Genetics of a head-start program to guide conservation of an endangered Galápagos tortoise (Chelonoidis ephippium)

Abstract

Critically endangered wildlife species typically require intensive management using a variety of in situ and ex situ approaches. Yet, despite broad application of ex situ conservation strategies, comparatively few programs incorporate genetic tools into management decisions and monitoring efforts. This is the case with the giant Galá-pagos tortoise endemic to Pinzón Island (Chelonoidis ephippium); a head-start program has been in place for 50 years without an evaluation of whether this conservation intervention has captured the breadth of diversity present in the wild population. Here we used microsatellite genotypic data to reconstruct patterns of within-and among-population genetic variation in the wild and captivity, and to assess the degree to which head-start cohorts and adult captive founders are representative of the gene pool in situ. We found that Pinzón giant tortoises maintain high levels of variation in situ despite their welldocumented decline and that the founders of the captive population are a reasonably diverse and representative group. However, we also found that the head-start cohorts are not representative of the wild population, as evidenced by significant genetic differentiation between the in situ and ex situ samples and by the private alleles detected in both. Future head-start activities should broaden the source locations of eggs and hatchlings to more comprehensively capture the extent and distribution of genetic variation in this critically endangered keystone herbivore. More broadly, this study further highlights the utility of integrating genetic information within ex situ conservation programs.

Population genomics through time provides insights into the consequences of decline and rapid demographic recovery through head‐starting in a Galapagos giant tortoise

“…One persistent pattern found in all previous studies of Pinzón giant tortoises using microsatellites has been heterozygote deficit relative to Hardy–Weinberg expectations and significantly positive inbreeding coefficients (Beheregaray, Ciofi, Caccone, Gibbs, & Powell, ; Garrick et al., ; Jensen et al., ). Similar results were found in a recent study employing double‐digest RAD (ddRAD) sequencing to quantify genetic diversity and reconstruct population structure across all 12 extant species of Galapagos giant tortoises (Miller et al., ).…”

“…No population structure was evident between temporal samples based on STRUCTURE or DAPC clustering analyses, although there were very small, but significant, Phi ST values (Table ). A previous microsatellite‐based study of Pinzón giant tortoises found mixed evidence in tests for a bottleneck, with no genetic signature of population decline in heterozygote excess tests, a normal distribution in the mode‐shift test indicating a stable population size, and M ‐ratio tests suggesting a population bottleneck (Jensen, Tapia, Caccone, & Russello, ). Unfortunately, in this study, we were unable to explicitly test for genetic signatures of a bottleneck in the Pinzón tortoise contemporary samples given the lack of an appropriate mutation model for SNPs using the conventional heterozygote excess test (Cornuet & Luikart, ) and the fact that the size of our data set precluded the application of site frequency spectrum‐based methods (e.g., Excoffier, Dupanloup, Huerta‐Sanchez, Sousa, & Foll, ).…”

“…This scenario may have occurred if some mate pairs naturally produced more offspring than others, and/or if eggs or pre‐emergent individuals were collected nonrandomly. A previous microsatellite study evaluated the genetic representativeness of the cohorts of the head‐start programme hatched in 2007 and 2009, relative to a sample of 72 adults from the wild population (Jensen et al., ). The conclusions were that the cohorts were genetically diverse, but that there was genetic variation in the wild adults not represented in the head‐start cohorts.…”

“…The conclusions were that the cohorts were genetically diverse, but that there was genetic variation in the wild adults not represented in the head‐start cohorts. Surprisingly, there were a number of alleles present in the hatchlings that were not found in the sample of adults, indicating that despite constituting a large proportion of the reproducing population, that adult sample was not fully representative of the breadth of genetic variation in the population (Jensen et al., ).…”

A question of scale: Replication and the effective evaluation of conservation interventions

“…Thus, evaluations of headstarting as an intervention can encompass projects using turtle eggs from any source, although selective pressures (e.g., local adaptation, artificial selection) warrant consideration in evaluations of post-release success. Although this selection is unlikely to be as strong in captive turtles because of their different mating strategies and long generation times (but see Jensen et al 2015), selection on hatchery-raised fish can have major impacts on post-release survival (Le Cam et al 2015;Jensen et al 2016), and this possibility should not be discounted in other taxa.…”