Regional‐scale aquifer hydrogeology as a driver of phylogeographic structure in the Neotropical catfish Rhamdia guatemalensis (Siluriformes: Heptapteridae) from cenotes of the Yucatán Peninsula, Mexico

Abstract

Abstract The Yucatán Peninsula (YP) contains one of the most spectacular and developed karstic aquifers in the world, which connects to the surface through water‐filled sinkholes locally known as cenotes. Cenotes and their associated submerged caves are home to a remarkable diversity of aquatic fauna, yet very little is known about spatial patterns of intraspecific genetic and morphological variation across the aquifer. The strong affinity to cenotes (vs. submerged caves) exhibited by most fishes inhabiting the YP aquifer raises a fundamental question about the ecology and evolutionary history of its ichthyofauna: how genetically structured and morphologically divergent are fish populations from different cenotes across the YP? To shed light on this question, we investigated phylogeographic structure in the Neotropical catfish Rhamdia guatemalensis, arguably the most ubiquitous representative of the YP aquifer ichthyofauna. Geographic patterns of genetic variation were determined through phylogeographic and population genetics analyses of mitochondrial (mt)DNA sequence data. Body shape variation was investigated using both traditional and geometric morphometrics. Dense sampling across the previously overlooked YP region, coupled with the inclusion of samples from basins unrepresented in past studies, allowed for revision of previous estimates of phylogeographic structuring across the species’ range. Our results reveal a striking spatial correspondence between major mtDNA lineages and physiographic regions defined on the basis of broad‐scale patterns of groundwater flow. Morphological variation in populations from the YP, although considerable, neither reflects the observed spatial signal of genetic differentiation nor displays any other discernible geographic pattern. The resulting range‐wide phylogeographic pattern is largely consistent with a latitudinal, isolation‐by‐distance gradient, and the expectations from catchment hydrology, while revealing an unexpectedly close relationship between YP aquifer and epigean populations (both inside and outside the YP). Although the inferred range‐wide phylogeographic history is consistent with a single aquifer colonisation event followed by multiple instances of dispersal out of the aquifer and into neighbouring epigean basins, hypotheses regarding the colonisation and exodus of the YP by R. guatemalensis require further investigation. Within the YP aquifer, regional‐scale hydrogeological differences might impose limits to underground dispersal, potentially driving genetic divergence in populations of R. guatemalensis, and possibly in other cenote‐dwelling fishes as well. Future research focused on other YP aquifer species, however, is needed to test the generality of our findings. Phylogeographic research on the stygofauna of the YP aquifer is a relatively nascent field of inquiry. Besides shedding novel light into the patterns and drivers of genetic differentiation in fish populations from across the aquifer, this study sets the stage for future research aimed at unravelling the evolutionary history of the stygofauna that inhabits the cenotes and submerged caves of the YP. The remarkable and hitherto undocumented phylogeographic pattern revealed herein (i.e. correspondence of major mtDNA lineages with physiographic regions defined by regional‐scale fracture zones) adds to a growing body of evidence in support of the notion that the architecture of freshwater aquifers may include physical barriers that can act as regional‐scale drivers of groundwater faunal distributions and genetic structuring.