Selection In Captivity Research Articles

Maintenance of genetic variation in quantitative traits of a woodland rodent during generations of captive breeding

Breeding programs to conserve diversity are predicated on the assumption that genetic variation in adaptively important traits will be lost in parallel to the loss of variation at neutral loci. To test this assumption, we monitored quantitative traits across 18 generations of Peromyscus leucopus mice propagated with protocols that mirror breeding programs for threatened species. Ears, hind feet, and tails became shorter, but changes were reversible by outcrossing and therefore were due to accumulated inbreeding. Heritability of ear length decreased, because of an increase in phenotypic variance rather than the expected decrease in additive genetic variance. Additive genetic variance in hind foot length increased. This trait initially had low heritability but large dominance or common environmental variance contributing to resemblance among full-sibs. The increase in the additive component indicates that there was conversion of interaction variances to additive variance. For no trait did additive genetic variation decrease significantly across generations. These findings indicate that the restructuring of genetic variance that occurs with genetic drift and novel selection in captivity can prevent or delay the loss of phenotypic and heritable variation, providing variation on which selection can act to adapt populations to captivity and perhaps later to readapt to more natural habitats after release. Therefore, the importance of minimizing loss of gene diversity from conservation breeding programs for threatened wildlife species might lie in preventing immediate reduction in individual fitness due to inbreeding and protecting allelic diversity for long-term evolutionary change, more so than in protecting variation in quantitative traits for rapid re-adaptation to wild environments.

Domestication and fitness in the wild: A multivariate view.

Domesticated species continually escaping and interbreeding with wild relatives impose a migration load on wild populations. As domesticated stocks become increasingly different as a result of artificial and natural selection in captivity, fitness of escapees in the wild is expected to decline, reducing the effective rate of migration into wild populations. Recent theory suggest that this may alleviate and eventually eliminate the resulting migration load. I develop a multivariate model of trait and wild fitness evolution resulting from the joint effects of artificial and natural selection in the captive environment. Initially, the evolutionary trajectory is dominated by the effects of artificial selection causing a fast initial decline in fitness of escapees in the wild. In later phases, through the counteracting effects of correlational multivariate natural selection in captivity, the mean phenotype is pushed in directions of weak stabilizing selection, allowing a sustained response in the trait subject to artificial selection. Provided that there is some alignment between the adaptive landscapes in the wild and in captivity, these phases are associated with slower rates of decline in wild fitness of the domesticated stock, suggesting that detrimental effects on wild populations are likely to remain a concern in the foreseeable future.

Family Dominance at the Fry Stage Weakly Influences Mean Family Body Length at Smolting in Hatchery‐Reared Steelhead

AbstractSteelhead Oncorhynchus mykiss reared in hatcheries rapidly adapt to captivity. However, the traits under selection in captivity are not well understood. Hatchery‐reared salmonids are generally more aggressive than wild fish. Therefore, it is possible that selection in hatcheries favors increased aggressiveness because aggressive fish may dominate food resources and grow larger, resulting in a fitness advantage at release. We tested whether family dominance at the fry stage correlates with mean family fork length at smolting of the same families raised in a parallel experiment. Family dominance was assessed when families were first interacting with each other as fry. Juveniles in the parallel experiment were raised at high or low density to determine whether the effect of family dominance on mean family fork length was stronger at low density. More‐dominant families were slightly larger at smolting, and the effect changed little between density treatments. Although the effect we observed was modest, these data are consistent with the hypothesis that dominance as fry is a trait under selection in hatcheries.Received April 8, 2016; accepted July 28, 2016 Published online October 7, 2016

The efficiency of close inbreeding to reduce genetic adaptation to captivity.

Although ex situ conservation is indispensable for thousands of species, captive breeding is associated with negative genetic changes: loss of genetic variance and genetic adaptation to captivity that is deleterious in the wild. We used quantitative genetic individual-based simulations to model the effect of genetic management on the evolution of a quantitative trait and the associated fitness of wild-born individuals that are brought to captivity. We also examined the feasibility of the breeding strategies under a scenario of a large number of loci subject to deleterious mutations. We compared two breeding strategies: repeated half-sib mating and a method of minimizing mean coancestry (referred to as gc/mc). Our major finding was that half-sib mating is more effective in reducing genetic adaptation to captivity than the gc/mc method. Moreover, half-sib mating retains larger allelic and adaptive genetic variance. Relative to initial standing variation, the additive variance of the quantitative trait increased under half-sib mating during the sojourn in captivity. Although fragmentation into smaller populations improves the efficiency of the gc/mc method, half-sib mating still performs better in the scenarios tested. Half-sib mating shows two caveats that could mitigate its beneficial effects: low heterozygosity and high risk of extinction when populations are of low fecundity and size and one of the following conditions are met: (i) the strength of selection in captivity is comparable with that in the wild, (ii) deleterious mutations are numerous and only slightly deleterious. Experimental validation of half-sib mating is therefore needed for the advancement of captive breeding programs.

Evaluating Alternative Strategies for Minimizing Unintended Fitness Consequences of Cultured Individuals on Wild Populations

Artificial propagation strategies often incur selection in captivity that leads to traits that are maladaptive in the wild. For propagation programs focused on production rather than demographic contribution to wild populations, effects on wild populations can occur through unintentional escapement or the need to release individuals into natural environments for part of their life cycle. In this case, 2 alternative management strategies might reduce unintended fitness consequences on natural populations: (1) reduce selection in captivity as much as possible to reduce fitness load (keep them similar), or (2) breed a separate population to reduce captive-wild interactions as much as possible (make them different). We quantitatively evaluate these 2 strategies with a coupled demographic-genetic model based on Pacific salmon hatcheries that incorporates a variety of relevant processes and dynamics: selection in the hatchery relative to the wild, assortative mating based on the trait under selection, and different life cycle arrangements in terms of hatchery release, density dependence, natural selection, and reproduction. Model results indicate that, if natural selection only occurs between reproduction and captive release, the similar strategy performs better. However, if natural selection occurs between captive release and reproduction, the different and similar strategies present viable alternatives to reducing unintended fitness consequences because of the greater opportunity to purge maladaptive individuals. In this case, the appropriate approach depends on the feasibility of each strategy and the demographic goal (e.g., increasing natural abundance, or ensuring that a high proportion of natural spawners are naturally produced). In addition, the fitness effects of hatchery release are much greater if hatchery release occurs before (vs. after) density-dependent interactions. Given the logistical challenges to achieving both the similar and different strategies, evaluation of not just the preferred strategy but also the consequences of failing to achieve the desired target is critical.

Behavioural type in newly emerged steelhead Oncorhynchus mykiss does not predict growth rate in a conventional hatchery rearing environment

Behavioural assays were conducted on newly emerged steelhead Oncorhynchus mykiss to investigate the presence of behavioural syndromes and to determine whether behavioural type in young fish predicts growth rate in a conventional hatchery rearing environment. Individual fry were consistent in their position choice and activity behaviours across safe and unsafe contexts, as well as among assays conducted on different days. Position choice and activity behaviours, however, were not necessarily correlated to each other. Both behaviours predicted feeding rates during behavioural assays, but there was no relationship between fry behaviour and subsequent growth rate or survival during the first 3 months of hatchery rearing. These results support the hypothesis that selection in captivity may be relaxed with respect to behavioural type rather than directional, allowing for increased behavioural variance in domesticated populations. Modest magnitudes of correlations among fry behaviours, however, suggest that behavioural type may be unstable at the onset of the juvenile feeding stage.

Captive breeding genetics and reintroduction success

Since threatened species are generally incapable of surviving in their current, altered natural environments, many conservation programs require to preserve them through ex situ conservation techniques prior to their reintroduction into the wild. Captive breeding provides species with a benign and stable environment but has the side effect to induce significant evolutionary changes in ways that compromise fitness in natural environments. I developed a model integrating both demographic and genetic processes to simulate a captive-wild population system. The model was used to examine the effect of the relaxation of selection in captivity on the viability of the reintroduced population, in interaction with the reintroduction method and various species characteristics. Results indicate that the duration of the reintroduction project (i.e., time from the foundation of the captive population to the last release event) is the most important determinant of reintroduction success. Success is generally maximized for intermediate project duration allowing to release a sufficient number of individuals, while maintaining the number of generations of relaxed selection to an acceptable level. In cases where a long residence time in captivity cannot be avoided, the use of distinct, genetically independent captive breeding units allows more efficient purging of the genetic load in the reintroduced population, and substantially improves its viability. Overall, the study allows to identify situations in which the genetic cost associated with selection relaxation may overwhelm the demographic benefits of programs.

Wildlife conservation and animal temperament: causes and consequences of evolutionary change for captive, reintroduced, and wild populations

AbstractWe argue that animal temperament is an important concept for wildlife conservation science and review causes and consequences of evolutionary changes in temperament traits that may occur in captive‐breeding programmes. An evolutionary perspective is valid because temperament traits are heritable, linked to fitness and potentially subject to intense selection in captivity. Natural, sexual and artificial selection can cause permanent shifts in temperament, reducing the diversity of temperament traits, diversity that may be critical to reintroduction success. Breeding programmes that ignore temperament risk leading the captive population towards domestication. Furthermore, shifts in temperament may involve alterations in linked morphological and physiological traits, and selection may even change functional relationships between traits. Captive‐breeding programmes can reduce changes in temperaments by closely monitoring temperament traits, equalizing reproductive success between temperament morphs and using environmental enrichment to reduce captive stress. Under certain circumstances, knowledge about temperament may also provide a useful tool to optimize captive reproduction and to increase reintroduction success. Outside reintroduction programmes, temperament can mediate responses to human contact, hunting, exploitation, habitat fragmentation and disease transmission. Consideration of temperaments could strengthen both captive and wild conservation efforts.

Rapid evolution of egg size in captive salmon.

Captive breeding and release programs, widely used to supplement populations of declining species, minimize juvenile mortality to achieve rapid population growth. However, raising animals in benign environments may promote traits that are adaptive in captivity but maladaptive in nature. In chinook salmon, hatchery rearing relaxes natural selection favoring large eggs, allowing fecundity selection to drive exceptionally rapid evolution of small eggs. Trends toward small eggs are also evident in natural populations heavily supplemented by hatcheries, but not in minimally supplemented populations. Unintentional selection in captivity can lead to rapid changes in critical life-history traits that may reduce the success of supplementation or reintroduction programs.

Selection in Captivity during Supportive Breeding May Reduce Fitness in the Wild

Abstract: I used a quantitative genetic model to explore the effects of selection on the fitness of a wild population subject to supportive breeding. Supportive breeding is the boosting of a wild population's size by breeding part of the population in captivity and releasing the captive progeny back into the wild. The model assumes that a single trait is under selection with different optimum trait values in the captive and wild environments. The model shows that when the captive population is closed to gene flow from the wild population, even low levels of gene flow from the captive population to the wild population will shift the wild population's mean phenotype so that it approaches the optimal phenotype in captivity. If the captive population receives gene flow from the wild, the shift in the wild population's mean phenotype becomes less pronounced but can still be substantial. The approach to the new mean phenotype can occur in less than 50 generations. The fitness consequences of the phenotypic shift depend on the details of the model, but a>30% decline in fitness can occur over a broad range of parameter values. The rate of gene flow between the two environments, and hence the outcome of the model, is sensitive to the wild environment's carrying capacity and the population growth rate it can support. The results have two important implications for conservation efforts. First, they show that selection in captivity may significantly reduce a wild population's fitness during supportive breeding and that even continually introducing wild individuals into the captive population will not eliminate this effect entirely. Second, the sensitivity of the model's outcome to the wild environment's quality suggests that conserving or restoring a population's habitat is important for preventing fitness loss during supportive breeding.

Behavioral development in animals undergoing domestication

The process of domestication involves adaptation, usually to a captive environment. Domestication is attained by some combination of genetic changes occurring over generations and developmental mechanisms (e.g., physical maturation, learning) triggered by recurring environmental events or management practices in captivity that influence specific biological traits. The transition from free-living to captive status is often accompanied by changes in availability and/or accessibility of shelter, space, food and water, and by changes in predation and the social environment. These changes set the stage for the development of the domestic phenotype. Behavioral development in animals undergoing domestication is characterized by changes in the quantitative rather than qualitative nature of responses. The hypothesized loss of certain behavior patterns under domestication can usually be explained by the heightening of response thresholds. Increases in response frequency accompanying domestication can often be explained by atypical rates of exposure to certain forms of perceptual and locomotor stimulation. Genetic changes influencing the development of the domestic phenotype result from inbreeding, genetic drift, artificial selection, natural selection in captivity, and relaxed selection. Experiential contributions to the domestic phenotype include the presence or absence of key stimuli, changes in intraspecific aggressive interactions and interactions with humans. Man's role as a buffer between the animal and its environment is also believed to have an important effect on the development of the domestic phenotype. The domestication process has frequently reduced the sensitivity of animals to changes in their environment, perhaps the single-most important change accompanying domestication. It has also resulted in modified rates of behavioral and physical development. Interest in breeding animals in captivity for release in nature has flourished in recent decades. The capacity of domestic animals to survive and reproduce in nature may depend on the extent to which the gene pool of the population has been altered during the domestication process and flexibility in behavioral development. “Natural” gene pools should be protected when breeding wild animals in captivity for the purpose of reestablishing free-living natural populations. In some cases, captive-reared animals must be conditioned to live in nature prior to their release.

Diet selection in captivity by a generalist herbivorous rodent (Octodon degus) from the Chilean coastal desert

Five captive adult female degus (Octodon degus) were offered leaves and twigs to eat from three woody (Adesmia bedwellii,Porlieria chilensisandProustia pungens) and two suffruticose (Baccharis paniculataandChenopodium petiolase) shrubs that provide cover in their natural habitat. The degus discriminated among the plant species, consuming lower amounts ofP. chilensis. Daily body mass losses of degus were significantly higher when they were fed uponP. pungensandP. chilensis. The nutritional value of plants, concomitant with degu nutritional requirements, may explain changes in shrub cover previously found to follow removal of degus from experimental plots.

Conservation Genetics and the Management of Endangered Fishes.

The emerging field of endangered fishes management has yet to fully incorporate conservation genetics into recovery programs. Genetic aspects of small populations must be considered at the outset of management programs in order to maximize probability of their long‐term survival and continued adaptability. Total genetic variance of a species consists of within population genetic diversity, and the differences found among populations; both types of variance should be maintained to maximize adaptive flexibility of endangered fishes. Forces that erode genetic variation include small population size, population bottlenecks, genetic drift, inbreeding depression, artificial selection in captivity, and mixing of distinct genetic stocks. These can lead to increased homozygosity, loss of quantitative variation, and exposure of deleterious recessive alleles, all of which may reduce fitness. Suggestions for genetically sound management of endangered fishes include genetic monitoring of natural and captive populations, use of large numbers for captive breeding where feasible, selective mating to avoid inbreeding where necessary, minimization of time in captivity, and separate maintenance of distinct stocks.

Size specific predation by herons and its effect on the sex-ratio of natural populations of the mosquito fish Gambusia affinis baird and girard.

Sex-ratios of Gambusia affinis populations in freshwater marshes in the Camargue (Rhône Delta), are highly biased in favour of males, whereas the sex-ratios in ditches are close to unity. Studies of the diet of free living birds and experimental studies on prey size selection in captivity show that the abnormal sex-ratios in marshes can be attributed to differential heron predation. Ditches are relatively free from predation. Mature female Gambusia are larger, and have an energy content 5-25 times greater than that of mature males. Handling times of Grey Heron (Ardea cinerea) and Little Egret (Egretta garzetta) are only slightly longer for female Gambusia than males. Hence, females represent a much more profitable prey.Analysis of nestling regurgitates show that Gambusia makes up a considerable proportion of the diet of four species of Camargue herons, and that the majority of Gambusia taken are females. Under experimental conditions, captive herons consume almost exclusively female fish, even when offered in ratios where they are heavily outnumbered by males.The relevance of these results to optimal diet theory is discussed.