Molecular phylogeography and reproductive biology of the freshwater snail Tarebia granifera in Thailand and Timor (Cerithioidea, Thiaridae): morphological disparity versus genetic diversity

Abstract

The freshwater thiarid gastropod Tarebiagranifera (Lamarck, 1816), including taxa considered either congeneric or conspecific by earlier authors, is widespread and abundant in various lentic and lotic water bodies in mainland and insular Southeast Asia, with its range extending onto islands in the Indo-West-Pacific. This snail is, as one of the most frequent and major first intermediate host, an important vector for digenic trematodes causing several human diseases. As a typical thiarid T.granifera is viviparous and parthenogenetic, with various embryonic stages up to larger shelled juveniles developing within the female’s subhemocoelic (i.e non-uterine) brood pouch. Despite the known conchological disparity in other thiarids as well as this taxon, in Thailand Tarebia has been reported with the occurrence of one species only. In light of the polytypic variations found in shell morphology of freshwater snails in general and this taxon in particular, the lack of a modern taxonomic-systematic revision, using molecular genetics, has hampered more detailed insights to date, for example, into the locally varying trematode infection rates found in populations of Tarebia from across its range in Thailand as well as neighboring countries and areas. Here, we integrate evidence from phylogeographical analyses based on phenotypic variation (shell morphology, using biometry and geometric morphometrics) with highly informative and heterogeneous mtDNA sequence data (from the gene fragments cytochrome c oxidase subunit 1 and 16 S rRNA). We evaluate both the morphological and molecular genetic variation (using several phylogenetic analyses, including haplotype networks and a dated molecular tree), in correlation with differences in the reproductive biology among populations of Tarebia from various water bodies in the north, northwest, central, and south of Thailand, supplementing our respective analyses of parasite infections of this thiarid by cercaria of 15 trematode species, reported in a parallel study. Based on the comparison of topotypical material from the island of Timor, with specimens from 12 locations as reference, we found significant, albeit not congruent variation of both phenotype and genotype in Tarebiagranifera, based on 1,154 specimens from 95 Thai samples, representing a geographically wide-ranging, river-based cross-section of this country. Our analyses indicate the existence of two genetically distinct clades and hint at possible species differentiation within what has been traditionally considered as T.granifera. These two lineages started to split about 5 mya, possibly related to marine transgressions forming what became known as biogeographical barrier north of the Isthmus of Kra. Grounded on the site-by-site analysis of individual Tarebia populations, our country-wide chorological approach focussing on the conchologically distinct and genetically diverse lineages of Tarebia allows to discuss questions of this either reflecting subspecific forms versus being distinct species within a narrowly delimited species complex. Our results, therefore, provide the ground for new perspectives on the phylogeography, evolution and parasitology of Thai freshwater gastropods, exemplified here by these highly important thiarids.