A molecular and morphometric assessment of the systematics of the Macropus complex clarifies the tempo and mode of kangaroo evolution

Abstract

Kangaroos and wallabies of the Macropus complex include the largest extant marsupials and hopping mammals. They have traditionally been divided among the genus Macropus (with three subgenera: Macropus, Osphranter and Notamacropus) and the monotypic swamp wallaby, Wallabia bicolor. Recent retrotransposon and genome-scale phylogenetic analyses clarify the placement of Wallabia as sister to Notamacropus, with Osphranter and Macropus branching successively deeper. In view of the traditional Macropus concept being paraphyletic, we undertake to resolve the species-level phylogeny and genus-level taxonomy of the Macropus complex. For the first time, we include nuclear and mitochondrial DNA covering all extant species, and the first DNA sequences from the extinct Toolache wallaby (Notamacropus greyi), which we find groups with the black-gloved wallaby (Notamacropus irma). Morphological variation was examined using geometric morphometric methods on three-dimensional surface-scanned skulls. Wallabia skull shape fell close to Notamacropus (or Thylogale when controlling for allometry). We recommend the subgenera Macropus, Osphranter and Notamacropus be elevated to genera, alongside Wallabia, based on comparisons with other established macropodine genera for cranial disparity, ecology and molecular divergence. Our time tree estimates that all four 'Macropus' genera diverged close to the Miocene-Pliocene boundary (~6-5 Mya), then diversified coincident with Pliocene expansion of grasslands in Australia.

Incorporating uncertainty is essential to macroecological inferences: Grass, grit, and the evolution of kangaroos

“…Removing Ganguroo and Ngamaroo node priors results in divergence estimates from 295 combined evidence analyses (with priors on extinct taxa ages) which are generally in agreement with another recent phylogenetic assessment of this group (Celik et al 2019). This places the crown divergences of the Macropodinae at 7.8-10 MYA, Dendrolagini 6-8.5 MYA, Dorcopsini 6.5-9 MYA, and Macropodini 6.5-9.5 MYA, slightly older than another molecular-only estimate (Fig.2).…”

“…One step in simplifying this process may be instead to remove node priors based on these ambiguous taxa, and instead estimate their phylogenetic position, divergence times, and fossil ages jointly. By implementing this process in dating analyses, I recovered divergence estimates that are broadly concordant with recent node-calibrated molecular based studies (Celik et al 2019) and interpretations from the fossil record (Couzens & Prideaux 2018). These divergence estimates differ considerably from analyses implementing fixed fossil ages (as minimum, mean, or maximum stratigraphic bounds), including another tip-dating study (Cascini et al 2018), and generally fall between estimates from mean and maximum fixed 380 dates (Fig.2).…”

“…Divergence dates estimated from fossils 280 with tip age priors are broadly overlapping with those of mean and maximum fixed ages, often fall between estimates from those dating schemes, and do not solely return prior values ( Fig.S11). Divergence analyses using fossil tips and all five node priors result in date estimates which are at odds with recent molecular results (Dodt et al 2017;Couzens & Prideaux 285 2018; Nilsson et al 2018;Celik et al 2019). This is primarily driven by the hard minimum prior age of Ganguroo bilamina which limits the divergence of the Lagostrophinae and Macropodinae to 17.79 MYA (Neville's Garden Site (Woodhead et al 2016)), and to a lesser extent, the minimum prior age of Ngamaroo archeri (Fig.S1-S2).…”

“…Fossil ages for two extinct taxa Ganguroo bilamina and Ngamaroo archeri are often used as node priors to calibrate marsupial trees. Ngamaroo is generally used to provide a late Oligocene (24.7 Mya) or early Miocene (16 Mya (Phillips et al 2013;Cascini et al 2018;Celik et al 2019). Morphological phylogenetic analyses however, 360 tend to place this taxon within the clade comprising Potoroidae and Macropodidae (Prideaux & Warburton 2010;Butler et al 2016Butler et al , 2018.…”

“…Applying this minimum bound to the potoroid-macropodid split ultimately dramatically increases divergence date estimates across the macropodoid tree (Fig.S1,S2), pulling dates outside 365 of reasonable estimates. Similarly, Ganguroo is typically used to provide an early-to-mid Miocene minimum (17.79) (Woodhead et al 2016) on the Potoroidae-Macropodidae split (Cascini et al 2018;Celik et al 2019). This taxon alternately falls within the potoroidmacropodid crown, or the Lagostrophus-Macropodinae clade.…”