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

Abstract

Population genetic theory related to the consequences of rapid population decline is well‐developed, but there are very few empirical studies where sampling was conducted before and after a known bottleneck event. Such knowledge is of particular importance for species restoration, given links between genetic diversity and the probability of long‐term persistence. To directly evaluate the relationship between current genetic diversity and past demographic events, we collected genome‐wide single nucleotide polymorphism data from prebottleneck historical (c.1906) and postbottleneck contemporary (c.2014) samples of Pinzón giant tortoises (Chelonoidis duncanensis; n = 25 and 149 individuals, respectively) endemic to a single island in the Galapagos. Pinzón giant tortoises had a historically large population size that was reduced to just 150–200 individuals in the mid 20th century. Since then, Pinzón's tortoise population has recovered through an ex situ head‐start programme in which eggs or pre‐emergent individuals were collected from natural nests on the island, reared ex situ in captivity until they were 4–5 years old and subsequently repatriated. We found that the extent and distribution of genetic variation in the historical and contemporary samples were very similar, with the latter group not exhibiting the characteristic genetic patterns of recent population decline. No population structure was detected either spatially or temporally. We estimated an effective population size (N e) of 58 (95% CI = 50–69) for the postbottleneck population; no prebottleneck N e point estimate was attainable (95% CI = 39–infinity) likely due to the sample size being lower than the true N e. Overall, the historical sample provided a valuable benchmark for evaluating the head‐start captive breeding programme, revealing high retention of genetic variation and no skew in representation despite the documented bottleneck event. Moreover, this work demonstrates the effectiveness of head‐starting in rescuing the Pinzón giant tortoise from almost certain extinction.

Population genomics for wildlife conservation and management

“…Jensen et al. (2018) compared variation at >2,000 SNPs in Pinzón giant tortoise ( Chelonoidis duncanensis ) samples from a single island in the Galápagos Island from before and after a bottleneck that reduced N e to just 150–200 in the mid‐20th century. They found that the extent and distribution of genetic variation in the historical and contemporary samples was very similar, which they attributed to a successful ex situ head‐start and release programme.…”

Benefits of Head‐starting for Blanding's Turtle Size Distributions and Recruitment

“…These challenges are not unique to Blanding's turtles. Head‐starting has been used extensively to augment existing populations and re‐establish extirpated populations of turtles more generally (Burke and citations therein, Caillouet et al , Peñaloza et al , Shaver and Caillouet , Tuberville et al , Jensen et al ). Although outcomes have been less widely monitored and reported than desirable (Burke ), case studies demonstrating growth and survival of head‐starts (Vander Haegen et al , Masin et al , Michell and Michell , Tuberville et al , Quinn et al ), recruitment of reproductive adults (Vander Haegen et al , Masin et al , Shaver and Caillouet ), and shifts in size distribution (Peñaloza et al ) similar to what we report for Blanding's turtles are accumulating.…”

“…Although outcomes have been less widely monitored and reported than desirable (Burke ), case studies demonstrating growth and survival of head‐starts (Vander Haegen et al , Masin et al , Michell and Michell , Tuberville et al , Quinn et al ), recruitment of reproductive adults (Vander Haegen et al , Masin et al , Shaver and Caillouet ), and shifts in size distribution (Peñaloza et al ) similar to what we report for Blanding's turtles are accumulating. Future refinements to the use of head‐starting will benefit from studies of phenotypic effects of head‐starting (Geist et al ), disease status of head‐starts (Smith ), behavior following release (Hazard et al ), and genetic consequences of head‐starting (Dresser et al , Jensen et al ). A larger, more challenging goal will be to determine whether head‐starting can be used as a conservation tactic carried out over a modest time frame (e.g., while threat mitigation is implemented, Vander Haegen et al ) or is a necessary long‐term strategy to ensure persistence of a conservation‐reliant species (Scott et al ).…”

Patterns, Mechanisms and Genetics of Speciation in Reptiles and Amphibians

“…Moreover, the publication of the Galapagos giant tortoise genome [426] and recent/on-going population genomic studies have enabled new and exciting opportunities to enhance society’s understanding of speciation within and among the islands. This includes a new understanding of the relative importance of introgression and fusion events in species formation and persistence, and the study of the genomic architecture of traits associated with their ecological and morphological diversification [427,428,429,430].…”