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Rainfall and topography predict gene flow among populations of the declining northern quoll (Dasyurus hallucatus)

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Abstract

Landscape attributes often shape the spatial genetic structure of species. As the maintenance of genetic connectivity is increasingly a conservation priority, the identification of landscape features that influence connectivity can inform targeted management strategies. The northern quoll (Dasyurus hallucatus) is a carnivorous marsupial that has experienced dramatic population declines in recent decades. To inform management of surviving D. hallucatus populations across north-western Australia we examined the genetic structure of populations, and identified landscape features that influence gene flow within the Kimberley region. We sampled 249 individuals from 28 populations in three regions of north-western Australia, including the Kimberley, Pilbara and Kakadu. Genetic structuring was evident between the three regions and to a lesser extent between the north and central Kimberley. Landscape genetic analysis of Kimberley populations suggest this structuring may be due in part to the indirect effects of differences in rainfall between these two areas. Also, D. hallucatus populations with large areas of open habitat between them tended to be more genetically similar. Managing threats such as the occurrence of intense and frequent fires, and the density of introduced herbivores, could support the persistence of D. hallucatus populations, particularly in areas with high rainfall and flat terrain, where greater genetic connectivity confers a better chance of long-term population survival.

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References

  • Adamack AT, Gruber B (2014) PopGenReport: simplifying basic population genetic analyses in R. Methods Ecol Evol 5:384–387

    Article  Google Scholar 

  • Andersen AN et al (1998) Fire research for conservation management in tropical savannas: introducing the Kapalga fire experiment. Aust J Ecol 23:95–110. doi:10.1111/j.1442-9993.1998.tb00708.x

    Article  Google Scholar 

  • Archer M (1979) The status of Australian Dasyurids, Thylacinids and Myrmecobids. In: Tyler MJ (ed) The status of endangered Australasian wildlife. Royal Zoological Society of South Australia, Adelaide

    Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4, R package version 1.1-7

  • Beirnacki C, Celeux G, Golaert G, Langrognet F (2006) Model-based cluster and discriminant analysis with the MIXMOD software. J Comput Stat Data Anal 51:587–600

    Article  Google Scholar 

  • Blair C, Arcos VHJ, de la Cruz FRM, Murphy RW (2013) Landscape genetics of leaf-toed geckos in the tropical dry forest of Northern Mexico. PLoS one 8:e57433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradley A, Kemper C, Kitchener D, Humphreys W, How R (1987) Small mammals of the Mitchell Plateau region, Kimberley, Western Australia. Wildl Res 14:397–413. doi:10.1071/WR9870397

    Article  Google Scholar 

  • Braithwaite R, Griffiths A (1994) Demographic variation and range contraction in the northern quoll, Dasyurus hallucatus (Marsupialia: Dasyuridae). Wildl Res 21:203–217. doi:10.1071/WR9940203

    Article  Google Scholar 

  • Braunisch V, Segelbacher G, Hirzel AH (2010) Modelling functional landscape connectivity from genetic population structure: a new spatially explicit approach. Mol Ecol 19:3664–3678

    Article  PubMed  Google Scholar 

  • Bureau of Meteorology (2015) Climate data online. Commonwealth of Australia, Bureau of Meteorology. http://www.bom.gov.au/climate/data/?ref=ftr. Accessed 1 March 2014

  • Carwardine J, O’Connor T, Legge S, Mackey B, Possingham HP, Martin TG (2011) Priority threat management to protect Kimberley wildlife. CSIRO Ecosystem Sciences, Brisbane

    Google Scholar 

  • Cook AC (2010) Habitat use and home range of the northern quoll, Dasyurus hallucatus: effects of fire. The University of Western Australia

  • Danley PD, DeCarvalho TN, Fergus DJ, Shaw KL (2007) Reproductive asynchrony and the divergence of hawaiian crickets. Ethology 113:1125–1132. doi:10.1111/j.1439-0310.2007.01430.x

    Article  Google Scholar 

  • Darriba D, Taboada GI, Doallo R, Posada D (2012) jModelTest2: more models, newheuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dlugosch K, Parker I (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    Article  CAS  PubMed  Google Scholar 

  • Dudaniec RY, Wilmer JW, Hanson JO, Warren M, Bell S, Rhodes JR (2016) Dealing with uncertainty in landscape genetic resistance models: a case of three co-occurring marsupials. Mol Ecol 25:470–486

    Article  PubMed  Google Scholar 

  • Earl D, vonHoldt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Res 4:359–361

    Article  Google Scholar 

  • Edwards LJ, Muller KE, Wolfinger RD, Qaqish BF, Schabenberger O (2008) An R statistic for fixed effects in the linear mixed model. Stat Med 27:6137–6157

    Article  PubMed  PubMed Central  Google Scholar 

  • EPBC (1999) Dasyurus hallucatus ed. 2007 Deparment of the Environment and Water Resources. Australian Government, Canberra

  • Epps CW, Wehausen JD, Bleich VC, Torres SG, Brashares JS (2007) Optimizing dispersal and corridor models using landscape genetics. J Appl Ecol 44:714–724

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study Molecular. Evolution 14:2611–2620

    CAS  Google Scholar 

  • Fisher R, Vigilante T, Yates C, Russell-Smith J (2003) Patterns of landscape fire and predicted vegetation response in the north Kimberley region of Western Australia. Int J Wildland Fire 12:369–379. doi:10.1071/wf03021

    Article  Google Scholar 

  • Fisher DO et al (2014) The current decline of tropical marsupials in Australia: is history repeating? Glob Ecol Biogeogr 23:181–190. doi:10.1111/geb.12088

    Article  Google Scholar 

  • Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993

    Article  PubMed  PubMed Central  Google Scholar 

  • Frank ASK et al (2014) Experimental evidence that feral cats cause local extirpation of small mammals in Australia’s tropical savannas. J Appl Ecol 51:1486–1493. doi:10.1111/1365-2664.12323

    Article  Google Scholar 

  • Frankham R (1995a) Conservation genetics. Annu Rev Genet 29:305–327

    Article  CAS  PubMed  Google Scholar 

  • Frankham R (1995b) Inbreeding and extinction: a threshold effect. Conserv Biol 9:792–799

    Article  Google Scholar 

  • Funk WC, Blouin MS, Corn PS, Maxell BA, Pilliod DS, Amish S, Allendorf FW (2005) Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Mol Ecol 14:483–496

    Article  CAS  PubMed  Google Scholar 

  • Garrick R, Nason J, Meadows C, Dyer R (2009) Not just vicariance: phylogeography of a Sonoran Desert euphorb indicates a major role of range expansion along the Baja Peninsula. Mol Ecol 18:1916–1931

    Article  CAS  PubMed  Google Scholar 

  • Geosciences Australia (2014) Data and Publications. http://www.ga.gov.au/data-pubs

  • Geosciences Australia (2015) GEODATA 9 Second DEM and D8 Flow Direction Grid 2008 Version 3.0. Commonwealth of Australia. http://www.ga.gov.au

  • Giordano AR, Ridenhour BJ, Storfer A (2007) The influence of altitude and topography on genetic structure in the long-toed salamander (Ambystoma macrodactulym). Mol Ecol 16:1625–1637. doi:10.1111/j.1365-294X.2006.03223.x

    Article  CAS  PubMed  Google Scholar 

  • Gittleman JL, Funk SM, Macdonald DW, Wayne RK (2001) Carnivore conservation. Cambridge University Press, Cambridge

    Google Scholar 

  • Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Article  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate mothod to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Halekoh U, Højsgaard S (2014) A Kenward-Roger approximation and parametric bootstrap methods for tests of linear mixed models—the R package pbkrtest. J Stat Softw 59:1–30

    Article  Google Scholar 

  • Hill B, Ward S (2008) National recovery plan for the northern quoll Dasyurus hallucatus. Australian government deparment of the Environment and Water Resources, Canberra

    Google Scholar 

  • How RA, Dell J, Cooper NK (1991) Vertebrate fauna of the Abydos-Woodstock Reserve, northeast Pilbara. Rec West Aust Mus 37:78–125

    Google Scholar 

  • How RA, Spencer PBS, Schmitt LH (2009) Island populations have high conservation value for northern Australia’s top marsupial predator ahead of a threatening process. J Zool 278:206–217

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914. doi:10.2307/2640449

    Article  Google Scholar 

  • Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. doi:10.1093/bioinformatics/btn129

    Article  CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Dufour A, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101:92–103

    Article  CAS  PubMed  Google Scholar 

  • Jost L (2008) Gst and its relatives do not measure differentiation Mol Ecol 17:4015–4026. doi:10.1111/j.1365-294X.2008.03887.x

    Google Scholar 

  • Kitchener DJ (1978) Mammals of the Ord River area, Kimberley, Western Australia. Rec West Aust Mus 6:192–219

    Google Scholar 

  • Kitchener DJ, Keller LE, Chapman A, McKenzie NL, Start AN, Kenneally KF (1981) Observations of mammals of the Mitchell Plateau and Admiralty Gulf, Western Australia, vol 4. Western Australian Museam, Perth

    Google Scholar 

  • Lamont BB, He T, Enright NJ, Krauss SL, Miller BP (2003) Anthropogenic disturbance promotes hybridization between Banksia species by altering their biology. J Evol Biol 16:551–557. doi:10.1046/j.1420-9101.2003.00548.x

    Article  CAS  PubMed  Google Scholar 

  • Landguth EL, Cushman SA, Murphy MA, Luikart G (2010) Relationships between migration rates and landscape resistance assessed using individual-based simulations. Mol Ecol Res 10:854–862. doi:10.1111/j.1755-0998.2010.02867.x

    Article  CAS  Google Scholar 

  • Leahy L, Legge SM, Tuft K, McGregor H, Barmuta L, Jones M, Johnson CN (2016) Amplified predation after fire suppresses rodent populations in Australia’s tropical savannas. Wildl Res 42:705–716

    Article  Google Scholar 

  • Legendre P (2014) lmodel2: Model II regression. https://cran.r-project.org/web/packages/lmodel2/index.html

  • Legge S, Kennedy MS, Lloyd R, Murphy SA, Fisher A (2011a) Rapid recovery of mammal fauna in the central Kimberley, northern Australia, following the removal of introduced herbivores. Aust Ecol 36:791–799. doi:10.1111/j.1442-9993.2010.02218.x

    Article  Google Scholar 

  • Legge S, Murphy SA, Kingswood R, Maher B, Swan D (2011b) EcoFire: restoring the biodiversity values of the Kimberley region by managing fire. Ecol Manag Restor 12:84–92

    Article  Google Scholar 

  • Litvaitis JA et al (2015) Bobcats (Lynx rufus) as a model organism to investigate the effects of roads on wide-ranging carnivores. Environ Manag 55:1366–1376. doi:10.1007/s00267-015-0468-2

    Article  Google Scholar 

  • McKenzie NL (1981) Mammals of the Phanerozoic south-west Kimberley, Western Australia: biogeography and recent changes. J Biogeogr 8:263–270

    Article  Google Scholar 

  • McKenzie NL et al (2007) Analysis of factors implicated in the recent decline of Australia’s mammal fauna. J Biogeogr 34:597–611. doi:10.1111/j.1365-2699.2006.01639.x

    Article  Google Scholar 

  • McRae BH, Dickson BG, Keitt TH, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution and conservation. Ecology 89:2712–2724

    Article  PubMed  Google Scholar 

  • Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures. Mol Ecol Resour 11:5–18

    Article  PubMed  Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • Moran PAP (1948) The interpretation of statistical maps. J R Stat Soc B 10:243–251

    Google Scholar 

  • Moritz C (1994) Defining evolutionarily significant units for conservation. Trends Ecol Evol 9:373–375. doi:10.1016/0169-5347(94)90057-4

    Article  CAS  PubMed  Google Scholar 

  • Narum S (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787. doi:10.1007/s10592-005-9056-y

    Article  CAS  Google Scholar 

  • Neel MC (2008) Patch connectivity and genetic diversity conservation in the federally endangered and narrowly endemic plant species Astragalus albens (Fabaceae). Biol Conserv 141:938–955

    Article  Google Scholar 

  • Oakwood M (2000) Reproduction and deomgraphy of the northern quoll, Dasyurus hallucatus, in the lowland savanna of northern Australia Australian. J Zool 48:519–539

    Google Scholar 

  • Oakwood M (2002) Spatial and social organization of a carnivorous marsupial Dasyurus hallucatus (Marsupialia: Dasyuridae). J Zool 257:237–248. doi:10.1017/s0952836902000833

    Article  Google Scholar 

  • O’Donnell S, Webb JK, Shine R (2010) Conditioned taste aversion enhances the survival of an endangered predator imperilled by a toxic invader. J Appl Ecol 47:558–565. doi:10.1111/j.1365-2664.2010.01802.x

    Article  Google Scholar 

  • Pérez-Espona S, Pérez-Barbería F, McLeod J, Jiggins C, Gordon I, Pemberton J (2008) Landscape features affect gene flow of Scottish Highland red deer (Cervus elaphus). Mol Ecol 17:981–996

    Article  PubMed  Google Scholar 

  • Phillips BL, Chipperfield JD, Kearney MR (2008) The toad ahead: challenges of modelling the range and spread of an invasive species. Wildl Res 35:222–234. doi:10.1071/WR07101

    Article  Google Scholar 

  • Pritchard J, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Article  Google Scholar 

  • R Development Core Team (2005) R (version 3.03). R Foundation for Statistical Computing, Vienna, Austria

  • Radford IJ et al (2014) Mammals of Australia’s tropical savannas: a conceptual model of assemblage structure and regulatory factors in the Kimberley region. PLoS One 9:e92341

    Article  PubMed  PubMed Central  Google Scholar 

  • Rambaut A (2007a) Fig tree. http://tree.bio.ed.ac.uk/software/figtree/

  • Rambaut A, Suchard MM, Xile D, Drummond AJ (2007b) Tracer v1.5. http://tree.bio.ed.ac.uk/software/tracer/

  • Rankmore BR, Griffiths AD, Woinarski JCZ, Ganambarr BL, Taylor R, Firestone K, Cardoso M (2008) Island traslocation of the northern quoll Dasyurus hallucatus as a conservation response to the spread of the cane toad Chaunus (Bufo) marinus in the Northern Territory, Australia

  • Raymond M, Rousset F (1995) Genepop (Version-1.2)—population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Riley SJ, DeGloria SD, Elliot R (1999) A terrain ruggedness index that qualifies topographic heterogeneity. Intermt J Sci 1999:23–27

    Google Scholar 

  • Schwalm D, Waits L, Ballard W (2014) Little fox on the prairie: genetic structure and diversity throughout the distribution of a grassland carnivore in the United States. Conserv Genet 15:1503–1514. doi:10.1007/s10592-014-0634-8

    Article  Google Scholar 

  • Sergio F et al (2008) Top predators as conservation tools: ecological rationale, assumptions, and efficacy. Annu Rev Ecol Evol Syst 39:1–19. doi:10.2307/30245151

    Article  Google Scholar 

  • Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analysis. Can J Zool 69:82–90

    Article  CAS  Google Scholar 

  • Simcharoen S, Barlow ACD, Simcharoen A, Smith JLD (2008) Home range size and daytime habitat selection of leopards in Huai Kha Khaeng Wildlife Sanctuary, Thailand. Biol Conserv 141:2242–2250. doi:10.1016/j.biocon.2008.06.015

    Article  Google Scholar 

  • Smith AL, Friesen VL (2007) Differentiation of sympatric populations of the band-rumped storm-petrel in the Galapagos Islands: an examination of genetics, morphology, and vocalizations. Mol Ecol 16:1593–1603. doi:10.1111/j.1365-294X.2006.03154.x

    Article  CAS  PubMed  Google Scholar 

  • Spencer PBS, Cardoso M, How RA, Williams J, Bunce M, Schmitt LH (2007) Cross-species amplification at microsatellite loci in Australian quolls including the description of five new markers from the Chuditch (Dasyurus geoffroii). Mol Ecol Notes 7:1100–1103. doi:10.1111/j.1471-8286.2007.01791.x

    Article  CAS  Google Scholar 

  • Storfer A et al (2007) Putting the landscape in landscape genetics. Heredity 98:128–142

    Article  CAS  PubMed  Google Scholar 

  • Thomassen HA, Freedman AH, Brown DM, Buermann W, Jacobs DK (2013) Regional differences in seasonal timing of rainfall discriminate between genetically distinct East African giraffe taxa. PLoS ONE 8:e77191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Oosterhout C, Hutchinson B, Wills D, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Van Strien MJ, Keller D, Holderegger R (2012) A new analytical approach to landscape genetic modelling: least cost transect analysis and linear mixed models. Mol Ecol 21:4010–4023

    Article  Google Scholar 

  • Vigilante T (2001) Analysis of explorers’ records of aboriginal landscape burning in the Kimberley region of Western Australia. Aust Geogr Stud 39:135–155. doi:10.1111/1467-8470.00136

    Article  Google Scholar 

  • Vigilante T, Bowman D, Fisher R, Russell-Smith J, Yates C (2004) Contemporary landscape burning patterns in the far north Kimberley region of north-west Australia: human influences and environmental determinants. J Biogeogr 31:1317–1333. doi:10.1111/j.1365-2699.2004.01104.x

    Article  Google Scholar 

  • Wasserman T, Cushman S, Schwartz M, Wallin D (2010) Spatial scaling and multi-model inference in landscape genetics: Martes americana in northern Idaho. Landsc Ecol 25:1601–1612. doi:10.1007/s10980-010-9525-7

    Article  Google Scholar 

  • Wikramanayake E, McKnight M, Dinerstein E, Joshi A, Gurung B, Smith D (2004) Designing a conservation landscape for tigers in human-dominated environments. Conserv Biol 18:839–844. doi:10.2307/3589094

    Article  Google Scholar 

  • Woinarski J, Burbidge A, Harrison P (2014) The action plan for Australian mammals 2012. CSIRO Publishing, Collingwood

    Google Scholar 

  • Woinarski JCZ et al (2011) The disappearing mammal fauna of northern Australia: context, cause, and response. Conserv Lett 4:192–201. doi:10.1111/j.1755-263X.2011.00164.x

    Article  Google Scholar 

  • Woinarski JCZ et al (2008) Surviving the toads: patterns of persistence of the northern quoll Dasyurus hallucatus in Queensland. The Australian Government’s Natural Heritage Trust

  • Woolley PA, Krajewski C, Westerman M (2015) Phylogenetic relationships within Dasyurus (Dasyuromorphia: Dasyuridae): quoll systematics based on molecular evidence and male characteristics. J Mammal 96:37–46

    Article  Google Scholar 

  • Yamamoto S, Beljaev EA, Sota T (2016) Phylogenetic analysis of the winter geometrid genus Inurois reveals repeated reproductive season shifts. Mol Phylogenet Evol 94:47–54. doi:10.1016/j.ympev.2015.08.016

    Article  PubMed  Google Scholar 

  • Ziembicki MR, Woinarski JC, Mackey BG (2013) Evaluating the status of species using indigenous knowledge: novel evidence for major native mammal declines in northern Australia. Biol Conserv 157:78–92

    Article  Google Scholar 

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Acknowledgments

This study was funded by supporters of the Australian Wildlife Conservancy, an Australian Research Council Linkage Grant (100100033), and the Department of Parks and Wildlife (Western Australia). The study methods were approved by the University of Tasmania Animal Ethics Committee (permit number A12516). This project would not have been possible without the support of staff at Australian Wildlife Conservancy’s Mornington Wildlife Sanctuary. Terry Webb also gave tremendous assistance sourcing and processing GIS layers. Also, thankyou to Alex Hartshorne, Hannah Cliff, Jillian Smith, Joel Murray, David James, Peter Richardson, Kaely Kreger, Davina Bright, Tom Crawford and Iris Bleach for their help with fieldwork.

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Hohnen, R., D. Tuft, K., Legge, S. et al. Rainfall and topography predict gene flow among populations of the declining northern quoll (Dasyurus hallucatus). Conserv Genet 17, 1213–1228 (2016). https://doi.org/10.1007/s10592-016-0856-z

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