Natural history shapes genetic structure: Comparative range-wide population genetics of endemic aquatic turtles in the Chihuahuan desert

Habitat fragmentation is important in shaping population genetic structure. Habitat requirements of different species, however, may translate to different effective levels of fragmentation, as dispersal may not be as limited for species as it is for others. In desert-spring ecosystem of Cuatro Ciénegas, the desert surrounding aquatic habitats may be a formidable barrier to dispersal for aquatic species, but relatively traversable for semi-aquatic species. Here I compare the population genetic structure across the entire species’ ranges for three endemic turtle species with differing aquatic requirements. A previous study characterized the semi-aquatic box turtle, Terrapene coahuila, as having little population genetic structure and high rates of dispersal among most habitats. Here I compare the genetic structure of the box turtle to two aquatic species. The aquatic pond turtle, Trachemys taylori, exhibited significant isolation by distance and high genetic differentiation among subpopulations, with a global FST of 0.076 (0.044, 0.108)— consistent with reduced dispersal among subpopulations. Even stronger genetic structure was identified across habitats for the softshell turtle, Apalone atra, a species that is highly sensitive to desiccation and leaves water for nesting only. For the softshell turtle, global FST was equal to 0.161 (0.006, 0.016), and nearly all of localities were significantly different from one another, indicating that dispersal is more limited for the softshell than for the other two turtle species. No correlation of genetic differentiation with geographic distance was exhibited. This evidence, combined with allelic patterns, support a scenario of softshell turtles from each pond being isolated from the others since the basin became substantially drier near the beginning of the Holocene. Taken together, these results suggest that the natural history of an organism is a substantial factor for current population genetic structure in this ecosystem. As a by-product of this work, 6.6% of Apalone atra genome was sequenced using next-generation sequences, and microsatellite markers were developed from these data. Code for developing microsatellite markers from 454 reads, and the marker resource for this species are made publically available.