Abstract
The Chilean Altiplano and the Atacama Desert in northern Chile harbor isolated hydrological systems or oases where it is possible to find minute aquatic snails of the genus Heleobia whose taxonomy is uncertain and where many populations remain unknown. Here, we obtained samples from 30 localities distributed in the region and used molecular (12S and 16S mitochondrial genes) and morphological (penis) characters to investigate diversity of this poorly known fauna. Molecular phylogenetic analysis consistently recovered five clades, one of which constitutes a cryptic species previously assigned to a species recognized in the area. Four other clades contained sequences of one nominal species consistent with its type locality and at least two additional candidate species, which were corroborated by a particular penis morphology. Furthermore, some morphological differences in penis morphology were observed in two Altiplano populations not resolved by the DNA sequences, providing support for two additional candidate species in the genus. A molecular clock analysis allowed tracing the origin of lineages back to the Early Pleistocene. We found support for recognizing four nominal species, one undescribed species and at least other four candidate species of the genus Heleobia in northern Chile. We also suggest that the current level of species diversity of Heleobia in the region is underestimated by the use of conchological criteria to recognize species and by the limited sampling conducted to date.
Highlights
The Chilean Altiplano and the Atacama Desert in northern Chile harbor isolated hydrological systems or oases where it is possible to find minute aquatic snails of the genus Heleobia whose taxonomy is uncertain and where many populations remain unknown
We investigate penis morphology considering that the organ is discriminatory in Heleobia species (Gaillard and de Castellanos 1976; Cazzaniga 1980, 1982a, b; Hershler and Thompson 1992; Pons da Silva 1993; Collado et al 2011b; Ovando and De Francesco 2011)
The greatest distance among the nominal species occurred between H. ascotanensis and H. atacamensis (1.95%), and between the latter species and H. chimbaensis (1.95%, data not shown)
Summary
The Chilean Altiplano and the Atacama Desert in northern Chile harbor isolated hydrological systems or oases where it is possible to find minute aquatic snails of the genus Heleobia whose taxonomy is uncertain and where many populations remain unknown. The diversity of the killifish of the genus Orestias Valenciennes, 1839 and the lunged aquatic snails of the genus Biomphalaria Preston, 1910 is hypothesized to be principally a consequence of the fragmentation of populations during the Middle and Late Pleistocene after the regression of several paleolakes that existed in the area (Lüssen et al 2003; Vila 2006; Vila et al 2011, 2013; Collado et al 2011a) West of this area, the Atacama Desert, the driest place in the world (McKay 2002; Vesilind 2003) with thousands of square miles of arid desert interrupted by occasional oases, is a hyperarid system thought to be relatively simple ecologically and with low productivity (Noy-Meier 1973), but containing endemic species, for example, within the genus Basilichthys Girard, 1855 (Atheriniformes), that has allopatric distribution (Dyer 2000). The species have a wide range of ecological tolerances and reproductive strategies (Marcus and Marcus 1963, 1965; Cazzaniga 1982a; Martín 2002; Neves et al 2010; Collado and Méndez 2011), and some of them serve as intermediate hosts in the life cycles of digenean trematodes (Etchegoin and Martorelli 1997; Simões et al 2008, 2009, 2010; Alda et al 2010; Merlo and Etchegoin 2011). Kroll et al (2012) studied the phylogenetic relationships of species mainly distributed in the Altiplano region and its major internal Lake Titicaca, and this is the only phylogenetic study performed in the genus Heleobia
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