Going underground: Postcranial morphology of the early miocene marsupial mole naraboryctes philcreaseri and the evolution of fossoriality in notoryctemorphians

Abstract

We present the first detailed descriptions of postcranial elements of the fossil marsupial mole Naraboryctes philcreaseri (Marsupialia: Notoryctemorphia), from early Miocene freshwater limestone deposits in the Riversleigh World Heritage Area, northwestern Queensland. Qualitative functional analysis of these elements suggest that Na. philcreaseri was very well-adapted for burrowing, albeit somewhat less so than the living marsupial moles Notoryctes typhlops and N. caurinus. Quadratic discriminant analysis of limb measurements suggests that Na. philcreaseri was subterranean, and its Index of Fossorial Ability is almost identical to that of Notoryctes species, being among the highest known for any mammal. These results suggest that notoryctemorphians evolved their specialised, “mole-like” subterranean lifestyle prior to the early Miocene. Given that forested environments predominated in Australia until the middle-late Miocene, this transition to subterranean behaviour may have occurred via burrowing in forest floors, in which case fossorial mammals that live in tropical rainforests today (such as the placental golden moles Chrysospalax trevelyani and Huetia leucorhina) may represent reasonable living analogues for early notoryctemorphians. However, alternative scenarios, such as a cave-dwelling or semi-aquatic ancestry, should be considered. Phylogenetic analysis using a Bayesian total evidence dating approach places Naraboryctes as sister to Notoryctes with strong support (Bayesian posterior probability = 0.91), and indicates that Naraboryctes and Notoryctes diverged 30.3 MYA (95% HPD: 17.7-46.3 MYA). The age and known morphology of Na. philcreaseri does not preclude its being ancestral to Notoryctes. Using estimates of divergence times and ratios of nonsynonymous to synonymous substitutions per site, we infer that the nuclear gene “Retinol-binding protein 3, interstitial” (RBP3), which plays a key role in vision, became inactive in the Notoryctes lineage ~5.4 MYA (95% HPD: 4.5-6.3 MYA). This is much younger than previous published estimates, and postdates considerably the age of Na. philcreaseri, implying that RBP3 was active in this fossil taxon; hence, Na. philcreaseri may have retained a functional visual system. Our estimate for the inactivation of RBP3 in the Notoryctes lineage coincides with palaeobotanical evidence for a major increase in the abundance of grasses in Australia, which may indicate the appearance of more open environments, and hence selection pressure on notoryctemorphians to spend less time on the surface, leading to relaxed selection on RBP3. Ultimately, however, a fuller understanding of the origin and evolution of notoryctemorphians-including when and why they became “mole-like”-will require improvements in the Palaeogene fossil record of mammals in Australia