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 arid conditions. Our robustly supported phylogenies nest Caloprymnus amongst the bettongs Aepyprymnus and Bettongia. Dated ancestral range estimations further reveal that the Caloprymnus-Bettongia lineage originated in nascent xeric settings during the middle to late Miocene, ~ 12 million years ago (Ma), but subsequently radiated into fragmenting mesic habitats after the Pliocene to mid-Pleistocene. This timeframe parallels the ancestral divergences of kangaroos in woodlands and forests, but predates their adaptive dispersal into proliferating dry shrublands and grasslands from the late Miocene to mid-Pleistocene, after ~ 7 Ma. We thus demonstrate that protracted changes in both climate and vegetation likely staged the emergence of modern arid zone macropodoids.

A review of the late Cenozoic genus Bohra (Diprotodontia: Macropodidae) and the evolution of tree-kangaroos

“…For the next century most authorities leaned toward an alliance between Dendrolagus and the New Guinea forest wallabies Dorcopsis Schlegel & Müller, 1845and Dorcopsulus Matschie, 1916(e.g., Bensley 1903Raven & Gregory 1946;Tate 1948;Kirsch 1977), although by the 1980s, the suspicion had arisen that the oft-mentioned dental similarities (e.g., blade-like premolars, simple low-crowned molars) were actually symplesiomorphies (Archer 1984;Flannery 1989). Since then, results from several molecular studies (e.g., Baverstock et al 1989;Campeau-Péloquin et al 2001;Westerman et al 2002Westerman et al , 2022Meredith et al 2009;Mitchell et al 2014), our earlier osteological analysis , and a total-evidence analysis (Beck et al 2022) have supported a sister relationship between rock-wallabies and tree-kangaroos in the tribe Dendrolagini.…”

“…Several molecular-clock estimates have been produced for the divergence timing of the dendrolaginan and Petrogale lineages: (Westerman et al 2022). Together, these estimates span the entire late Miocene.…”

“…By favouring the normal prior distribution because it had the lowest mean rate of evolution, Eldridge et al (2018) advocated for a mean molecular-clock estimate of 7.1 Ma ago for the split between the Australian and New Guinean clades of Dendrolagus. Westerman et al (2022) proposed an even earlier mean estimate of 7.8 Ma ago. An obvious implication is that the Bohra-Dendrolagus divergence would have to have occurred even earlier.…”

“…The only described late Miocene macropodine is Dorcopsoides fossilis from the Alcoota LF of central Australia. Nevertheless, both molecular and osteological data (Meredith et al 2009; have been used to posit that most major macropodine divergences occurred in the late Miocene, including that between tree-kangaroos and rock-wallabies (Campeau-Péloquin et al 2001;Potter et al 2012;Cascini et al 2019;Celik et al 2019;Westerman et al, 2022). A likely centre of evolution for the Dendrolagina cannot yet be identified with any confidence.…”

Finite element analysis of kangaroo astragali: A new angle on the ankle

“…Kangaroos belong to the superfamily Macropodoidea, family Macropodidae. By ~20 million years ago (Early Miocene) the Macropodidae divided into three subfamilies: Lagostrophinae (the only extant member is the banded hare‐wallaby Lagostrophus faciatus ), Macropodinae (all other extant macropodids), and Sthenurinae (the short‐faced kangaroos, that became extinct approximately 30 kya; Cascini et al, 2019; Westerman et al, 2022).…”