The endemic gastropod fauna of Lake Titicaca: correlation between molecular evolution and hydrographic history

Abstract

Lake Titicaca, situated in the Altiplano high plateau, is the only ancient lake in South America. This 2- to 3-My-old (where My is million years) water body has had a complex history that included at least five major hydrological phases during the Pleistocene. It is generally assumed that these physical events helped shape the evolutionary history of the lake's biota. Herein, we study an endemic species assemblage in Lake Titicaca, composed of members of the microgastropod genus Heleobia, to determine whether the lake has functioned as a reservoir of relic species or the site of local diversification, to evaluate congruence of the regional paleohydrology and the evolutionary history of this assemblage, and to assess whether the geographic distributions of endemic lineages are hierarchical. Our phylogenetic analyses indicate that the Titicaca/Altiplano Heleobia fauna (together with few extralimital taxa) forms a species flock. A molecular clock analysis suggests that the most recent common ancestor (MRCAs) of the Altiplano taxa evolved 0.53 (0.28–0.80) My ago and the MRCAs of the Altiplano taxa and their extralimital sister group 0.92 (0.46–1.52) My ago. The endemic species of Lake Titicaca are younger than the lake itself, implying primarily intralacustrine speciation. Moreover, the timing of evolutionary branching events and the ages of two precursors of Lake Titicaca, lakes Cabana and Ballivián, is congruent. Although Lake Titicaca appears to have been the principal site of speciation for the regional Heleobia fauna, the contemporary spatial patterns of endemism have been masked by immigration and/or emigration events of local riverine taxa, which we attribute to the unstable hydrographic history of the Altiplano. Thus, a hierarchical distribution of endemism is not evident, but instead there is a single genetic break between two regional clades. We also discuss our findings in relation to studies of other regional biota and suggest that salinity tolerance was the most likely limiting factor in the evolution of Altiplano species flocks.

Constant diversification rates of endemic gastropods in ancient Lake Ohrid: ecosystem resilience likely buffers environmental fluctuations

“…Preliminary data of the SCOPSCO deep-drilling program based on core catcher data for the last 1.2 My and high-resolution data for the last 640 thousand years (ky) so far do not indicate the occurrence of catastrophic environmental events Wagner et al, 2014), i.e., events that lead to sudden drastic regime shifts (sensu Scheffer and Carpenter, 2003;Scheffer et al, 2001) and thus potentially to mass extinction. By comparison, such events have been observed in other ancient lakes, including Lake Titicaca (Kroll et al, 2012;Lavenu, 1992) and Lake Malawi Schultheiß et al, 2009Schultheiß et al, , 2011. We do, however, see signatures of severe environmental/climatic perturbations in Lake Ohrid, including significant lake-level drops (Lindhorst et al, 2010), volcanic ash deposits Wagner et al, 2014), and glacial-interglacial cycles (Lézine et al, 2010;Reed et al, 2010;Wagner et al, 2014).…”

“…Another theory suggests that diversification rates can be higher in the initial phase of diversification (particularly in groups that diversify through an adaptive radiation) and may decline once niche spaces becomes successively occupied (e.g., Purvis et al, 2009;Schluter, 2000). This may happen after a lake first came into existence or after the occurrence of major environmental events such as volcanic ash deposits, severe lake-level drops, and desiccation or salinization events (Cristescu et al, 2010;Kroll et al, 2012;Salzburger et al, 2014). A forth theory proposes the opposite, i.e., the existence of a pronounced lag phase between colonization and onset of diversification (e.g., Cristescu et al, 2010).…”

“…Some lakes, despite being old, have gone through a series of major environmental events, and the respective endemic species are often comparable young, as observed in Lake Malawi (e.g., Schultheiß et al, 2009Schultheiß et al, , 2011 and Lake Titicaca (Kroll et al, 2012). Other lakes such as Lake Baikal (e.g., Ivanov et al, 2013) and Lake Tanganyika (e.g., Salzburger et al, 2014; might be sufficiently old but lack a continuous paleo-limnological record.…”

Hidden diversity in spring snails from the Andean Altiplano, the second highest plateau on Earth, and the Atacama Desert, the driest place in the world

“…The species have a wide range of ecological tolerances and reproductive strategies 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 2008Simões et al , 2009Simões et al , 2010Alda 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.…”

“…The taxonomic status of these species and several previously unexamined populations distributed in the region has never been investigated. Additionally, the distribution ranges and relationships among the species have been addressed by few studies (Biese 1944(Biese , 1947Kroll et al 2012). Considering that these two geographical areas are difficult to access and concomitantly poorly explored, it is highly possible that the biodiversity of Heleobia is underestimated.…”