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.

Maximizing Molecular Data From Low-Quality Fluid-Preserved Specimens in Natural History Collections

“…Morphological inspection of voucher specimens is indeed important for studying diversity and the processes that generate it, but may be hampered by poor specimen quality or changes in commonly-measured traits (Maayan et al, 2022). Opportunities provided by natural history collections have now expanded, with genetic and genomic sequencing of museum specimens facilitating species (re)discovery (Rasmussen et al, 2012) and determining past evolutionary dynamics (Mikheyev et al, 2017;Tsai et al, 2019;Roycroft et al, 2021). Our approach and methodology were successful for incorporating both nuclear and mitochondrial data for phylogenetics, the latter of which is often used in museum genomics studies due to its ofteneasier acquisition over nuclear loci.…”

“…The current era of genomics has been met with several protocols to obtain useable DNA from these intractable museum specimens (e.g., Rohland et al, 2004;Hykin et al, 2015;Ruane and Austin, 2017;O'Connell et al, 2021;reviewed in Ruane, 2021). As a result, the taxonomic identity and phylogenetic placement of poorly known snakes (Allentoft et al, 2018;Deepak et al, 2018), lizards (Hykin et al, 2015;McGuire et al, 2018), frogs (Rancilhac et al, 2020), salamanders (Pyron et al, 2022), crustaceans (France and Kocher, 1996), spiders (Wood et al, 2018), and birds (McCormack et al, 2016) have been successful, and with some studies on birds (Linck et al, 2017;Tsai et al, 2019) and mammals (Roycroft et al, 2021) obtaining levels of informativeness adequate to determine biogeographic histories and extinction patterns. Studies involving 'museum genomics' research involve materials from traditional museums and cryogenic collections, as well as the respective supporting infrastructure (Card et al, 2021).…”

Understanding “Alexandrian” extinctions using genomic DNA from fluid-preserved museum specimens of Desmognathus salamanders

“…Similarly, historical genomic DNA can be used to assess the taxonomic identity of historical specimens and the nomenclatural validity of putatively extinct taxa (Kirchman et al 2010;McGuire et al 2018;Kehlmaier et al 2020). However, few if any studies have combined these to study what we term Alexandrian extinctions; enigmatic declines or extinctions of historically named taxa whose identity is of immediate conservation relevance (Roycroft et al 2021). We provide a test case for Desmognathus fuscus carri, a synonym of D. "auriculatus" associated with populations that disappeared from peninsular Florida in the late 1960s or early 1970s (Means 2015).…”

“…Extinct named taxa may also be of particular relevance if they represent distinct phylogenetic lineages associated with speci c traits, habitats, or other factors affecting extinction risk (Roycroft et al 2021).…”

Diet and occurrences of the letter-winged kite in a predation refuge

“…Many Australian arid-zone rodents are irruptive species whose populations display dramatic increases in response to pulses of primary productivity (Predavec 1994;Greenville et al 2012). Unfortunately, around 20 Australian rodent species have become extinct since European arrival and many more have experienced significant range declines (Woinarski et al 2015;Roycroft et al 2021). Predation by the introduced mesopredators the red fox (Vulpes vulpes) and the cat (Felis catus) are key drivers of previous and ongoing rodent extinction (Smith and Quin 1996;Woinarski et al 2019).…”