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

Evelyn L Jensen,James P Gibbs,Linda J Cayot,Adalgisa Caccone,Michael A Russello,Ryan C Garrick,Danielle L Edwards,Joshua M Miller,Washington Tapia

doi:10.1111/eva.12682

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.

Highlights

A broader understanding of the genetic consequences of population decline is of fundamental importance for species restoration, as standing levels of genetic diversity are associated with the probability of long-term population persistence (Frankham, 1997, 2005; Frankham et al, 2017), ability to survive novel disease threats (Smith, Acevedo-Whitehouse, & Pedersen, 2009) and adaptation to changing environments (Barrett & Schluter, 2008; Jump, Marchant, & Peñuelas, 2009)
Many empirical studies have examined the genetic consequences of bottlenecks indirectly, either in natural populations postdecline or in experimental settings (Leberg, 1992)
Given that the majority of the tortoises in the contemporary sample are the product of the head-start programme, we evaluated the degree to which genetic variation has been impacted by this conservation intervention

Summary

| INTRODUCTION

A broader understanding of the genetic consequences of population decline is of fundamental importance for species restoration, as standing levels of genetic diversity are associated with the probability of long-term population persistence (Frankham, 1997, 2005; Frankham et al, 2017), ability to survive novel disease threats (Smith, Acevedo-Whitehouse, & Pedersen, 2009) and adaptation to changing environments (Barrett & Schluter, 2008; Jump, Marchant, & Peñuelas, 2009). Given the long lifespan (>100 years) and generation time of Galapagos giant tortoises (25 years, Throp, 1975), coupled with the well-documented history of decline in the Pinzón species, these museum specimens are likely representative of the prebottleneck population. They provide a valuable reference point for investigating changes in both the extent and distribution of genetic variation over the past century. We paired restriction-site-associated DNA sequencing (RAD-seq) with targeted capture techniques to collect genome-wide single nucleotide polymorphism (SNP) genotypic data from historical (prebottleneck) and contemporary (postbottleneck) samples We used this SNP data set to directly investigate changes in genome-wide diversity over time. Given that the majority of the tortoises in the contemporary sample are the product of the head-start programme, we evaluated the degree to which genetic variation has been impacted by this conservation intervention

| MATERIALS AND METHODS

| DISCUSSION

Findings

| CONCLUSIONS