Cryptic Population Structuring and the Role of the Isthmus of Tehuantepec as a Gene Flow Barrier in the Critically Endangered Central American River Turtle

Abstract

The critically endangered Central American River Turtle (Dermatemys mawii) is the only remaining member of the Dermatemydidae family, yet little is known about its population structuring. In a previous study of mitochondrial (mt) DNA in the species, three main lineages were described. One lineage (Central) was dominant across most of the range, while two other lineages were restricted to Papaloapan (PAP; isolated by the Isthmus of Tehuantepec and the Sierra de Santa Marta) or the south-eastern part of the range (1D). Here we provide data from seven polymorphic microsatellite loci and the R35 intron to re-evaluate these findings using DNA from the nuclear genome. Based on a slightly expanded data set of a total of 253 samples from the same localities, we find that mtDNA and nuclear DNA markers yield a highly congruent picture of the evolutionary history and population structuring of D. mawii. While resolution provided by the R35 intron (sequenced for a subset of the samples) was very limited, the microsatellite data revealed pronounced population structuring. Within the Grijalva-Usumacinta drainage basin, however, many populations separated by more than 300 kilometers showed signals of high gene flow. Across the entire range, neither mitochondrial nor nuclear DNA show a significant isolation-by-distance pattern, but both genomes highlight that the D. mawii population in the Papaloapan basin is genetically distinctive. Further, both marker systems detect unique genomic signals in four individuals with mtDNA clade 1D sampled on the southeast edge of the Grijalva-Usumacinta basin. These individuals may represent a separate cryptic taxon that is likely impacted by recent admixture.

Molecular Characterization of the Common Snook, Centropomus undecimalis (Bloch, 1792) in the Usumacinta Basin

“…These results support the confluence of two different genotypic clusters of the common snook in the Usumacinta River basin, one of which was widely distributed in the lower part of the basin (the delta zone) and reached the uplands (the rainforest zone), while the second cluster, which showed a more restricted distribution, occurred in the rainforest and floodplain zones, possibly extending to the upper part of the Usumacinta basin in Guatemala. A similar pattern was previously reported in the white turtle (Dermatemys mawii) [26][27][28], in which two genetic clusters were recovered along the Usumacinta River basin.…”

“…Hydrological connectivity, together with historical processes, could have played a major role in the genetic structure of the common snook population in the Usumacinta basin over different temporal and geographical scales [26][27][28]. Further studies including wider geographical sampling in the Gulf of Mexico and the Caribbean could help us to test these differential patterns of connectivity and genetic structure within the common snook across different regions.…”

“…Previous genetic studies of the common snook in the Usumacinta River basin recovered a single genetic pool, including samples from the San Pedro River, at the basin's floodplain, to the coastal area at Tabasco, Mexico [25]. However, other studies using freshwater species diversity and molecular data have suggested that the upper and lower part of the Usumacinta basin are different biogeographic units [10,[26][27][28][29]. In this sense, Ornelas-García et al [10] reported that despite the connectivity within the basin, the genetic diversity could be heterogeneously distributed, at least in Astyanax aeneus species, where the upper and lower basin present different levels of haplotype diversity, while the middle part of the basin presents the highest diversity, tentatively associated with a transition zone.…”

The Maya Preclassic to Classic transition observed through faunal trends from Ceibal, Guatemala

“…It seems unusual, then, that they are uncommon in the Preclassic, particularly during the late Middle and Late Preclassic periods when Ceibal reached one of its peak populations. One possible explanation for this may be that the turtle was actively transported throughout the Peten area during the Classic period, as has been suggested by biologists who found disjunct populations of related Dermatemys sharing a unique haplotype across the Maya region [113,114]. There is a notable genetic affinity between Dermatemys populations in the Isthmus of Tehuantepec area and the Salinas River near the Pasión with those of the Sartsún River of the southern Belize/Guatemala border region that does not seem possible without humans having actively transported the turtle at some point.…”

Distribution and Abundance of the Central American River Turtle, Dermatemys Mawii, in Southern Quintana Roo, Mexico: Implications for a Regional Conservation Strategy

“…This suggests that despite its prolonged use as a source of food for centuries [37,38], this species has been understudied. Notwithstanding the geographic proximity of the studies done in Belize up to date and as a result of the present work [16], Rio Hondo has started to be considered as a priority site for the conservation of the species [8].…”