Ecological and biogeographic underpinnings of spectacular diversification of murine rodents in Australasia (Sulawesi)

A project undertaken at Museum Victoria, and supervised by Kevin Rowe

Understanding why some lineages display higher taxonomic diversity and eco-morphological disparity than other lineages is one of the most intensive fields of study in evolutionary biology. Rodents of the subfamily Murinae (old world rats and mice) are dominant ecological components of every terrestrial ecosystem across the Indo-Australian Archipelago (IAA) and are the only non-flying, terrestrial mammals to have colonised Australia. They have independently colonised each of the major landmasses of the IAA (Asia, Australia, Philippines and Sulawesi) multiple times over the last 5 million years. Coupled with these colonisations, they have diversified into a myriad of ecological specialisations including invertebrate-feeding, aquatic living, and arboreality.

Sulawesi, Indonesia lies at the biogeographic crossroads of the IAA and has one of the highest levels of endemism on Earth. The island is home to over 50 endemic species of murine rodents in 14 genera (11 endemic) characterised by a suite of ecological specialists, morphological oddities, and phylogenetically enigmatic lineages. Until our recent expeditions, most of the rodent fauna of Sulawesi had not been sampled since 1975. The paucity of specimens and lack of genetic material from rodents of Sulawesi has stymied assessments of conservation threats and forced phylogenetic studies of Indo-Australian rodents to largely ignore Sulawesi’s potential role in generating regional biodiversity.

Our recent surveys of Sulawesi have led to the collection of over 50 species including all but one genus from Sulawesi and many rare species and genera (e.g. Sommeromys, a genus known previously from a single specimen collected in 1973). In addition, our surveys have resulted in discovery of several new species with four new species described to date. Most remarkable among these is the new genus and species Paucidentomys vermidax that is a specialized worm-feeder and is the only rodent with no cheek teeth and bifid (fang-like) upper incisors (Image1, Image 2, Image3). We also discovered the new genus and species, Waiomys mamasae, the first amphibious mammal known from Sulawesi (Image4). We also discovered the new genus and species, Hyorhinomys stuempkei, a hog-nosed carnivorous rat (Image5, Image6).

With these discoveries, new samples, and tissues from across the IAA we reconstructed a well-resolved molecular phylogeny showing that murine rodents colonised Sulawesi seven times, the Philippines five times and the Australian continent two times over the last five million years. Our analysis shows a central role of Sulawesi in the evolutionary origins of both Philippine and Australian rodents, with higher support for models incorporating Sulawesi as a stepping-stone. Our results also show that speciation following colonisation is the dominant source of species diversity across the IAA. For instance on Sulawesi in situ speciation accounts for more than 85% of species diversity in murine rodents.

Our results show that the earliest lineage to colonise Sulawesi evolved into the extreme ecomorphology of the shrew rats and now water rat, including nine species in seven genera. Previous morphological assessments spread these genera among three separate divisions and did not include our recently discovered taxa. Across the IAA, we demonstrate phylogenetically that carnivory, an exceptional trait among rodents, evolved independently four times after over-water colonisation, including in situ origins on the Philippines, Sulawesi, and Sahul. In each of these biogeographic units the origin of carnivory was followed by independent evolution of more specialized carnivorous ecomorphs including vermivores, diurnal insectivores, and amphibious rats. Our quantitative morphometric data demonstrate the striking convergence among ecomorphs from different biogeographic units including repeated expansion of the realised morphological space beyond what has evolved anywhere else in Murinae. Together these results demonstrate the extreme ecological opportunity afforded murine colonists of the IAA and suggest a deterministic role for natural selection in shaping the forms of life that evolved across the region.

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