Long-term demographic and genetic effects of releasing captive-born individuals into the wild

Because of continued habitat destruction and species extirpations, the need to use captive breeding for conservation purposes has been increasing steadily. However, the long-term demographic and genetic effects associated with releasing captive-born individuals with varied life histories into the wild remain largely unknown. To address this question, we developed forward-time, agent-based models for 4 species with long-running captive-breeding and release programs: coho salmon (Oncorhynchus kisutch), golden lion tamarin (Leontopithecus rosalia), western toad (Anaxyrus boreas), and Whooping Crane (Grus americana). We measured the effects of supplementation by comparing population size and neutral genetic diversity in supplemented populations to the same characteristics in unaltered populations 100 years after supplementation ended. Releasing even slightly less fit captive-born individuals to supplement wild populations typically resulted in reductions in population sizes and genetic diversity over the long term when the fitness reductions were heritable (i.e., due to genetic adaptation to captivity) and populations continued to be regulated by density-dependent mechanisms over time. Negative effects for species with longer life spans and lower rates of population replacement were smaller than for species with shorter life spans and higher rates of population replacement. Programs that released captive-born individuals over fewer years or that avoided breeding individuals with captive ancestry had smaller reductions in population size and genetic diversity over the long term. Relying on selection in the wild to remove individuals with reduced fitness mitigated some negative demographic effects, but at a substantial cost to neutral genetic diversity. Our results suggest that conservation-focused captive-breeding programs should take measures to prevent even small amounts of genetic adaptation to captivity, quantitatively determine the minimum number of captive-born individuals to release each year, and fully account for the interactions among genetic adaptation to captivity, population regulation, and life-history variation.