Coping With Dynamism: Phylogenetics and Phylogeographic Analyses Reveal Cryptic Diversity in Heleobia Snails of Atacama Saltpan, Chile

Abstract

The species that inhabit systems highly affected by anthropic activities usually exhibit this external influence in their gene pool. In this study, we investigated the genetic patterns of populations of Heleobia atacamensis, a freshwater microgastropod endemic to the Atacama Saltpan, a system historically exposed to environmental changes, and currently subjected to conditions associated with metallic and non-metallic mining and other anthropic activities. Molecular analyses based on nuclear and mitochondrial sequences indicate that the saltpan populations are highly fragmented and that the genetic structure is mainly explained by historical geographic isolation, with little influence of contemporary factors. The microsatellite results suggest a moderate genetic diversity and sharp differentiation mediated by isolation by distance. Additionally, despite the high environmental heterogeneity detected and the marked historical dynamism of the region, our data reveal no signs of demographic instability. The patterns of contemporary gene flow suggest a change in the current genetic structure, based on the geographic proximity and specific environmental conditions for each population. Our results, highlight the role of fragmentation as a modulator of genetic diversity, but also suggest that the historical persistence of isolated populations in naturally dynamic environments could explain the apparent demographic stability detected.

Genetic Diversity, Morphometric Characterization, and Conservation Reassessment of the Critically Endangered Freshwater Snail, Heleobia atacamensis, in the Atacama Saltpan, Northern Chile

“…DNA extraction, PCR amplification conditions and sequencing of the COI gene of snails from Peine and Tilomonte were obtained following Valladares et al [ 29 ]. Both strands of the amplified products were sequenced by Macrogen Inc. (Seoul, Korea).…”

“…The sequences were edited and then aligned using the algorithm of MAFFT v7.505 [ 36 ] in the online server by Katoh and Standley [ 37 ]. In all analyses, we included sequences of different populations of H. atacamensis from the Atacama Saltpan [ 29 ]. This dataset considered eight sites inside the Atacama Saltpan, including Tilopozo, type locality of the species, and two outside the coast (Peine and Tilomonte) ( Figure 1 ).…”

“…In the phylogenetic reconstructions, the sequences were concatenated, and posterior analyses were implemented using a partitioned dataset. The sequences of individuals from Peine and Tilomonte were included in a comprehensive dataset depicting main lineages of Heleobia [ 18 , 19 , 28 , 29 , 42 ] from the South American Altiplano and Atacama Desert. Three species of Semisalsa Radoman were used as sister group and Heleobops carrikeri Davis and McKee was used as outgroup ( Table S1 ).…”

“…from Tilomonte as the sister group of H. atacamensis , although specimens from Peine were not included. More recently, Valladares et al [ 29 ] used a multilocus approach (mitochondrial and nuclear sequences) to analyze samples of H. atacamensis from Tilopozo and other seven undescribed Heleobia populations located inside the Atacama Saltpan, recovering the eight populations in a monophyletic group as part of a larger clade also containing other congeneric species from the Chilean Altiplano and the Atacama Desert. In addition, based on microsatellite markers, they detected a marked genetic structure and a high level of fragmentation among populations of the species.…”

“…In addition, based on microsatellite markers, they detected a marked genetic structure and a high level of fragmentation among populations of the species. However, despite the fact that Valladares et al [ 29 ] significantly extended the range of H. atacamensis within the Atacama Saltpan, the snails from the peripherical towns of Peine and Tilomonte were not included.…”