Mitogenome of the Extinct Desert ‘Rat-Kangaroo’ Times the Adaptation to Aridity in Macropodoids

Abstract

The evolution of Australia’s distinctive marsupial fauna has long been linked to the onset of continent-wide aridity. However, how this profound climate change event affected the diversification of extant lineages is still hotly debated. Here, we assemble a DNA sequence dataset of Macropodoidea — the clade comprising kangaroos and their relatives — that incorporates a complete mitogenome for the Desert ‘rat-kangaroo’, Caloprymnus campestris. This enigmatic species went extinct nearly 90 years ago and is known from a handful of museum specimens. Caloprymnus is significant because it was the only macropodoid restricted to extreme desert environments, and therefore calibrates the group’s specialisation for increasingly xeric conditions. Our robustly supported phylogenies nest Caloprymnus amongst the bettongs Aepyprymnus and Bettongia. Dated ancestral area optimisations further reveal that the Caloprymnus-Bettongia lineage originated in nascent arid zone settings from the later-middle to early-late Miocene, ~12 million years ago (Ma), but subsequently dispersed into mesic habitats during the Pliocene and Pleistocene. This coincides with ancestral divergences amongst kangaroos in disparate woodland-forest and shrubland settings, but predates their adaptive radiation into proliferating grasslands during the late Miocene to Pliocene, after ~7 Ma. We thus demonstrate that protracted changes in both climate and vegetation likely staged the emergence of modern arid zone macropodoids.