Panpulmonate habitat transitions: tracing the evolution of Acochlidia (Heterobranchia, Gastropoda)

The evolution and diversification of euthyneuran slugs and snails was likely strongly influenced by habitat transitions from marine to terrestrial and limnic systems. Wellsupported euthyneuran phylogenies with detailed morphological data can provide information on the historical, biological and ecological background in which these habitat shifts took place allowing for comparison across taxa. Acochlidian slugs are ‘basal pulmonates’ with uncertain relationships to other major panpulmonate clades. They present a unique evolutionary history with representatives in the marine mesopsammon, but also benthic lineages in brackish water, limnic habitats and (semi-)terrestrial environments. We present the first comprehensive molecular phylogeny on Acochlidia, based on a global sampling that covers nearly 85 % of the described species diversity, and additionally, nearly doubles known diversity by undescribed taxa. Our phylogenetic hypotheses are highly congruent with previous morphological analyses and confirm all included recognized families and genera. We further establish an ancestral area chronogram for Acochlidia, document changes in diversification rates in their evolution via the birth-death-shift-model and reconstruct the ancestral states for major ecological traits. Based on our data, Acochlidia originated from a marine, mesopsammic ancestor adapted to tropical waters, in the mid Mesozoic Jurassic. We found that the two major subclades present a remarkably different evolutionary history. The Microhedylacea are morphologically highly-adapted to the marine mesopsammon. They show a circum-tropical distribution with several independent shifts to temperate and temperate coldhabitats, but remained in stunning morphological and ecological stasis since the late Mesozoic. Their evolutionary specialization, which includes a remarkable and potentially irreversible ‘meiofaunal syndrome’, guaranteed long-term survival and locally high species densities but also resembles a dead-end road to morphological and ecological diversity. In contrast, the Hedylopsacea are characterized by morphological flexibility and ecologically by independent habitat shifts out of the marine mesopsammon, conquering (semi-)terrestrial and not peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission. The copyright holder for this preprint (which was . http://dx.doi.org/10.1101/010322 doi: bioRxiv preprint first posted online Oct. 15, 2014;