Modeling problems in conservation genetics using captive Drosophila populations: Consequences of equalizing founder representation

Equalizing founder representation is a recommended practice for maintaining captive populations. However, this procedure has not been subject to controlled experimental evaluation. The effects on inbreeding, genetic variation, and reproductive fitness of maintaining small captive populations by equalizing founder representation (EFR) versus randomly choosing parents (RC) were compared. Ten replicate lines were created with unequal founder representations, split into EFR and RC lines, and maintained for a further eight generations. Founder representations computed from pedigrees were closer to equality in the EFR lines than in the RC lines or the base population, most of the changes being evident after one generation. Significant benefits of EFR were found in lowered inbreeding (mean inbreeding coefficients of 0.35 and 0.41, respectively, for EFR and RC lines) and average heterozygosity (0.141 for EFR, 0.084 for RC, compared with 0.216 in the base population). However, EFR was not significantly better than RC in moving allele frequencies towards equalized founder representation. No significant difference was found in reproductive fitness between EFR and RC (relative fitnesses compared to the base population were 0.179 for EFR and 0.182 for RC). The use of equalization of founder representation for a few generations can be recommended in the genetic management of captive populations derived from a small number of founders that contribute unequally. © 1992 Wiley-Liss, Inc.     

Dynamics of genetic adaptation to captivity

Many species require captive breeding to savethem from extinction, with reintroduction intothe wild being the eventual aim of mostprograms. Adaptation to captive environmentstypically results in reduced fitness under wildconditions. Consequently, unintentionaladaptation during captive breeding programs mayseriously compromise the success ofreintroduction programs. However, there islittle experimental evidence on the rate orextent of adaptation for captive populationsmaintained under benign captive conditions forextended periods of time. To investigate thedynamics of genetic adaptation to captivity,large captive populations of Drosophilamelanogaster were assessed for relativefitness under captive conditions for up to 87generations in captivity. Captive fitnessincreased to 3.33 times the initial fitnessover 87 generations. The pattern of adaptationwas curvilinear, with an exponential curveproviding the best fit. Fitness reached 25% ofits maximum within 6 generations, 50% within15 generations, 75% within 31 generations and95% within 67 generations. The model predictedthat the asymptotic level of fitness reachedwould be 3.38 times the initial fitness. Thus,very large genetic adaptations to captivity mayoccur under relatively benign captiveconditions. Captive populations destined forreintroduction need to be managed to minimisegenetic adaptation to captivity.     

Hereditary defects and conservation genetic management of captive populations

The occurrence of hereditary disorders in conservation breeding programs may severely hamper the overall aim of such programs. The obstacles that arise in this context and the particular management strategies needed to deal with the problems are yet to be adequately addressed. Results from a literature review indicate that hereditary disorders may be fairly common in zoo populations. An example with albinism in a captive brown bear population bred in Nordic zoos is presented. It is demonstrated that the segregation pattern is consistent with an autosomal recessive allele, and carrier probabilities of live animals indicate that the allele occurs in high frequency in the present population. Removing animals with a probability of carrying the allele will result in loss of founder alleles considered particularly valuable. Zoo Biol 18:81–99, 1999. © 1999 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.     

Modelling problems in conservation genetics using Drosophila: consequences of fluctuating population sizes

Many natural populations fluctuate widely in population size. This is predicted to reduce effective population size, genetic variation, and reproductive fitness, and to increase inbreeding. The effects of fluctuating population size were examined in small populations of Drosophila melanogaster of the same average size, but maintained using either fluctuating ( FPS ) or equal ( EPS ) population sizes.FPS lines were maintained using seven pairs and one pair in alternate generations, and EPS lines with four pairs per generation. Ten replicates of each treatment were maintained. After eight generations, FPS had a higher inbreeding coefficient than EPS (0.60 vs. 0.38), a lower average allozyme heterozygosity (0.068 vs. 0.131), and a much lower relative fitness (0.03 vs. 0.25). Estimates of effective population sizes for FPS and EPS were 3.8 and 7.9 from pedigree inbreeding, and 4.9 vs. 7.1 from changes in average heterozygosities, as compared to theoretical expectations of 3.3 vs. 8.0. Results were generally in accordance with theoretical predictions. Management strategies for populations of rare and endangered species should aim to minimize population fluctuations over generations.     

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.     

Inbreeding and fitness in captive populations: Lessons from Drosophila

The avoidance of inbreeding is a primary goal of endangered species population management. In order to fully understand the effects of inbreeding on the fitness of natural and captive populations, it is necessary to consider fitness components which span the entire life cycle of the organism. Using Drosophila melanogaster as a model organism for conservation genetics studies, we constructed 18 experimental lines derived from wild-type stocks which were homozygous for chromosome 2 (this chromosome constitutes 38% of the genome or is equivalent to F = 0.38). For six of these lines which exhibited a reduced homozygous fitness, we estimated the relative values of fitness components operating at both the juvenile stage (pre-adult viability) and adult stage (female fecundity and male-mating ability) of the life cycle. Males in these lines showed a markedly reduced mating ability, while viability and female fecundity were much less affected. Equilibrium values of the wild-type chromosomes in these lines were accurately predicted using a model that incorporated into it these independently estimated fitness components. These results emphasize the importance of studying all fitness components directly to determine overall fitness. A reduced mating ability among inbred males of a captive population can have serious consequences for its future sustainability, and can further jeopardize reintroduction efforts; consequently, a program to carefully monitor the reproductive success of individual males, as well as other fitness components, is recommended. © 1993 Wiley-Liss, Inc.     

Modeling problems in conservation genetics using captive Drosophila populations: Improvement of reproductive fitness due to immigration of one individual into small partially inbred populations

Immigration into small isolated captive and wild populations is recommended to alleviate inbreeding depression. The effects on reproductive fitness of introducing one immigrant into 10 small partially inbred captive populations of D. melanogaster were evaluated. The relative reproductive fitness of the immigrant populations (0.628) was approximately double that of the isolated populations (0.294) and about halfway between the isolated populations and the outbred base population (1.00). Every replicate population increased in fitness following the introduction of an immigrant. The improvements in reproductive fitness shown by the immigrant populations were not due to F₁ hybrid vigor, as the experimental populations underwent three generations of random mating prior to the fitness tests. These results indicate substantial benefits can be gained by the translocation of as few as a single animal between small, partially inbred populations. © 1992 Wiley-Liss, Inc.     

Strategies for maintaining genetic diversity in captive populations through reproductive technology

The maintenance of genetic diversity in captive populations is a primary goal of captive breeding plans, and it is becoming increasingly apparent that reproductive technology has much to offer captive breeding programs in attaining this goal. Reproductive technology can best assist captive breeding programs in this task by developing strategies that effectively increase the genetic contribution of new wild founders to a population as well as increase the reproductive life span of existing founders and their close descendents. This will act to reduce genetic drift and inbreeding effects in the population and thereby minimize the loss of genetic diversity. Considering only one aspect of reproductive technology, semen collection, this paper examines some of the genetic considerations that might be used for choosing which males in a population to collect semen from, assuming the goal of the captive breeding program is the preservation of genetic diversity. It is shown that semen collection and preservation, with future intent of artificial insemination, can make significant contributions to the maintenance of genetic diversity if careful consideration is given to the selection of donor males. Finally, the pedigree of the captive population of Asian lions (Panthera leo persica) is used to illustrate some of these genetic concepts that might be important in selecting males as semen donors.     

Parallel trait adaptation across opposing thermal environments in experimental Drosophila melanogaster populations

Thermal stress is a pervasive selective agent in natural populations that impacts organismal growth, survival, and reproduction. Drosophila melanogaster exhibits a variety of putatively adaptive phenotypic responses to thermal stress in natural and experimental settings; however, accompanying assessments of fitness are typically lacking. Here, we quantify changes in fitness and known thermal tolerance traits in replicated experimental D. melanogaster populations following more than 40 generations of evolution to either cyclic cold or hot temperatures. By evaluating fitness for both evolved populations alongside a reconstituted starting population, we show that the evolved populations were the best adapted within their respective thermal environments. More strikingly, the evolved populations exhibited increased fitness in both environments and improved resistance to both acute heat and cold stress. This unexpected parallel response appeared to be an adaptation to the rapid temperature changes that drove the cycling thermal regimes, as parallel fitness changes were not observed when tested in a constant thermal environment. Our results add to a small, but growing group of studies that demonstrate the importance of fluctuating temperature changes for thermal adaptation and highlight the need for additional work in this area.     

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.     

Use of behavior to evaluate reproductive problems in captive mammals

Behavioral analyses constitute a logical starting point for discerning the causes of reproductive failure in captive mammals and should be completed before moving on to more invasive diagnostic procedures. Behavioral inadequacies affecting reproductive performance may be attributable to deficient early rearing environments, to the social milieux in which breeding-age animals are held on a long-term basis, or in the way pairings for mating are staged. Diagnoses may be focused on uncovering motivational, motoric, social, or communicative deficiencies. A biologically based approach which integrates species-typical behavior with concerns for genetics, physiology, and health in designing breeding programs will improve prospects for success. © 1994 Wiley-Liss, Inc.     

Research in zoos: a growth area in conservation

Despite early menageries being the source of much useful biological information on anatomy and taxonomy, it is only more recently that the potential for research in zoos has been recongnized. Collections of captive animals are unique and irreplaceable resources for conservation; but without research in zoological parks, progress in conservation science would diminish. There is a flow of information from zoo researchers to field scientists that assists in providing new insights into species biology. Reciprocally, data collected in the field enhance efforts in captive breeding. This paper summarizes the new research initiatives undertaken in zoos, e.g., in the fields of reproductive and genetic technologies, and highlights their significance for conservation and management of threatened species. It is evident that zoo research has a vital role in linking in situ and ex situ conservation. This role needs to be expanded and developed to meet the challenge posed by expanding human and declining wildlife populations and ecosystems.     

Life span,reproductive output,and reproductive opportunity in captive Goeldi's monkeys (Callimico goeldii)

In the absence of long‐term field studies, demographic and reproductive records from animals housed in zoos and research laboratories are a valuable tool for the study of life history variables relating to reproduction. In this study, we analyzed studbook records of more than 2,000 individuals born over a 40‐year period (1965–2004) to describe life history patterns of captive Goeldi's monkeys (Callimico goeldii) housed in North America and Europe. Using Kaplan–Meier survival analysis methods, we found the mean life span to be 5.5 years. The rate of infant mortality, defined as death before 30 days, was approximately 30%, with European animals being more likely to survive infancy than North American animals. When individuals surviving at least 1.5 years are considered, lifetime reproductive output averaged 3.5 offspring, yet more than one‐third of individuals did not produce any offspring. Using a smaller dataset of individuals with known pairing histories, we developed a measure of opportunity for reproduction (OFR), which represented the total time an individual was known to be housed with a potential mate. For both sexes, we found that the correlation between OFR and number of offspring produced was much higher than the correlation between life span and number of offspring produced. This result highlights the importance of taking into account an individual's OFR. As a whole, our findings help characterize the life histories of captive Goeldi's monkeys and emphasize the impact management practices may have on reproductive success. Zoo Biol 29:1–15, 2010. © 2009 Wiley‐Liss, Inc.     

The population genetics of adaptation: the adaptation of DNA sequences

I describe several patterns characterizing the genetics of adaptation at the DNA level. Following Gillespie (1983, 1984, 1991), I consider a population presently fixed for the ith best allele at a locus and study the sequential substitution of favorable mutations that results in fixation of the fittest DNA sequence locally available. Given a wild type sequence that is less than optimal, I derive the fitness rank of the next allele typically fixed by natural selection as well as the mean and variance of the jump in fitness that results when natural selection drives a substitution. Looking over the whole series of substitutions required to reach the best allele, I show that the mean fitness jumps occurring throughout an adaptive walk are constrained to a twofold window of values, assuming only that adaptation begins from a reasonably fit allele. I also show that the first substitution and the substitution of largest effect account for a large share of the total fitness increase during adaptation. I further show that the distribution of selection coefficients fixed throughout such an adaptive walk is exponential (ignoring mutations of small effect), a finding reminiscent of that seen in Fisher's geometric model of adaptation. Last, I show that adaptation by natural selection behaves in several respects as the average of two idealized forms of adaptation, perfect and random.     

Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendants in the wild

Supplementation of wild populations with captive-bred organisms is a common practice for conservation of threatened wild populations. Yet it is largely unknown whether such programmes actually help population size recovery. While a negative genetic effect of captive breeding that decreases fitness of captive-bred organisms has been detected, there is no direct evidence for a carry-over effect of captive breeding in their wild-born descendants, which would drag down the fitness of the wild population in subsequent generations. In this study, we use genetic parentage assignments to reconstruct a pedigree and estimate reproductive fitness of the wild-born descendants of captive-bred parents in a supplemented population of steelhead trout (Oncorhynchus mykiss). The estimated fitness varied among years, but overall relative reproductive fitness was only 37 per cent in wild-born fish from two captive-bred parents and 87 per cent in those from one captive-bred and one wild parent (relative to those from two wild parents). Our results suggest a significant carry-over effect of captive breeding, which has negative influence on the size of the wild population in the generation after supplementation. In this population, the population fitness could have been 8 per cent higher if there was no carry-over effect during the study period.     

Introducing mother's curse: low male fertility associated with an imported mtDNA haplotype in a captive colony of brown hares

Mitochondrial DNA mutations create variation in the efficiency of the oxidative phosphorylation pathway and therefore cellular energy production. Mildly deleterious mutations may reduce the performance of sperm cells in particular, due to their high energy requirements and low number of mitochondria, yet have little or no effect on the viability of somatic cells or ova. Mutations will be maintained in the population, despite the fitness cost for males, because mtDNA is passed down the female line. We looked for this so-called mother's curse effect in our captive colony of European brown hares. Significantly reduced male reproductive success was detected for a divergent haplotype that could be traced back to hares imported from a remote population. Median reproductive success for these hares was 0.17 compared to 0.49 for the indigenous haplotypes (Wilcoxon rank-sum, P  = 0.002). No difference was detected for female reproductive success, nor were we able to find a nuclear DNA component to variation in male fertility. Our data are strong evidence for a mother's curse effect persisting despite multiple crossings over seven generations. These data raise important issues relating to the reproductive fitness of small or intermixing populations and have particular implications for the management of populations for conservation.     

Captive breeding and the genetic fitness of natural populations

Many populations of endangered species are subject to recurrent introductions of individuals from an alternative setting where selection is either relaxed or in a direction opposite to that in the natural habitat. Such population structures, which are common to captive breeding and hatchery programs, can lead to a scenario in which alleles that are deleterious (and ordinarily keptat low levels) in the wild can rise to high frequencies and, in some cases, go to fixation. We outline how these genetic responses to supplementation candevelop to a large enough extent to impose a substantial risk of extinction for natural populations on time scales of relevance to conservation biology.The genetic supplementation load can be especially severe when a captive population that is largely closed to import makes a large contribution to the breeding pool of individuals in the wild, as these conditions insure thatthe productivity of the two-population system is dominated by captive breeders. However, a substantial supplementation load can even develop when the captive breeders are always derived from the wild, and in general, a severe restriction of gene flow into the natural population is required to reduce this load to an insignificant level. Domestication selection (adaptation to the captive environment) poses a particularly serious problem because it promotes fixations of alleles that are deleterious in nature, thereby resulting in a permanent load that cannot be purged once the supplementation program is truncated. Thus, our results suggest that the apparent short-term demographic advantages of a supplementation program can be quite deceiving. Unless the selective pressures of the captive environmentare closely managed to resemble those in the wild, long-term supplementation programs are expected to result in genetic transformations that can eventually lead to natural populations that are no longer capable of sustaining themselves.     

Genetic diversity analysis of captive populations: The Vietnamese sika deer (Cervus nippon pseudaxis) in zoological parks

The Vietnamese sika deer (Cervus nippon pseudaxis) is an endangered subspecies; it has disappeared in the wild, but is being bred in zoological parks. We studied the neutral genetic diversity and population structure of herds kept in different European zoos, using nine microsatellite loci. The goal was to evaluate the consequences of founding effects and breeding practices on the level and structure of genetic variability. The level of genetic diversity within the European zoos is not lower than that of the populations kept in Vietnamese farms. Strong differences among zoological parks and between the European group and the Vietnamese population were detected. This is probably due to founding effects, genetic drift, and possibly hybridization in both Europe and Vietnam. We expected to find a much lower level of genetic diversity in Europe. The current overall level of genetic diversity is probably due to the recent introduction of Cuc Phuong individuals, and to important differences among the populations of different zoological parks, which increase the total genetic variability. Although the current level of genetic variability is not particularly low, future levels are probably threatened by the current herd sizes and structure. Based on these results, management guidelines are proposed. Zoo Biol 22:465–475, 2003. © 2003 Wiley‐Liss, Inc.