Genetic introgression and hybridization in Antillean freshwater turtles (Trachemys) revealed by coalescent analyses of mitochondrial and cloned nuclear markers

Abstract

Determining whether a conflict between gene trees and species trees represents incomplete lineage sorting (ILS) or hybridization involving native and/or invasive species has implications for reconstructing evolutionary relationships and guiding conservation decisions. Among vertebrates, turtles represent an exceptional case for exploring these issues because of the propensity for even distantly related lineages to hybridize. In this study we investigate a group of freshwater turtles (Trachemys) from a part of its range (the Greater Antilles) where it is purported to have undergone reticulation events from both natural and anthropogenic processes. We sequenced mtDNA for 83 samples, sequenced three nuDNA markers for 45 samples, and cloned 29 polymorphic sequences, to identify species boundaries, hybridization, and intergrade zones for Antillean Trachemys and nearby mainland populations. Initial coalescent analyses of phased nuclear alleles (using (*)BEAST) recovered a Bayesian species tree that strongly conflicted with the mtDNA phylogeny and traditional taxonomy, and appeared to be confounded by hybridization. Therefore, we undertook exploratory phylogenetic analyses of mismatched alleles from the "coestimated" gene trees (Heled and Drummond, 2010) in order to identify potential hybrid origins. The geography, morphology, and sampling context of most samples with potential introgressed alleles suggest hybridization over ILS. We identify contact zones between different species on Jamaica (T. decussata × T. terrapen), on Hispaniola (T. decorata × T. stejnegeri), and in Central America (T. emolli × T. venusta). We are unable to determine whether the distribution of T. decussata on Jamaica is natural or the result of prehistoric introduction by Native Americans. This uncertainty means that the conservation status of the Jamaican T. decussata populations and contact zone with T. terrapen are unresolved. Human-mediated dispersal events were more conclusively implicated for the prehistoric translocation of T. stejnegeri between Puerto Rico and Hispaniola, as well as the more recent genetic pollution of native species by an invasive pet turtle native to the USA (T. scripta elegans). Finally, we test the impact of introgressed alleles using the multispecies coalescent in a Bayesian framework and show that studies that do not phase heterozygote sequences of hybrid individuals may recover the correct species tree, but overall support for clades that include hybrid individuals may be reduced.

Conservation Genetics and Genomics of Amphibians and Reptiles

“…Much more rarely, hybrids were identified between endangered spiny-tailed iguanas (Ctenosaura bakeri) and a widespread congener (Ctenosaura similis) on the island of Utila (Honduras), suggesting that hybridization may not pose an immediate threat to the single island-endemic C. bakeri, as initially hypothesized (67). Finally, turtles appear to be particularly sensitive to threats from hybridization, and both human-mediated and natural hybrids between endangered and widespread species have been uncovered in many clades and geographic regions (68,69). Given the rate and extent of the trade of turtles at a global level, and their status as the most endangered major clade of vertebrates on earth, hybridization is a threat to the genetic integrity of many species that must be considered in management and conservation.…”

Testing Taxon Tenacity of Tortoises: evidence for a geographical selection gradient at a secondary contact zone

“…Many turtle species are known to hybridize (Lutterschmidt et al 2007;Vilaca et al 2012;Parham et al 2013), and we documented that hybridization naturally occurs between G. agassizii and G. morafkai at a secondary contact zone in northwestern Arizona. However, we did not always have continuity of results across the different methods we used to detect hybrids (Table 4).…”

Interspecies introgressive hybridization in spiny frogsQuasipaa(Family Dicroglossidae) revealed by analyses on multiple mitochondrial and nuclear genes

“…This phenomenon may be interpreted as an ancient hybridization between a female Stenella coeruleoalba and a male S. longirostris . Discrepancies were also found in the hybrid origin of Trachemys and Hyla arborea (Gvoždík et al., 2015; Parham et al., 2013). …”