Offspring survival changes over generations of captive breeding

Conservation breeding programs such as zoos play a major role in preventing extinction, but their sustainability may be impeded by neutral and adaptive population genetic change. These changes are difficult to detect for a single species or context, and impact global conservation efforts. We analyse pedigree data from 15 vertebrate species – over 30,000 individuals – to examine offspring survival over generations of captive breeding. Even accounting for inbreeding, we find that the impacts of increasing generations in captivity are highly variable across species, with some showing substantial increases or decreases in offspring survival over generations. We find further differences between dam and sire effects in first- versus multi-generational analysis. Crucially, our multispecies analysis reveals that responses to captivity could not be predicted from species’ evolutionary (phylogenetic) relationships. Even under best-practice captive management, generational fitness changes that cannot be explained by known processes (such as inbreeding depression), are occurring.


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The study used existing studbook data from 15 species to investigate factors influencing offspring survival to age of reproductive maturity in captivity. Generalised linear mixed models were used to investigate seven "treatment" factors including dam inbreeding, sire inbreeding, offspring inbreeding, dam generation, sire generation, dam age at breeding and sire age at breeding. A binomial response was fitted where 1= survived, 0 = died. A nested random factor design was applied, to control for differences between Species, Birth Program and Year. Birth Program was nested within Species to account for regional specialisation.
Year was also nested within Species to control for improvements in husbandry over the different time frames of the species studied. A total of 37,484 individuals met our criteria for analysis (see exclusions below). We randomly sampled one individual per litter/clutch to avoid issues of statistical non-independence and repeated this process five times to assess reproducibility.
Existing studbook data from 15 species managed in captivity was analysed. Studbooks were selected on the basis of availability, size, taxonomic diversity, generations of captive breeding and limited unknown ancestry. Table 1 provides details of the 15 studbooks, including the sample size, effective population size, year of first record, age at maturity, and summary statistics for pedigree inbreeding, generations of captive breeding and age at breeding. The dataset represents the entirety of the managed captive populations of the 15 species included in the analysis.
All 58,611 individuals recorded in the 15 studbooks selected were initially considered for analysis. After exclusions (detailed below), 37,484 data points remained. This sample size is sufficient for analysis as it represents the total captive populations of the 15 species included in the analysis.
Studbook data was obtained from the relevant studbook keepers that collate it as part of routine management. Studbook data consists of records of individual animals, their date of birth, date of death, parents (if known), and location; and was collected prior to and independently of this study. Permission was sought from the studbook keepers and the relevant regional zoo and aquarium association, and their contributions are appropriately acknowledged.
This retrospective analysis includes all studbook data collected for the 15 species in the analysis where it met our criteria. The timescale ranged from 1850 to the present, though the timescales of captive breeding differ between species (presented in Table 1 and controlled for in the hierarchical analysis through the nested Species:Year interaction). The spatial scale of each of the studbooks is specified in Table 1 as either international (representing all zoos that breed the species of interest globally) or regional.
The initial dataset contained 58,611 individuals. Data exclusions include: individuals with unknown parents, all data within the last 364 days of the date of the studbook (to minimise possibility of recent deaths not having been updated), individuals born within the timeframe of the reproductive maturity age (specified in Table 1) from the truncated date (as they would not have the chance to have reached reproductive maturity yet), red wolf animals identified as hybrids in the studbook, and animals born in the wild or released to the wild before the age of reproductive maturity (affected red wolf and Tasmanian devil studbooks). 37,493 remaining individuals had complete data, but 9 outliers were identified and removed, resulting in N = 37,484 individuals for analysis. Missing data appeared random with respect to time.
Findings were based on retrospective analysis rather than experimental design. As we randomly sampled one offspring per litter/ clutch to avoid non-independence issues, we repeated the analysis using five random subsets. Results did not substantially change across the five data subsets (Supplementary Figure 2), and also did not differ substantially from sensitivity testing using the full dataset (without respect to shared litter-mates).
Not relevant to study as not an experimental design, therefore there were no treatments to randomize.
Not relevant to study as not an experimental design, therefore there were no treatments to blind participants or researchers to.