Evolution of Peromyscus leucopus Mice in Response to a Captive Environment

Abstract

Many wildlife species are propagated in captivity as models for behavioral, physiological, and genetic research or to provide assurance populations to protect threatened species. However, very little is known about how animals evolve in the novel environment of captivity. The histories of most laboratory strains are poorly documented, and protected populations of wildlife species are usually too small and too short-term to allow robust statistical analysis. To document the evolutionary change in captive breeding programs, we monitored reproduction and behavior across 18 generations in six experimental populations of Peromyscus leucopus mice started from a common set of 20 wild-caught founders. The mice were propagated under three breeding protocols: a strategy to retain maximal genetic diversity, artificial selection against stereotypic behaviors that were hypothesized to reflect poor adaptation to captivity, and random bred controls. Two replicates were maintained with each protocol, and inter-replicate crosses at generations 19 and 20 were used to reverse accumulated inbreeding. We found that one of the stereotypic behaviors (repetitive flipping) was positively associated with reproductive fitness, while the other (gnawing) was relatively invariant. Selection to reduce these stereotypic behaviors caused marked reduction in reproduction, and populations not under artificial selection to reduce these behaviors responded with large increases in flipping. In non-selected populations, there was rapid evolution toward much higher proportion of pairs breeding and more rapid conception. Litter size, pup survival, and weaning mass all declined slowly, to the extent that would be predicted based on inbreeding depression. Inter-crossing between replicate populations reversed these declines in fitness components but did not reverse the changes in behavior or the accelerated breeding. These findings indicate that adaptation to captivity can be rapid, affecting reproductive patterns and behaviors, even under breeding protocols designed to minimize the rate of genetic change due to random drift and inadvertent selection.

The impacts of inbreeding, drift and selection on genetic diversity in captive breeding populations

“…The loss of the second DOC population suggests that fitness was reduced by inbreeding depression [see Lacy et al . () for details of the reproductive trends]. The remaining DOC population and both RAN populations accrued inbreeding at the same rate throughout the duration of the study.…”

Demystifying animal ‘personality’ (or not): why individual variation matters to experimental biologists

“…Sampling biases are likely if using domesticated laboratory populations to address questions about behavioural or physiological trait variation. For example, laboratory conditions rapidly select for certain behavioural and physiological traits as a result of domestication (Lacy et al, 2013). This probably reduces trait variation and inter-individual differences compared with those of wild populations.…”

A father effect explains sex-ratio bias

“…We also used Akaike's information criterion (AIC) to assess model support and to select the best model. Given that males from different breeding protocols [16,38] varied in the rate of inbreeding accumulation through the 10 generations (see electronic supplementary material S1.2 for details), we accounted for this variable in the relevant models. The models vary in sample sizes because the total number of males was 58, while the total number of fathers siring offspring was 40.…”