期刊论文详细信息
BMC Evolutionary Biology
Age estimates for an adaptive lake fish radiation, its mitochondrial introgression, and an unexpected sister group: Sailfin silversides of the Malili Lakes system in Sulawesi
Fabian Herder4  Ulrich K Schliewen2  Renny K Hadiaty1  Isabella Stöger2  Björn Stelbrink3 
[1]Museum Zoologicum Bogoriense, Ichthyology Laboratory, Division of Zoology, Research Center for Biology, Indonesian Institute of Sciences (LIPI), Jl, Raya Bogor Km 46, 16911 Cibinong, Indonesia
[2]Department of Ichthyology, Bavarian State Collection of Zoology (ZSM), Münchhausenstr. 21, D-81247 München, Germany
[3]Museum für Naturkunde Leibniz-Institute für Evolutions- und Biodiversitätsforschung an der Humboldt, Universität zu Berlin, Invalidenstr. 43, D-10115 Berlin, Germany
[4]Zoologisches Forschungsmuseum Alexander Koenig, Sektion Ichthyologie, Adenauerallee 160,D-53113 Bonn, Germany
关键词: Introgressive hybridization;    Adaptive radiation;    Biogeography;    Sulawesi;    Southeast Asia;    Mitochondrial DNA;    Molecular clock;   
Others  :  856607
DOI  :  10.1186/1471-2148-14-94
 received in 2014-04-17, accepted in 2014-04-22,  发布年份 2014
PDF
【 摘 要 】

Background

The Malili Lakes system in central Sulawesi (Indonesia) is a hotspot of freshwater biodiversity in the Wallacea, characterized by endemic species flocks like the sailfin silversides (Teleostei: Atherinomorpha: Telmatherinidae) radiation. Phylogenetic reconstructions of these freshwater fishes have previously revealed two Lake Matano Telmatherina lineages (sharpfins and roundfins) forming an ancient monophyletic group, which is however masked by introgressive hybridization of sharpfins with riverine populations. The present study uses mitochondrial data, newly included taxa, and different external calibration points, to estimate the age of speciation and hybridization processes, and to test for phylogeographic relationships between Kalyptatherina from ancient islands off New Guinea, Marosatherina from SW Sulawesi, and the Malili Lakes flock.

Results

Contrary to previous expectations, Kalyptatherina is the closest relative to the Malili Lakes Telmatherinidae, and Marosatherina is the sister to this clade. Palaeogeographic reconstructions of Sulawesi suggest that the closer relationship of the Malili Lakes radiation to Kalyptatherina might be explained by a 'terrane-rafting’ scenario, while proto-Marosatherina might have colonized Sulawesi by marine dispersal. The most plausible analysis conducted here implies an age of c. 1.9 My for the onset of divergence between the two major clades endemic to Lake Matano. Diversification within both lineages is apparently considerably more recent (c. 1.0 My); stream haplotypes present in the sharpfins are of even more recent origin (c. 0.4 My).

Conclusions

Sulawesi’s Telmatherinidae have most likely originated in the Sahul Shelf area, have possibly reached the island by both, marine dispersal and island/terrane-rafting, and have colonized the Malili Lakes system from rivers. Estimates for the split between the epibenthic sharpfins and the predominantly pelagic to benthopelagic roundfins in Lake Matano widely coincide with geological age estimates of this rift lake. Diversification within both clades clearly predates hybridization events with stream populations. For Lake Matano, these results support a scenario of initial benthic-pelagic divergence after colonization of the lake by riverine populations, followed by rapid radiation within both clades within the last 1 My. Secondary hybridization of stream populations with the sharpfins occurred more recently, and has thus most likely not contributed to the initial divergence of this benthic species flock.

【 授权许可】

   
2014 Stelbrink et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20140723034533748.pdf 1075KB PDF download
201KB Image download
50KB Image download
70KB Image download
129KB Image download
【 图 表 】

【 参考文献 】
  • [1]Schluter D: The Ecology of Adaptive Radiation. Oxford: Oxford University Press; 2000:1-284.
  • [2]Losos JB, Mahler DL: Adaptive radiation: The interaction of ecological opportunity, adaptation, and speciation. In Evolution since Darwin: the first 150 years. Edited by Bell MA, Futuyma DJ, Eanes WF, Levinton JS. Sunderland, MA: Sinauer Associates; 2010:381-420.
  • [3]Martin CH, Wainwright PC: Multiple fitness peaks on the adaptive landscape drive adaptive radiation in the wild. Science 2013, 339:208-211.
  • [4]Santos ME, Salzburger W: How cichlids diversify. Science 2012, 338:619-621.
  • [5]Bess EC, Catanach TA, Johnson KP: The importance of molecular dating analyses for inferring Hawaiian biogeographical history: A case study with bark lice (Psocidae: Ptycta). J Biogeogr 2014, 1:158-167.
  • [6]Lerner HRL, Meyer M, James HF, Hofreiter M, Fleischer RC: Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers. Curr Biol 2011, 21:1838-1844.
  • [7]Friedman M, Keck BP, Dornburg A, Eytan RI, Martin CH, Darrin C, Wainwright PC, Near TJ, Hulsey CD: Molecular and fossil evidence place the origin of cichlid fishes long after Gondwanan rifting. Proc R Soc London B 2013, 280:1-8.
  • [8]Schwarzer J, Misof B, Ifuta SN, Schliewen UK: Time and origin of cichlid colonization of the lower Congo rapids. PLoS One 2011, 6:e22380.
  • [9]Willis SC, Farias IP, Ortí G: Testing mitochondrial capture and deep coalescence in Amazonian cichlid fishes (Cichlidae: Cichla). Evolution 2014, 68:256-268.
  • [10]von Rintelen T, von Rintelen K, Glaubrecht M, Schubart CD, Herder F: Aquatic biodiversity hotspots in Wallacea: the species flocks in the ancient lakes of Sulawesi, Indonesia. In Biotic Evolution and Environmental Change in Southeast Asia. Edited by Gower DJ, Johnson KG, Richardson JE, Rosen BR, Rüber L, Williams ST. Cambridge: Cambridge University Press; 2012:290-315.
  • [11]Herder F, Schwarzer J, Pfaender J, Hadiaty RK, Schliewen UK: Preliminary checklist of sailfin silversides (Teleostei: Telmatherinidae) in the Malili Lakes of Sulawesi (Indonesia), with a synopsis of systematics and threats. Verhandlungen der Gesellschaft für Ichthyologie 2006, 5:139-163.
  • [12]Gray SM, Dill LM, Tantu FY, Loew ER, Herder F, McKinnon JS: Environment-contingent sexual selection in a colour polymorphic fish. Proc R Soc London B 2008, 275:1785-1791.
  • [13]Pfaender J, Gray SM, Rick IP, Chapuis S, Hadiaty RK FH: Spectral data reveal unexpected cryptic colour polymorphism in female sailfin silverside fish from ancient Lake Matano. Hydrobiologia 2013. doi:10.1007/s10750-013-1557-y
  • [14]Pfaender J, Schliewen UK, Herder F: Phenotypic traits meet patterns of resource use in the radiation of “sharpfin” sailfin silverside fish in Lake Matano. Evol Ecol 2010, 24:957-974.
  • [15]Pfaender J, Miesen FW, Hadiaty RK, Herder F: Adaptive speciation and sexual dimorphism contribute to diversity in form and function in the adaptive radiation of Lake Matano’s sympatric roundfin sailfin silversides. J Evol Biol 2011, 24:2329-2345.
  • [16]Cerwenka AF, Wedekind JD, Hadiaty RK, Schliewen UK, Herder F: Alternative egg-feeding tactics in Telmatherina sarasinorum, a trophic specialist of Lake Matano’s evolving sailfin silversides fish radiation. Hydrobiologia 2012, 693:131-139.
  • [17]Herder F, Nolte AW, Pfaender J, Schwarzer J, Hadiaty RK, Schliewen UK: Adaptive radiation and hybridization in Wallace’s dreamponds: evidence from sailfin silversides in the Malili lakes of Sulawesi. Proc R Soc London B 2006, 273:2209-2217.
  • [18]Schwarzer J, Herder F, Misof B, Hadiaty RK, Schliewen UK: Gene flow at the margin of Lake Matano’s adaptive sailfin silverside radiation: Telmatherinidae of River Petea in Sulawesi. Hydrobiologia 2008, 615:201-213.
  • [19]Herder F, Schliewen UK: Beyond sympatric speciation: radiation of sailfin silverside fishes in the Malili lakes (Sulawesi). In Evolution in Action. Edited by Glaubrecht M. Berlin: Springer; 2010:465-483.
  • [20]Aarn WI, Ivantsoff W, Kottelat M: Phylogenetic analysis of telmatherinidae (Teleostei: Atherinomorpha), with description of Marosatherina, a new genus from Sulawesi. Ichthyol Explor Freshw 1998, 9:311-323.
  • [21]Roy D, Paterson G, Hamilton PB, Heath DD, Haffner GD: Resource-based adaptive divergence in the freshwater fish Telmatherina from Lake Matano, Indonesia. Mol Ecol 2007, 16:35-48.
  • [22]Sparks JS, Smith WL: Phylogeny and biogeography of the Malagasy and Australasian rainbowfishes (Teleostei: melanotaenioidei): gondwanan vicariance and evolution in freshwater. Mol Phylogenet Evol 2004, 33:719-734.
  • [23]Setiamarga DHE, Miya M, Yamanoue Y, Mabuchi K, Satoh TP, Inoue JG, Nishida M: Interrelationships of Atherinomorpha (medakas, flyingfishes, killifishes, silversides, and their relatives): the first evidence based on whole mitogenome sequences. Mol Phylogenet Evol 2008, 49:598-605.
  • [24]Unmack PJ, Allen GR, Johnson JB: Phylogeny and biogeography of rainbowfishes (Melanotaeniidae) from Australia and New Guinea. Mol Phylogenet Evol 2013, 67:15-27.
  • [25]Parenti LR: Relationships of atherinomorph fishes (Teleostei). Bull Mar Sci 1993, 52:170-196.
  • [26]Kocher TD, Conroy JA, McKaye KR, Stauffer JR, Lockwood SF: Evolution of NADH dehydrogenase subunit 2 in East African cichlid fish. Mol Phylogenet Evol 1995, 4:420-432.
  • [27]Rüber L, Van Tassell JL, Zardoya R: Rapid speciation and ecological divergence in the American seven-spined gobies (Gobiidae, Gobiosomatini) inferred from a molecular phylogeny. Evolution 2003, 57:1584-1598.
  • [28]Katoh K, Toh H: Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 2008, 9:286-298.
  • [29]Vaidya G, Lohman DJ, Meier R: SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 2011, 27:171-180.
  • [30]Stamatakis A, Hoover P, Rougemont J: A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 2008, 57:758-771.
  • [31]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
  • [32]Bloom DD, Unmack PJ, Gosztonyi AE, Piller KR, Lovejoy NR: It’s a family matter: molecular phylogenetics of Atheriniformes and the polyphyly of the surf silversides (Family: Notocheiridae). Mol Phylogenet Evol 2012, 62:1025-1030.
  • [33]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-1256.
  • [34]Drummond AJ, Suchard MA, Xie D, Rambaut A: Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012, 29:1969-1973.
  • [35]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). New Orleans; 2010:1-8.
  • [36]Setiamarga DHE, Miya M, Yamanoue Y, Azuma Y, Inoue JG, Ishiguro NB, Mabuchi K, Nishida M: Divergence time of the two regional medaka populations in Japan as a new time scale for comparative genomics of vertebrates. Biol Lett 2009, 5:812-816.
  • [37]Hill KC, Hall R: Mesozoic-Cenozoic evolution of Australia’s New Guinea margin in a west Pacific context. Geol Soc Aust Spec Publ Soc Am Spec Pap 2003, 22/372:265-289.
  • [38]Rambaut A, Drummond AJ: Tracer v. 1.5.. 2007. Available from http://tree.bio.ed.ac.uk/software/tracer webcite
  • [39]Saeed B, Ivantsoff W, Crowley LELM: Systematic relationships of atheriniform fishes within division 1 of the series Atherinomorpha (Actinopterygii) with relevant historical perspectives. Vopr Ichtiologii 1994, 34:1-32.
  • [40]Near TJ, Dornburg A, Eytan RI, Keck BP, Smith WL, Kuhn KL, Moore JA, Price SA, Burbrink FT, Friedman M, Wainwright PC: Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes. Proc Natl Acad Sci USA 2013, 110:12738-12743.
  • [41]Vaillant JJ, Haffner GD, Cristecu ME: The ancient lakes of Indonesia: towards integrated research on speciation. Integr Comp Biol 2011, 51:634-643.
  • [42]Wilson MEJ, Moss SJ: Cenozoic palaeogeographic evolution of Sulawesi and Borneo. Palaeogeogr Palaeoclimatol Palaeoecol 1999, 145:303-337.
  • [43]Saeed B, Ivantsoff W: Kalyptatherina, the first telmatherinid genus known outside of Sulawesi. Ichthyol Explor Freshw 1991, 2:227-238.
  • [44]Parenti LR: Phylogenetic systematics and biogeography of phallostethid fishes (Atherinomorpha, Phallostethidae) of Northwestern Borneo, with description of a new species. Copeia 1996, 1996:703-712.
  • [45]Parenti LR, Louie KD: Neostethus djajaorum, new species, from Sulawesi, Indonesia, the first phallostethid fish (Teleostei: Atherinomorpha) known from east of Wallace’s line. Raffles Bull Zool 1998, 43:139-150.
  • [46]Moss SJ, Wilson MEJ: Biogeographic implications of the Tertiary palaeogeographic evolution of Sulawesi and Borneo. In Biogeography and Geological Evolution of SE Asia. Edited by Hall R, Holloway JD. Leiden: Backhuys Publishers; 1998:133-163.
  • [47]Hall R: Southeast Asia’s changing palaeogeography. Blumea 2009, 54:148-161.
  • [48]Spakman W, Hall R: Surface deformation and slab–mantle interaction during Banda arc subduction rollback. Nat Geosci 2010, 3:562-566.
  • [49]Lohman DJ, de Bruyn M, Page T, von Rintelen K, Hall R, Ng PKL, Shih HT, Carvalho GR, von Rintelen T: Biogeography of the Indo-Australian archipelago. Annu Rev Ecol Evol Syst 2011, 42:205-226.
  • [50]Stelbrink B, Albrecht C, Hall R, von Rintelen T: The biogeography of Sulawesi revisited: is there evidence for a vicariant origin of taxa on Wallace’s “anomalous island”? Evolution 2012, 66:2252-2271.
  • [51]Hall R: Late Jurassic-Cenozoic reconstructions of the Indonesian region and the Indian Ocean. Tectonophysics 2012, 570–571:1-41.
  • [52]Hall R: Sundaland and Wallacea: geology, plate tectonics and palaeogeography. In Biotic Evolution and Environmental Change in Southeast Asia. Edited by Gower DJ, Johnson KG, Richardson JE, Rosen BR, Rüber L, Williams ST. Cambridge: Cambridge University Press; 2012:32-78.
  • [53]Abell R, Thieme ML, 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 JV, Heibel TJ, Wikramanayake E, Olson D, Lopéz HL, Reis RE, Lundberg JG, Sabaj Pérez MH, Petry P: Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. Bioscience 2008, 58:403-414.
  • [54]McGuigan K: Phylogenetic relationships and historical biogeography of melanotaeniid fishes in Australia and New Guinea. Mar Freshw Res 2000, 51:713-723.
  • [55]Walter RP, Hogan JD, Haffner GD, Heath DD: Genetic structure and connectivity among lake populations of threatened Paratherina sailfin silversides from Sulawesi, Indonesia. Conserv Genet 2011, 12:1387-1393.
  • [56]Kottelat M: Sailfin silversides (Pisces: Telmatherinidae) of Lakes Towuti, Mahalona and Wawontoa (Sulawesi, Indonesia) with descriptions of two new genera and two new species. Ichthyol Explor Freshw 1990, 1:35-54.
  • [57]von Rintelen T, Wilson AB, Meyer A, Glaubrecht M: Escalation and trophic specialization drive adaptive radiation of viviparous freshwater gastropods in the ancient lakes on Sulawesi, Indonesia. Proc R Soc London B 2004, 271:2541-2549.
  • [58]Stelbrink B, Stöger I, Hadiaty RK, Schliewen UK, Herder F: Age estimates for an adaptive lake fish radiation, its mitochondrial introgression, and an unexpected sister group: Sailfin silversides of the Malili Lakes system in Sulawesi. Dryad Digital Repository 2014. doi:10.5061/dryad.8dh7r at http://datadryad.org webcite
  • [59]Miya M, Takeshima H, Endo H, Ishiguro NB, Inoue JG, Mukai T, Satoh TP, Yamaguchi M, Kawaguchi A, Mabuchi K, Shirai SM, Nishida M: Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol Phylogenet Evol 2003, 26:121-138.
  文献评价指标  
  下载次数:41次 浏览次数:25次