Catchment-scale conservation units identified for the threatened Yarra pygmy perch (Nannoperca obscura) in highly modified river systems

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Brauer, Chris J ^a   Unmack, Peter J ^b   Hammer, Michael P ^c,d,e   Adams, Mark ^c,e   Beheregaray, Luciano B ^a  

^a FLINDERS UNIVERSITY   (Australia)

^b UNIVERSITY OF CANBERRA   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

^d Museum and Art Gallery of the Northern Territory   (Australia)

^e SOUTH AUSTRALIAN MUSEUM   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MICROSATELLITE DNA;

ANIMAL DISPERSAL; ARTICLE; CATCHMENT; ENDANGERED SPECIES; GENETIC VARIABILITY; HETEROZYGOSITY; NONHUMAN; PERCH; POPULATION MIGRATION; POPULATION STRUCTURE; RIVER; SPECIES CONSERVATION; SPECIES RICHNESS; YARRA PYGMY PERCH; ALLELE; ANIMAL; AUSTRALIA; BIOLOGICAL MODEL; GENETICS; HUMAN;

ALLELES; ANIMALS; AUSTRALIA; ENDANGERED SPECIES; GENETIC VARIATION; HUMANS; MICROSATELLITE REPEATS; MODELS, GENETIC; PERCHES; RIVERS;

EID: 84892644951     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082953     Document Type: Article

References (91)

1. Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Global Ecol Biogeogr 16: 265-280.
2. Lande R (1998) Anthropogenic, ecological and genetic factors in extinction and conservation. Res Popul Ecol 40: 259-269.
3. Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19: 3038-3051.
4. Lande R (1988) Genetics and demography in biological conservation. Science 241: 1455-1460.
5. Frankham R (2005) Genetics and extinction. Biol Conserv 126: 131-140.
6. Hanski I (1998) Metapopulation dynamics. Nature 396: 41-49.
7. Segelbacher G, Cushman S, Epperson B, Fortin M-J, Francois O, et al. (2010) Applications of landscape genetics in conservation biology: concepts and challenges. Conserv Genet 11: 375-385.
8. Frankham R (2010) Where are we in conservation genetics and where do we need to go? Conserv Genet 11: 661-663.
9. Fausch KD, Torgersen CE, Baxter CV, Li HW (2002) Landscapes to riverscapes: bridging the gap between research and conservation of stream fishes. Bioscience 52: 483-498.
10. Palmer MA, Reidy Liermann CA, Nilsson C, Flörke M, Alcamo J, et al. (2008) Climate change and the world's river basins: anticipating management options. Front Ecol Environ 6: 81-89.
11. Hughes JM, Schmidt DJ, Finn DS (2009) Genes in streams: using DNA to understand the movement of freshwater fauna and their riverine habitat. Bioscience 59: 573-583.
12. Cook BD, Kennard MJ, Real K, Pusey BJ, Hughes JM (2011) Landscape genetic analysis of the tropical freshwater fish Mogurnda mogurnda (Eleotridae) in a monsoonal river basin: importance of hydrographic factors and population history. Freshwat Biol 56: 812-827.
13. Faulks LK, Gilligan DM, Beheregaray LB (2011) The role of anthropogenic vs. natural in-stream structures in determining connectivity and genetic diversity in an endangered freshwater fish, Macquarie perch (Macquaria australasica) . Evol Appl 4: 589-601.
14. Huey JA, Baker AM, Hughes JM (2006) Patterns of gene flow in two species of eel-tailed catfish, Neosilurus hyrtlii and Porochilus argenteus (Siluriformes: Plotosidae), in western Queensland's dryland rivers. Biol J Linn Soc 87: 457-467.
15. Cooke GM, Chao NL, Beheregaray LB (2012) Natural selection in the water: freshwater invasion and adaptation by water colour in the Amazonian pufferfish. J Evol Biol 25: 1305-1320.
16. Anderson CD, Epperson BK, Fortin M-J, Holderegger R, James PMA, et al. (2010) Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol 19: 3565-3575.
17. Peakall R, Ruibal M, Lindenmayer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes Evolution 57: 1182-1195.
18. Diniz-Filho JAF, De Campos Telles MP (2002) Spatial autocorrelation analysis and the identification of operational units for conservation in continuous populations. Conserv Biol 16: 924-935.
19. Primmer CR, Veselov AJ, Zubchenko A, Poututkin A, Bakhmet I, et al. (2006) Isolation by distance within a river system: genetic population structuring of Atlantic salmon, Salmo salar, in tributaries of the Varzuga River in northwest Russia. Mol Ecol 15: 653-666.
20. Moritz C (1994) Defining 'Evolutionarily Significant Units' for conservation. Trends Ecol Evol 9: 373-375.
21. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15: 290-295.
22. Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51: 238-254.
23. Unmack PJ (2001) Biogeography of Australian freshwater fishes. J Biogeogr 28: 1053-1089.
24. Murray-Darling Basin Authority (2010) Guide to the proposed basin plan: overview. Murray-Darling Basin Authority, Canberra.
25. Lintermans M (2013) Conservation and management. In: Humphries P, Walker K, editors. Ecology of Australian freshwater fishes. Collingwood, VIC: CSIRO Publishing. pp. 283-316.
26. Kingsford RT, Walker KF, Lester RE, Young WJ, Fairweather PG, et al. (2011) A Ramsar wetland in crisis - the Coorong, Lower Lakes and Murray Mouth, Australia. Mar Freshwat Res 62: 255-265.
27. Hammer M, Bice C, Hall A, Frears A, Watt A, et al. (2013) Freshwater fish conservation in the face of critical water shortages in the southern Murray-Darling Basin, Australia. Mar Freshwat Res 64: 807-821.
28. Stein JL, Stein JA, Nix HA (2002) Spatial analysis of anthropogenic river disturbance at regional and continental scales: identifying the wild rivers of Australia. Landscape Urban Plann 60: 1-25.
29. Taffs KH (2001) The role of surface water drainage in environmental change: a case example of the upper south east of South Australia; an historical review. Aust Geogr Stud 39: 279-301.
30. Saddlier S, Koehn J, Hammer M (2013) Lets not forget the small fishes - conservation of two threatned species of pygmy perch in south-eastern Australia. Mar Freshwat Res 64: 874-886.
31. Kuiter RH, Humphries P, Arthington A (1996) Pygmy perches: Family Nannopercidae. In: McDowall RM, editor. Freshwater Fishes of South-Eastern Australia 2nd Edition. Chatswood, NSW: Reed Books.
32. Hammer M, Unmack P, Adams M, Johnson J, Walker K (2010) Phylogeographic structure in the threatened Yarra pygmy perch Nannoperca obscura (Teleostei: Percichthyidae) has major implications for declining populations. Conserv Genet 11: 213-223.
33. IUCN (2011) International union for conservation of nature red list of threatned species. Available: http://www.iucnredlist.org/details/39301/0. Accessed 2013 Nov 11.
34. Hammer M, Wedderburn S, van Weenen J (2009) Action plan for South Australian freshwater fishes. Native Fish Australia (SA) Inc. Adelaide.
35. Victorian Government Department of Sustainability and Environment (2013) Advisory list of threatned vertebrate fauna in Victoria. Melbourne.
36. Saddlier S, Hammer M (2010) National recovery plan for the Yarra pygmy perch Nannoperca obscura . Department of Sustainability and Environment, Melbourne.
37. Wedderburn S, Hammer M, Bice C (2012) Shifts in small-bodied fish assemblages resulting from drought-induced water level recession in terminating lakes of the Murray-Darling Basin, Australia. Hydrobiologia 691: 35-46.
38. Sunnucks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol 13: 510-524.
39. Carvalho D, Rodriguez-Zarate C, Hammer M, Beheregaray L (2011) Development of 21 microsatellite markers for the threatened Yarra pygmy perch (Nannoperca obscura) through 454 shot-gun pyrosequencing. Conserv Genet Resour 3: 601-604.
40. Beheregaray LB, Möller LM, Schwartz TS, Chao NL, Caccone A (2004) Microsatellite markers for the cardinal tetra Paracheirodon axelrodi, a commercially important fish from central Amazonia. Mol Ecol Notes 4: 330-332.
41. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Microchecker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4: 535-538.
42. Rousset F (2008) genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8: 103-106.
43. 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.
44. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43: 223-225.
45. Kalinowski ST (2005) hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5: 187-189.
46. Peakall R, Smouse P (2012) GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research, an update. Bioinformatics 28: 2537-2539.
47. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
48. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457-462.
49. Excoffier L, Lischer HEL (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.
50. Hardy OJ, Charbonnel N, Freville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163: 1467-1482.
51. Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2: 618-620.
52. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
53. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611-2620.
54. Gilbert KJ, Andrew RL, Bock DG, Franklin MT, Kane NC, et al. (2012) Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program structure. Mol Ecol 21: 4925-4930.
55. Earl D, vonHoldt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4: 359-361.
56. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801-1806.
57. Rosenberg NA (2004) distruct: a program for the graphical display of population structure. Mol Ecol Notes 4: 137-138.
58. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, et al. (2004) GENECLASS2: A software for genetic assignment and first-generation migrant detection. J Hered 95: 536-539.
59. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences 94: 9197-9201.
60. Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82: 561-573.
61. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163: 1177-1191.
62. Rambaut A, Drummond AJ (2009) Tracer v1.5, Available: http://beast.bio.ed.ac.uk/Tracer.Accessed 2013 Nov 11.
63. Meirmans PG (2012) The trouble with isolation by distance. Mol Ecol 21: 2839-2846.
64. Drummond CS, Hamilton MB (2007) Hierarchical components of genetic variation at a species boundary: population structure in two sympatric varieties of Lupinus microcarpus (Leguminosae). Mol Ecol 16: 753-769.
65. Legendre P (1993) Spatial autocorrelation: trouble or new paradigm? Ecology 74: 1659-1673.
66. DeWoody JA, Avise JC (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J Fish Biol 56: 461-473.
67. Faulks LK, Gilligan DM, Beheregaray LB (2010) Islands of water in a sea of dry land: hydrological regime predicts genetic diversity and dispersal in a widespread fish from Australia's arid zone, the golden perch (Macquaria ambigua). Mol Ecol 19: 4723-4737.
68. Coleman RA, Pettigrove V, Raadik TA, Hoffmann AA, Miller AD, et al. (2010) Microsatellite markers and mtDNA data indicate two distinct groups in dwarf galaxias, Galaxiella pusilla (Mack) (Pisces: Galaxiidae), a threatened freshwater fish from south-eastern Australia. Conserv Genet 11: 1911-1928.
69. Cook BD, Bunn SE, Hughes JM (2007) Molecular genetic and stable isotope signatures reveal complementary patterns of population connectivity in the regionally vulnerable southern pygmy perch (Nannoperca australis). Biol Conserv 138: 60-72.
70. Hughes JM, Real KM, Marshall JC, Schmidt DJ (2012) Extreme genetic structure in a small-bodied freshwater fish, the purple spotted gudgeon, Mogurnda adspersa (Eleotridae). PLoS ONE 7: e40546.
71. Huey JA, Baker AM, Hughes JM (2008) The effect of landscape processes upon gene flow and genetic diversity in an Australian freshwater fish, Neosilurus hyrtlii. Freshwat Biol 53: 1393-1408.
72. Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15: 199-203.
73. Unmack PJ, Hammer MP, Adams M, Johnson JB, Dowling TE (2013) The role of continental shelf width in determining freshwater phylogeographic patterns in south-eastern Australian pygmy perches (Teleostei: Percichthyidae). Mol Ecol 22: 1683-1699.
74. Hughes JM, Huey JA, Schmidt DJ (2013) Is realised connectivity among populations of aquatic fauna predictable from potential connectivity? Freshwat Biol 58: 951-966.
75. Luque S, Saura S, Fortin M-J (2012) Landscape connectivity analysis for conservation: insights from combining new methods with ecological and genetic data. Landscape Ecol 27: 153-157.
76. Hughes J, Ponniah M, Hurwood D, Chenoweth S, Arthington A (1999) Strong genetic structuring in a habitat specialist, the Oxleyan Pygmy Perch Nannoperca oxleyana . Heredity 83: 5-14.
77. Unmack PJ, Bagley JC, Adams M, Hammer MP, Johnson JB (2012) Molecular phylogeny and phylogeography of the Australian freshwater fish genus Galaxiella, with an emphasis on dwarf galaxias (G. pusilla) . PLoS ONE 7: e38433.
78. Rourke ML, McPartlan HC, Ingram BA, Taylor AC (2010) Biogeography and life history ameliorate the potentially negative genetic effects of stocking on Murray cod (Maccullochella peelii peelii). Mar Freshwat Res 61: 918-927.
79. Frankham R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv 143: 1919-1927.
80. McGlashan DJ, Hughes JM (2002) Extensive genetic divergence among populations of the Australian freshwater fish, Pseudomugil signifer (Pseudomugilidae), at different hierarchical scales. Mar Freshwat Res 53: 897-907.
81. Meffe GK, Vrijenhoek RC (1988) Conservation genetics in the management of desert fishes. Conserv Biol 2: 157-169.
82. Wear RJ, Eaton A, Tanner JE, Murray-Jones S (2006) The impact of drain discharges on seagrass beds in the south east of South Australia. Final report prepared for the south east natural resource consultative committee and the south east catchment water management board. Adelaide: South Australian Research and Development Institute (Aquatic sciences) and the Department of Environment and Heritage, Coast Protection branch.
83. IPCC (2001) Climate change 2001: working group I: the scientific basis. Contribution of working group I to the third assessment report of the intergovernmental panel on climate change. Eds J. T. Houghton, Y. Ding, D. J. Griggs, M. Noguer, P. J. van der Linden, X. Dai, K. Maskell and C. A. Johnson. Cambridge University Press. Cambridge.
84. Marie AD, Bernatchez L, Garant D (2012) Environmental factors correlate with hybridization in stocked brook charr (Salvelinus fontinalis). Can J Fish Aquat Sci 69: 884-893.
85. Seehausen O, van Alphen JJM, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277: 1808-1811.
86. Heath D, Bettles CM, Roff D (2010) Environmental factors associated with reproductive barrier breakdown in sympatric trout populations on Vancouver Island. Evol Appl 3: 77-90.
87. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11: 697-709.
88. Groce MC, Bailey LL, Fausch KD (2012) Evaluating the success of Arkansas darter translocations in Colorado: an occupancy sampling approach. Trans Am Fish Soc 141: 825-840.
89. Weeks AR, Sgro CM, Young AG, Frankham R, Mitchell NJ, et al. (2011) Assessing the benefits and risks of translocations in changing environments: a genetic perspective. Evol Appl 4: 709-725.
90. Fischer J, Lindenmayer DB (2000) An assessment of the published results of animal relocations. Biol Conserv 96: 1-11.
91. Huff DD, Miller LM, Chizinski CJ, Vondracek B (2011) Mixed-source reintroductions lead to outbreeding depression in second-generation descendents of a native North American fish. Mol Ecol 20: 4246-4258.