Diversification, biogeography and the evolution of twig-lining behaviours in the Australian trapdoor spider genus Idiosoma (Araneae: Idiopidae: Aganippini): the role of parallel evolution and adaptive shifts in a continental radiation of mygalomorph spiders

The terrestrial biota of modern Australia is a highly diverse mix of taxa exhibiting an array of adaptations to a range of habitats across three major biomes. With the vast majority of Australia now covered by dry, fire-tolerant vegetation communities that have evolved since the Eocene, Australia can be considered an arid continent, with xeric habitats of varying degrees of aridity dominating the Arid Zone, Mesic Zone and Monsoon Tropics biomes. Molecular phylogenetic studies exploring the evolutionary and biogeographic histories of Australian arid-adapted lineages cover a wide spectrum of animal and plant taxa, and have together highlighted the important role evolutionary adaptive radiations have played since the Miocene in shaping the composition and distributions of lineages. In this study, we apply a taxon-rich, multi-locus molecular dataset (of 252 specimens), to infer a continent-scale phylogeny of the Australian endemic trapdoor spider genus Idiosoma Ausserer (Idiopidae). This mega-diverse lineage of mygalomorph spiders is notable for being found across most of continental mainland Australia in both the Arid Zone and Mesic Zone biomes, in predominantly transitional and arid habitats to the exclusion of ever-wet mesic refugia. Idiosoma is further notable in the sheer variety of different burrow entrance morphologies constructed by species in different parts of Australia, with a suite of taxa known to construct burrows with an unusual and conspicuous addition of leaves or twigs (i.e., ‘twig-lines’) fanning out from the burrow entrance. This twig-lining behaviour has been postulated to be an adaptive shift associated with higher aridity environments. With the aim of characterising the Idiosoma adaptive radiation, including potential phenotypic adaptive shifts, we revealed a genus with at least 120 putative species in our molecular dataset, and a total Australian fauna that likely exceeds 200 species. Phylogenetic structure within the genus showed remarkably strong geographic fidelity at all levels, indicating an evolutionary history that has been heavily influenced by biogeographic factors. Ancestral range reconstruction recovered a temperate south-western or arid origin for crown-group Idiosoma, with divergence dating showing that the major diversification of lineages occurred from ca. 10–4 million years ago. Combined, these results support a Mio-Pliocene model of Idiosoma speciation across continental Australia, at a time when the country was undergoing extensive aridification. Finally, results of a maximum likelihood analysis using continuous-time Markov models were consistent with a model of parallel evolution of twig-lining burrowing behaviours in Idiosoma, driven by discrete adaptive shifts in biomes with contrasting levels of aridity. This is the first study to have quantified phenotypic adaptive shifts in a continental radiation of invertebrate animals across arid Australia, providing further evidence of the importance of climate-driven biotic change during the Miocene and Pliocene in shaping the distribution and composition of the Australian Arid Zone biota.