Recent range expansion of an intermediate host for animal schistosome parasites in the Indo-Australian Archipelago: phylogeography of the freshwater gastropod Indoplanorbis exustus in South and Southeast Asia

Abstract

Background: The planorbid snail Indoplanorbis exustus is the sole intermediate host for the Schistosoma indicum species group, trematode parasites responsible for cattle schistosomiasis and human cercarial dermatitis. This freshwater snail is widely distributed in Southern Asia, ranging from Iran to China eastwards including India and from the southeastern Himalayas to Southeast Asia southwards. The veterinary and medical importance of this snail explains the interest in understanding its geographical distribution patterns and evolutionary history. In this study, we used a large and comprehensive sampling throughout Indo-Malaya, including specimens from South India and Indonesia, areas that have been formerly less studied. Results: The phylogenetic inference revealed five highly divergent clades (genetic distances among clades: 4.4 13.9%) that are morphologically indistinguishable, supporting the assumption that this presumed nominal species may represent a cryptic species complex. The species group may have originated in the humid subtropical plains of Nepal or in southern adjacent regions in the Early Miocene. The major cladogenetic events leading to the fives clades occurred successively from the Early Miocene to the Early Pleistocene, coinciding with major periods of monsoonal intensification associated with major regional paleogeographic events in the Miocene and repeated climate changes due to the Plio-Pleistocene climatic oscillations. Our coverage of the Indo-Australian Archipelago (IAA) highlights the presence of a single clade there. Contrary to expectations, an AMOVA did not reveal any population genetic structure among islands or along a widely recognised zoogeographical regional barrier, suggesting a recent colonisation independent of natural biogeographical constraints. Neutrality tests and mismatch distributions suggested a sudden demographic and spatial population expansion that could have occurred naturally in the Pleistocene or may possibly result of a modern colonisation triggered by anthropogenic activities. Conclusions: Even though Indoplanorbis is the main focus of this study, our findings may also have important implications for fully understanding its role in hosting digenetic trematodes. The existence of a cryptic species complex, the historical phylogeographical patterns and the recent range expansion in the IAA provide meaningful insights to the understanding and monitoring of the parasites potential spread. It brings a substantial contribution to veterinary and public health issues.