Register      Login
Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Significant population genetic structuring but a lack of phylogeographic structuring in the endemic Tasmanian tree frog (Litoria burrowsae)

Z. Y. Zhang A , S. Cashins B , A. Philips B and C. P. Burridge A C
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, University of Tasmania, Private Bag 55, Hobart, Tas. 7001, Australia.

B Department of Primary Industries, Parks, Water and Environment, GPO Box 44, Hobart, Tas. 7001, Australia.

C Corresponding author. Email: Chris.Burridge@utas.edu.au

Australian Journal of Zoology 62(3) 238-245 https://doi.org/10.1071/ZO14028
Submitted: 17 April 2014  Accepted: 20 June 2014   Published: 5 August 2014

Abstract

Conservation of frogs is of global concern, owing to declines resulting from habitat destruction, global climate change, and disease. Knowledge of genetic variation in frog species is therefore desirable for the identification of management units. Here we surveyed mitochondrial DNA sequence variation in the Tasmanian endemic hylid frog Litoria burrowsae, which is infected by chytrid fungus, Batrachochytrium dendrobatidis, and may be declining. Neither phylogeographic structure nor deep phylogenetic divergence was detected in the species, although its populations were highly differentiated with respect to haplotype frequencies. The low-haplotype diversity in L. burrowsae suggests a recent bottleneck in the species, and population genetic structuring may reflect isolation by distance as well as founder effects associated with range expansion. Three putative management units were identified that require verification based on nuclear DNA variation and adaptation to local environments.

Additional keywords: conservation genetics, genetic diversity, phylogeography.


References

Alford, R. A., and Richards, S. J. (1999). Global amphibian declines: a problem in applied ecology. Annual Review of Ecology and Systematics 30, 133–165.
Global amphibian declines: a problem in applied ecology.Crossref | GoogleScholarGoogle Scholar |

Altizer, S., Harvell, D., and Friedle, E. (2003). Rapid evolutionary dynamics and disease threats to biodiversity. Trends in Ecology & Evolution 18, 589–596.
Rapid evolutionary dynamics and disease threats to biodiversity.Crossref | GoogleScholarGoogle Scholar |

Arens, P., van der Sluis, T., van’t Westende, W. P. C., Vosman, B., Vos, C. C., and Smulders, M. J. M. (2007). Genetic population differentiation and connectivity among fragmented Moor frog (Rana arvalis) populations in The Netherlands. Landscape Ecology 22, 1489–1500.
Genetic population differentiation and connectivity among fragmented Moor frog (Rana arvalis) populations in The Netherlands.Crossref | GoogleScholarGoogle Scholar |

Aris-Brosou, S., and Excoffier, L. (1996). The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Molecular Biology and Evolution 13, 494–504.
The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xht1Kgurs%3D&md5=a70f766b8d75e2fb93a77e05b8d48735CAS |

Berger, L., Speare, R., Daszak, P., Green, D. E., Cunningham, A. A., Goggin, C. L., Slocombe, R., Ragan, M. A., Hyatt, A. D., Mcdonald, K. R., Hines, H. B., Lips, K. R., Marantelli, G., and Parkes, H. (1998). Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America 95, 9031–9036.
Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvFaltbc%3D&md5=982dc125bd22605cd0dc9b74c7af3678CAS |

Bisconti, R., Canestrelli, D., Colangelo, P., and Nascetti, G. (2011). Multiple lines of evidence for demographic and range expansion of a temperate species (Hyla sarda) during the last glaciation. Molecular Ecology 20, 5313–5327.
Multiple lines of evidence for demographic and range expansion of a temperate species (Hyla sarda) during the last glaciation.Crossref | GoogleScholarGoogle Scholar |

Blaustein, A. R., and Kiesecker, J. M. (2002). Complexity in conservation: lessons from the global decline of amphibian populations. Ecology Letters 5, 597–608.
Complexity in conservation: lessons from the global decline of amphibian populations.Crossref | GoogleScholarGoogle Scholar |

Blouin, M. S., Phillipsen, I. C., and Monsen, K. J. (2010). Population structure and conservation genetics of the Oregon spotted frog, Rana pretiosa. Conservation Genetics 11, 2179–2194.
Population structure and conservation genetics of the Oregon spotted frog, Rana pretiosa.Crossref | GoogleScholarGoogle Scholar |

Bohonak, A. J. (2002). IBD (isolation by distance): a program for analyses of isolation by distance. The Journal of Heredity 93, 153–154.
IBD (isolation by distance): a program for analyses of isolation by distance.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zptVSlug%3D%3D&md5=2bc4f086901f893137d281ed9194f32aCAS |

Booy, G., Hendriks, R. J. J., Smulders, M. J. M., Van Groenendael, J. M., and Vosman, B. (2000). Genetic diversity and the survival of populations. Plant Biology 2, 379–395.
Genetic diversity and the survival of populations.Crossref | GoogleScholarGoogle Scholar |

Burns, E. L., Eldridge, M. D. B., Crayn, D. M., and Houlden, B. A. (2007). Low phylogeographic structure in a wide spread endangered Australian frog Litoria aurea (Anura: Hylidae). Conservation Genetics 8, 17–32.
Low phylogeographic structure in a wide spread endangered Australian frog Litoria aurea (Anura: Hylidae).Crossref | GoogleScholarGoogle Scholar |

Byrne, M. (2008). Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography. Quaternary Science Reviews 27, 2576–2585.
Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography.Crossref | GoogleScholarGoogle Scholar |

Clark, C. M., and Carbone, I. (2008). Chloroplast DNA phylogeography in long-lived Huon pine, a Tasmanian rain forest conifer. Canadian Journal of Forest Research 38, 1576–1589.
Chloroplast DNA phylogeography in long-lived Huon pine, a Tasmanian rain forest conifer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvVGks7k%3D&md5=44649d04abccd6a96c51786f09655244CAS |

Colhoun, E. A., Hannan, D., and Kiernan, K. (1996). Late Wisconsin glaciation of Tasmania. Papers and Proceedings of the Royal Society of Tasmania 130, 33–45.

Crandall, K. A., Bininda-Emonds, O. R. P., Mace, G. M., and Wayne, R. K. (2000). Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution 15, 290–295.
Considering evolutionary processes in conservation biology.Crossref | GoogleScholarGoogle Scholar |

Dever, J. A. (2007). Fine-scale genetic structure in the threatened foothill yellow-legged frog (Rana boylii). Journal of Herpetology 41, 168–173.
Fine-scale genetic structure in the threatened foothill yellow-legged frog (Rana boylii).Crossref | GoogleScholarGoogle Scholar |

Driscoll, D. A. (1998). Genetic structure, metapopulation processes and evolution influence the conservation strategies for two endangered frog species. Biological Conservation 83, 43–54.
Genetic structure, metapopulation processes and evolution influence the conservation strategies for two endangered frog species.Crossref | GoogleScholarGoogle Scholar |

Eizirik, E., Kim, J. H., Menotti-Raymond, M., Crawshaw, P. G., O’Brien, S. J., and Johnson, W. E. (2001). Phylogeography, population history and conservation genetics of jaguars (Panthera onca, Mammalia, Felidae). Molecular Ecology 10, 65–79.
Phylogeography, population history and conservation genetics of jaguars (Panthera onca, Mammalia, Felidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjs1ejtL0%3D&md5=0056c1d0bc37a788a9b92e5d8eb2a5d9CAS |

Excoffier, L., and Smouse, P. E. (1994). Using allele frequencies and geographic subdivision to reconstruct gene trees within a species: molecular variance parsimony. Genetics 136, 343–359.
| 1:STN:280:DyaK2c7os1Smug%3D%3D&md5=71706b528b2fe4d8c7b323ac15171635CAS |

Excoffier, L., Smouse, P. E., and Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.
| 1:CAS:528:DyaK38XlsVCntro%3D&md5=6628e8b7a35e76738c4f7bfac04760fbCAS |

Excoffier, L., Laval, G., and Schneider, S. (2007). Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.

Frankham, R., Ballou, J. D., and Briscoe, D. A. (2003). ‘A Primer of Conservation Genetics.’ (Cambridge University Press: New York.)

Frankham, R., Ballou, J. D., and Briscoe, D. A. (2010). ‘Introduction to Conservation Genetics.’ (Cambridge University Press: New York.)

Freeland, J. (2005). Molecular markers in ecology. In ‘Molecular Ecology’. (Ed. H. Kirk.) pp. 31–62. (Wiley-Blackwell: West Sussex.)

Fu, Y. X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.
| 1:STN:280:DyaK2svns1egtQ%3D%3D&md5=00e196ca387b3be1d46959efd0dd8b1bCAS |

Hedrick, P. W. (2005). A standardized genetic differentiation measure. Evolution 59, 1633–1638.
A standardized genetic differentiation measure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVKlt7bO&md5=67dfe153276a977e64466de8e927f669CAS |

Hewitt, G. (2000). The genetic legacy of the Quaternary ice ages. Nature 405, 907–913.
The genetic legacy of the Quaternary ice ages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXks1Wmu78%3D&md5=6b3eba47fab6de5fa019ac9d74be5a3fCAS |

Jensen, J. L., Bohonak, A. J., and Kelley, S. T. (2005). Isolation by distance, web service. BMC Genetics 6: 13. v.3.23. http://ibdws.sdsu.edu/

Kirkpatrick, J. B., and Fowler, M. (1998). Locating likely glacial forest refugia in Tasmania using palynological and ecological information to test alternative climatic models. Biological Conservation 85, 171–182.
Locating likely glacial forest refugia in Tasmania using palynological and ecological information to test alternative climatic models.Crossref | GoogleScholarGoogle Scholar |

Lande, R., and Shannon, S. (1996). The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50, 434–437.
The role of genetic variation in adaptation and population persistence in a changing environment.Crossref | GoogleScholarGoogle Scholar |

Legge, J. T., Roush, R., Desalle, R., Vogler, A. P., and May, B. (1996). Genetic criteria for establishing evolutionarily significant units in Cryan’s buckmoth. Conservation Biology 10, 85–98.
Genetic criteria for establishing evolutionarily significant units in Cryan’s buckmoth.Crossref | GoogleScholarGoogle Scholar |

Littlejohn, M. (2003). ‘Frogs of Tasmania.’ (University of Tasmania Press: Hobart.)

Luquet, E., Garner, T. W. J., Léna, J. P., Bruel, C., Joly, P., Lengagne, T., Grolet, O., and Plénet, S. (2012). Genetic erosion in wild populations makes resistance to a pathogen more costly. Evolution 66, 1942–1952.
Genetic erosion in wild populations makes resistance to a pathogen more costly.Crossref | GoogleScholarGoogle Scholar |

Macey, J. R., Schulte, J. A., Larson, A., Fang, Z., Wang, Y., Tuniyev, B. S., and Papenfuss, T. J. (1998). Phylogenetic relationships of toads in the Bufo bufo species group from the eastern escarpment of the Tibetan Plateau: a case of vicariance and dispersal. Molecular Phylogenetics and Evolution 9, 80–87.
Phylogenetic relationships of toads in the Bufo bufo species group from the eastern escarpment of the Tibetan Plateau: a case of vicariance and dispersal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXht1yhurk%3D&md5=15673b95f90c4e2126a68c42ed6084c0CAS |

Macqueen, P., Goldizen, A. W., and Seddon, J. M. (2009). Response of a southern temperate marsupial, the Tasmanian pademelon (Thylogale billardierii), to historical and contemporary forest fragmentation. Molecular Ecology 18, 3291–3306.
Response of a southern temperate marsupial, the Tasmanian pademelon (Thylogale billardierii), to historical and contemporary forest fragmentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFaisbrI&md5=faf8744bdb2837a41f582b180046d8c0CAS |

Maggs, C. A., Castilho, R., Foltz, D., Henzler, C., Jolly, M. T., Kelly, J., Olsen, J., Perez, K. E., Stam, W., Vainola, R., Viard, F., and Wares, J. (2008). Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89, S108–S122.
Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa.Crossref | GoogleScholarGoogle Scholar |

Markgraf, V., McGlone, M., and Hope, G. (1995). Neogene paleoenvironmental and paleoclimatic change in southern temperate ecosystems – a southern perspective. Trends in Ecology & Evolution 10, 143–147.
Neogene paleoenvironmental and paleoclimatic change in southern temperate ecosystems – a southern perspective.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFajug%3D%3D&md5=7cbc6e19584d2e5909a001427fedf330CAS |

McKinnon, G. E., Vaillancourt, R. E., Jackson, H. D., and Potts, B. M. (2001). Chloroplast sharing in the Tasmanian eucalypts. Evolution 55, 703–711.
Chloroplast sharing in the Tasmanian eucalypts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktleqtLs%3D&md5=2b6f3c8f8af038a68c361ad2bb8aaa38CAS |

McKinnon, G. E., Jordan, G. J., Vaillancourt, R. E., Steane, D. A., and Potts, B. M. (2004). Glacial refugia and reticulate evolution: the case of the Tasmanian eucalypts. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 359, 275–284.
Glacial refugia and reticulate evolution: the case of the Tasmanian eucalypts.Crossref | GoogleScholarGoogle Scholar |

Meirmans, P. G. (2006). Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60, 2399–2402.
Using the AMOVA framework to estimate a standardized genetic differentiation measure.Crossref | GoogleScholarGoogle Scholar |

Meirmans, P. G., and Van Tienderen, P. H. (2004). Genotype and Genodive: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes 4, 792–794.
Genotype and Genodive: two programs for the analysis of genetic diversity of asexual organisms.Crossref | GoogleScholarGoogle Scholar |

Merila, J., Soderman, F., O’Hara, R., Rasanen, K., and Laurila, A. (2004). Local adaptation and genetics of acid-stress tolerance in the moor frog, Rana arvalis. Conservation Genetics 5, 513–527.
Local adaptation and genetics of acid-stress tolerance in the moor frog, Rana arvalis.Crossref | GoogleScholarGoogle Scholar |

Moritz, C. (1994). Applications of mitochondrial DNA analysis in conservation: a critical review. Molecular Ecology 3, 401–411.
Applications of mitochondrial DNA analysis in conservation: a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtlyktrw%3D&md5=a061a71614dc9e17edc081352e3b3cceCAS |

Moritz, C. (1995). Uses of molecular phylogenies for conservation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 349, 113–118.
Uses of molecular phylogenies for conservation.Crossref | GoogleScholarGoogle Scholar |

Moritz, C. (1999). Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130, 217–228.
Conservation units and translocations: strategies for conserving evolutionary processes.Crossref | GoogleScholarGoogle Scholar |

Muellner, A. N., Tremetsberger, K., Stuessy, T., and Baeza, C. M. (2005). Pleistocene refugia and recolonization routes in the southern Andes: insights from Hypochaeris palustris (Asteraceae, Lactuceae). Molecular Ecology 14, 203–212.
Pleistocene refugia and recolonization routes in the southern Andes: insights from Hypochaeris palustris (Asteraceae, Lactuceae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M%2FhvVykug%3D%3D&md5=5b951f20b870c502e7a868ec892a62dbCAS |

Nei, M., Maruyama, T., and Chakraborty, R. (1975). Bottleneck effect and genetic variability in populations. Evolution 29, 1–10.
Bottleneck effect and genetic variability in populations.Crossref | GoogleScholarGoogle Scholar |

Nurnberger, B., and Harrison, R. G. (1995). Spatial population structure in the whirligig beetle Dineutus assimilis: evolutionary inferences based on mitochondrial DNA and field data. Evolution 49, 266–275.
Spatial population structure in the whirligig beetle Dineutus assimilis: evolutionary inferences based on mitochondrial DNA and field data.Crossref | GoogleScholarGoogle Scholar |

Obendorf, D. L. (2005). Application of field and diagnostic methods for chytridiomycosis in Tasmanian frogs. Central North Field Naturalists Inc. Tasmania, Australia.

Opgenoorth, L., Vendramin, G. G., Mao, K., Miehe, G., Miehe, S., Liepelt, S., Liu, J., and Ziegenhagen, B. (2010). Tree endurance on the Tibetan Plateau marks the world’s highest known tree line of the Last Glacial Maximum. New Phytologist 185, 332–342.
Tree endurance on the Tibetan Plateau marks the world’s highest known tree line of the Last Glacial Maximum.Crossref | GoogleScholarGoogle Scholar |

Palumbi, S. R. (1996). Nucleic acids II: the polymerase chain reaction. In ‘Molecular Systematics’. (Eds D. M. Hillis, C. M. Moritz and N. K. Mable.) pp. 205–247. (Sinauer Associates, Inc.: Massachusetts.)

Pauza, M. D., Driessen, M. M., and Skerratt, L. F. (2010). Distribution and risk factors for spread of amphibian chytrid fungus Batrachochytrium dendrobatidis in the Tasmanian Wilderness World Heritage Area, Australia. Diseases of Aquatic Organisms 92, 193–199.
Distribution and risk factors for spread of amphibian chytrid fungus Batrachochytrium dendrobatidis in the Tasmanian Wilderness World Heritage Area, Australia.Crossref | GoogleScholarGoogle Scholar |

Petit, R., 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 |

Reed, D. H., and Frankham, R. (2003). Correlation between fitness and genetic diversity. Conservation Biology 17, 230–237.
Correlation between fitness and genetic diversity.Crossref | GoogleScholarGoogle Scholar |

Richardson, J. L. (2012). Divergent landscape effects on population connectivity in two co-occurring amphibian species. Molecular Ecology 21, 4437–4451.
Divergent landscape effects on population connectivity in two co-occurring amphibian species.Crossref | GoogleScholarGoogle Scholar |

Rogell, B., Berglund, A., Laurila, A., and Hoglund, J. (2011). Population divergence of life history traits in the endangered green toad: implications for a support release programme. Journal of Zoology 285, 46–55.

Rogers, A. R. (1995). Genetic evidence for a Pleistocene population explosion. Evolution 49, 608–615.
Genetic evidence for a Pleistocene population explosion.Crossref | GoogleScholarGoogle Scholar |

Rousset, F. (1997). Genetic differentiation and estimation of gene flow from F-statistics under Isolation by Distance. Genetics 145, 1219–1228.
| 1:STN:280:DyaK2s3kslOntQ%3D%3D&md5=ff0f85699e11e4c8e5fd086f92fef835CAS |

Rull, V. (2009). Microrefugia. Journal of Biogeography 36, 481–484.
Microrefugia.Crossref | GoogleScholarGoogle Scholar |

Schmidtling, R. C., and Hipkins, V. (1998). Genetic diversity in longleaf pine (Pinus palustris): influence of historical and prehistorical events. Canadian Journal of Forest Research 28, 1135–1145.
Genetic diversity in longleaf pine (Pinus palustris): influence of historical and prehistorical events.Crossref | GoogleScholarGoogle Scholar |

Skerratt, L. F., Berger, L., Speare, R., Cashins, S., McDonald, K. R., Phillott, A. D., Hines, H. B., and Kenyon, N. (2007). Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125–134.
Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs.Crossref | GoogleScholarGoogle Scholar |

Smith, K. L., Hale, J. M., Austin, J. J., and Melville, J. (2011). Isolation and characterization of microsatellite markers for the Litoria ewingii complex and their use in conservation and hybridization studies. Conservation Genetics Resources 3, 621–624.
Isolation and characterization of microsatellite markers for the Litoria ewingii complex and their use in conservation and hybridization studies.Crossref | GoogleScholarGoogle Scholar |

Spielman, D., Brook, B., Briscoe, D., and Frankham, R. (2004a). Does inbreeding and loss of genetic diversity decrease disease resistance? Conservation Genetics 5, 439–448.
Does inbreeding and loss of genetic diversity decrease disease resistance?Crossref | GoogleScholarGoogle Scholar |

Spielman, D., Brook, B. W., and Frankham, R. (2004b). Most species are not driven to extinction before genetic factors impact them. Proceedings of the National Academy of Sciences of the United States of America 101, 15 261–15 264.
Most species are not driven to extinction before genetic factors impact them.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpsVSgu7k%3D&md5=bb11cdedef4621a9bfec8c75ee2be030CAS |

Stewart, J. R., Lister, A. M., Barnes, I., and Dalén, L. (2010). Refugia revisited: individualistic responses of species in space and time. Proceedings of the Royal Society B - Biological Sciences 277, 661–671.
Refugia revisited: individualistic responses of species in space and time.Crossref | GoogleScholarGoogle Scholar |

Storfer, A. (2003). Amphibian declines: future directions. Diversity & Distributions 9, 151–163.
Amphibian declines: future directions.Crossref | GoogleScholarGoogle Scholar |

Taberlet, P., Fumagalli, L., Wust-Saucy, A. G., and Cosson, J. F. (1998). Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology 7, 453–464.
Comparative phylogeography and postglacial colonization routes in Europe.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3ptFCksg%3D%3D&md5=94830766c6c69d22e19bb4d84a03870dCAS |

Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
| 1:CAS:528:DyaK3cXhslentA%3D%3D&md5=49669c67a5ff0cb37882e6937feec8b2CAS |

Teacher, A. G. F., and Griffiths, D. J. (2011). HapStar: automated haplotype network layout and visualisation. Molecular Ecology Resources 11, 151–153.
HapStar: automated haplotype network layout and visualisation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M3ptFaqsg%3D%3D&md5=75778370ec926e87306c03f61491d2c8CAS |

Vogler, A. P., Knisley, C. B., Glueck, S. B., Hill, J. M., and Desalle, R. (1993). Using molecular and ecological data to diagnose endangered populations of the puritan tiger beetle Cicindela puritana. Molecular Ecology 2, 375–383.
Using molecular and ecological data to diagnose endangered populations of the puritan tiger beetle Cicindela puritana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXisVSksr4%3D&md5=c771fec96b01555964eb3a8ff98123eaCAS |

Waters, J. M., Fraser, C. I., and Hewitt, G. M. (2013). Founder takes all: density-dependent processes structure biodiversity. Trends in Ecology & Evolution 28, 78–85.
Founder takes all: density-dependent processes structure biodiversity.Crossref | GoogleScholarGoogle Scholar |

Worth, J. R. P., Jordan, G. J., Marthick, J. R., McKinnon, G. E., and Vaillancourt, R. E. (2010). Chloroplast evidence for geographic stasis of the Australian bird-dispersed shrub Tasmannia lanceolata (Winteraceae). Molecular Ecology 19, 2949–2963.
Chloroplast evidence for geographic stasis of the Australian bird-dispersed shrub Tasmannia lanceolata (Winteraceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyktb3L&md5=69b2821a6ee2b7bb365ff27201ee1a0aCAS |

Zeisset, I., and Beebee, T. J. C. (2008). Amphibian phylogeography: a model for understanding historical aspects of species distributions. Heredity 101, 109–119.
Amphibian phylogeography: a model for understanding historical aspects of species distributions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cvmvVWhsw%3D%3D&md5=0b5dc23ebebd0ef3f01e93faf65fee31CAS |