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Urban development explains reduced genetic diversity in a narrow range endemic freshwater fish

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Abstract

Whereas the negative impact of human caused habitat degradation on community species richness is well established, less is known about its effect on within species genetic diversity. Here we investigate how different aspects of habitat degradation affects genetic diversity of an Australian native freshwater fish, Rhadinocentrus ornatus, and what impacts this may have on this species’ conservation status. We perform this investigation for R. ornatus across southeast Queensland. Based on mtDNA sequence data from 327 individuals and 20 populations, we identified three distinct genetic lineages that were allopatric at the stream level. Indicators of habitat degradation have large negative effects on measures of genetic diversity, with close proximity to urban development and alterations to waterways associated with drastically reduced measures of genetic diversity across three distinct mtDNA lineages (evolutionary significant units). Low effective population sizes and low standing genetic variation in degraded habitats may result in reduced adaptive potential in this already threatened narrow range endemic. The only surveyed populations with high genetic diversity are found in protected National Parks. Many historical populations of R. ornatus in the highly developed Greater Brisbane Region are already probably extinct, and without further study and management this may be the fate of presently genetically depauperate populations in urban areas.

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References

  • Aljanabi S, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR- based techniques. Nucl Acids Res 25:4692–4693

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell Pub, Malden

    Google Scholar 

  • Arthington AH, Marshall CJ (1995) Threatened fishes of the world Pseudomugil mellis Allen & Ivantsoff, 1982 (Pseudomugilidae). Environ Biol Fishes 43:268

    Article  Google Scholar 

  • Arthington AH, Marshall CJ (1996) Threatened fishes of the world Nannoperca oxleyana Whitley, 1940 (Nannopercidae). Environ Biol Fishes 46:150

    Article  Google Scholar 

  • Arthington AH, Marshall CJ (1999) Diet of the exotic mosquitofish, Gambusia holbrooki, in an Australian lake and potential for competition with indigenous fish species. Asian Fish Sci 12:1–16

    Google Scholar 

  • Arthington AH, Milton DA, McKay RJ (1983) Effects of urban development and habitat alterations on the distribution and abundance of native and exotic freshwater fish in the Brisbane region, Queensland. Aust J Ecol 8:87–101

    Article  Google Scholar 

  • Arthington AH, Chandica AL, Marshall CJ (1994) Geographical information systems and distribution maps for the Honey blue-eye, Pseudomugil mellis and other freshwater fishes in South-eastern Queensland, pp. in Final report to the Australian Nature Conservation Agency Endangered Species Program Centre for Catchment and In-stream Research, Griffith University: Nathan, Australia

  • Atton FM (1959) The invasion of Manitoba and Saskatchewan by carp. Trans Am Fish Soc 88:203–205

    Article  Google Scholar 

  • Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific Phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522

    Google Scholar 

  • Bermingham E, McCafferty SS, Martin AP (1997) Fish biogeography and molecular clocks: perspectives from the Panamanian Isthmus. Mol Syst Fishes: 113–128

  • Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT, Moritz C (2009) Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science 323:785–789

    Article  CAS  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Cucherousset J, Olden JD (2011) Ecological impacts of nonnative freshwater fishes. Fisheries 36:215–230

    Article  Google Scholar 

  • Dinnage R (2009) Disturbance alters the phylogenetic composition and structure of plant communities in an old field system. Plos One 4:e7071

    Article  PubMed Central  PubMed  Google Scholar 

  • Evanno G, Castella E, Antoine C, Paillat G, Goudet J (2009) Parallel changes in genetic diversity and species diversity following a natural disturbance. Mol Ecol 18:1137–1144

    Article  PubMed  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed Central  CAS  PubMed  Google Scholar 

  • Finn DS, Bogan MT, Lytle DA (2009) Demographic Stability Metrics for Conservation Prioritization of Isolated Populations. Conserv Biol 23:1185–1194

    Article  PubMed  Google Scholar 

  • Fox J, Weisberg S, Hong J, Andersen R, Firth D et al. (2012) Package for the R software: effect displays for linear, generalized linear, multinomial-logit, proportional-odds logit models and mixed-effects models. www.r-project.org. http://www.r-project.org, http://socserv.socsci.mcmaster.ca/jfox

  • Fu Y (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed Central  CAS  PubMed  Google Scholar 

  • Helm A, Oja T, Saar L, Takkis K, Talve T et al (2009) Human influence lowers plant genetic diversity in communities with extinction debt. J Ecol 97:1329–1336

    Article  Google Scholar 

  • Helmus MR, Keller WB, Paterson MJ, Yan ND, Cannon CH et al (2010) Communities contain closely related species during ecosystem disturbance. Ecol Lett 13:162–174

    Article  PubMed  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913

    Article  CAS  PubMed  Google Scholar 

  • Howe E, Howe C, Lim R, Burchett M (1997) Impact of the introduced poeciliid Gambusia holbrooki (Girard, 1859) on the growth and reproduction of Pseudomugil signifer (Kner, 1865) in Australia. Mar Freshw Res 48:425–434

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Huey JA, Espinoza T, Hughes JM (2013) Natural and anthropogenic drivers of genetic structure and low genetic variation in the endangered freshwater cod, Maccullochella mariensis. Conserv Genet 14(5):997–1008

    Article  Google Scholar 

  • Hughes J, Ponniah M, Hurwood DA, Chenoweth SF, Arthington AH (1999) Strong genetic structuring in a habitat specialist, the Oxleyan Pygmy Perch Nannoperca oxleyana. Heredity 83:5–14

    Article  PubMed  Google Scholar 

  • Ivantsoff W (1999) Detection of predation on Australian native fishes by Gambusia holbrooki. Mar Freshw Res 50:467–468

    Article  Google Scholar 

  • Kellermann V, van Heerwaarden B, Sgro CM, Hoffmann AA (2009) Fundamental evolutionary limits in ecological traits drive drosophila species distributions. Science 325:1244–1246

    Article  CAS  PubMed  Google Scholar 

  • Knapp S, Kühn I, Schweiger O, Klotz S (2008) Challenging urban species diversity: contrasting phylogenetic patterns across plant functional groups in Germany. Ecol Lett 11:1054–1064

    Article  PubMed  Google Scholar 

  • Koehn JD (2004) Carp (Cyprinus carpio) as a powerful invader in Australian waterways. Freshw Biol 49:882–894

    Article  Google Scholar 

  • Krueger CC, May B (1991) Ecological and genetic effects of salmonid introductions in North America. Can J Fish Aquat Sci 48:66–77

    Article  Google Scholar 

  • Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species: a selection from the global invasive species database. Invasive Species Specialist Group Auckland, Auckland

    Google Scholar 

  • Mabuchi K, Senou H, Nishida M (2008) Mitochondrial DNA analysis reveals cryptic large-scale invasion of non-native genotypes of common carp (Cyprinus carpio) in Japan. Mol Ecol 17:796–809

    Article  CAS  PubMed  Google Scholar 

  • Marshall J (1988) An extension of the known range of Rhadinocentrus ornatus. Fishes Sahul 5:196–197

    Google Scholar 

  • Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375

    Article  CAS  PubMed  Google Scholar 

  • Page TJ, Hughes JM (2014) Contrasting insights provided by single and multi-species data in a regional comparative phylogeographic study. Biol J Linn Soc 111:554–569

    Article  Google Scholar 

  • Page TJ, Sharma S, Hughes JM (2004) Deep phylogenetic structure has conservation implications for ornate rainbowfish (Melanotaeniidae : Rhadinocentrus ornatus) in Queensland, eastern Australia. Mar Freshw Res 55:165–172

    Article  Google Scholar 

  • Pinto L, Chandrasena N, Pera J, Hawkins P, Eccles D et al (2005) Managing invasive carp (Cyprinus carpio) for habitat enhancement at Botany Wetlands, Australia. Aquat Conserv: Mar Freshw Ecosyst 15:447–462

    Article  Google Scholar 

  • R Development Core Team (2010) R: A language and environment for statistical computing, pp. R Foundation for Statistical Computing

  • Rambaut A, Drummond AJ (2012) FigTree version 1.4, available at: tree.bio.ed.ac.uk/software/figtree

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Sharma S, Hughes JM (2011) Genetic structure and phylogeography of two freshwater fishes, Rhadinocentrus ornatus and Hypseleotris compressa, in southern Queensland, Australia, inferred from allozymes and mitochondrial DNA. J Fish Biol 78:57–77

    Article  CAS  PubMed  Google Scholar 

  • Simon KS, Townsend CR (2003) Impacts of freshwater invaders at different levels of ecological organisation, with emphasis on salmonids and ecosystem consequences. Freshw Biol 48:982–994

    Article  Google Scholar 

  • Struebig MJ, Kingston T, Petit EJ, Le Comber SC, Zubaid A et al (2011) Parallel declines in species and genetic diversity in tropical forest fragments. Ecol Lett 14:582–590

    Article  PubMed  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Tappin AR (2010) Rainbowfishes: they care & keeping in captivity. Art Publications, Australia

    Google Scholar 

  • Torgersen T, Jones MR, Stephens AW, Searle DE, Ullman WJ (1985) Late quaternary hydrological changes in the Gulf of Carpentaria. Nature 313:785–787

    Article  Google Scholar 

  • Unmack PJ (2001) Biogeography of Australian freshwater fishes. J Biogeogr 28:1053–1089

    Article  Google Scholar 

  • Vellend M (2004) Parallel effects of land-use history on species diversity and genetic diversity of forest herbs. Ecology 85:3043–3055

    Article  Google Scholar 

  • Vigliano PH, Alonso MF, Aquaculture M (2007) Salmonid introductions in patagonia: a mixed blessing. In: Bert T (ed) Ecological and genetic implications of aquaculture activities. Springer, Dordretch, pp 315–331

    Chapter  Google Scholar 

  • Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167

    Article  Google Scholar 

  • Wei X, Jiang M (2012) Contrasting relationships between species diversity and genetic diversity in natural and disturbed forest tree communities. New Phytol 193:779–786

    Article  PubMed  Google Scholar 

  • Willmott WF (2004) Giant Sandcastles: Parks of the coastal sand masses, Geological Society of Australia Inc., Queensland Division, pp 139–148

  • Zambrano L, Martínez-Meyer E, Menezes N, Peterson AT (2006) Invasive potential of common carp (Cyprinus carpio) and Nile tilapia (Oreochromis niloticus) in American freshwater systems. Can J Fish Aquat Sci 63:1903–1910

    Article  Google Scholar 

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Acknowledgments

We would like to thank L. Evans, P. Waldie, T. Richards, C. Byewater, J. Hereward and G. David for assistance in sample collection, and T. Page for providing samples. Our thanks to two anonymous reviewers for suggesting improvements to this manuscript. Fish were collected under permit number WITK06370609 (Queensland EcoAccess) and 95992 (Queensland Fisheries). All work complies with University of Queensland annual ethics standards (permit number SIB/936/08).

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  1. School of Biological Sciences, The University of Queensland, St Lucia, 4072, Australia

    Andrew Mather, Daniel Hancox & Cynthia Riginos

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  1. Andrew Mather
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  3. Cynthia Riginos
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Correspondence to Andrew Mather.

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Mather, A., Hancox, D. & Riginos, C. Urban development explains reduced genetic diversity in a narrow range endemic freshwater fish. Conserv Genet 16, 625–634 (2015). https://doi.org/10.1007/s10592-014-0688-7

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