As species extinction rates increase, genomics provides a powerful tool to support intensive management of threatened species. We use the Tasmanian devil (Sarcophilus harrisii) to demonstrate how conservation genomics can be implemented in threatened species management. We conducted whole genome sequencing (WGS) of 25 individuals from the captive breeding programme and reduced-representation sequencing (RRS) of 98 founders of the same programme. A subset of the WGS samples was also sequenced by RRS, allowing us to directly compare genome-wide heterozygosity with estimates from RRS data. We found good congruence in interindividual variation and gene-ontology classifications between the two data sets, indicating that our RRS data reflect the genome well. We also attempted genome-wide association studies with both data sets (regarding breeding success), but the genomic data suffered from small sample size, while the RRS data suffered from lack of precision, highlighting a key trade-off in the design of conservation genomic research. Nevertheless, we identified a number of candidate genes that may be associated with variation in breeding success. Individual heterozygosity, as measured by WGS or RRS, was not associated with breeding success in captivity but was negatively associated with litter sizes of breeding females in the RRS data set. Our findings enable conservation managers to have confidence in RRS data while understanding its limitations, and provide avenues for further investigation into which processes underlie variation in breeding success in captive Tasmanian devils. We caution, however, that deep functional insights using RRS may be impaired by a lack of precision, especially when marker density is low.
Background Recent advances in genomics have greatly increased research opportunities for non-model species. For wildlife, a growing availability of reference genomes means that population genetics is no longer restricted to a small set of anonymous loci. When used in conjunction with a reference genome, reduced-representation sequencing (RRS) provides a cost-effective method for obtaining reliable diversity information for population genetics. Many software tools have been developed to process RRS data, though few studies of non-model species incorporate genome alignment in calling loci. A commonly-used RRS analysis pipeline, Stacks, has this capacity and so it is timely to compare its utility with existing software originally designed for alignment and analysis of whole genome sequencing data. Here we examine population genetic inferences from two species for which reference-aligned reduced-representation data have been collected. Our two study species are a threatened Australian marsupial (Tasmanian devil Sarcophilus harrisii ; declining population) and an Arctic-circle migrant bird (pink-footed goose Anser brachyrhynchus ; expanding population). Analyses of these data are compared using Stacks versus two widely-used genomics packages, SAMtools and GATK. We also introduce a custom R script to improve the reliability of single nucleotide polymorphism (SNP) calls in all pipelines and conduct population genetic inferences for non-model species with reference genomes. Results Although we identified orders of magnitude fewer SNPs in our devil dataset than for goose, we found remarkable symmetry between the two species in our assessment of software performance. For both datasets, all three methods were able to delineate population structure, even with varying numbers of loci. For both species, population structure inferences were influenced by the percent of missing data. Conclusions For studies of non-model species with a reference genome, we recommend combining Stacks output with further filtering (as included in our R pipeline) for population genetic studies, paying particular attention to potential impact of missing data thresholds. We recognise SAMtools as a viable alternative for researchers more familiar with this software. We caution against the use of GATK in studies with limited computational resources or time. Electronic supplementary material The online version of this article (10.1186/s12864-019-5806-y) contains supplementary material, which is available to authorized users.
Captive breeding programs are an increasingly popular tool to augment the conservation of threatened wild populations. Many programs keep detailed pedigrees, which are used to prescribe breeding targets to meet demographic and genetic goals. Annual breeding targets are based on previous productivity, but do not account for changes in reproductive success that may occur over generations in captivity and which may impair the ability of a program to meet its goals. We utilize a large studbook from the Tasmanian devil (Sarcophilus harrisii) captive breeding program to investigate biological, genetic, and environmental factors that affect variation in reproductive success among individuals and over generations of captive breeding. Reproductive success declined with increasing generations in captivity: wild-born females had a 56.5% chance of producing a litter compared to a 2.8% chance for generation 5 captive-born females (N = 182) and when they did, wild-born females produced more offspring (3.1 joeys, 95% CI: 2.76-3.38, compared to 2.7 joeys, 95% CI: 2.55-2.90, in captive-born females [N = 105]). Reproductive success also declined as dam age at first breeding increased. Our results reveal a conflict with the widely cited conservation strategy to limit opportunity for selection by extending generation length through delaying reproduction, as captive breeding programs that delay female breeding with this goal in mind risk reduced productivity. Our data demonstrate the benefit of pedigree analysis to identify biological processes that reveal crucial trade-offs with conservation best-practice.
Context Conservation management relies on baseline demographic data of natural populations. For Tasmanian devils (Sarcophilus harrisii), threatened in the wild by two fatal and transmissible cancers (devil facial tumour disease DFTD: DFT1 and DFT2), understanding the characteristics of healthy populations is crucial for developing adaptive management strategies to bolster populations in the wild. Aims Our analysis aims to evaluate contemporary reproductive rates for wild, DFTD-free Tasmanian devil populations, and to provide a baseline with which to compare the outcome of current translocation activities. Methods We analysed 8 years of field-trapping data, including demographics and reproductive rates, across 2004–16, from the largest known DFTD-free remnant population at Woolnorth, Tasmania. Key results Surprisingly, we found a dramatic and statistically significant decline in female breeding rate when comparing data collected from 2004–2009 with data from 2014–2016. Unfortunately we do not have any data from the intermediate years. This decline in breeding rate was accompanied by a subtle but statistically significant decline in litter sizes. These changes were not associated with a change in body condition over the same period. Furthermore, we could not attribute the decline in breeding to a change in population size or sex ratio. Preliminary analysis suggested a possible association between annual breeding rate and coarse measures of environmental variation (Southern Oscillation Index), but any mechanistic associations are yet to be determined. Conclusions The decline in breeding rates was unexpected, so further monitoring and investigation into potential environmental and/or biological reasons for the decline in breeding rate are recommended before the arrival of DFTD at Woolnorth. Implications Our results provide valuable data to support the conservation management of Tasmanian devils in their native range. They also highlight the importance of continued monitoring of ‘safe’ populations, in the face of significant threats elsewhere.
Successfully establishing captive breeding programs is a priority across diverse industries to address food security, demand for ethical laboratory research animals, and prevent extinction. Differences in reproductive success due to birth origin may threaten the long-term sustainability of captive breeding. Our meta-analysis examining 115 effect sizes from 44 species of invertebrates, fish, birds, and mammals shows that, overall, captive-born animals have a 42% decreased odds of reproductive success in captivity compared to their wild-born counterparts. The largest effects are seen in commercial aquaculture, relative to conservation or laboratory settings, and offspring survival and offspring quality were the most sensitive traits. Although a somewhat weaker trend, reproductive success in conservation and laboratory research breeding programs is also in a negative direction for captive-born animals. Our study provides the foundation for future investigation of non-genetic and genetic drivers of change in captivity, and reveals areas for the urgent improvement of captive breeding.
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