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Genomic and biogeographic patterns of endemic geckos in the Galapagos Islands reveal population structure and species delimitation on inhabited islands

Abstract:

Islands offer invaluable opportunities for studying evolutionary processes due to their isolation and distinct environmental conditions. The Galapagos Islands, renowned for their rich biodiversity, host several endemic gecko species of the genus Phyllodactylus (Gekkota: Phyllodactylidae). Despite their importance derived from their specialized adaptations and their crucial role in maintaining ecosystem balance, few studies have been conducted on these geckos. This highlights the need for comprehensive genomic research to understand their evolutionary patterns and population dynamics. This study elucidates the genetic diversity and population structure of six endemic Phyllodactylus species found on four human-inhabited islands in the Galapagos using a RAD-Seq approach. The analysis of over 9000 loci from 93 individuals revealed five distinct genetic clusters, corresponding to P. baurii, P. galapagensis, P. darwini, P. leei, and a combined cluster of P. simpsoni and P. andysabini. Our results indicate that P. galapagensis clusters with the combined P. simpsoni–P. andysabini group, while P. baurii shows close genetic relationships with both clusters, in accordance with the obtained phylogeny and the sequential emergence of the Galapagos Islands where each species is found. Substantial genetic differentiation was observed between species, with high F<inf>ST</inf> and D<inf>XY</inf> values. However, our analyses indicate that gecko populations from across Isabela and Fernandina islands exhibit very low genetic differentiation, leading us to propose the synonymization of P. andysabini with P. simpsoni. Within-species population structure was associated with geographic barriers and gene flow restrictions. Surprisingly, human activity does not appear to be causing significant admixture among these populations; instead, population boundaries remain intact, indicating that geographic or behavioral barriers are stronger than human influences in limiting gene flow. Overall, we found low genetic diversity across species, probably due to their endemic nature and island isolation. This genomic study provides insights into the evolutionary dynamics shaping these unique geckos and highlights the importance of employing high-resolution genomic tools in insular ecosystems for their effective conservation and management.