Captive Populations Of Endangered Species Research Articles

Enforced monoandry over generations induces a reduction of female investment into reproduction in a promiscuous bird.

While uncovering the costs and benefits of polyandry has attracted considerable attention, assessing the net effect of sexual selection on population fitness requires the experimental manipulation of female mating over generations, which is usually only achievable in laboratory populations of arthropods. However, knowing if sexual selection improves or impairs the expression of life‐history traits is key for the management of captive populations of endangered species, which are mostly long‐lived birds and mammals. It might therefore be questionable to extrapolate the results gathered on laboratory populations of insects to infer the net effect of sexual selection on populations of endangered species. Here, we used a longitudinal dataset that has been collected on a long‐lived bird, the houbara bustard, kept in a conservation breeding program, to investigate the effect of enforced monoandry on female investment into reproduction. In captivity, female houbara bustards are artificially inseminated with sperm collected from a single male (enforced monoandry), or sequentially inseminated with semen of different males (polyandry), allowing postcopulatory sexual selection to operate. We identified female lines that were produced either by monoandrous or polyandrous inseminations over three generations, and we compared reproductive investment of females from the two mating system groups. We found that females in the polyandrous lines had higher investment into reproduction as they laid more eggs per season and produced heavier hatchlings. Higher reproductive investment into reproduction in the polyandrous lines did not result from inherited differences from females initially included in the two mating system groups. These results show that removal of sexual selection can alter reproductive investment after only few generations, potentially hindering population fitness and the success of conservation breeding programs.

One of these wolves is not like the other: morphological effects and conservation implications of captivity in Mexican wolves

AbstractMaintaining animal populations in captivity can be a useful way to conserve species, especially those that are extinct in the wild or endangered in their native habitats. These animals could be reintroduced into the wild from captivity if conditions improve. However, captive populations of endangered species are often established with few wild‐caught individuals and are maintained in novel habitats, conditions which may make these populations prone to morphological divergence. Changes in cranial morphology, in particular, may limit reintroduction success because these morphological changes may alter cranial functionality related to capturing and consuming prey. To assess whether unintentional morphological changes occur in captivity, we examined the crania and mandibles of 275 specimens of wild, captive and reintroduced Mexican wolvesCanis lupus baileyi. We detected significant differences in skull size and shape among these populations. Captive specimens displayed the greatest overall shape variation and were significantly differentiated from the wild population in regions of the skull that are essential to cranial functionality. The reintroduced population displayed the narrowest trait distribution, with cranial morphology that grouped consistently with the captive morphotype. The small number of individuals of the founding population along with the increased variation in cranial morphology among captive Mexican wolves suggests that morphological changes in captivity may be related to genetic changes such as genetic drift or relaxed selection. This study helps to define the changes that may occur in captivity, the potential mechanisms behind these shifts, and the ways in which morphological variation in captive populations may impact conservation initiatives.

Captive individuals of endangered Philippine raptors maintain native feather mites (Acariformes: Pterolichoidea) species.

Endangered species of hosts are coupled with endangered species of parasites, which share the risk of co-extinction. Conservation efforts sometimes include breeding of rare species in captivity. Data on parasites of captive populations of endangered species is scarce and the ability of small numbers of captive host individuals to support the biodiversity of native parasites is limited. Examination of ectosymbionts of the critically endangered Philippine eagles and the endangered Mindanao Hawk-Eagle kept at the Philippine Eagle Center, Philippines, revealed three feather mite species despite regular treatment with insecticide powder. No other ectosymbiont taxa were detected. Studies in morphology and molecular phylogeny of these feather mites based on mitochondrial and nuclear DNA markers indicate that species found were typical for Accipitridae. Three new pterolichoid feather mite species (Acari: Pterolichoidea) were described from two species of eagles (Accipitriformes: Accipitridae) endemic to the Philippines: Hieracolichus philippinensis sp. n. (Gabuciniidae) and Pseudalloptinus pithecophagae sp. n. (Pterolichidae) from the Great Philippine Eagle Pithecophaga jefferyi Ogilvie-Grant, 1896, and Pseudogabucinia nisaeti sp. n. (Kramerellidae) from the Mindanao Hawk-Eagle Nisaetus pinskeri Gould, 1863. The presence of H. philippinensis on P. jefferyi supports the recent finding that the Great Philippine Eagle belongs to the lineage of serpent eagles (Circaetinae) rather than to the Harpy and other eagles.

Winning the Genetic Lottery: Biasing Birth Sex Ratio Results in More Grandchildren

Population dynamics predicts that on average parents should invest equally in male and female offspring; similarly, the physiology of mammalian sex determination is supposedly stochastic, producing equal numbers of sons and daughters. However, a high quality parent can maximize fitness by biasing their birth sex ratio (SR) to the sex with the greatest potential to disproportionately outperform peers. All SR manipulation theories share a fundamental prediction: grandparents who bias birth SR should produce more grandoffspring via the favored sex. The celebrated examples of biased birth SRs in nature consistent with SR manipulation theories provide compelling circumstantial evidence. However, this prediction has never been directly tested in mammals, primarily because the complete three-generation pedigrees needed to test whether individual favored offspring produce more grandoffspring for the biasing grandparent are essentially impossible to obtain in nature. Three-generation pedigrees were constructed using 90 years of captive breeding records from 198 mammalian species. Male and female grandparents consistently biased their birth SR toward the sex that maximized second-generation success. The most strongly male-biased granddams and grandsires produced respectively 29% and 25% more grandoffspring than non-skewing conspecifics. The sons of the most male-biasing granddams were 2.7 times as fecund as those of granddams with a 50∶50 bias (similar results are seen in grandsires). Daughters of the strongest female-biasing granddams were 1.2 times as fecund as those of non-biasing females (this effect is not seen in grandsires). To our knowledge, these results are the first formal test of the hypothesis that birth SR manipulation is adaptive in mammals in terms of grandchildren produced, showing that SR manipulation can explain biased birth SR in general across mammalian species. These findings also have practical implications: parental control of birth SR has the potential to accelerate genetic loss and risk of extinction within captive populations of endangered species.

The relative effects of mutation accumulation versus inbreeding depression on fitness in experimental populations of the housefly

AbstractLoss of fitness due to inbreeding depression in small captive populations of endangered species is widely appreciated. Populations of all sizes may also experience loss in fitness when environmental conditions are ameliorated because deleterious alleles may be rendered neutral and accumulate rapidly. Few data exist, however, to demonstrate loss in fitness due to relaxed selection. Loss of fitness in life‐history traits were compared between LARGE (Ne ≥ 500) and SMALL (Ne = 50) populations of the housefly Musca domestica L that were subjected to curtailed life span at 21 days to remove selection on late‐acting deleterious alleles. During the early part of the life history (≤21 days), the rate of decline in fecundity and progeny production over 24 generations was greater in the small (1.5%) than in the large populations <0.2%), but rate of loss in late‐life fecundity and progeny production (>21 days) was equivalent across populations, consistent with neutral theory, and amounted to 1.7% per generation. This rate of loss due to relaxed selection was equivalent to the rate of loss due to inbreeding in populations with an effective size of 50 individuals. Even if captive populations are kept large to avoid inbreeding, breeding them in benign environments where the forces of natural selection are curtailed may jeopardize the capability of these populations to exist in natural environments within few generations. Zoo Biol 20:145–156, 2001. © 2001 Wiley‐Liss, Inc.

Application of Reproduction Technologies to the Conservation of Genetic Resources.

Maintaining the levels of genetic variability in captive populations of endangered species is an important objective of conservation biology. Because of the generally low sizes of captive populations, genetic drift is the main cause of loss of diversity. Several simple management rules, such as equalization of contributions from parents to the next generation, are recommended for minimizing genetic drift, but it cannot be removed completely because of the unavoidable random segregation of heterozygotes. Recent advances in reproductive technology, particularly developed for mammals, are now making a reality of the possibility of using more than one cell from a single meiosis in reproduction. With this technology it is possible to reduce or even completely cancel the genetic drift caused by segregation of heterozygotes. We evaluated the theoretical benefits of the use of such technologies to conservation biology. The effective population size can be increased enormously and, consequently, the amount of drift can be greatly reduced if manipulations in reproduction are made.

Does equalization of family sizes reduce genetic adaptation to captivity?

Genetic adaptation to captive environments is likely to reduce the reproductive fitness of endangered species when they are reintroduced into natural environments. Equalization of family sizes is predicted to halve genetic adaptation to captivity as it removes selection among families and is recommended in captive management of threatened species. This prediction was evaluated by comparing the reproductive fitnesses of replicate populations of Drosophila maintained using either equal (EFS) or variable family sizes (VFS) for 25 generations in captivity under uncrowded conditions on a medium containing CuSO4. After 25 generations, EFS populations produced 8.8% more offspring per pair than their outbred base population on CuSO4 medium, while VFS produced 17.5% more. Consequently, the rate of genetic adaptation to captivity in EFS was about half that in VFS, as predicted. In simulated ‘wild’ conditions (crowded, competitive conditions on medium lacking CuSO4), both treatments showed much lower reproductive fitness than their outbred base population, the reductions being 38% in EFS populations and 43% in VFS populations. Surprisingly, reproductive fitness of the two treatments did not differ significantly under these conditions. These results raise doubts about the ability of equalization of family sizes to reduce genetic deterioration that adversely affects reintroduction success for captive populations of endangered species.

Does equalization of family sizes reduce genetic adaptation to captivity?

AbstractGenetic adaptation to captive environments is likely to reduce the reproductive fitness of endangered species when they are reintroduced into natural environments. Equalization of family sizes is predicted to halve genetic adaptation to captivity as it removes selection among families and is recommended in captive management of threatened species. This prediction was evaluated by comparing the reproductive fitnesses of replicate populations of Drosophila maintained using either equal (EFS) or variable family sizes (VFS) for 25 generations in captivity under uncrowded conditions on a medium containing CuSO4. After 25 generations, EFS populations produced 8.8% more offspring per pair than their outbred base population on CuSO4 medium, while VFS produced 17.5% more. Consequently, the rate of genetic adaptation to captivity in EFS was about half that in VFS, as predicted. In simulated ‘wild’ conditions (crowded, competitive conditions on medium lacking CuSO4), both treatments showed much lower reproductive fitness than their outbred base population, the reductions being 38% in EFS populations and 43% in VFS populations. Surprisingly, reproductive fitness of the two treatments did not differ significantly under these conditions. These results raise doubts about the ability of equalization of family sizes to reduce genetic deterioration that adversely affects reintroduction success for captive populations of endangered species.

Quantitative genetics in conservation biology.

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

Environmental Enrichment for Australian Mammals

AbstractMany of Australia's nocturnal mammals are rare or endangered in the wild. The behavioural integrity of captive populations of endangered species can be maintained through the application of environmental enrichment techniques. This study investigated the effectiveness of feeding enrichment in promoting behavioural diversity, enclosure usage and species-typical behaviours in the ghost bat(Macroderma gigas)and the yellow-bellied glider(Petaurus australis). Animals were observed for 300 min day-1 over three consecutive time periods: baseline (12 non-consecutive days); enrichment: (12 consecutive days); and post-enrichment: (12 non-consecutive days). The use of a live insect dispenser decreased grooming and increased out-of-sight and social behaviour in the ghost bat. Artificial gum trees promoted species-typical behaviours in the yellow-bellied glider. Enrichment for nocturnal mammals had variable results and different welfare implications for these animals.

Potential of assisted breeding techniques for the conservation of endangered mammalian species in captivity: a review

An alarming worldwide extinction of animal species is taking place as a result of the activities of the increasing global human population. The original ranges of many animal species are...

Paternity determination in captive lowland gorillas and orangutans and wild mountain gorillas by microsatellite analysis

Paternity exclusion studies provide useful information for testing certain theories of behavioral ecology and for the management and conservation of both wild and captive populations of endangered species. This study used eight human nuclear microsatellite loci, in the absence of species-specific PCR primers, to genetically identify the sires of 12 captive lowland gorillas (Gorilla gorilla gorilla) and 2 captive orangutans (Pongo pygmaeus pygmaeus andPongo p. abelii). Parentage assignments were confirmed by excluding all except a single potential sire for each offspring with the least two loci. Sire-offspring relationships were verified in 12 of the 14 cases, and reassigned in the case of two gorilla offspring. The orangutan paternity typing was supplemented by DNA fingerprinting. Additionally, five of the eight microsatellite loci, in conjunction with behavioral data, were used for a non-exhaustive set of paternity exclusions for five wild mountain gorillas (Gorilla g. beringei). The eight loci described in this study should be useful additions to the tools available for the study of genetics in the great apes.

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

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

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

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

Minimizing kinship in captive breeding programs

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

THE GENETIC INTERPRETATION OF INBREEDING DEPRESSION AND OUTBREEDING DEPRESSION.

Inbreeding with close relatives and outbreeding with members of distant populations can both result in deleterious shifts in the means of fitness-related characters, most likely for very different reasons. Such processes often occur simultaneously and have important implications for the evolution of mating systems, dispersal strategies, and speciation. They are also relevant to the design of breeding strategies for captive populations of endangered species. A general expression is presented for the expected phenotype of an individual under the joint influence of inbreeding and crossbreeding. This expression is a simple function of the inbreeding coefficient, of source and hybridity indices of crossbreeding, and of specific forms of gene action. Application of the model may be of use in identifying the mechanistic bases for a number of evolutionary phenomena such as the shift from outbreeding enhancement to outbreeding depression that occurs with population divergence.

THE DIVERGENCE OF NEUTRAL QUANTITATIVE CHARACTERS AMONG PARTIALLY ISOLATED POPULATIONS.

The neutral model of phenotypic evolution has yielded several simple predictions about the long-term rates of between-population divergence of polygenic traits and about the equilibrium level of within-population variance when mutation and random genetic drift are the sole evolutionary forces. These conclusions must be modified if populations are only partially isolated. A quantitative model is presented for the development of within- and between-population variance for neutral quantitative characters in pairs of populations with arbitrary effective sizes and migration rates. Both the variance in the base population and subsequent variance generated by mutation are considered, and several dynamical and equilibrium properties are shown to be adequately described by simple approximations. The resultant formulations provide some insight into the sensitivity of measures of morphological distance to gene flow, the necessity of isolation for the accumulation of variation between incipient species, and the consequences of gene flow into captive populations of endangered species.