Museum genomics reveals the rapid decline and extinction of Australian rodents since European settlement

Abstract

Australia has the highest historically recorded rate of mammalian extinction in the world, with 34 terrestrial species declared extinct since European colonization in 1788. Among Australian mammals, rodents have been the most severely affected by these recent extinctions; however, given a sparse historical record, the scale and timing of their decline remain unresolved. Using museum specimens up to 184 y old, we generate genomic-scale data from across the entire assemblage of Australian hydromyine rodents (i.e., eight extinct species and their 42 living relatives). We reconstruct a phylogenomic tree for these species spanning ∼5.2 million years, revealing a cumulative total of 10 million years (>10%) of unique evolutionary history lost to extinction within the past ∼150 y. We find no evidence for reduced genetic diversity in extinct species just prior to or during decline, indicating that their extinction was extremely rapid. This suggests that populations of extinct Australian rodents were large prior to European colonization, and that genetic diversity does not necessarily protect species from catastrophic extinction. In addition, comparative analyses suggest that body size and biome interact to predict extinction and decline, with larger species more likely to go extinct. Finally, we taxonomically resurrect a species from extinction, Gould's mouse (Pseudomys gouldii Waterhouse, 1839), which survives as an island population in Shark Bay, Western Australia (currently classified as Pseudomys fieldi Waite, 1896). With unprecedented sampling across a radiation of extinct and living species, we unlock a previously inaccessible historical perspective on extinction in Australia. Our results highlight the capacity of collections-based research to inform conservation and management of persisting species.

Keywords: biodiversity; conservation; exon capture; phylogenomics; phylogeny.

Fig. 1.

Time-calibrated phylogeny of endemic Australian murine rodents based on 1,245 genes. Blue bars represent the 95% highest posterior density for each calibrated node. Colored squares indicate the current IUCN status for each species. A subset of illustrations are by Subir Shakya, and reprinted with permission from ref. . Top to bottom: Ls. apicalis, C. albipes, Zyzomys woodwardi, N. longicaudatus, N. alexis, Pseudomys fumeus, P. gouldii (×2), Pseudomys delicatulus.

Fig. 2.

(A) Distribution of interspecies and intraspecies divergences across all species, calculated as substitutions per site since split from sister species (above the species threshold) or split from geographically disparate subpopulation (below the species threshold). The dotted line demarcates the interspecies/intraspecies threshold based on species boundaries in Australian rodents. (B) Subsection taken from the full phylogeny to illustrate the close relationship between P. gouldii and P. fieldi (including from the type locality of P. gouldii) in relation to their otherwise closest sister species, P. higginsi; map of Australia showing collected specimens from live animals (colored points) and recent subfossil (open points) records of P. gouldii and P. fieldi. Sampled sites are indicated with boxes.

Fig. 3.

Individual whole-exome heterozygosity for extinct (red, including the mainland extinction of P. gouldii) and extant Australian rodents. Extant species are categorized as either originating from “small/geographically restricted” populations (gold) or “large/geographically connected” (gray) populations. Year of collection is indicated for specimens of extinct species. CR indicates critically endangered status.

Fig. 4.

Predictors of extinction and decline in Australian rodents. (A) Relationship between body size (log₁₀ g) and the “proportion of extinction or severe decline” (SD). (B) Differences among biomes in the “proportion of extinction or severe decline”. Inset map of Australia shows geographic regions defined as arid, mesic, and monsoon biomes, with biomes indicated by corresponding colors on both panels.