Aridification-driven evolution of a migratory fish revealed by niche modelling and coalescence simulations

Aim: Major knowledge gaps exist regarding the evolution of arid zone organisms. For freshwater species with high dispersal potential, little is known if historical aridification influenced connectivity across drainage divides and impacted on their divergence and diversification. We tested the hypothesis that the historical aridification of Australia promoted the isolation and influenced the demographic histories and evolutionary divergence of a migratory group of freshwater obligates. Location: Central arid eastern Australia; Murray-Darling Basin (MDB), Lake Eyre Basin (LEB), Fitzroy Basin (FIT). Taxon: Three lineages of golden perch (Macquaria ambigua), a widespread fishery resource from inland Australia. Methods: We obtained genome-wide data for golden perch sampled throughout their range. Phylogenetic relationships were reconstructed using maximum likelihood. Species distribution modelling was used to predict contemporary and past distributions for the three lineages and to develop hypotheses regarding their biogeographic and demographic histories. Hypotheses were independently tested using coalescent simulations in fastsimcoal and DIYABC with the genomic dataset. Results: We found evidence for three reciprocally monophyletic lineages that have experienced little to nil genetic connectivity since divergence. Coalescent models suggest that the coastal (FIT) and inland (MDB and LEB) lineages diverged similar to 103 thousand years ago (ka), followed by the split of MDB and LEB lineages similar to 58 ka. These timings agree with reductions of large freshwater environments in Australia during the late Pleistocene. Species distribution models show an extreme decrease in habitat during the Last Glacial Maximum similar to 21 ka, consistent with inferred demographic contractions in coalescent tests. Main conclusions: We reveal that aridification of Australia during the late Pleistocene has driven and reinforced the divergence of a migratory freshwater obligate. Our findings are important for informing the conservation management of aquatic organisms under climate change. This work further demonstrates the value of using species distribution modelling to formulate diversification hypotheses and to improve interpretation of coalescent analyses.