Statistical phylogeographic tests of competing ‘Lake Carpentaria hypotheses’ in the mouth-brooding freshwater fish, Glossamia aprion (Apogonidae)
Benjamin D. Cook A B F , Mark Adams C D , Peter B. Mather E and Jane M. Hughes A
+ Author Affiliations
- Author Affiliations
A Tropical Rivers and Coastal Knowledge Commonwealth Environmental Research Facility, Australian Rivers Institute, Griffith University, Nathan, Qld 4111, Australia.
B Present address: frc environmental, PO Box 2363, Wellington Point, Qld 4160, Australia.
C Evolutionary Biology Unit, South Australian Museum, Adelaide, SA 5000, Australia.
D Australian Centre for Evolutionary Biology and Biodiversity, School of Earth and Environmental Science, The University of Adelaide, SA 5005, Australia.
E Faculty of Science and Technology, Queensland University of Technology, Brisbane, Qld 4000, Australia.
F Corresponding author. Email: bencook@frcenv.com.au
Marine and Freshwater Research 63(5) 450-456 https://doi.org/10.1071/MF11222
Submitted: 30 September 2011 Accepted: 3 March 2012 Published: 4 May 2012
Abstract
Glacial cycles during the Pleistocene reduced sea levels and created new land connections in northern Australia, where many currently isolated rivers also became connected via an extensive paleo-lake system, ‘Lake Carpentaria’. However, the most recent period during which populations of freshwater species were connected by gene flow across Lake Carpentaria is debated: various ‘Lake Carpentaria hypotheses’ have been proposed. Here, we used a statistical phylogeographic approach to assess the timing of past population connectivity across the Carpentaria region in the obligate freshwater fish, Glossamia aprion. Results for this species indicate that the most recent period of genetic exchange across the Carpentaria region coincided with the mid- to late Pleistocene, a result shown previously for other freshwater and diadromous species. Based on these findings and published studies for various freshwater, diadromous and marine species, we propose a set of ‘Lake Carpentaria’ hypotheses to explain past population connectivity in aquatic species: (1) strictly freshwater species had widespread gene flow in the mid- to late Pleistocene before the last glacial maximum; (2) marine species were subdivided into eastern and western populations by land during Pleistocene glacial phases; and (3) past connectivity in diadromous species reflects the relative strength of their marine affinity.
Additional keywords: diadromy, last glacial maximum, Pleistocene, Slatkin and Maddison’s s.
References
Allen, G. R., and Hoese, D. F. (1980). A collection of fishes from Cape York Peninsula, Australia. Journal of the Royal Society of Western Australia 63, 53–61.Avise, J. C. (2000). ‘Phylogeography: the History and Formation of Species.’ (Harvard University Press: Cambridge, MA.)
Bermingham, E., McCafferty, S., and Martin, A. (1997). Fish biogeography and molecular clocks: perspectives from the Panamanian Isthmus. In ‘Molecular Systematics of Fishes’. (Eds T. Kocher and C. Stepien.) pp. 113–128 (Academic Press: New York.)
Bowman, D. M. J. S., Brown, G. K., Braby, M. F., Brown, J. R., Cook, L. G., Crisp, M. D., Ford, F., Haberle, S., Hughes, J., Isagi, Y., Joseph, L., McBride, J., Nelson, G., and Ladiges, P. Y. (2010). Biogeography of the Australian monsoon tropics. Journal of Biogeography 37, 201–216.
| Biogeography of the Australian monsoon tropics.Crossref | GoogleScholarGoogle Scholar |
Carstens, B. C., Degenhardt, J. D., Stevenson, A. L., and Sullivan, J. (2005). Accounting for coalescent stochasticity in testing phylogeographic hypotheses: modelling Pleistocene population structure in the Idaho giant salamander Dicamptodon aterrimus. Molecular Ecology 14, 255–265.
| Accounting for coalescent stochasticity in testing phylogeographic hypotheses: modelling Pleistocene population structure in the Idaho giant salamander Dicamptodon aterrimus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M%2FhvVyrsA%3D%3D&md5=a9682067845ed15517717db516b4e877CAS |
Chenoweth, S. F., Hughes, J. M., Keenan, C. P., and Lavery, S. (1998). When oceans meet: a teleost shows secondary intergradation at an Indian–Pacific interface. Proceedings. Biological Sciences 265, 415–420.
| When oceans meet: a teleost shows secondary intergradation at an Indian–Pacific interface.Crossref | GoogleScholarGoogle Scholar |
Clement, M., Posada, D., and Crandall, K. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
| TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvV2gtbw%3D&md5=938635643268b9e69bbf715e7ea75a46CAS |
Cook, B. D., and Hughes, J. M. (2010). Historical population connectivity and fragmentation in a freshwater fish with a disjunct distribution (pennyfish, Denariusa bandata). Journal of the North American Benthological Society 29, 1119–1131.
| Historical population connectivity and fragmentation in a freshwater fish with a disjunct distribution (pennyfish, Denariusa bandata).Crossref | GoogleScholarGoogle Scholar |
Cook, B. D., Bunn, S. E., and Hughes, J. M. (2007). Molecular genetic and stable isotope signatures reveal complementary patterns of population connectivity in the regionally vulnerable southern pygmy perch (Nannoperca australis). Biological Conservation 138, 60–72.
| Molecular genetic and stable isotope signatures reveal complementary patterns of population connectivity in the regionally vulnerable southern pygmy perch (Nannoperca australis).Crossref | GoogleScholarGoogle Scholar |
Cook, B. D., Page, T. J., and Hughes, J. M. (2011). Molecular and conservation biogeography of freshwater caridean shrimps in north-western Australia. In ‘Phylogeography and Population Genetics in Crustacea’. (Eds C. H. Held, S. Koenemann and C. D. Schubart.) pp. 273–290. (CRC Press: London.)
de Bruyn, M., Wilson, J. C., and Mather, P. B. (2004). Reconciling geography and genealogy: phylogeography of giant freshwater prawns from the Lake Carpentaria region. Molecular Ecology 13, 3515–3526.
| Reconciling geography and genealogy: phylogeography of giant freshwater prawns from the Lake Carpentaria region.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWkurnI&md5=9c0b2ace1ead65bef723acd77a834d73CAS |
Elliott, N. (1996). Allozyme and mitochondrial DNA analysis of the tropical saddle-tail sea perch, Lutjanus malabaricus (Schneider) in Australian waters. Marine and Freshwater Research 47, 869–876.
| Allozyme and mitochondrial DNA analysis of the tropical saddle-tail sea perch, Lutjanus malabaricus (Schneider) in Australian waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XntF2lurg%3D&md5=773998de86a6aa1a07fa741d0de97af6CAS |
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=66933462771599b40b8f7404942213beCAS |
Gopurenko, D., and Hughes, J. M. (2002). Regional patterns of genetic structure among Australian populations of the mud crab, Scylla serrata (Crustacea: Decapoda): evidence from mitochondrial DNA. Marine and Freshwater Research 53, 849–857.
| Regional patterns of genetic structure among Australian populations of the mud crab, Scylla serrata (Crustacea: Decapoda): evidence from mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xoslenur4%3D&md5=f146d5e9dd7bd1943367c9e5090a76ceCAS |
Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
| A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.Crossref | GoogleScholarGoogle Scholar |
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=0f1fb3c1909a1becb9d9d03d0d941b0bCAS |
Hewitt, G. M. (2001). Speciation, hybrid zones and phylogeography – or seeing genes in space and time. Molecular Ecology 10, 537–549.
| Speciation, hybrid zones and phylogeography – or seeing genes in space and time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFKgtbY%3D&md5=0c68e382fcd029d4887c146b2696bd56CAS |
Hewitt, G. M. (2004). Genetic consequences of climatic oscillations in the Quaternary. Proceedings. Biological Sciences 359, 183–195.
| Genetic consequences of climatic oscillations in the Quaternary.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c3gsVSjuw%3D%3D&md5=4e7d3b7644ba3a735498b2c3792fa680CAS |
Hudson, R. R. (1990). Gene genealogies and the coalescent process. In ‘Oxford Surveys in Evolutionary Biology. Vol. 7’. (Eds D. Futuyma and J. Antonovics.) pp. 1–44. (Oxford University Press: Oxford.)
Huey, J. A., Baker, A. M., and Hughes, J. M. (2010). High levels of genetic structure in the Australian freshwater fish, Ambassis macleayi. Journal of the North American Benthological Society 29, 1148–1160.
| High levels of genetic structure in the Australian freshwater fish, Ambassis macleayi.Crossref | GoogleScholarGoogle Scholar |
Knowles, L. L. (2001). Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshoppers. Molecular Ecology 10, 691–701.
| Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshoppers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFKgurk%3D&md5=4234354b4b5d2d07c26e829fa8643b7aCAS |
Knowles, L. L., and Maddison, W. P. (2002). Statistical phylogeography. Molecular Ecology 11, 2623–2635.
| Statistical phylogeography.Crossref | GoogleScholarGoogle Scholar |
Librado, P., and Rozas, J. (2009). DnaSP v5: software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
| DnaSP v5: software for comprehensive analysis of DNA polymorphism data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFeqtr8%3D&md5=8ec9364da447684c6d55141ff6879eb4CAS |
Lisiecki, L. E., and Raymo, M. E. (2005). A Pliocene-Pleistocene stack of 57 globally distributed benthic δ18O records. Paleoceanography 20, PA1003.
| A Pliocene-Pleistocene stack of 57 globally distributed benthic δ18O records.Crossref | GoogleScholarGoogle Scholar |
Lohman, D. J., de Bruyn, M., Page, T. J., von Rintelen, K., Hall, R., Ng, P. K. L., Shih, H.-T., Carvalho, G. C., and von Rintelen, T. (2011). Biogeography of the Indo-Australian Archipelago. Annual Review of Ecology Evolution and Systematics 42, 205–226.
| Biogeography of the Indo-Australian Archipelago.Crossref | GoogleScholarGoogle Scholar |
Maddison, W. P., and Maddison, D. R. (2000). MESQUITE: a modular system for evolutionary analysis. ver. 2.72. Available at http://mesquiteproject.org/mesquite/mesquite.html [Accessed 12 June 2011].
McGuigan, K., Zhu, D., Allen, G. R., and Moritz, C. (2000). Phylogenetic relationships and historical biogeography of melanotaeniid fishes in Australia and New Guinea. Marine and Freshwater Research 51, 713–723.
| Phylogenetic relationships and historical biogeography of melanotaeniid fishes in Australia and New Guinea.Crossref | GoogleScholarGoogle Scholar |
Norman, J. A., Moritz, C., and Limpus, C. J. (1994). Mitochondrial DNA control region polymorphisms: genetic markers for ecological studies of marine turtles. Molecular Ecology 3, 363–373.
| Mitochondrial DNA control region polymorphisms: genetic markers for ecological studies of marine turtles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtlyksbc%3D&md5=2a76dc31d2baf6b7f557319be30f45f3CAS |
Ovenden, J. R., and Street, R. (2003). Genetic population structure of mangrove jack, Lutjanus argentimaculatus (Forsskål). Marine and Freshwater Research 54, 127–137.
| Genetic population structure of mangrove jack, Lutjanus argentimaculatus (Forsskål).Crossref | GoogleScholarGoogle Scholar |
Playà, E., Cendón, D. I., Travé, A., Chivas, A. R., and García, A. (2007). Non-marine evaporites with both inherited marine and continental signatures: the Gulf of Carpentaria, Australia, at ~70 ka. Sedimentary Geology 201, 267–285.
| Non-marine evaporites with both inherited marine and continental signatures: the Gulf of Carpentaria, Australia, at ~70 ka.Crossref | GoogleScholarGoogle Scholar |
Posada, D., and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.
| MODELTEST: testing the model of DNA substitution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlCltw%3D%3D&md5=84f91ead5424fe4266d2c65de2bd77eeCAS |
Pusey, B., Kennard, M., and Arthington, A. (2004). ‘Freshwater Fishes of North-Eastern Australia.’ (CSIRO Publishing: Melbourne.)
Schneider, S., Kuffer, J., Rossli, D., and Excoffier, L. (2000). ARLEQUIN 2.0. Software for population genetic data analysis. Biometry Laboratory, University of Geneva, Switzerland.
Slatkin, M., and Maddison, W. P. (1989). A cladistic measure of gene flow inferred from the phylogeny of alleles. Genetics 123, 603–613.
| 1:STN:280:DyaK3c%2Fpt12ktg%3D%3D&md5=4fe3eb53cd3fd5ea01da298d11a07b7fCAS |
Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) ver. 4.0b5. (Sinauer Associates: MA.)
Unmack, P. J. (2001). Biogeography of Australian freshwater fishes. Journal of Biogeography 28, 1053–1089.
| Biogeography of Australian freshwater fishes.Crossref | GoogleScholarGoogle Scholar |
Voris, H. K. (2000). Maps of Pleistocene sea levels in South East Asia: shorelines, river systems, time durations. Journal of Biogeography 27, 1153–1167.
| Maps of Pleistocene sea levels in South East Asia: shorelines, river systems, time durations.Crossref | GoogleScholarGoogle Scholar |
