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

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 unra...

Genetic and morphological evidence cast doubt on the validity of Mexican troglobitic species of the Neotropical catfish genus Rhamdia (Siluriformes: Heptapteridae)

“…Without discounting other possible explanations, this counterintuitive finding could be attributed to the relative recency of the divergence between R. laticauda and hypogean species/populations (none of the cave-dwelling forms has on average shorter barbels than R. laticauda). Furthermore, the presence of comparatively longer barbels in the epigean R. guatemalensis is unsurprising when considering its strong nyctophilia (Arroyave et al, 2020;Wilkens, 2001).…”

La cochinilla Creaseriella anops (Crustacea: Isopoda: Cirolanidae) de las cuevas anquihalinas de Yucatán, México ¿Existen patrones de variación en la talla?

“…Aunque todavía es especulativo, C. anops podría haber pasado por cambios similares lo que tendría un efecto homogeneizador de las tallas y proporciones corporales como ahora se observa. En contraste, es interesante notar que el bagre Rhamdia guatemalensis (Günther, 1864), ampliamente distribuido en las zonas abiertas de los cenotes de la PY, muestra cierto grado de estructura genética dentro de las 2 grandes áreas de cenotes, anillo de cenotes y Riviera Maya, y también variantes morfológicas, pero sin ningún patrón espacial (Arroyave et al, 2020).…”

Identity Crisis: An Integrative Re-Evaluation of Typhlatya Shrimp within the Karst Aquifer of the Yucatán Peninsula, Mexico.

“…The presence of Typhlatya within inland and coastal cenotes throughout the Peninsula, and their strict affinity to particular salinities and hydrogeological constraints, identifies member species as potential models to assess groundwater health. Given temporal high energy meteorological events (e.g., hurricanes) 74 , and other environmental impacts 67,71,72 , prevalent in Yucatán region and continuing sea-level rise [58][59][60] , Typhlatya species can serve as biological indicators 75,76 and/or indicators of ecological resilience 77 to environmental change. The phylogeny presented here provides a robust evolutionary hypothesis for conducting comparative studies among closely related species to understand adaptation and key functional roles 70 .…”

“…Yucatán freshwater cyclopinid copepods are hypothesized to have followed a similar biogeographic pattern, with southern populations migrating northward and experiencing isolation events post-Pliocene 64,65 , however divergence times for Typhlatya species are likely due to older events . Vertebrates, such as the cave dwelling freshwater catfish, Rhamdia guatemalensis (Günther, 1864), show patterns consistent with colonization from the southernmost region of the northern Peninsula and subsequently expanded north and north-eastward 66,67 .…”