August 2012, 12:142,
Open Access This content is freely available online to anyone, anywhere at any time.
Date: 09 Aug 2012
Pleistocene climate change promoted rapid diversification of aquatic invertebrates in Southeast Australia
The Pleistocene Ice Ages were the most recent geohistorical event of major global impact, but their consequences for most parts of the Southern hemisphere remain poorly known. We investigate a radiation of ten species of Sternopriscus, the most species-rich genus of epigean Australian diving beetles. These species are distinct based on genital morphology but cannot be distinguished readily by mtDNA and nDNA because of genotype sharing caused by incomplete lineage sorting. Their genetic similarity suggests a Pleistocene origin.
We use a dataset of 3858 bp of mitochondrial and nuclear DNA to reconstruct a phylogeny of Sternopriscus using gene and species trees. Diversification analyses support the finding of a recent rapid speciation event with estimated speciation rates of up to 2.40 species per MY, which is considerably higher than the proposed average rate of 0.16 species per MY for insects. Additionally, we use ecological niche modeling and analyze data on habitat preferences to test for niche divergence between species of the recent Sternopriscus radiation. These analyses show that the species can be characterized by a set of ecological variables referring to habitat, climate and altitude.
Our results suggest that the repeated isolation of populations in glacial refugia might have led to divergent ecological adaptations and the fixation of morphological traits supporting reproductive isolation and therefore may have promoted speciation. The recent Sternopriscus radiation fulfills many characteristics of a species flock and would be the first described example of an aquatic insect species flock. We argue that the species of this group may represent a stage in speciation past the species flock condition because of their mostly broad and often non-overlapping ranges and preferences for different habitat types.
Barraclough TG, Vogler AP, Harvey PH: Revealing the factors that promote speciation. Phil Trans R Soc B 1998, 353:241-249.CrossRef
Mittelbach GG, Schemske DW, Cornell HV, Allen AP, Brown JM, Bush MB, Harrison SP, Hurlbert AH, Knowlton N, Lessios HA, McCain CM, McCune AR, McDade LA, McPeek MA, Near TJ, Price TD, Ricklefs RE, Roy K, Sax DF, Schluter D, Sobel JM, Turelli M: Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol Lett 2007, 10:315-331.PubMedCrossRef
Benton MJ: When life nearly died: The greatest mass extinctions of all time. London, UK: Thames & Hudson; 2005.
Beheregaray LB: Twenty years of phylogeography: the state of the field and the challenges for the Southern Hemisphere. Mol Ecol 2008, 17:3754-3774.PubMed
Jansson R, Dynesius M: The fate of clades in a world of recurrent climatic change: Milankovitch oscillations and evolution. Ann Rev Ecol Syst 2002, 33:741-777.CrossRef
Frakes LA, McGowran B, Bowler JM: Evolution of Australian Environments. In Fauna of Australia. General Articles. 1A edition. Edited by: Dyne GR, Walton DW. Canberra: Australian Government Publishing Service; 1987:1-17.
Leys R, Watts CHS, Cooper SJB, Humphreys WF: Evolution of subterranean Diving Beetles (Coleoptera: Dytiscidae: Hydroporini, Bidessini) in the arid zone of Australia. Evolution 2003, 57:2819-2834.PubMed
Coyne JA, Orr HA: Speciation. Sunderland, MA: Sinauer Ass; 2004.
Funk DJ, Omland KE: Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Evol Syst 2003, 34:397-423.CrossRef
Degnan JH, Rosenberg NA: Discordance of species trees with their most likely gene trees. PLoS Genetics 2006, 2:762-768.CrossRef
Graham CH, Ron SR, Santos JC, Schneider CJ, Moritz C: Integrating phylogenetics and environmental niche models to explore speciation mechanisms in dendrobatid frogs. Evolution 2004, 58:1781-1793.PubMed
Soberón J, Peterson AT: Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodiv Infor 2005, 2:1-10.
Guisan A, Zimmermann N: Predictive habitat distribution models in ecology. Ecol Model 2000, 135:147-189.CrossRef
Kozak KH, Wiens JJ: Does niche conservatism promote speciation? A case study in North American salamanders. Evolution 2006, 60:2604-2621.PubMed
Hendrich L, Watts CHS: Taxonomic revision of the Australian genus Sternopriscus Sharp, 1882 (Coleoptera: Dytiscidae, Hydroporinae). Koleopterol Rdsch 2004, 74:75-142.
Hendrich L, Watts CHS: Update of Australian Sternopriscus Sharp, 1882 with description of three new species (Coleoptera: Dytiscidae: Hydroporinae). Koleopterol Rdsch 1882, 77:49-59.
Abell R, Thieme M, Revenga C, Bryer M, Kottelat M, Bogutskaya N, Coad B, Mandrak N, Contreras-Balderas S, Bussing W, Stiassny MLJ, Skelton P, Allen GR, Unmack P, Naseka A, Ng R, Sindorf N, Robertson J, Armijo E, Higgins J, Heibel TJ, Wikramanayake E, Olson D, Lopez HL, Reis RE, Lundberg JG, Sabaj Perez MH, Petry P: Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. BioScience 2008, 58:403-414.CrossRef
Rambaut A, Drummond AJ: Tracer v1.4. 2007. http://beast.bio.ed.ac.uk/Tracer
Silvestro D, Michalak I: raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 2012. in press
Goloboff PA, Farris JS, Nixon KC: TNT, a free program for phylogenetic analysis. Cladistics 2008, 24:774-786.CrossRef
Rabosky DL: LASER, a maximum likelihood toolkit for detecting temporal shifts in diversification rates from molecular phylogenies. Evol Bioinform Online 2006, 2:247-250.
Rabosky DL: Likelihood methods for detecting temporal shifts in diversification rates. Evolution 2006, 60:1152-1164.PubMed
Fu YH: Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 1997, 147:915-925.PubMed
Tajima F: Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989, 123:585-595.PubMed
Excoffier L, Lischer HEL: Arlequin suite ver 3.5: A new series of programs to performpopulation genetics analyses under Linux and Windows. Mol Ecol Res 2010, 10:564-567.CrossRef
Teacher AGF, Griffiths DJ: HapStar: Automated haplotype network layout and visualisation. Mol Ecol Res 2011, 11:151-153.CrossRef
Joly S, McLenachan PA, Lockhart PJ: A statistical approach for distinguishing hybridization and incomplete lineage sorting. Am Nat 2009, 174:54-70.CrossRef
Joyce DA, Lunt DH, Genner MJ, Turner GF, Bills R, Seehausen O: Repeated colonization and hybridization characterize the Lake Malawi cichlid fish species flock. Curr Biol 2011, 21:108-109.CrossRef
Nylander JAA: MrModeltest v2. Uppsala University: Program distributed by the author. Evolutionary Biology Centre; 2004.
Joly S: JML: testing hybridization from species trees. Mol Ecol Res 2012, 12:179-184.CrossRef
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A: Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 2005, 2:1965-1978.CrossRef
Phillips SJ, Anderson RP, Schapire RE: Maximum entropy modelling of species geographic distributions. Ecol Model 2006, 190:231-259.CrossRef
Warren DL, Glor RE, Turelli M: ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 2010, 33:607-611.CrossRef
Rogers AR, Harpending H: Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 1992, 9:552-569.PubMed
Salzbuger W, Baric S, Sturmbauer C: Speciation via introgressive hybridization in East African cichlids? Molec Ecol 2002, 11:619-625.CrossRef
Vedenina V: Variation in complex courtship traits across a hybrid zone between grasshopper species of the Chorthippus albomarginatus group. Biol J Linn Soc 2011, 102:275-291.CrossRef
Usami T, Yokoyama J, Kubota K, Kawata M: Genital lock-and-key system and premating isolation by mate preference in Carabid beetles (Carabus subgenus Ohomopterus). Biol J Linn Soc 2006, 87:145-154.CrossRef
Schluter D: The ecology of adaptive radiation. Oxford, UK: Oxford University Press; 2000.
Nitecki MH: Evolutionary innovations. Chicago, IL: The University of Chicago Press; 2000.
Farrell BD, Mitter C: Adaptive radiation in insects and plants: time and opportunity. Am Zool 1994, 34:57-69.
Simpson GG: The major features of evolution. New York: Columbia University Press; 1953.
Grant PR: Ecology and evolution of Darwin's Finches. Princeton, NJ: Princeton University Press; 1984.
Ribera I, Vogler AP: Habitat type as a determinant of species range sizes: the example of lotic-lentic differences in aquatic Coleoptera. Biol J Lin Soc 2000, 71:33-52.
Greenwood PH: What is a species flock? In Evolution of fish species flocks. Edited by: Echelle AA, Kornfield I. Maine: Orono Press; 1994:13-19.
Schön I, Martens K: Adaptive, pre-adaptive and non-adaptive components of radiations in ancient lakes: a review. Org Divers Evol 2004, 4:137-156.CrossRef
Albrecht C, Trajanovski S, Kuhna K, Streita B, Wilke T: Rapid evolution of an ancient lake species flock: Freshwater limpets (Gastropoda: Ancylidae) in the Balkan Lake Ohrid. Org Divers Evol 2006, 6:294-307.CrossRef
Miller MA, Pfeiffer W, Schwartz T: Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010. New Orleans, Louisiana; 2010:1-8. http://www.ngbw.org/ee/index.php/portal/cite_us CrossRef
- Pleistocene climate change promoted rapid diversification of aquatic invertebrates in Southeast Australia
- Open Access
- Available under Open Access This content is freely available online to anyone, anywhere at any time.
BMC Evolutionary Biology
- Online Date
- August 2012
- Online ISSN
- BioMed Central
- Additional Links
- Author Affiliations
- 1. Zoologische Staatssammlung, Münchhausenstr. 21, Munich, 81247, Germany
- 2. Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA
- 3. School of Biological Sciences, University of Bristol, Woodland Road, Bristol, BS8 1UG, UK
- 4. GeoBioCenter, Ludwig-Maximilians-Universität, Richard-Wagner-Str. 10, Munich, 80333, Germany