Turtles and tortoises (chelonians) have been integral components of global ecosystems for about 220 million years and have played important roles in human culture for at least 400,000 years. The chelonian shell is a remarkable evolutionary adaptation, facilitating success in terrestrial, freshwater and marine ecosystems. Today, more than half of the 360 living species and 482 total taxa (species and subspecies combined) are threatened with extinction. This places chelonians among the groups with the highest extinction risk of any sizeable vertebrate group. Turtle populations are declining rapidly due to habitat loss, consumption by humans for food and traditional medicines and collection for the international pet trade. Many taxa could become extinct in this century. Here, we examine survival threats to turtles and tortoises and discuss the interventions that will be needed to prevent widespread extinction in this group in coming decades.
Human-induced transformations of ecosystems usually result in fragmented populations subject to increased extinction risk. Fragmentation is also often associated with novel environmental heterogeneity, which in combination with restricted gene flow may increase the opportunity for local adaptation. To manage at-risk populations in these landscapes, it is important to understand how gene flow is changing, and how populations respond to habitat loss. We conducted a landscape genomics analysis using Restriction-site Associated DNA sequencing to investigate the evolutionary response of the critically endangered Dahl´s Toad-headed turtle (Mesoclemmys dahli)to severe habitat modification. The species has lost almost all of its natural habitat in the southwestern part of its range and about 70% in the northeast. Based on least cost path analysis across different resistance surfaces for 3,211 SNPs, we found that the landscape matrix is restricting gene flow, causing the fragmentation of the species into at least six populations. Genome scans and allele-environment association analyses indicate that the population fragments in the deforested grasslands of the southwest are adaptively different from those in the more forested northeast.Populations in areas with no forest had low levels of adaptive genetic diversity and the fixation of ancestrally-polymorphic SNPs, consistent with directional selection in this novel environment. Our results suggest that this forest-stream specialist is adapting to pond-grassland conditions, but it is also suffering from negative consequences of habitat loss, including genetic erosion, isolation, small effective population sizes, and inbreeding. We recommend gene flow restoration via genetic rescue to counteract these threats, and provide guidance for this strategy.
K E Y W O R D SColombia, conservation genomics, genetic-environment associations, Mesoclemmys dahli, population fragmentation, RADseq
| INTRODUC TI ONHuman activities including agriculture, infrastructure, and transportation, have transformed tropical forests, resulting in decreased forest connectivity, smaller patch sizes, and the concomitant isolation and reduction of previously contiguous large populations.Small and isolated populations are at a higher risk of extinction because they are more vulnerable to environmental and demographic
As genomic-scale data sets become economically feasible for most organisms, a key question for conservation biology is whether the increased resolution offered by new genomic approaches justifies repeating earlier studies based on traditional markers, rather than investing those same time and monetary resources in less-known species. Genomic studies offer clear advantages when the objective is to identify adaptive loci that may be critical to conservation policy-makers. However, the answer is far less certain for the population and landscape studies based on neutral loci that dominate the conservation genetics research agenda. We used RADseq to revisit earlier molecular studies of the IUCN Critically Endangered Magdalena River turtle (Podocnemis lewyana), documenting the conservation insights gained by increasing the number of neutral markers by several orders of magnitude. Earlier research indicated that P. lewyana has the lowest genetic diversity known for any chelonian, and little or no population differentiation among independent rivers. In contrast, the RADseq data revealed discrete population structure with isolation-by-distance within river segments and identified precise population breaks clearly delineating management units. It also confirmed that the species does not have extremely low heterozygosity and that effective population sizes are probably sufficient to maintain long-term evolutionary potential. Contrary to earlier inferences from more limited population genetic markers, our genomic data suggest that management strategies should shift from active genetic rescue to more passive protection without extreme interventions. We conclude with a list of examples of conservation studies in other vertebrates indicating that for many systems a genomic update is worth the investment.
Mesoclemmys dahliandM. zuliaeare two endangered, little-known toad-headed turtles with small distribution ranges in Colombia and Venezuela, respectively. Using the mitochondrial cytochromebgene as a marker, we investigate their phylogeographic differentiation. Furthermore, based on 2341 bp of mtDNA and 2109 bp of nDNA ofM. dahli,M. zuliaeand allied chelid turtles, we infer their divergence time using a fossil-calibrated relaxed molecular clock approach.Mesoclemmys dahliandM. zuliaeare closely related species, with an estimated mean divergence time of 10.6 million years. This estimate correlates with the uplift of the Serranía de Perijá, an Andean mountain chain separating their distribution ranges, suggesting that this event could have caused the evolution of the two species. Haplotype and nucleotide diversities ofM. dahliare markedly higher than inPodocnemis lewyana, another endemic turtle species of Colombia. This pronounced dissimilarity may reflect differences in the phylogeographies and demographic histories of the two species, but also different habitat preferences.
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