Molecular signatures of Pleistocene sea-level changes that affected connectivity among freshwater shrimp in Indo-Australian waters
MARK DE BRUYN
School of Biological Sciences, University of Durham, South Road, Durham, DH1 3LE, UK,
School of Natural Resource Sciences, Queensland University of Technology, GPO Box 2434, Brisbane, Qld 4001, Australia
Search for more papers by this authorPETER B MATHER
School of Natural Resource Sciences, Queensland University of Technology, GPO Box 2434, Brisbane, Qld 4001, Australia
Search for more papers by this authorMARK DE BRUYN
School of Biological Sciences, University of Durham, South Road, Durham, DH1 3LE, UK,
School of Natural Resource Sciences, Queensland University of Technology, GPO Box 2434, Brisbane, Qld 4001, Australia
Search for more papers by this authorPETER B MATHER
School of Natural Resource Sciences, Queensland University of Technology, GPO Box 2434, Brisbane, Qld 4001, Australia
Search for more papers by this authorAbstract
A major paradigm in evolutionary biology asserts that global climate change during the Pleistocene often led to rapid and extensive diversification in numerous taxa. Recent phylogenetic data suggest that past climatic oscillations may have promoted long-distance marine dispersal in some freshwater crustacea from the Indo-Australian Archipelago (IAA). Whether this pattern is common, and whether similar processes are acting on diversification below the species level is unknown. We used nuclear and mitochondrial molecular variation in a freshwater-dependent decapod crustacean (Macrobrachium rosenbergii), sampled widely from the IAA, to assess the impact of Pleistocene sea-level changes on lineage diversification in this species. Fitting of an isolation with migration model enabled us to reject ongoing migration among lineages, and results indicate that isolation among both mainland–mainland and mainland–island lineages arose during the mid-Pleistocene. Our data suggest a scenario of widespread marine dispersal during Pleistocene glacial maxima (in support of the ‘Pleistocene marine dispersal hypothesis’) when sea levels were low, and geographical distances between fresh watersheds were greatly reduced, followed by increased isolation as sea levels subsequently rose.
References
- Archbold NW, Pigram CJ, Ratman N, Hakim S (1982) Indonesian Permian Brachipod fauna and Gondwana — South-East Asia relationships. Nature, 296, 556–558.
- Audley-Charles MG (1983) Reconstruction of eastern Gondwanaland. Nature, 306, 48–50.
- Avise JC (2000) Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, Massachusetts.
10.1046/j.1365-294X.2003.01731.x Google Scholar
- Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.
- Bennett KJ (1997) Evolution and Ecology: the Pace of Life. Cambridge University Press, Cambridge, UK.
- Bermingham E, Avise JC (1986) Molecular zoogeography of freshwater fishes in the southeastern United States. Genetics, 113 (4), 939–965.
- Birky CW, Fuerst P, Maruyama T (1989) Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics, 121, 613–627.
- Bohonak AJ (2002) ibd (isolation by distance): a program for analyses of isolation by distance. Journal of Heredity, 93, 153–154.
- Brandon-Jones D (1998) Pre-glacial Bornean primate impoverishment and Wallace's Line. In: Biogeography and Geological Evolution of SE Asia (eds JD Holloway, R Hall), pp. 393–404. Backhuys Publishers, Leiden, The Netherlands.
- Briggs JC (2000) Centrifugal speciation and centres of origin. Journal of Biogeography, 27, 1183–1188.
- Brown RM, Guttman SI (2002) Phylogenetic systematics of the Rana signata complex of Philippine and Bornean stream frogs: reconsideration of Huxley's modification of Wallace's Line at the Oriental–Australian faunal zone interface. Biological Journal of the Linnean Society, 76, 393–461.
- De Bruyn M, Wilson JC, Mather PB (2004a) Huxley's line demarcates extensive genetic divergence between eastern and western forms of the giant freshwater prawn, Macrobrachium rosenbergii. Molecular Phylogenetics and Evolution, 30, 251–257.
- De Bruyn M, Wilson JC, Mather PB (2004b) Reconciling geography and genealogy: phylogeography of giant freshwater prawns from the Lake Carpentaria region. Molecular Ecology, 13, 3515–3526.
- De Bruyn M, Nugroho E, Hossain Md. M, Wilson JC, Mather PB (2005) Phylogeographic evidence for the existence of an ancient biogeographic barrier: the Isthmus of Kra Seaway. Heredity, 94, 370–378.
- Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. American Journal of Human Genetics, 19, 233–257.
- Chand V, De Bruyn M, Mather PB (2005) Microsatellite loci in the eastern form of the giant freshwater prawn (Macrobrachium rosenbergii). Molecular Ecology Notes, 5, 308–310.
- Chappell J, Shackleton NJ (1986) Oxygen isotopes and sea level. Nature, 324, 137–140.
- Clement M, Posada D, Crandall KA (2000) tcs: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.
- Coope GR (1994) The response of insect faunas to glacial-interglacial climatic fluctuations. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 344, 19–26.
- Cowie RH, Holland BS (2006) Dispersal is fundamental to biogeography and the evolution of biodiversity on oceanic islands. Journal of Biogeography, 33, 193–198.
- Darwin C (1859) The Origin of Species. John Murray, London.
- Davis MB, Shaw RG (2001) Range shifts and adaptive responses to Quaternary climate change. Science, 292, 673–679.
- Epica Community Members (2004) Eight glacial cycles from an Antarctic ice core. Nature, 429, 623–628.
- Felsenstein J (1993) phylip Version. 3.5 (Phylogeny Inference Package). University of Washington, Seattle.
- Gathorne-Hardy FJ, Syaukani Davies RG, Eggleton P, Jones DT (2002) Quaternary rainforest refugia in south-east Asia: using termites (Isoptera) as indicators. Biological Journal of the Linnean Society, 75, 453–466.
- Goudet J (1995) fstat, version 1.2: a computer program to calculate F-statistics. Journal of Heredity, 86, 485–486.
- Guthrie RD (2003) Rapid body size decline in Alaskan Pleistocene horses before extinction. Nature, 426, 169–171.
- Hall R (1998) The plate tectonics of Cenozoic SE Asia and the distribution of land and sea. In: Biogeography and Geological Evolution of SE Asia (eds R Hall, JD Holloway), pp. 99–131. Backhuys Publishers, Leiden, The Netherlands.
- Hall R (2001) Cenozoic reconstructions of SE Asia and the SW Pacific: changing patterns of land and sea. In: Faunal and Floral Migrations and Evolution in SE Asia-Australasia (eds I Metcalfe, JMB Smith, M Morwood, I Davidson), pp. 35–56. A.A. Balkema Publishers, Lisse, The Netherlands.
- Hall R (2002) Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations. Journal of Asian Earth Sciences, 20, 353–431.
- Hallam A (1984) Pre-Quaternary sea-level changes. Annual Review of Earth and Planetary Sciences, 12, 205–243.
- Heaney LR (1986) Biogeography of mammals in SE Asia: estimates of rates of colonization, extinction and speciation. Biological Journal of the Linnean Society, 28, 127–165.
- Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature, 405, 907–913.
- Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics, 167, 747–760.
- Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Molecular Biology and Evolution, 22 (7), 1561–1568.
- Hofreiter M, Serre D, Rohland N et al . (2003) Lack of phylogeography in European mammals before the last glaciation. Proceedings of the National Academy of Sciences, USA, 101, 12963–12968.
- Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics, 111, 147–164.
- Johnson DS (1973) Notes on some species of the genus Macrobrachium (Crustacea: Decapoda: Caridea: Palaemonidae). Journal of the Singapore National Academy of Sciences, USA, 3 (3), 273–291.
- Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proceedings of the Royal Society of London. Series B, Biological Sciences, 265, 2257–2263.
- Kumar S, Tamura K, Nei M (2004) mega3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics, 5, 150–163.
- Lindenfelser ME (1984) Morphometric and allozymic congruence: evolution in the prawn Macrobrachium rosenbergii (Decapoda: Palaemonidae). Systematic Zoology, 33, 195–204.
- Lisiecki LE, Raymo ME (2005) A Pliocene-Pleistocene stack of 57 globally distributed benthic δ18O records. Paleoceanography, 20, PA1003, doi: 10.1029/2004PA001071.
- McDonald JH, Kreitman ME (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature, 351, 652–654.
- Meyers G, Bailey RJ, Worby AP (1995) Geostrophic transport of Indonesian Throughflow. Deep Sea Research, 42 (7), 1163–1174.
- Mittermeier RA, Myers N, Robles-Gil P, Mittermeier CG (1999) Hotspots: Earth's Biologically Richest and Most Endangered Terrestrial Ecoregions. Cemex, Conservation International, Agrupacion, Sierra Madre.
- Morrison CL, Rió R, Duffy JE (2004) Phylogenetic evidence for an ancient rapid radiation of Caribbean sponge-dwelling snapping shrimps (Synalpheus). Molecular Phylogenetics and Evolution, 30, 563–581.
- Moss SJ, Wilson MEJ (1998) Biogeographic implications of the Tertiary palaeogeographic evolution of Sulawesi and Borneo. In: Biogeography and Geological Evolution of SE Asia (eds R Hall, JD Holloway), pp. 133–163. Backhuys Publishers, Leiden, The Netherlands.
10.1086/282971 Google Scholar
- Murphy NP, Austin CM (2005) Phylogenetic relationships of the globally distributed freshwater prawn genus Macrobrachium (Crustacea: Decapoda: Palaemonidae): biogeography, taxonomy and the convergent evolution of abbreviated larval development. Zoologica Scripta, 34, 187–197.
- Myers N, Mittermeier RA, Mittermeier CG, De Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853–858.
- Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics, 158, 885–896.
- Page TJ, Von Rintelen K, Hughes JM (2007) An island in the stream: Australia's place in the cosmopolitan world of Indo-West Pacific freshwater shrimp (Decapoda: Atyidae: Caridina). Molecular Phylogenetics and Evolution, 43, 645–659.
- Palsbøll PJ, Bėrubė M, Aguilar A, Notarbartolo-Di-Sciara G, Nielsen R (2004) Discerning between recurrent gene flow and recent divergence under a finite-site mutation model applied to North Atlantic and Mediterranean Sea fin whale (Balaenoptera physalus) populations. Evolution, 58, 670–675.
- Penny D (2005) Relativity for molecular clocks. Nature, 436, 183–184.
- Posada D, Crandall KA (1998) modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817–818.
- Raymond M, Rousset F (1995) genepop (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248–249.
- Ronquist F, Huelsenbeck JP (2003) mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
- Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics, 145, 1219–1228.
- Sandifer PA, Hopkins JS, Smith TIJ (1975) Observations on salinity tolerance and osmoregulation in laboratory-reared Macrobrachium rosenbergii postlarvae (Crustacea: Caridea). Aquaculture, 6, 103–114.
- Schmidt HA, Strimmer K, Vingron M, Von Haeseler A (2002) tree-puzzle: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics, 18, 502–504.
- Schmitt LH, Kitchener DJ, How RA (1995) A genetic perspective of mammalian variation and evolution in the Indonesian Archipelago: biogeographic correlates in the fruit bat genus Cynopterus. Evolution, 49, 399–412.
- Schneider SD, Roessli D, Excoffier L (2000) arlequin, Version 2.0: A Software for Population Genetic Data Analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva.
- Shapiro B, Drummond AJ, Rambaut A et al . (2004) Rise and fall of the Beringian steppe bison. Science, 306, 1561–1565.
- Short JW (2004) A revision of Australian river prawns, Macrobrachium (Crustacea: Decapoda: Palaemonidae). Hydrobiologia, 525, 1–100.
- Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512–526.
- Unmack PJ (2001) Biogeography of Australian freshwater fishes. Journal of Biogeography, 28, 1053–1089.
- Voris HK (2000) Maps of Pleistocene sea levels in South East Asia: shorelines, river systems, time durations. Journal of Biogeography, 27, 1153–1167.
- Wallace AR (1862) Narrative of search after birds of paradise. Proceedings of the Zoological Society of London, 1862, 153–161.
10.1111/j.1469-7998.1862.tb06487.x Google Scholar
- Wallace AR (1869) The Malay Archipelago. Macmillan, London.
10.2307/3025162 Google Scholar
- Wowor D (2004) A systematic revision of the freshwater prawns of the genus Macrobrachium (Crustacea: Decapoda: Caridea: Palaemonidae). PhD Thesis, National University of Singapore, Singapore.