Whole-genome sequencing confirms multiple species of Galapagos giant tortoises

Abstract Galapagos giant tortoises are endemic to the Galapagos Archipelago, where they are found in isolated populations. While these populations are widely considered distinguishable in morphology, behavior, and genetics, the recent divergence of these taxa has made their status as species controversial. Here, we apply multispecies coalescent methods for species delimitation to whole genome resequencing data from 38 tortoises across all 13 extant taxa to assess support for delimiting these taxa as species. In contrast to previous studies based solely on divergence time, we find strong evidence to reject the hypothesis that all Galapagos giant tortoises belong to a single species. Instead, a conservative interpretation of model-based and divergence-based results indicates that these taxa form a species complex consisting of a minimum of 9 species, with some analyses supporting as many as 13 species. There is mixed support for the species status of taxa living on the same island, with some methods delimiting them as separate species and others suggesting multiple populations of a single species per island. These results make clear that Galapagos giant tortoise taxa represent different stages in the process of speciation, with some taxa further along in that evolutionary process than others. A better understanding of the more complex parts of that process is urgently needed, given the threatened status of Galapagos giant tortoises. Lay Summary Species delimitation is a challenging problem in evolutionary biology, but one that is central to the field. Distinguishing species can affect conservation management practices, from conservation status assessments to strategies for breeding programs. More fundamentally, understanding species boundaries affects our ability to assess biodiversity and to study evolutionary processes. The Galapagos Archipelago presents several radiations of closely related taxa that inspired Charles Darwin to develop his theory of evolution by natural selection and later led to foundational case studies in speciation. The Galapagos giant tortoises were one such inspiration. Nearly two centuries later, there is still an ongoing debate about the taxonomic status of these tortoises, with opinions on their status ranging from barely differentiated populations to separate species. Here, we present the first genomic species delimitation of Galapagos giant tortoises and provide convincing evidence that this group is a complex consisting of between 9 and 13 species. These results provide valuable guidance to conservation stakeholders in the Galapagos, while also adding an important case study to the delimitation of island species.

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