This may be the author’s version of a work that was submitted/accepted for publication in the following source: Mutton, Thomas, Fuller, Susan, Tucker, David,& Baker, Andrew (2018) Discovered and disappearing? Conservation genetics of a recently named Australian carnivorous marsupial. Ecology and Evolution, 8(18), pp. 9413-9425. This file was downloaded from: https://eprints.qut.edu.au/123092/ c Consult author(s) regarding copyright matters This work is covered by copyright. Unless the document is being made available under a Creative Commons Licence, you must assume that re-use is limited to personal use and that permission from the copyright owner must be obtained for all other uses. If the docu- ment is available under a Creative Commons License (or other specified license) then refer to the Licence for details of permitted re-use. It is a condition of access that users recog- nise and abide by the legal requirements associated with these rights. If you believe that this work infringes copyright please provide details by email to [email protected] License: Creative Commons: Attribution 2.5 Notice: Please note that this document may not be the Version of Record (i.e. published version) of the work. Author manuscript versions (as Sub- mitted for peer review or as Accepted for publication after peer review) can be identified by an absence of publisher branding and/or typeset appear- ance. If there is any doubt, please refer to the published source. https://doi.org/10.1002/ece3.4376 Received: 6 October 2017 | Revised: 14 March 2018 | Accepted: 15 March 2018 DOI: 10.1002/ece3.4376 ORIGINAL RESEARCH Discovered and disappearing? Conservation genetics of a recently named Australian carnivorous marsupial Thomas Y. Mutton1 | Susan J. Fuller1 | David Tucker1 | Andrew M. Baker1,2 1School of Earth, Environmental and Biological Sciences, Science and Engineering Abstract Faculty, Queensland University of Five new species within the Australian carnivorous marsupial genus Antechinus have Technology, Brisbane, QLD, Australia recently been named, at least two of which are threatened. Important facets of the 2Natural Environments Program, South Brisbane, QLD, Australia habitat use and extinction risk of one of these new species, the buff- footed antechi- nus, A. mysticus, are not well understood. Previous research has suggested that the Correspondence Thomas Y. Mutton, School of Earth, species utilizes a broad range of inter- connected forest habitats in southeast Environmental and Biological Sciences, Queensland (Qld), Australia. Based on this potentially connected habitat, we pre- Science and Engineering Faculty, Queensland University of Technology, 2 dicted that A. mysticus should have low population genetic structure, particularly in George Street, Brisbane, QLD, Australia. relation to its congener, the spatially restricted, high altitude, closed- forest A. sub- Email: [email protected] tropicus. We genotyped nine microsatellite loci for six populations of A. mysticus, Funding information sampled throughout their known range in eastern Australia, and compared them with ABRS BushBlitz Capacity Building; Australian Postgraduate Award Scholarship four proximate populations of A. subtropicus. Surprisingly, genetic structuring among Awarded southeast Qld populations of A. mysticus was moderate to high and similar to that between A. subtropicus populations. We postulate that all A. mysticus populations have declined recently (<100 generations), particularly the northernmost southeast Qld population, which may be at risk of extinction. Our results suggest that A. mysti- cus is limited to a more scattered and fragmented distribution than previously thought and may be in decline. The identification of population decline in this study and re- cently in other Antechinus suggests the extinction risk of many Australian mammals should be reassessed. KEYWORDS Antechinus mysticus, Antechinus subtropicus, connectivity, conservation, dasyurid, population genetics 1 | INTRODUCTION similar range, a comparative analysis of population genetics allows the formulation and testing of assumptions about differential hab- Differences in population genetic patterns between species with itat use, past connectivity, and biogeography (Avise, 2000; Manel, similar ranges and life histories can reveal previously overlooked Schwartz, Luikart, & Taberlet, 2003). Understanding these patterns facets of a species’ ecology or biogeography. The range and histor- is integral to effective conservation management of a species, as are ical connectivity of a species are often assumed on the basis of the the estimates of genetic diversity such studies provide. habitat types in which they have been found. In closely related spe- Antechinus are one of only a few mammal genera worldwide cies, which are believed to occupy largely separate habitats across a which exhibit semelparous reproduction and, as a consequence, This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Ecology and Evolution. 2018;8:9413–9425. www.ecolevol.org | 9413 9414 | MUTTON ET AL. have been widely studied as a model in breeding biology (Naylor, diversity in southeast Qld, comprising just two haplotypes, only Richardson, & Mcallan, 2008). Such interest has also encouraged a one base pair different (0.2%), across its range (Baker et al., 2012; number of genetic studies on Antechinus, with a principal focus on Mutton, 2017). In contrast, A. subtropicus showed four times as much deeper level systematics (Mitchell et al., 2014; Westerman et al., genetic divergence (0.8%) over only half the geographic distance 2015), taxonomy (Baker, Mutton, Mason, & Gray, 2015; Van Dyck, (75 km; Mutton, 2017) and greater divergence in Cytb has been re- 2002) and a range of single population studies mainly focusing on corded within antechinus populations and across similar geographic habitat use (Banks et al., 2005; Kraaijeveld- Smit, Lindenmayer, distances in a number of species (Beckman, Banks, Sunnucks, Lill, & Taylor, Macgregor, & Wertheim, 2007; Lada, Thomson, Mac Nally, & Taylor, 2007; Mutton, 2017). The two species, which are not closely Taylor, 2008). However, genetic studies of the genus have generally related within the genus, show a deep interspecies divergence not been undertaken across a species’ total geographic range. Such (13.3%–14.3% at Cytb - Baker et al. (2012)). The differing habitat a comprehensive evaluation may provide invaluable information on preference of these species also appears to hold in known areas of the life history, habitat use, and extinction risk of a species. Recently, sympatry. The two species can co- occur at mid- altitude (~250 m) and five new Antechinus species have been named based on combined transitional environments/ecotones where open forest and closed, phylogenetic, morphology and breeding biology data, and at least vine forest, and rainforest communities merge, but each occur in the two of these are at risk of extinction (Baker, Mutton, & Hines, 2013; absence of congeners in higher altitude rainforest (A. subtropicus) Baker, Mutton, Hines, & Van Dyck, 2014; Baker, Mutton, & Van Dyck, and lower altitude open forest (A. mysticus) of southeast Qld (Baker 2012; Baker et al., 2015). Currently, little is known about the ecology et al., 2012; Mutton et al., 2017). or population genetics of these five species. Consequently, there is a To test the hypothesis of greater population connectivity in vital need for fine- scale, yet geographically detailed molecular stud- A. mysticus than A. subtropicus, we sampled the majority of known ies on the suite of newly discovered species. Understanding species’ populations of A. mysticus and representative populations through- ranges, population structure, demography, and habitat preference out the range of A. subtropicus. We compared the species’ popula- is crucial for effective conservation and is particularly important in tion structures using nine microsatellite loci and examined levels of Australia where mammals have suffered an extremely high rate of genetic diversity within and between populations, which is essential extinction in the last 200 years (Woinarski, Burbidge, & Harrison, for effective conservation management. Microsatellites evolve more 2015). rapidly than mitochondrial markers, allowing more recent divergence The buff- footed antechinus, A. mysticus, was discovered in 2012 and finer scale genetic structuring to be revealed. Mitochondrial (Baker et al., 2012). Antechinus mysticus and its congener, the sub- genes can also be biased by sex- specific dispersal patterns, as they tropical antechinus, A. subtropicus, share a similar range in southeast are maternally inherited. In contrast, microsatellites are inherited Queensland (Qld) but occupy largely separate habitats (Baker et al., from both parents and population size and stochastic factors can 2012; Mutton, Gray, Fuller, & Baker, 2017; Pearce, 2016). Antechinus have a significant influence on genetic estimates (Selkoe & Toonen, subtropicus inhabits high altitude subtropical vine forest and rain- 2006). These attributes make microsatellites an ideal marker to test forest patches scattered throughout the protected habitats of near the ideas posed in this study. coastal southeast Qld (Baker et al., 2012; Van Dyck, Gynther, & Baker, 2013). Antechinus mysticus