Population genomics of the endangered giant Galápagos tortoise

Abstract

BackgroundThe giant Galápagos tortoise, Chelonoidis nigra, is a large-sized terrestrial chelonian of high patrimonial interest. The species recently colonized a small continental archipelago, the Galápagos Islands, where it has been facing novel environmental conditions and limited resource availability. To explore the genomic consequences of this ecological shift, we analyze the transcriptomic variability of five individuals of C. nigra, and compare it to similar data obtained from several continental species of turtles.ResultsHaving clarified the timing of divergence in the Chelonoidis genus, we report in C. nigra a very low level of genetic polymorphism, signatures of a weakened efficacy of purifying selection, and an elevated mutation load in coding and regulatory sequences. These results are consistent with the hypothesis of an extremely low long-term effective population size in this insular species. Functional evolutionary analyses reveal a reduced diversity of immunity genes in C. nigra, in line with the hypothesis of attenuated pathogen diversity in islands, and an increased selective pressure on genes involved in response to stress, potentially related to the climatic instability of its environment and its elongated lifespan. Finally, we detect no population structure or homozygosity excess in our five-individual sample.ConclusionsThese results enlighten the molecular evolution of an endangered taxon in a stressful environment and point to island endemic species as a promising model for the study of the deleterious effects on genome evolution of a reduced long-term population size.

Extreme genomic erosion after recurrent demographic bottlenecks in the highly endangered Iberian lynx

“…Accordingly, we also observed values of average genome-wide nucleotide diversity and synonymous nucleotide diversity that are to our knowledge the lowest reported for any organism [50] (Table 1; Additional file 1: Sections 20 and 21). At the same time, the ratio of non-synonymous to synonymous diversity is high (π N /π S  = 0.286), similar to those observed in other bottlenecked populations, such as humans (π N /π S  = 0.241) [51] or the Galápagos giant tortoise, Chelonoidis nigra (π N /π S  = 0.310) [52], indicating a relative abundance of potentially deleterious mutations segregating at moderate to high frequencies.…”

Patterns of cross-contamination in a multispecies population genomic project: detection, quantification, impact, and solutions

“…The relative bias was substantial – the median ratio of corrected to uncorrected π S was 0.90 when γ was 0.1, and 0.81 when γ was 0.2. The relative bias, however, was fairly constant across species, and much smaller that the between-species differences in π S , suggesting that our published comparative analyses of π S across species [17, 19, 21, 22] are robust to within-species contamination. We checked that the correlation reported by Romiguier et al [21] between π S and species life history traits were still valid after control for contamination.…”

A genomic perspective timely needed for re-evaluating the species delimitations, evolutionary trajectories, and conservation strategies of the Galapagos giant tortoises

“…In 2013, Loire et al [9] provided the first population genomic analyses based on genome scale data (~1000 coding loci derived from blood-transcriptomes) from five individuals, encompassing three putative "species": Chelonnoidis becki, C. porteri and C. vandenburghi. Their results raised doubts about the validity/accuracy of the currently accepted designations of "genetic distinctiveness".…”

“…In 2017, Loire and Galtier [4] have re-appraised this issue using an original multi-species comparative population genomic analysis of their previous data set [9]. Based on a comparison of 53 animal species, they show that both the level of genome-wide neutral diversity (πS) and level of population structure estimated using the inbreeding coefficient (F) are much lower than would be expected from a sample covering multiple species.…”