A preliminary study on the social relationships in a semi-free ranging colony of sun-tailed monkeys (Cercopithecus solatus), a species recently discovered in Gabon

In 1984, a species of guenon endemic to Gabon was discovered: the sun-tailed monkey (Cercopithecus solatus). This species is difficult to locate and observe in the wild, and hence to date has been little studied. The Centre International de Recherches Médicales de Franceville (CIRMF), Gabon, houses the world’s only breeding colony ofC. solatus, on which eco-ethological investigations can be carried out in a semi-free ranging environment. The data reported here present the first results of observations on the social relationships of this colony and support the scant field observations available on this species, showing a basic social unit of one adult male and several females with their offspring. The resident male systematically repulses any second adult male in proximity to the group. A clear hierarchy exists among the females, with mature female offspring eventually acquiring a rank just below that of their mother.     

Sustainability of the South China tiger: implications of inbreeding depression and introgression

The South China tiger (Panther tigris amoyensis) is critically endangered with 73 remaining individuals living in captivity, all derived from six wild founders since 1963. The population shows a low level of juvenile survivorship and reproductive difficulties, and faces a huge conservation challenge. In this study, inbreeding depression and genetic diversity decline were examined by using pedigree data and 17 microsatellites. The constant B, which is related to the number of lethal equivalents, was estimated to be 0 for the offspring of noninbred parents, but was >0 for the offspring of inbred parents and for all offspring. Percentage of successfully breeding tigers inversely correlated with inbreeding level (r = −0.626, α = 0.05). Taken together, these findings suggest the population is suffering from inbreeding depression in juvenile survivorship and fecundity. No significant correlation was detectable for the mean litter size with f of either dams (r = −0.305, α = 0.46) or kittens (r = 0.105, α = 0.71), indicating litter size was not strongly subject to inbreeding depression. The average number of alleles per locus was 4.24 ± 1.03 (SE), but effective number of alleles was only 2.53 ± 0.91. Twenty-one alleles carried by early breeders at 13 loci were absent in the present breeders and potential breeders. Multilocus heterozygosity was inversely correlated with inbreeding levels (r = −0.601, α = 0.004). These findings suggest rapid allelic diversity loss is occurring in this small captive population and that heterozygosity is being lost as it becomes more inbred. Our phylogenetic analysis supports past work indicating introgression from northern Indochinese tigers in the population. As no wild representatives of the South China tiger can be added to the captive population, we may consider the alternate scenario of further introgression in the interest of countering inbreeding depression and declining genetic diversity.     

Inbreeding depression in development,survival, and reproduction in the adzuki bean beetle (<Emphasis Type="Italic">Callosobruchus chinensis</Emphasis>)

Inbreeding depression of an aspect of fitness is observed in many insects, but the traits that are of importance for inbreeding depression of fitness remain poorly understood. Here the magnitude of inbreeding depression of fitness-related traits in the development and adult stages was measured in a captive population of the adzuki bean beetle, Callosobruchus chinensis (Coleoptera: Bruchidae). Beetles produced by full-sib matings had 8% lower survival in the development stage than did beetles produced by unrelated matings. Although inbred and outbred offspring did not differ in body size after emergence, inbred offspring took 2–3% longer to develop to emergence. This indicates inbreeding depression of growth rate. At the adult stage, inbreeding had no significant effect on longevity, however lifetime offspring production was reduced by 11%. Thus, the magnitude of inbreeding depression was relatively large for offspring production. This suggests inbreeding depression of fitness manifests, to a particularly significant extent, in reduced productivity. This study shows the C. chinensis population, which has been in captivity for more than 100 generations, harbors genetic loads.     

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.     

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.     

Inbreeding depression in an insect with maternal care: influences of family interactions,life stage and offspring sex

Although inbreeding is commonly known to depress individual fitness, the severity of inbreeding depression varies considerably across species. Among the factors contributing to this variation, family interactions, life stage and sex of offspring have been proposed, but their joint influence on inbreeding depression remains poorly understood. Here, we demonstrate that these three factors jointly shape inbreeding depression in the European earwig, Forficula auricularia. Using a series of cross‐breeding, split‐clutch and brood size manipulation experiments conducted over two generations, we first showed that sib mating (leading to inbred offspring) did not influence the reproductive success of earwig parents. Second, the presence of tending mothers and the strength of sibling competition (i.e. brood size) did not influence the expression of inbreeding depression in the inbred offspring. By contrast, our results revealed that inbreeding dramatically depressed the reproductive success of inbred adult male offspring, but only had little effect on the reproductive success of inbred adult female offspring. Overall, this study demonstrates limited effects of family interactions on inbreeding depression in this species and emphasizes the importance of disentangling effects of sib mating early and late during development to better understand the evolution of mating systems and population dynamics.     

Survival of captive-born Ovis canadensis in North American zoos

The survival rate of North American bighorn sheep, Ovis canadensis, housed in several zoological gardens was analyzed. Complete herd histories, including birth and death data as well as causes of mortality, were collected from seven institutions. Lambs were divided into inbred and noninbred animals, with lambs being considered inbred if they had an inbreeding coefficient greater than zero. The rate of survival of inbred and noninbred lambs was compared using “survival equalling one year” and “survival equalling six months.” Another analysis compared the survival rate of male and female inbred lambs and male and female noninbred lambs. Age at death was also compared in inbred and noninbred lambs. The analysis of the data for the seven collections, located in various geographic areas and housing various subspecies, indicates that inbreeding depression is a mortality factor in the captive management of North American bighorn sheep. Therefore, long-term survival of captive or isolated wild populations will depend on maintaining genetic diversity within the herds through careful selection of breeding stock in captive populations and introduction of nonrelated animals into isolated wild populations.     

Inbreeding,inbreeding depression,and infidelity in a cooperatively breeding bird*

Inbreeding depression plays a major role in shaping mating systems: in particular, inbreeding avoidance is often proposed as a mechanism explaining extra‐pair reproduction in socially monogamous species. This suggestion relies on assumptions that are rarely comprehensively tested: that inbreeding depression is present, that higher kinship between social partners increases infidelity, and that infidelity reduces the frequency of inbreeding. Here, we test these assumptions using 26 years of data for a cooperatively breeding, socially monogamous bird with high female infidelity, the superb fairy‐wren (Malurus cyaneus). Although inbred individuals were rare (～6% of offspring), we found evidence of inbreeding depression in nestling mass (but not in fledgling survival). Mother–son social pairings resulted in 100% infidelity, but kinship between a social pair did not otherwise predict female infidelity. Nevertheless, extra‐pair offspring were less likely to be inbred than within‐pair offspring. Finally, the social environment (the number of helpers in a group) did not affect offspring inbreeding coefficients or inbreeding depression levels. In conclusion, despite some agreement with the assumptions that are necessary for inbreeding avoidance to drive infidelity, the apparent scarcity of inbreeding events and the observed levels of inbreeding depression seem insufficient to explain the ubiquitous infidelity in this system, beyond the mother–son mating avoidance.     

CORRELATED INBREEDING AMONG RELATIVES: OCCURRENCE,MAGNITUDE, AND IMPLICATIONS

Understanding the magnitude and causes of genetic and phenotypic resemblance among relatives is key to understanding evolutionary processes. Contrary to basic expectation, individual coefficients of inbreeding ( f) were recently hypothesized to be intrinsically correlated across parents and offspring in structured populations, potentially creating an additional source of phenotypic resemblance in traits that show inbreeding depression. To test this hypothesis, we used individual‐based simulations to quantify the parent–offspring correlations in f arising under random mating in populations of different size, immigration rate, and mating system. Parent–offspring correlations in f were typically positive (median r≈ 0.2–0.4) in relatively small and isolated populations. Relatively inbred parents therefore produced relatively inbred offspring on average, although the magnitude of this effect varied considerably among replicate populations. Correlations were higher given more generations of random mating, greater variance in reproductive success, polygynous rather than monogamous mating, and for midparent–offspring rather than parent–offspring relationships. Furthermore, f was also positively correlated across half‐siblings, and closer relatives had more similar inbreeding coefficients across entire generations. Such intrinsic resemblance in f among relatives could provide an additional genetic benefit of mate choice and bias quantitative genetic analyses that do not account for correlated inbreeding depression.     

Inbreeding depression in ring-tailed lemurs (<Emphasis Type="Italic">Lemur catta</Emphasis>): genetic diversity predicts parasitism,immunocompetence, and survivorship

The consequences of inbreeding have been well studied in a variety of taxa, revealing that inbreeding has major negative impacts in numerous species, both in captivity and in the wild; however, as trans-generational health data are difficult to obtain for long-lived, free-ranging species, similar analyses are generally lacking for nonhuman primates. Here, we examined the long-term effects of inbreeding on numerous health estimates in a captive colony of ring-tailed lemurs (Lemur catta), housed under semi-natural conditions. This vulnerable strepsirrhine primate is endemic to Madagascar, a threatened hotspot of biodiversity; consequently, this captive population represents an important surrogate. Despite significant attention to maintaining the genetic diversity of captive animals, breeding colonies invariably suffer from various degrees of inbreeding. We used neutral heterozygosity as an estimate of inbreeding and showed that our results reflect genome-wide inbreeding, rather than local genetic effects. In particular, we found that genetic diversity affects several fitness correlates, including the prevalence and burden of Cuterebra parasites and a third (N = 6) of the blood parameters analyzed, some of which reflect immunocompetence. As a final validation of inbreeding depression in this captive colony, we showed that, compared to outbred individuals, inbred lemurs were more likely to die earlier from diseases. Through these analyses, we highlight the importance of monitoring genetic variation in captive animals—a key objective for conservation geneticists—and provide insight into the potential negative consequences faced by small or isolated populations in the wild. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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.     

Testing alternative captive breeding strategies with the subsequent release into the wild

We used the housefly (Musca domestica L.) as an experimental model to compare two strategies for the captive breeding of an endangered species: a strategy to minimize inbreeding and balance founder contributions (termed “MAI” for “maximum avoidance of inbreeding”) versus a scheme to select against less fit individuals (disregarding relatedness). By balancing the initial founder contributions, the MAI protocol was analogous to methods for minimizing kinship. In both breeding strategies, the population growth rate was limited to a maximum increase of 50% per generation. Five replicate populations, each starting with five male–female pairs, were subjected to five generations of captive breeding. Six generations of simulated “release into the wild” allowed ad lib breeding with less restrictive population growth potential, in either a benign or stressful environment (i.e., constant or variable temperature). Population size, fecundity, and fertility were assayed throughout the experiment, with juvenile‐to‐adult survival assayed in the second phase of the project. Allozyme assays determined the resultant inbreeding coefficients from the captive breeding schemes. The MAI breeding scheme resulted in significantly lower inbreeding coefficients and higher fitness, with qualitatively reduced extinction potential, most notable in the stressful environment. Spontaneous fitness rebounds suggested that the MAI strategy facilitated some form of purging of inbreeding depression effects. Importantly, the advantages of the MAI strategy were difficult to detect during the captive breeding phase, suggesting that the long‐term advantages of the MAI approach could be underestimated in actual breeding programs. We concur with the common recommendation of maximum avoidance of inbreeding at least for systems with low reproductive potential. Zoo Biol 0:1–18, 2005. © 2005 Wiley‐Liss, Inc.     

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.     

Differential inbreeding tolerance in two geographically distinct strains of root voles Microtus oeconomus

Two geographically distinct strains of Microtus oeconomus, each consisting of an inbred (sibling mating) and an outbred treatment group, were bred in the laboratory over three generations to determine the effects of inbreeding on reproductive parameters, growth rates of young and paternal behavior The southern strain (orginating from southern Norway) suffered from depressed reproductive rate (litter size and pregnancy rates) most likely due to inbreeding, while no effects of inbreeding were detected m the northern strain (originating from northern Norway) This result questions previous generalizations about inbreeding tolerance at the species level for Microtus Growth rates and paternal behavior did not differ significantly between inbred and outbred voles in either strain Inbreeding depression rather than inbreeding avoidance is the most likely mechanism behind the depression in reproductive parameters of inbred southern voles This is suggested by the decrease in the proportion of breeding pairs with the number of generations of inbreeding, and by the reduced litter size of inbred compared with outbred pairs Field and laboratory studies have shown that behavioral and demographic traits, possibly related to the degree of inbreeding, differ between the two strains which suggests that inbreeding tolerance might be a life history adaptation     

Absence of deleterious effects of inbreeding in rhesus macaques

The limited availability of rhesus macaques through importation and the need for large numbers of them for use in biomedical research in this country have led to large- scale efforts to breed them domestically in captive groups. Since gene flow into the groups is usually restricted, consanguineous inbreeding can lead to inbreeding depression, which is characterized by increases in mortality, declines in fertility, and reductions in traits associated with physiological efficiency. For this reason, it is desirable to determine the level of inbreeding at which inbreeding depression occurs in rhesus macaques. I compared fertility, mortality, and the rate of weight gain in inbred and noninbred rhesus monkeys in three captive groups. There is no evidence of inbreeding depression in rhesus macaques whose inbreeding coefficients are ≤ 0.125, a level at which inbreeding depression is known to occur in some species.     

Significant genetic admixture after reintroduction of peregrine falcon (<Emphasis Type="Italic">Falco peregrinus</Emphasis>) in Southern Scandinavia

The peregrine falcon (Falco peregrinus) population in southern Scandinavia was almost extinct in the 1970’s. A successful reintroduction project was launched in 1974, using captive breeding birds of northern and southern Scandinavian, Finnish and Scottish origin. We examined the genetic structure in the pre-bottleneck population using eleven microsatellite markers and compared the data with the previously genotyped captive breeding population and contemporary wild population. Museum specimens between 53 and 130 years old were analyzed. Despite an apparent loss of historical genetic diversity, the contemporary population shows a relatively high level of genetic variation. Considerable gene introgression from captive breeding stock used to repopulate the former range of southern Scandinavian peregrines may have altered the genetic composition of this population. Both the historical and contemporary northern and southern Scandinavian populations are genetically differentiated. The reintroduction project implemented in the region and the use of non-native genetic stock likely prevented the southern Scandinavian population from extinction and thus helped maintain the level of genetic diversity and prevent inbreeding depression. The population is rapidly increasing in numbers and range and shows no indication of reduced fitness or adaptive capabilities in the wake of the severe bottleneck and the reintroduction.     

Experimental evolution of the genetic load and its implications for the genetic basis of inbreeding depression

The degree to which, and rapidity with which, inbreeding depression can be purged from a population has important implications for conservation biology, captive breeding practices, and invasive species biology. The degree and rate of purging also informs us regarding the genetic mechanisms underlying inbreeding depression. We examine the evolution of mean survival and inbreeding depression in survival following serial inbreeding in a seed-feeding beetle, Stator limbatus, which shows substantial inbreeding depression at all stages of development. We created two replicate serially inbred populations perpetuated by full-sib matings and paired with outbred controls. The genetic load for the probability that an egg produces an adult was purged at approximately 0.45-0.50 lethal equivalents/generation, a reduction of more than half after only three generations of sib-mating. After serial inbreeding we outcrossed all beetles then measured (1) larval survival of outcrossed beetles and (2) inbreeding depression. Survival of outcrossed beetles evolved to be higher in the serially inbred populations for all periods of development. Inbreeding depression and the genetic load were significantly lower in the serially inbred than control populations. Inbreeding depression affecting larval survival of S. limbatus is largely due to recessive deleterious alleles of large effect that can be rapidly purged from a population by serial sib-mating. However, the effectiveness of purging varied among the periods of egg/larval survival and likely varies among other unstudied fitness components. This study presents novel results showing rapid and extensive purging of the genetic load, specifically a reduction of as much as 72% in only three generations of sib-mating. However, the high rate of extinction of inbred lines, despite the lines being reared in a benign laboratory environment, indicates that intentional purging of the genetic load of captive endangered species will not be practical due to high rates of subpopulation extinction.     

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.     

Molecular genetic analysis of a captive-breeding program: the vulnerable endemic Jamaican yellow boa

The endemic Jamaican boa (or “yellow boa”, Epicrates subflavus) is a vulnerable species of the Caribbean biodiversity hotspot whose natural populations greatly declined mainly due to predation by introduced species, human persecution, and habitat destruction. A captive breeding program was initiated in 1976 and rationalized in 2002 by the establishment of a European Endangered Species Program. During the last 30 years, more than 600 offspring, of which 80 are still alive today, have been produced and distributed among European host institutions and privates. Here, using nine nuclear microsatellite loci and a fragment of the mitochondrial cytochrome b gene, we (i) determine the natural population from which the founders originate, (ii) identify parental allocation errors and ambiguities in the studbook, and (iii) assess the genetic diversity and estimate levels of inbreeding of the current captive population based on loss of alleles, variance in reproductive success, and relatedness among individuals. Combining measures of relatedness derived from multilocus genotypes with practical parameters such as age of animals and localization of host institutions, we propose mating groups that would maximize genetic diversity in the captive population of the Jamaican boa. Our analyses provide guidance for a more efficient breeding program that, in turn, could be used as the starting point of a repatriation program to increase the probability of the species long-term survival. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

How relatedness between mates influences reproductive success: An experimental analysis of self‐fertilization and biparental inbreeding in a marine bryozoan

Kin associations increase the potential for inbreeding. The potential for inbreeding does not, however, make inbreeding inevitable. Numerous factors influence whether inbreeding preference, avoidance, or tolerance evolves, and, in hermaphrodites where both self‐fertilization and biparental inbreeding are possible, it remains particularly difficult to predict how selection acts on the overall inbreeding strategy, and to distinguish the type of inbreeding when making inferences from genetic markers. Therefore, we undertook an empirical analysis on an understudied type of mating system (spermcast mating in the marine bryozoan, Bugula neritina) that provides numerous opportunities for inbreeding preference, avoidance, and tolerance. We created experimental crosses, containing three generations from two populations to estimate how parental reproductive success varies across parental relatedness, ranging from self, siblings, and nonsiblings from within the same population. We found that the production of viable selfed offspring was extremely rare (only one colony produced three selfed offspring) and biparental inbreeding more common. Paternity analysis using 16 microsatellite markers confirmed outcrossing. The production of juveniles was lower for sib mating compared with nonsib mating. We found little evidence for consistent inbreeding, in terms of nonrandom mating, in adult samples collected from three populations, using multiple population genetic inferences. Our results suggest several testable hypotheses that potentially explain the overall mating and dispersal strategy in this species, including early inbreeding depression, inbreeding avoidance through cryptic mate choice, and differential dispersal distances of sperm and larvae.