Breeding program for the lesser kudu (Tragelaphus imberbis) in North America

The lesser kudu (Tragelaphus imberbis) has been kept in North American zoological parks since 1930 but has never been a common species in collections. In 1987 this population totaled 28 animals: 15 males and 13 females. A pedigree evaluation in 1987 of the existing population indicated that eight effective founders and one potential founder were represented in the North American herd. Three new potential founders from European captive populations were added to the population in 1987 to increase the number of existing founder lines to 12 animals. As this species is not endangered or threatened in its native habitat, it is not a high priority to qualify for designation as an SSP species. Because of this, the institutions holding lesser kudu in North America decided to join informally and draft a breeding program to better manage this small captive population. This program was designed to minimize inbreeding and equalize genetic representation of founder animals to maximize genetic diversity. It requires a shift in management philosophy to establish stable groups of breeding females at participating institutions while rotating appropriate breeder males through these herds in a controlled manner to ensure minimization of inbreeding and maximization of genetic diversity. It is hoped that this program can serve as a model for the management of other small captive populations of non-SSP species.     

The influence of captive breeding management on founder representation and inbreeding in the ‘Alalā, the Hawaiian crow

The ‘Alalā (Corvus hawaiiensis), or the Hawaiian crow, was historically only found on the island of Hawai‘i, declined greatly in the twentieth century, and was last seen in the wild in 2002. A captive breeding program was initiated in the 1970s and 113 individuals were in captivity in 2014. All of the present day individuals are descended from nine founders. From pedigree analysis, 50 % of the initial ancestry was from a single founder pair and as of 2014, 45 % of the ancestry was still from this pair. Six other founders have also contributed substantially to the population and managed breeding has increased and evened out their contributions in recent years. Managed breeding has also kept the inbreeding level at the relatively low level of 0.120 in 2014. However, for most of the history of the population, all of the inbreeding was from the single founder pair and in 2014, 76 % of the inbreeding was still from this pair. As a result, the high inbreeding depression previously seen in this population appears to descend from this single pair. Breeding management to maximize founder genome equivalents, which takes into account loss of variation from genetic drift, could increase the genetic representation from the founders, particularly if ancestry from the single founder with only one living descendant is increased.     

Incorporation of new founders into captive populations

This report describes preliminary studies intended to develop generalizations for the optimal incorporation of newcomers into breeding pools. Small populations, which grow from four to a stable size of 16 animals per generation, were simulated on a computer. New founders were introduced and various breeding schemes tried and evaluated for their effect on inbreeding coefficients and founder representation. Two variables were examined for their effects on inbreeding and founder representation: number of progeny produced by crossing new founders with the established population, and number of mates the new founder had from the established population. Increasing the value of these variables to the point at which new-founder representation was equal to the original founders' representations decreased inbreeding. Beyond this point, inbreeding increased.     

Quantifying and managing the loss of genetic variation in a free-ranging population of takahe through the use of pedigrees

Pedigree analysis has clear benefits for the genetic management of threatened populations through the evaluation of inbreeding, population structure and genetic diversity. The use of pedigrees is usually restricted to captive populations and few examples exist of their exclusive use in managing free-ranging populations. One such example is the management of the takahe (Porphyrio hochstetteri), a highly endangered, flightless New Zealand rail at risk from introduced mammalian predators and habitat loss. During the 1980’s and 90’s, as part of the takahe recovery programme, birds were translocated from the sole remnant population in Fiordland to four offshore islands from which introduced predators had been eradicated. The subsequent “island” population, now numbering 83 and thought to be at carrying capacity, has been closely monitored since founding. Detailed breeding records allow us to analyse the island pedigree, which is up to 7 generations deep. Gene-drop analysis indicated that 7.5% of genetic diversity has been lost over the relatively short timeframe since founding (2.1 generations on average; total genetic founders = 31) due to both a failure to equalise founder representation early on and subsequent disproportionate breeding success (founder equivalents = 12.5; founder genome equivalents = 6.6). A high prevalence of close inbreeding will have also impacted on genetic diversity. Predictions from pedigree modelling suggest that 90% genetic diversity will be maintained for only 12 years, but by introducing a low level of immigration from the Fiordland population and permitting the population to grow, 90% GD could be maintained over the next 100 years. More generally, the results demonstrate the value of maintaining pedigrees for wild populations, especially in the years immediately after a translocation event.     

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.     

Use of animals with unknown ancestries in scientifically managed breeding programs

Whether to incorporate animals with unknown ancestries as founders into scientifically managed captive breeding programs, can be a difficult decision. If the animals are offspring of known founders, their inclusion in the breeding program will result in an increased incidence of inbreeding in the captive population. If the animals are additional founders, excluding them from the breeding program will result in the loss of valuable genetic variation. In general, the practice in scientifically managed captive breeding programs is to exclude animals with unknown ancestries to avoid possible inbreeding. A method of estimating the cost of making an incorrect decision on whether to use animals of unknown ancestry as founders both in terms of lost genetic variation and increased inbreeding is presented. It was determined that the loss of genetic variation resulting from excluding founders is always greater than the loss of genetic variation caused by unequal founder line representation resulting from including related animals, as if they were founders. In addition, the increased rate of accumulation of inbreeding resulting from excluding founders will eventually overcome the initial inbreeding resulting from including related animals. However, in some cases, it will take a substantial number of generations for this to occur, and the benefits of possible lowered future expected inbreeding may never be realized. The decision concerning whether to use animals with unknown ancestry should, therefore, be based on the estimated relative costs of making an error, in terms of both lost genetic variation and expected future inbreeding, rather than on avoiding the immediate possibility of increased inbreeding alone. Two examples using studbook data are given to show how this method can be practically applied to the management of captive populations. © 1993 Wiley-Liss, Inc.     

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.     

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.     

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.     

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.     

Pedigrees and the Study of the Wild Horse Population of Assateague Island National Seashore

ABSTRACT Recently, a number of papers have addressed the use of pedigrees in the study of wild populations, highlighting the value of pedigrees in conservation management. We used pedigrees to study the horses (Equus caballus) of Assateague Island National Seashore, Maryland, USA, one of a small number of free-ranging animal populations that have been the subject of long-term studies. This population grew from 28 in 1968 to 175 in 2001, causing negative impacts on the island ecosystem. To minimize these effects, an immunocontraception program was instituted, and horse numbers are slowly decreasing. However, there is concern that this program may negatively affect the genetic health of the herd. We found that although mitochondrial DNA diversity is low, nuclear diversity is comparable to that of established breeds. Using genetic data, we verified and amended maternal pedigrees that had been primarily based on behavioral data and inferred paternity using genetic data along with National Park Service records of the historic ranges of males. The resulting pedigrees enabled us to examine demography, founder contributions, rates of inbreeding and loss of diversity over recent generations, as well as the level of kinship among horses. We then evaluated the strategy of removing individuals (using nonlethal means) with the highest mean kinship values. Although the removal strategy increased the retained diversity of founders and decreased average kinship between individuals, it disproportionately impacted sizes of the youngest age classes. Our results suggest that a combined strategy of controlled breeding and immunocontraception would be more effective than removing individuals with high mean kinships in preserving the long-term health and viability of the herd.     

Genetic structure and individual performance following a recent founding event in a small lizard

Reintroduced populations of threatened species are often founded by a small number of individuals, but maximising genetic diversity is often a criterion for founder selection. Reintroduction of pregnant females has been proposed as a means of maximising productivity and genetic diversity, but it is unclear whether the release of pregnant females increases the effective number of founders. Ten male and 20 gravid female egg-laying skinks (Oligosoma suteri) were reintroduced to Korapuki Island from Green Island, New Zealand in 1992. We sampled the populations on both Green and Korapuki Islands to examine the effect of reintroduction on the genetic structure and fitness of egg-laying skinks following release. The population on Korapuki Island showed multiple genetic signatures of a bottleneck that were not detected in the population on Green Island. At the individual level, juveniles on Korapuki Island were more homozygous than adults on Korapuki and Green Islands. However, we did not find evidence of inbreeding depression using two performance-based surrogates of fitness. Further, the population on Korapuki Island had a significantly larger effective population size than would have been expected by reintroduction of 30 skinks, based on 10,000 simulated populations. The reintroduction of gravid females aided in increasing the effective number of founders, and may be a viable option for maximizing genetic diversity in reintroduced populations, particularly for long-lived species. However, the continued loss of genetic variation in reintroduced populations may have more insidious long-term consequences, such as the loss of adaptive potential, which cannot be assessed in the short-term.     

Parentage analysis in a managed free ranging population of southern white rhinoceros: genetic diversity,pedigrees and management

Small populations are vulnerable to the consequences of breeding within closed groups as the loss of genetic variability can lead to inbreeding depression. Here, we use microsatellite genotypes to assess variability and parentage within a small, managed population of southern white rhinoceros in northern Namibia. Tissue samples gathered from either a modified biopsy darting technique or ear notches allowed us to obtain genotypic data for all individuals in the population. As expected for this species, genetic variability in the population was relatively low (overall H _obs 0.45). In combination with detailed management records for the period 1993–2009, we were able to assign both parents for all 23 offspring. Only one calf of seven in the F₂ generation arose from father–daughter inbreeding within the population. Our analysis revealed that paternity was initially dominated by a single founder bull siring 10 of 13 calves over 9 years; paradoxically, the other founder bull was selected for removal based on observations suggesting he was behaviourally dominant and therefore the likely sire of most calves. We also found that young introduced bulls were breeding successfully within 6 months of their arrival, well before having established their home ranges. We argue that in order to optimally manage and conserve the southern African white rhinoceros meta-population it is essential to have accurate pedigree information and genetic data for all individuals in the numerous small populations that are key to the survival of the species.     

Effects of a recent founding event and intrinsic population dynamics on genetic diversity in an ungulate population

Maintenance of genetic diversity has recently become a management goal for a number of species, due to its importance for present and future population viability. Genetic drift, primarily through differential reproductive success and inbreeding, can accelerate the loss of genetic diversity in recently recovered populations. We attempt to quantify the consequences of these factors on the genetic diversity contained in a small, recently founded wood bison (Bison bison athabascae) population by examining the genetic variation in this conservation herd, the calves born therein, and its large source population. The Hook Lake Wood Bison Recovery Project was initiated to found a disease-free herd of wood bison containing a representative amount of the genetic diversity present in the Wood Buffalo National Park metapopulation. Levels of diversity in the Hook Lake Wood Bison Recovery Project founders are higher than in previous salvage attempts. To examine the effects of differential reproductive success on this population, we monitored parentage of the calves born in the Hook Lake Wood Bison Recovery Project for 3 years since the founders reached sexual maturity. Two of the male founders sired over 90% of the offspring born in this population, which has led to a reduction in diversity in their calves. Monitoring of reproductive success, and incorporation of selective breeding strategies will be required to reduce the rate at which genetic diversity is lost from this small, isolated population. These steps should occur in other recovery projects, particularly when a small number of individuals are capable of dominating reproduction.     

Population Genetics of the Washington National Primate Research Center's (WaNPRC) Captive Pigtailed Macaque (Macaca nemestrina) Population

Pigtailed macaques (Macaca nemestrina) provide an important model for biomedical research on human disease and for studying the evolution of primate behavior. The genetic structure of captive populations of pigtailed macaques is not as well described as that of captive rhesus (M. mulatta) or cynomolgus (M. fascicularis) macaques. The Washington National Primate Research Center houses the largest captive colony of pigtailed macaques located in several different housing facilities. Based on genotypes of 18 microsatellite (short tandem repeat [STR]) loci, these pigtailed macaques are more genetically diverse than captive rhesus macaques and exhibit relatively low levels of inbreeding. Colony genetic management facilitates the maintenance of genetic variability without compromising production goals of a breeding facility. The periodic introduction of new founders from specific sources to separate housing facilities at different times influenced the colony's genetic structure over time and space markedly but did not alter its genetic diversity significantly. Changes in genetic structure over time were predominantly due to the inclusion of animals from the Yerkes National Primate Research Center in the original colony and after 2005. Strategies to equalize founder representation in the colony have maximized the representation of the founders’ genomes in the extant population. Were exchange of animals among the facilities increased, further differentiation could be avoided. The use of highly differentiated animals may confound interpretations of phenotypic differences due to the inflation of the genetic contribution to phenotypic variance of heritable traits. Am. J. Primatol. 74:1017‐1027, 2012. © 2012 Wiley Periodicals, Inc.     

The cryptic genetic structure of the North American captive gorilla population

Western lowland gorillas (Gorilla gorilla gorilla) were imported from across their geographical range to North American zoos from the late 1800s through 1974. The majority of these gorillas were imported with little or no information regarding their original provenance and no information on their genetic relatedness. Here, we analyze 32 microsatellite loci in 144 individuals using a Bayesian clustering method to delineate clusters of individuals among a sample of founders of the captive North American zoo gorilla collection. We infer that the majority of North American zoo founders sampled are distributed into two distinct clusters, and that some individuals are of admixed ancestry. This new information regarding the existence of ancestral genetic population structure in the North American zoo population lays the groundwork for enhanced efforts to conserve the evolutionary units of the western lowland gorilla gene pool. Our data also show that the genetic diversity estimates in the founder population were comparable to those in wild gorilla populations (Mondika and Cross River), and that pairwise relatedness among the founders is no different from that expected for a random mating population. However, the relatively high level of relatedness (R = 0.54) we discovered in a pair of known breeding pairs reveals the need for incorporating genetic relatedness estimates in the captive management of western lowland gorillas.     

The impact of assumptions about founder relationships on the effectiveness of captive breeding strategies

Many breeding programs managed by zoos and aquariums employ strategies that minimize mean kinship as a way of retaining genetic diversity (MK strategies). MK strategies depend on accurate and complete pedigrees, but population founders are generally assumed to be unrelated and not inbred. This assumption was historically necessitated by the unavailability of data on founder relationships, but with DNA techniques it is sometimes now possible to estimate those relationships. We used computer simulations to investigate the impact of founder assumptions on the effectiveness of MK strategies. Individuals with known pedigrees were managed in groups of 10, 30, and 100 founders at two different rates of reproduction and two different degrees of founder relationship. The impact of assuming founders were unrelated was quantified by calculating the differences in gene diversity and inbreeding that were observed between simulations that used known relationships and simulations that assumed founders were unrelated. Results indicated that utilizing known relationships retained 0–2% more gene diversity over ten generations than assuming founders were unrelated, with specific results dependent on the conditions of a given scenario. Similar results were observed for inbreeding, with long-term levels of inbreeding being 0–2% lower when relationships were known. There were higher benefits to knowing founder relationships as reproductive rate increased, as well as when full-siblings were included in small groups of founders. Overall, however, long-term benefits gained from knowing founder relationships were generally small. Therefore, MK strategies probably often produce near optimal results when standard founder assumptions are made.     

Genetic rescue in a severely inbred wolf population

Natural populations are becoming increasingly fragmented which is expected to affect their viability due to inbreeding depression, reduced genetic diversity and increased sensitivity to demographic and environmental stochasticity. In small and highly inbred populations, the introduction of only a few immigrants may increase vital rates significantly. However, very few studies have quantified the long‐term success of immigrants and inbred individuals in natural populations. Following an episode of natural immigration to the isolated, severely inbred Scandinavian wolf (Canis lupus) population, we demonstrate significantly higher pairing and breeding success for offspring to immigrants compared to offspring from native, inbred pairs. We argue that inbreeding depression is the underlying mechanism for the profound difference in breeding success. Highly inbred wolves may have lower survival during natal dispersal as well as competitive disadvantage to find a partner. Our study is one of the first to quantify and compare the reproductive success of first‐generation offspring from migrants vs. native, inbred individuals in a natural population. Indeed, our data demonstrate the profound impact single immigrants can have in small, inbred populations, and represent one of very few documented cases of genetic rescue in a population of large carnivores.     

Early colonisation population structure of a Norway rat island invasion

Colonists undergo non-equilibrium processes such as founder effects, inbreeding and changing population size which influence the mating system and demography of a population. Understanding these processes in colonising populations informs management and helps prevent further invasions. We sampled and genotyped most individuals of a Norway rat (Rattus norvegicus) reinvasion on Moturemu island (5 ha) in New Zealand. Population size was most likely between 30 and 33 rats. Genetic methods detected a clear bottleneck signal from the founding population. Parentage assignment revealed promiscuous mating dominated by a few individuals with increasing inbreeding, both putatively a result of small island size. Combining ecological and genetic data from a single sample allowed inferences on population structure and functioning. Invading Norway rats rapidly achieve population structure similar to established island populations despite a small number of colonists and associated inbreeding. Overcoming these initial obstacles to population establishment contributes to the global success of invasive rats.     

Limited Reintroduction Does Not Always Lead to Rapid Loss of Genetic Diversity: An Example from the American Chestnut (Castanea dentata; Fagaceae)

In restoring species, reasons for introducing limited numbers of individuals at different locations include costs of introduction and maintenance, limited founder supply, and risk “bet hedging.” However, populations initiated from few founders may experience increased genetic drift, inbreeding, and diversity loss. We examined the genetic diversity of an isolated stand of more than 5,000 American chestnut trees relative to that of the 9 surviving stand founders (out of 10 total) planted in the 1880s. We used minisatellite DNA probes to reveal 84 genetic markers (circa 24 loci) among the nine founders, and their genetic diversity was compared with three separate plots of descendant trees, as well as with two natural stands. The descendants were circa 7.3% more heterozygous than the founders (mean estimated H= 0.556 vs. 0.518, respectively; p < 0.0001). Genetic differentiation was not pronounced (F_ST < 0.031), and no markers, including those at low frequency among the founders, were lost in the descendants. The founders and natural transects were not significantly different in H or similarity (mean proportion of bands shared). Special planting or mating protocols for establishment of a vigorous American chestnut population from a low number of founders may not be required to avoid strong effects of genetic drift and inbreeding. These results demonstrate that loss of genetic diversity following reintroduction of a limited number of founders is not always inevitable, such as this case where the species is highly outcrossing, expression of heterozygous advantage may occur, the original founders remain as gene contributors over generations, and the establishing population expands constantly and rapidly.