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.

New freshwater mussel taxa discoveries clarify biogeographic division of Southeast Asia

“…www.nature.com/scientificreports www.nature.com/scientificreports/ approximately Myr ago 46 . The high level of genetic divergence between populations of the giant freshwater prawn Macrobrachium rosenbergii (de Man, 1879) (Palaemonidae) clearly supports the existence of a hypothetical seaway north of the Isthmus of Kra 37 .…”

“…All deleterious mutations were retained for the analyses. While numerous recent studies reveal that using an integrative approach for freshwater mussel taxonomic research is rather straightforward [4][5][6][7][70][71][72][73] , its application to freshwater gastropods is more difficult due to several shortcomings such as a possible incongruence in a mitochondrial phylogeny 76,77 and often higher DNA barcoding thresholds between species 46,78,79 . At first glance, the differences between these groups can be explained by slower evolutionary rates of freshwater mussels 20,65 compared with those of freshwater gastropods 80 . nomenclatural acts.…”

Exploring the evolutionary potential of parasites: Larval stages of pathogen digenic trematodes in their thiarid snail host Tarebia granifera in Thailand

“…The species has been introduced to Africa, the Near East, North and Central America as well as to the Caribbean region and is considered to be invasive there (Abbott 1952, Chaniotis et al 1980, Prentice 1983, Vargas et al 1991, Férnandez et al 1992, Gutierrez et al 1997, Pointier et al 1998, Appleton 2002, Mukaratirwa et al 2005, Facon and David 2006, Appleton et al 2009, Miranda et al 2010, 2011, Miranda and Perissinotto 2012. A parallel study on Tarebia granifera (also published in this journal; see Veeravechsukij et al 2018) shows this species to be widely distributed throughout Thailand, with several named and described congeneric constituent populations, as is revealed by respective collections carried out in the North, Northeast, South, East, and Central region, and morphological documentation conducted detailing the biometrical parameters of the adult shells. In addition, molecular phylogenies using fragments of the mitochondrial cytochrome c oxidase subunit 1 (cox1) and 16 S rRNA genes have been constructed, as well as the reproductive strategy documented (i.e.…”

A glimpse in the dark? A first phylogenetic approach in a widespread freshwater snail from tropical Asia and northern Australia (Cerithioidea, Thiaridae)

“…embryos without shell, develop and are released as veligers (ovoviviparity), other thiarid species brood and even transform their subhaemocoelic brood pouch into a matrotrophic organ or "pseudoplacenta" that apparently nourishes the developing juveniles, as e.g. in the Southeast Asian thiarid Tarebia granifera (Lamarck, 1816) (euviviparity, see Glaubrecht 1996;Glaubrecht et al 2009;Maaß and Glaubrecht 2012;Veeravechsukij et al 2018b). Finally, some thiarids also have an extraordinarily high invasive potential, such as Melanoides tuberculata (Müller, 1774) and Tarebia granifera and today have an almost pantropical distribution (e.g., Brown 1994;Glaubrecht 1996).…”

“…Glaubrecht et al (2009) and Maaß and Glaubrecht (2012) surveyed the thiarid fauna of Australia. Dechruska et al (2013) evaluated the status and identity of the nominal taxon Melania jugicostis Hanley & Theobald, 1876 from the Southeast Asian mainland, and Veeravechsukij et al (2018aVeeravechsukij et al ( , 2018b investigated the phylogeography and reproductive biology of T. granifera and its trematode parasites. However, many other named taxa have been rarely studied and, thus, remain enigmatic and even pure nomenclatorial "ghosts" with highly questionable status as evolutionary relevant entities, which hampers further insights into the systematics, biogeography, and evolution of these freshwater gastropods otherwise under scrutiny, e.g., in speciation and/ or radiation studies.…”