Genetic structure and diversity of the black-throated finch (Poephila cincta) across its current range
Lei Stanley Tang A B C E , Carolyn Smith-Keune A B , Anthony C. Grice C , James M. Moloney B and Britta Denise Hardesty DA Molecular Ecology and Evolutionary Laboratory, James Cook University, Townsville, Qld 4811, Australia.
B College of Science and Engineering, James Cook University, Townsville, Qld 4811, Australia.
C CSIRO Land and Water, Townsville, Qld 4811, Australia.
D CSIRO Oceans and Atmosphere Flagship, Hobart, Tas. 7000, Australia.
E Corresponding author. Email: stanley.tang@my.jcu.edu.au
Australian Journal of Zoology 64(6) 375-384 https://doi.org/10.1071/ZO16073
Submitted: 20 October 2016 Accepted: 17 February 2017 Published: 15 March 2017
Abstract
Understanding the patterns of population connectivity and level of genetic diversity can facilitate the identification of both ecologically relevant populations and the spatial scales at which conservation management may need to focus. We quantified genetic variation within and among populations of black-throated finches across their current distribution. To quantify genetic structure and diversity, we genotyped 242 individuals from four populations using 14 polymorphic microsatellite markers and sequenced 25 individuals based on a 302-base-pair segment of mitochondrial control region. We found modest levels of genetic diversity (average allelic richness r = 4.37 ± 0.41 (standard error) and average heterozygosity HO = 0.42 ± 0.040 (standard error)) with no bottleneck signature among sampled populations. We identified two genetic groups that represent populations of two subspecies based on Bayesian clustering analysis and low levels of genetic differentiation based on pairwise genetic differentiation statistics (all FST, RST and Nei’s unbiased D values < 0.1). Our data suggest that genetic exchange occurs among sampled populations despite recent population declines. Conservation efforts that focus on maintaining habitat connectivity and increasing habitat quality to ensure a high level of gene flow on a larger scale will improve the species’ ability to persist in changing landscapes. Conservation management should also support continuous monitoring of the bird to identify any rapid population declines as land-use intensification occurs throughout the species’ range.
Additional keywords: conservation genetics, habitat fragmentation, population structure.
References
Ardern, S., and Lambert, D. (1997). Is the black robin in genetic peril? Molecular Ecology 6, 21–28.| Is the black robin in genetic peril?Crossref | GoogleScholarGoogle Scholar |
Baldwin, M. (1976). Distribution of the black-throated finch. Australian Birds 11, 13–14.
Barrett, J. C., Fry, B., Maller, J., and Daly, M. J. (2005). Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263–265.
| Haploview: analysis and visualization of LD and haplotype maps.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkt1WitQ%3D%3D&md5=e1cac669e8b25dfb8c0de4202f73b7d2CAS |
Black-throated Finch Recovery Team (2007). National recovery plan for the black-throated finch southern subspecies Poephila cincta cincta, report to the Department of the Environment and Water Resources. New South Wales Department of Environment and Climate Change & Queensland Parks and Wildlife Serivce, Canberra.
Caparroz, R., Miyaki, C. Y., and Baker, A. J. (2009). Contrasting phylogeographic patterns in mitochondrial DNA and microsatellites: evidence of female philopatry and male-biased gene flow among regional populations of the blue-and-yellow macaw (Psittaciformes: Ara ararauna) in Brazil. The Auk 126, 359–370.
| Contrasting phylogeographic patterns in mitochondrial DNA and microsatellites: evidence of female philopatry and male-biased gene flow among regional populations of the blue-and-yellow macaw (Psittaciformes: Ara ararauna) in Brazil.Crossref | GoogleScholarGoogle Scholar |
Earl, D. A., and vonHoldt, B. M. (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
| STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |
El Mousadik, A., and Petit, R. J. (1996). High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theoretical and Applied Genetics 92, 832–839.
| High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2c7gs1answ%3D%3D&md5=5f77cecf2fffd2acb81cfb35d537e7e7CAS |
Environment Australia (2000). Revision of the Interim Biogeographic Regionalisation for Australia and development of version 5.1. Environment Australia, Canberra.
Evanno, G., Regnaut, S., and Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
| Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvF2qtrg%3D&md5=ea63a9f32dd3db49f95c38a12f824430CAS |
Excoffier, L., and Lischer, E. L. (2010). Arlequin Suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
| Arlequin Suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar |
Felsenstein, J. (2005). ‘PHYLIP (Phylogeny Inference Package) version 3.6.’ (Department of Genome Sciences, University of Washington: Seattle, WA.)
Forshaw, J., Shephard, M., and Pridham, A. (2012). ‘Grassfinches in Australia.’ (CSIRO Publishing: Melbourne.)
Frankham, R. (2005). Genetics and extinction. Biological Conservation 126, 131–140.
| Genetics and extinction.Crossref | GoogleScholarGoogle Scholar |
Frankham, R. (2010). Inbreeding in the wild really does matter. Heredity 104, 124.
| Inbreeding in the wild really does matter.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c%2FjvFOisg%3D%3D&md5=c7beaa5c71675ee9a47e74e2fe5dead7CAS |
Frankham, R., Briscoe, D. A., and Ballou, J. D. (2002). ‘Introduction to Conservation Genetics.’ (University of Cambridge Press: Cambridge.)
Franklin, D. C., Woinarski, C. Z., and Noske, R. A. (2000). Geographical patterning of species richness among granivorous birds in Australia. Journal of Biogeography 27, 829–842.
| Geographical patterning of species richness among granivorous birds in Australia.Crossref | GoogleScholarGoogle Scholar |
Franklin, D. C., Whitehead, P. J., Pardon, G., Matthews, J., McMahon, P., and McIntyre, D. (2005). Geographic patterns and correlates of the decline of granivorous birds in northern Australia. Wildlife Research 32, 399–408.
| Geographic patterns and correlates of the decline of granivorous birds in northern Australia.Crossref | GoogleScholarGoogle Scholar |
Garnett, S. T., and Crowley, G. M. (2000). ‘The Action Plan for Australian Birds.’ (Environment Australia: Canberra.)
Garza, J. C., and Williamson, E. (2001). Detection of reduction in population size using data from tandemly repeated loci. Molecular Ecology 10, 305–318.
| Detection of reduction in population size using data from tandemly repeated loci.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvgvFSntg%3D%3D&md5=48b144a3f9f713afe4afb740fba5664bCAS |
Gillooly, J. F., Allen, A. P., West, G. B., and Brown, J. H. (2005). The rate of DNA evolution: effects of body size and temperature on the molecular clock. Proceedings of the National Academy of Sciences of the United States of America 102, 140–145.
| The rate of DNA evolution: effects of body size and temperature on the molecular clock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtlehug%3D%3D&md5=c561a5357b107cf93517a7831fce9b51CAS |
Goudet, J. (1995). FSTAT (version 1.2): a computer program to calculate F-statistics. The Journal of Heredity 86, 485–486.
| FSTAT (version 1.2): a computer program to calculate F-statistics.Crossref | GoogleScholarGoogle Scholar |
Guo, S., and Thompson, E. (1992). Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48, 361–372.
| Performing the exact test of Hardy–Weinberg proportion for multiple alleles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38zksFGgsA%3D%3D&md5=c6b5af7594f8ea59a6cc654823dbf541CAS |
Hanski, I., and Ovaskainen, O. (2000). The metapopulation capacity of a fragmented landscape. Nature 404, 755–758.
| The metapopulation capacity of a fragmented landscape.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtVWntbg%3D&md5=eba2ac4f051210130c0283288b3165b1CAS |
Hefti-Gautschi, B., Pfunder, M., Jenni, L., Keller, V., and Ellegren, H. (2009). Identification of conservation units in the European Mergus merganser based on nuclear and mitochondrial DNA markers. Conservation Genetics 10, 87–99.
| Identification of conservation units in the European Mergus merganser based on nuclear and mitochondrial DNA markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvFOhug%3D%3D&md5=02b9aad2adc1503a65fe91e9dc138eb4CAS |
Höglund, J., Larsson, J. K., Corrales, C., Santafe, G., Baines, D., and Segelbacher, G. (2011). Genetic structure among black grouse in Britain: implications for designing conservation units. Animal Conservation 14, 400–408.
| Genetic structure among black grouse in Britain: implications for designing conservation units.Crossref | GoogleScholarGoogle Scholar |
Jakobsson, M., and Rosenberg, N. A. (2007). CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806.
| CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1ahtbs%3D&md5=91b587c937560a0bed6515d59b119006CAS |
Johnson, J. A., Toepfer, J. E., and Dunn, P. O. (2003). Contrasting patterns of mitochondrial and microsatellite population structure in fragmented populations of greater prairie-chickens. Molecular Ecology 12, 3335–3347.
| Contrasting patterns of mitochondrial and microsatellite population structure in fragmented populations of greater prairie-chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXks1yqsA%3D%3D&md5=cfe80c6cef2bbcd8739bd9c5c72e3e92CAS |
Johnson, J. A., Tingay, R. E., Culver, M., Hailer, F., Clarke, M. L., and Mindell, D. P. (2009). Long-term survival despite low genetic diversity in the critically endangered Madagascar fish-eagle. Molecular Ecology 18, 54–63.
| Long-term survival despite low genetic diversity in the critically endangered Madagascar fish-eagle.Crossref | GoogleScholarGoogle Scholar |
Lande, R. (1988). Genetics and demography in biological conservation. Science 241, 1455–1460.
| Genetics and demography in biological conservation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1czjs1yktA%3D%3D&md5=53dfc937ae48414222cdd8ee287b1c30CAS |
Librado, P., and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
| DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFeqtr8%3D&md5=d1d5c76c41013e58257d3a764486a01fCAS |
Lindenmayer, D. B. (2009). ‘Large-scale Landscape Experiments: Lessons from Tumut.’ (Cambridge University Press: Cambridge.)
Matocq, M. D., and Villablanca, F. X. (2001). Low genetic diversity in an endangered species: recent or historic pattern? Biological Conservation 98, 61–68.
| Low genetic diversity in an endangered species: recent or historic pattern?Crossref | GoogleScholarGoogle Scholar |
Maute, K. L. (2011). Variation in the health of tropical finches in relation to conservation status, season and land tenure. Ph.D. Thesis, University of Wollongong.
Milot, E., Weimerskirch, H., Duchesne, P., and Bernatchez, L. (2007). Surviving with low genetic diversity: the case of albatrosses. Proceedings of the Royal Society B: Biological Sciences 274, 779–787.
| Surviving with low genetic diversity: the case of albatrosses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktFOis7g%3D&md5=76d5ea3838d9b145eb24bb58bbbb5209CAS |
Mitchell, D. F. (1996). Foraging ecology of the black-throated finch, Poephila cincta cincta. M.Sc. Thesis, James Cook University, Townsville.
Natural Resource Assessment Environmental Consultants (2007). Survey and assessment of the black-throated finch (Poephila cincta cincta) at the Chisholm Trail Rural Residential Development, Townsville. Unpublished report prepared for the Department of Environment and Water Resources, Brisbane.
Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.
| 1:STN:280:DC%2BC3crpt1Kqtg%3D%3D&md5=574021dc3ebad4b641e4190e65fe0236CAS |
Paetkau, D., Waits, L. P., Clarkson, P. L., Craighead, L., Vyse, E., Ward, R., and Strobeck, C. (1998). Variation in genetic diversity across the range of North American brown bears. Conservation Biology 12, 418–429.
| Variation in genetic diversity across the range of North American brown bears.Crossref | GoogleScholarGoogle Scholar |
Peakall, R., and Smouse, P. E. (2006). GENALEX 6: genetic analysis in Excel: population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
| GENALEX 6: genetic analysis in Excel: population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |
Peakall, R., and Smouse, P. E. (2012). GENALEX 6.5: genetic analysis in Excel: population genetic software for teaching and research – an update. Bioinformatics 28, 2537–2539.
| GENALEX 6.5: genetic analysis in Excel: population genetic software for teaching and research – an update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVehtbjI&md5=f36d0bcb5d48b2df5606e724dad5896fCAS |
Petit, R. J., El Mousadik, A., and Pons, O. (1998). Identifying populations for conservation on the basis of genetic markers. Conservation Biology 12, 844–855.
| Identifying populations for conservation on the basis of genetic markers.Crossref | GoogleScholarGoogle Scholar |
Piry, S., Luikart, G., and Cornuet, J. M. (1999). BOTTLENECK: a program for detecting recent effective population size reductions from allele data frequencies. The Journal of Heredity 90, 502–503.
| BOTTLENECK: a program for detecting recent effective population size reductions from allele data frequencies.Crossref | GoogleScholarGoogle Scholar |
Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| 1:STN:280:DC%2BD3cvislKrtA%3D%3D&md5=ebd32f6e3060730a6655a20992d2ddc6CAS |
Rollins, L. A., Svedin, N., Pryke, S. R., and Griffith, S. C. (2012). The role of the Ord Arid Intrusion in the historical and contemporary genetic division of long-tailed finch subspecies in northern Australia. Ecology and Evolution 2, 1208–1219.
| The role of the Ord Arid Intrusion in the historical and contemporary genetic division of long-tailed finch subspecies in northern Australia.Crossref | GoogleScholarGoogle Scholar |
Rosenberg, N. A. (2004). DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4, 137–138.
| DISTRUCT: a program for the graphical display of population structure.Crossref | GoogleScholarGoogle Scholar |
Rousset, F. (2008). GENEPOP‘007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8, 103–106.
| GENEPOP‘007: a complete re-implementation of the GENEPOP software for Windows and Linux.Crossref | GoogleScholarGoogle Scholar |
Schodde, R., and Mason, I. J. (1999). ‘The Directory of Australian Birds: Passerines.’ (CSIRO Publishing: Melbourne.)
Schrey, A. W., Grispo, M., Awad, M., Cook, M. B., McCoy, E. D., Mushinsky, H. R., Albayrak, T., Bensch, S., Burke, T., Butler, L. K., Dor, R., Fokidis, H. B., Jensen, H., Imboma, T., Kessler-Rios, M. M., Marzal, A., Stewart, I. R., Westerdahl, H., Westneat, D. F., Zehtindjiev, P., and Martin, L. B. (2011). Broad-scale latitudinal patterns of genetic diversity among native European and introduced house sparrow (Passer domesticus) populations. Molecular Ecology 20, 1133–1143.
| Broad-scale latitudinal patterns of genetic diversity among native European and introduced house sparrow (Passer domesticus) populations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mvjt1Citg%3D%3D&md5=c65254a0d282a73d45fd899dde835e1eCAS |
Slatkin, M., and Barton, N. H. (1989). A comparison of three indirect methods for estimating average levels of gene flow. Evolution 43, 1349–1368.
| A comparison of three indirect methods for estimating average levels of gene flow.Crossref | GoogleScholarGoogle Scholar |
Slatkin, M., and Excoffier, L. (1996). Testing for linkage disequilibrium in genotypic data using the expectation–maximization algorithm. Heredity 76, 377–383.
| Testing for linkage disequilibrium in genotypic data using the expectation–maximization algorithm.Crossref | GoogleScholarGoogle Scholar |
State of the Environment Advisory Council (1996). ‘Australia: State of the Environment.’ (Department of the Environment, Sport and Territories: Melbourne.)
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
| MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=8da55d066d73877ea73394f77444cc5bCAS |
Tang, L. S., Smith-Keune, C., Gardner, M. G., and Hardesty, B. D. (2014). Development, characterisation and cross-species amplification of 16 novel microsatellite markers for the endangered black-throated finch (Poephila cincta) in Australia. Conservation Genetics Resources 6, 143–146.
| Development, characterisation and cross-species amplification of 16 novel microsatellite markers for the endangered black-throated finch (Poephila cincta) in Australia.Crossref | GoogleScholarGoogle Scholar |
Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
| MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOktb8%3D&md5=9cd3b93c23d1169be30f5281343cfa4eCAS |
Wahlund, S. (1928). Zusammensetzung von Populationen und Korrelationserscheinungen vom Standpunkt der Vererbungslehre ausbetrachtet. Hereditas 11, 65–106.
| Zusammensetzung von Populationen und Korrelationserscheinungen vom Standpunkt der Vererbungslehre ausbetrachtet.Crossref | GoogleScholarGoogle Scholar |
Wenzel, M. A., Webster, M. I., Blanco, G., Burgess, M. D., Kerbiriou, C., Segelbacher, G., Piertney, S. B., and Reid, J. M. (2012). Pronounced genetic structure and low genetic diversity in European red-billed chough (Pyrrhocorax pyrrhocorax). Conservation Genetics 13, 1213–1230.
| Pronounced genetic structure and low genetic diversity in European red-billed chough (Pyrrhocorax pyrrhocorax).Crossref | GoogleScholarGoogle Scholar |
Yeh, F. C., and Boyle, T. J. B. (1997). Population genetic analysis of co-dominant and dominant markers and quantitative traits. Belgian Journal of Botany 129, 157–163.
Zar, J. H. (1999). ‘Biostatistical Analysis.’ (Prentice Hall: Upper Saddle River, USA.)