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.