plants in adapting to ex-situ conservation, which had been usually overlooked. All the genetic risks can decrease the success of reintroduction and recovery. Therefore, appropriate genetic management should be carried out in botanical gardens to decrease or avoid genetic risks in ex-situ conservation.     

A comparison of pedigree‐ and DNA‐based measures for identifying inbreeding depression in the critically endangered Attwater's Prairie‐chicken

The primary goal of captive breeding programmes for endangered species is to prevent extinction, a component of which includes the preservation of genetic diversity and avoidance of inbreeding. This is typically accomplished by minimizing mean kinship in the population, thereby maintaining equal representation of the genetic founders used to initiate the captive population. If errors in the pedigree do exist, such an approach becomes less effective for minimizing inbreeding depression. In this study, both pedigree‐ and DNA‐based methods were used to assess whether inbreeding depression existed in the captive population of the critically endangered Attwater's Prairie‐chicken (Tympanuchus cupido attwateri), a subspecies of prairie grouse that has experienced a significant decline in abundance and concurrent reduction in neutral genetic diversity. When examining the captive population for signs of inbreeding, variation in pedigree‐based inbreeding coefficients (f_pedigree) was less than that obtained from DNA‐based methods (f_DNA). Mortality of chicks and adults in captivity were also positively correlated with parental relatedness (r_DNA) and f_DNA, respectively, while no correlation was observed with pedigree‐based measures when controlling for additional variables such as age, breeding facility, gender and captive/release status. Further, individual homozygosity by loci (HL) and parental r_DNA values were positively correlated with adult mortality in captivity and the occurrence of a lethal congenital defect in chicks, respectively, suggesting that inbreeding may be a contributing factor increasing the frequency of this condition among Attwater's Prairie‐chickens. This study highlights the importance of using DNA‐based methods to better inform management decisions when pedigrees are incomplete or errors may exist due to uncertainty in pairings.     

Inbreeding depression and low between-population heterosis in recently diverged experimental populations of a selfing species

In fragmented populations, genetic drift and selection reduce genetic diversity, which in turn results in a loss of fitness or in a loss of evolvability. Genetic rescue, that is, controlled input of diversity from distant populations, may restore evolutionary potential, whereas outbreeding depression might counteract the positive effect of this strategy. We carried out self-pollination and crosses within and between populations in an experimental subdivided population of a selfing species, Triticum aestivum L., to estimate the magnitude of these two phenomena. Surprisingly, for a self-fertilizing species, we found significant inbreeding depression within each population for four of the six traits studied, indicating that mildly deleterious mutations were still segregating in these populations. The progeny of within- and between-population crosses was very similar, indicating low between-population heterosis and little outbreeding depression. We conclude that relatively large population effective sizes prevented fixation of a high genetic load and that local adaptation was limited in these recently diverged populations. The kinship coefficient estimated between the parents using 20 neutral markers was a poor predictor of the progeny phenotypic values, indicating that there was a weak link between neutral diversity and genes controlling fitness-related traits. These results show that when assessing the viability of natural populations and the need for genetic rescue, the use of neutral markers should be complemented with information about the presence of local adaptation in the subdivided population.     

Minimizing kinship in captive breeding programs

Captive populations of endangered species are managed to preserve genetic diversity and retain reproductive fitness. Minimizing kinship (MK) has been predicted to maximize the retention of gene diversity in pedigreed populations with unequal founder representation. MK was compared with maximum avoidance of inbreeding (MAI) and random choice of parents (RAND) using Drosophila melanogaster. Forty replicate populations of each treatment were initiated with unequal founder representation and managed for four generations. MK retained significantly more gene diversity and allelic diversity based on six microsatellite loci and seven allozyme loci than MAI or RAND. Reproductive fitness under both benign and competitive conditions did not differ significantly among treatments. Of the methods considered, MK is currently the best available for the genetic management of captive populations. Zoo Biol 16:377–389, 1997. © 1997 Wiley-Liss, Inc.     

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。     

Unravelling first-generation pedigrees in wild endangered salmon populations using molecular genetic markers

There is increasing interest in the use of molecular genetic data to infer genealogical relationships among individuals in the absence of parental information. Such analyses can provide insight into mating systems and estimations of heritability in the wild. In addition, accurate pedigree reconstruction among the founders of endangered populations being reared in captivity would be invaluable. Many breeding programs for endangered species attempt to minimize loss of genetic variation and inbreeding through strategies designed to minimize global co-ancestry, but they assume a lack of relatedness among the founders. Yet populations that are the target of such programs are generally in serious demographic decline, and many of the available founders may be closely related. Here we demonstrate determination of full and half-sib relationships among the wild founders of a captive breeding program involving two endangered Atlantic salmon populations using two different approaches and associated software, pedigree and colony. A large portion of the juveniles collected in these two rivers appear to be derived from surprisingly few females mating with a large number of males, probably small precocious parr. Another group of potential founders, obtained from a local hatchery, clearly originated from a small number of full-sib crosses. These results allowed us to prioritize individuals on the basis of conservation value, and are expected to help minimize loss of genetic variation through time. In addition, insight is provided into the number of contributing parents and the mating systems that produced this last generation of endangered wild Atlantic salmon.