Speciation Generates Mosaic Genomes in Kangaroos

Abstract

The iconic Australasian kangaroos and wallabies represent a successful marsupial radiation. However, the evolutionary relationship within the two genera, Macropus and Wallabia, is controversial: mitochondrial and nuclear genes, and morphological data have produced conflicting scenarios regarding the phylogenetic relationships, which in turn impact the classification and taxonomy. We sequenced and analyzed the genomes of 11 kangaroos to investigate the evolutionary cause of the observed phylogenetic conflict. A multilocus coalescent analysis using ∼14,900 genome fragments, each 10 kb long, significantly resolved the species relationships between and among the sister-genera Macropus and Wallabia. The phylogenomic approach reconstructed the swamp wallaby (Wallabia) as nested inside Macropus, making this genus paraphyletic. However, the phylogenomic analyses indicate multiple conflicting phylogenetic signals in the swamp wallaby genome. This is interpreted as at least one introgression event between the ancestor of the genus Wallabia and a now extinct ghost lineage outside the genus Macropus. Additional phylogenetic signals must therefore be caused by incomplete lineage sorting and/or introgression, but available statistical methods cannot convincingly disentangle the two processes. In addition, the relationships inside the Macropus subgenus M. (Notamacropus) represent a hard polytomy. Thus, the relationships between tammar, red-necked, agile, and parma wallabies remain unresolvable even with whole-genome data. Even if most methods resolve bifurcating trees from genomic data, hard polytomies, incomplete lineage sorting, and introgression complicate the interpretation of the phylogeny and thus taxonomy.

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

“…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).…”

“…Dating the radiation of Macropodinae marsupials presents a 450 particularly interesting challenge because of conflicting intrinsic (molecular, morphological) and extrinsic (environmental, habitat, diet) signals. In addition, resolving the relationships among kangaroo groups and species has been complicated by evidence of ancient and recent introgression (Potter et al 2012;Phillips et al 2013;Nilsson et al 2018). While we work to find more accurate and more complete answers to these questions, we would be better served by recognizing current limitations and ambiguities, rather than ignoring them.…”

“…Removing Ganguroo and Ngamaroo node priors results in divergence estimates from 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 285 estimate (Nilsson et al 2018) (Fig.2). Because the dates inferred using Ganguroo and Ngamaroo fossil node calibrations differ so considerably from estimates in the literature, I removed them from further analyses, and consider divergence estimates and macroevolutionary inferences using trees that do not include these node calibrations.…”

“…Divergence analyses using fossil tips and all five node priors result in date estimates 270 which are at odds with recent molecular results (Dodt et al 2017;Nilsson et al 2018;Couzens and Prideaux 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).…”

“…The timing of the radiation of modern kangaroos remains a topic of debate. Most recently it has been suggested that kangaroos speciated rapidly in response to the expansion of C 4 grasses in the Pliocene (Nilsson et al 2018;Couzens and Prideaux 2018). This hypothesis conflicts with a number of molecular and morphological dating studies (Phillips et al 2013; package (Gavryushkina et al 2014).…”