Population genomics of a predatory mammal reveals patterns of decline and impacts of exposure to toxic toads

Abstract

Mammal declines across northern Australia are one of the major biodiversity loss events occurring globally. There has been no regional assessment of the implications of these species declines for genomic diversity. To address this, we conducted a species‐wide assessment of genomic diversity in the northern quoll (Dasyurus hallucatus), an Endangered marsupial carnivore. We used next generation sequencing methods to genotype 10,191 single nucleotide polymorphisms (SNPs) in 352 individuals from across a 3220‐km length of the continent, investigating patterns of population genomic structure and diversity, and identifying loci showing signals of putative selection. We found strong heterogeneity in the distribution of genomic diversity across the continent, characterized by (i) biogeographical barriers driving hierarchical population structure through long‐term isolation, and (ii) severe reductions in diversity resulting from population declines, exacerbated by the spread of introduced toxic cane toads (Rhinella marina). These results warn of a large ongoing loss of genomic diversity and associated adaptive capacity as mammals decline across northern Australia. Encouragingly, populations of the northern quoll established on toad‐free islands by translocations appear to have maintained most of the initial genomic diversity after 16 years. By mapping patterns of genomic diversity within and among populations, and investigating these patterns in the context of population declines, we can provide conservation managers with data critical to informed decision‐making. This includes the identification of populations that are candidates for genetic management, the importance of remnant island and insurance/translocated populations for the conservation of genetic diversity, and the characterization of putative evolutionarily significant units.

Population genomics and conservation management of the threatened black-footed tree-rat (Mesembriomys gouldii) in northern Australia

“…Our principal coordinate plot and analysis of differentiation patterns supports the previous subspecific circumscriptions for the black-footed tree-rat, with populations in Queensland ( M. g. rattoides ) and on Melville Island ( M. g. melvillensis ) displaying a high level of historical isolation from the rest of the mainland populations ( M. g. gouldii ). The population genomic structure of the black-footed tree-rat broadly aligns with other widespread mammal species across northern Australia, such as the brush-tailed rabbit-rat (von Takach et al 2021 ) and northern quoll (von Takach et al 2022 ), which also show genomic patterns consistent with 2–4 high-level evolutionary lineages. Similarly to the brachyotis group of rock wallabies (Potter et al 2014 ), major biogeographic barriers separating Queensland, the Northern Territory, Western Australia, and various islands (e.g., the Tiwi Islands and Groote Eylandt) tend to define genomic structure both within and among species.…”

“…Population genomic data can be used to inform conservation management and prioritise conservation actions and resources in a variety of ways, such as identifying areas with high levels of inbreeding or low adaptive capacity (Andersen et al 2004 ), investigating patterns of connectivity and adaptive divergence among populations (Sandoval-Castillo et al 2018 ), demonstrating results of, and identifying source populations for, translocations (Ottewell et al 2014 ; Rick et al 2019 ), and estimating historical and contemporary effective population sizes and trajectories (von Takach et al 2022 ). While detailed population genomic data is still unavailable for most Australian rodents, there are a small number of recent studies that have actively applied such data to conservation practice.…”

“…These subspecies broadly conform to major biogeographic barriers that separate the Queensland and north-western Australian populations, and Melville Island and mainland populations. The effects of such barriers on gene flow varies considerably amongst taxa, and genomic analysis helps to clarify the extent to which they impact population genetic differentiation (Melville et al 2011 ; Eldridge et al 2012 ; Catullo et al 2014 ; Edwards et al 2017 ; von Takach et al 2021 ; von Takach et al 2022 ). Such analyses refine our understanding of the geographic locations of evolutionary lineages and clarifies whether such lineages conform to current taxonomic nomenclature based on morphological study.…”

Geography, environment, and colonization history interact with morph type to shape genomic variation in an Arctic fish

“…Additionally, our results suggest the propensity for genetic drift in landlocked and freshwater resident populations (DeWoody & Avise, 2000; Gyllensten, 1985) as previously observed in Atlantic Salmon ( Salmo salar , Tonteri et al, 2007), Alewife ( Alosa pseudoharengus , Palkovacs et al, 2008) and Galaxias maculatus (Delgado et al, 2019, 2020, 2023). Such landlocked populations are therefore analogous to island populations (Frankham, 1997) that demonstrate similar reductions in connectivity and increased genetic distinctiveness compared to mainland populations (e.g., von Takach et al, 2022; Wiens et al, 2022).…”

Movement ecology of an endangered mesopredator in a mining landscape

“…This is supported by the fact that we were only able to collar one female northern quoll here. In highly fragmented landscapes—like mining habitats—northern quolls are often less abundant [ 148 ], and vast areas of non-rocky habitat can reduce genetic connectivity in the species [ 69 , 149 , 150 ]. To persist in fragmented landscapes like this, it often requires increased long-distance dispersal [ 29 ], which may be exacerbated in mining landscapes where naturally-fragmented habitats are broken up further.…”