Systematics of Bolivian frogs of the genus Telmatobius (Anura, Ceratophryidae) based on mtDNA sequences

Abstract

The aim of this work was to clarify the taxonomic status and phylogenetic relationships of the Bolivian frogs of the genus Telmatobius, which inhabit different kinds of habitats in the Andes. Sequences of the mitochondrial 16S and cytochrome b (cob) genes were analysed for representatives of most species and morphotypes of Telmatobius in the region; the morphologically diverse species of the T. marmoratus Complex were emphasized. Phylogenetic reconstructions (ML, MP, Bayesian) reveal three clades of Bolivian Telmatobius. A well-supported clade includes members of the T. verrucosus Group–T. sanborni, T. verrucosus and T. espadai, but relationships among them are not resolved. All the remaining taxa form a monophyletic group, the T. marmoratus–T. bolivianus Clade. Within this lineage, the well-defined T. marmoratus Clade includes all samples from the high-elevation Puna-Altiplano system (i.e. T. hintoni, T. huayra, T. marmoratus, T. culeus and T. gigas), whereas the poorly supported T. bolivianus Clade includes T. bolivianus, T. yuracare, T. sibiricus and T. simonsi. The only known population of T. gigas is deeply nested within T. marmoratus, indicating that there has not been enough time for mitochondrial lineages to achieve reciprocal monophyly. Telmatobius culeus, the Lake Titicaca frog, is sister to the T. marmoratus–T. gigas assemblage. Under different nucleotide substitution rate models for the cob gene, the analyses indicate that the divergence of the two clades from the common ancestor of all Bolivian Telmatobius occurred no more recently than 9 million years (My) ago (2%) and no earlier than 20 My ago (1%). During this time interval, the central Andes had not reached sufficient altitude to support Puna vegetation (assuming climatic conditions to have been similar to those today). A plausible rate of 2% implies that the appearance of highland species took place in the Pliocene, less than 5 My ago, which is consistent with the idea of an increased uplift rate for the Altiplano and eastern Cordillera of the central Andes since the late Miocene. This rapid uplift gave place to the Puna and highland dry vegetation types to which members of the T. hintoni and T. marmoratus groups are adapted. Under this model, the split of these two groups took place less than 2 My ago, and that of T. marmoratus (including T. gigas) and the ancestral lacustrine species T. culeus only c. 1.5 My ago.