Aridification shaped the diversification of Bothriembryon land snails in a global biodiversity hotspot

Aim
Resolving the spatio-temporal diversification patterns and systematic relationships of endemic Australian land snails against the backdrop of Neogene aridification through analyses of a combined nuclear and mitochondrial DNA sequence dataset.

Location
Western Australia.

Taxon
Mollusca, Stylommatophora, Bothriembryontidae, Bothriembryon.

Methods
We employed Bayesian Inference and Maximum Likelihood to reconstruct the phylogenetic relationships in a group of Australian land snails using mitochondrial (COI, 16S) and nuclear (ANT) DNA sequences. Divergence times have been estimated by employing optimised molecular clocks using BEAST2, and RelTime in MEGA12. Speciation and net-diversification rates have been modelled using revBayes to visualise diversification dynamics in lineage-through-time (LTT) plots. We employed automated species delimitation methods ASAP and bPTP to estimate taxonomic diversity.

Results
Our final sequence dataset contained 1052 new DNA sequences from 374 individuals, representing 97% of all accepted species plus 26 putatively new species based on morphology and distribution. Recognizing almost three times as many candidate species, both DNA-based species delimitation methods have excessively inflated diversity estimates, casting doubt on the usefulness of these methods in groups with marked phylogeographic structure. Nine well-supported principal clades were recovered. Fossil-calibrated chronograms revealed an early bifurcation of Bothriembryon followed by an accumulation of lineages over time. LTT plots revealed a relative flattening of the speciation curve from 15 to 10 Ma on. However, we also detected a steep increase in intraspecific lineage diversification during the last approx. 1 Ma. The modeled speciation and net diversification rates have continuously declined over the last 25 Ma, while extinction rates have remained relatively steady until about 5 Ma, when they also started to climb.

Main Conclusions
Declining diversification rates during much of the Neogene, followed by increasing extinction rates, coincided with increasing aridity throughout Western Australia. A more recent increase in lineage diversification rates, driven by intraspecific differentiation, coincides with the rise of mesic conditions since the end of the Pleistocene. Both trends imply that through influencing extinction and diversification rates, historical climate change has likely contributed to shaping the current distribution patterns in Bothriembryon land snails that are characterised by fragmentation. Moreover, by uncovering many undescribed taxa, including multiple short-range endemics, this study highlights the importance of continued conservation efforts in this globally important biodiversity hotspot. Key habitats, such as lithorefugia, in an otherwise harsh and exposed landscape are important strongholds for Bothriembryon to weather the impact of aridification.