Abstract
Oceans are home to much of the world's biodiversity, but we know little about the processes driving speciation in marine ecosystems with few geographical barriers to gene flow. Ecological speciation resulting from divergent natural selection between ecological niches can occur in the face of gene flow. Sister species in the young and ecologically diverse rockfish genus Sebastes coexist in the northeast Pacific, implying that speciation may not require geographical isolation. Here, I use a novel phylogenetic comparative analysis to show that rockfish speciation is instead associated with divergence in habitat depth and depth-associated morphology, consistent with models of parapatric speciation. Using the same analysis, I find no support for alternative hypotheses that speciation involves divergence in diet or life history, or that speciation involves geographic isolation by latitude. These findings support the hypothesis that rockfishes undergo ecological speciation on an environmental gradient.
References
- 1
Palumbi S. R. . 1994 Genetic divergence, reproductive isolation, and marine speciation. Ann. Rev. Ecol. Syst. 25, 547–572.doi:10.1146/annurev.es.25.110194.002555 (doi:10.1146/annurev.es.25.110194.002555). Crossref, Google Scholar - 2
Knowlton N., Weigt L. A., Solorzano L. A., Mills D. K.& Bermingham E. . 1993 Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science 260, 1629–1632.doi:10.1126/science.8503007 (doi:10.1126/science.8503007). Crossref, PubMed, Web of Science, Google Scholar - 3
Rocha L. A., Robertson D. R., Roman J.& Bown B. W. . 2005 Ecological speciation in tropical reef fishes. Proc. R. Soc. B 272, 573–579.doi:10.1098/2004.3005 (doi:10.1098/2004.3005). Link, Web of Science, Google Scholar - 4
Puebla O. . 2009 Ecological speciation in marine v. freshwater fishes. J. Fish Biol. 75, 960–996.doi:10.1111/j.1095-8649.2009.02358.x (doi:10.1111/j.1095-8649.2009.02358.x). Crossref, PubMed, Web of Science, Google Scholar - 5
Schluter D. . 2001 Ecological speciation. Trends Ecol. Evol. 16, 372–380.doi:10.1016/S0169-5347(01)02198-X (doi:10.1016/S0169-5347(01)02198-X). Crossref, PubMed, Web of Science, Google Scholar - 6
Pickett S. T. A.& Bazzaz F. A. . 1978 Organization of an assemblage of early successional species on a soil moisture gradient. Ecology 59, 1248–1255.doi:10.2307/1938238 (doi:10.2307/1938238). Crossref, Web of Science, Google Scholar - 7
Ackerly D. D., Schwilk D. W.& Webb C. O. . 2006 Niche evolution and adaptive radiation: testing the order of trait divergence. Ecology 87, S50–S61. Crossref, PubMed, Web of Science, Google Scholar - 8
Diamond J. M. . 1986 Evolution of ecological segregation in the New Guinea montane avifauna. Community ecology (eds, Diamond J. M.& Case T. J. ), pp. 98–125. Cambridge, MA: Harper and Row. Google Scholar - 9
Doebeli M.& Dieckmann U. . 2003 Speciation along environmental gradients. Nature 421, 259–264.doi:10.1038/nature01274 (doi:10.1038/nature01274). Crossref, PubMed, Web of Science, Google Scholar - 10
Richman A. D.& Price T. . 1992 Evolution of ecological differences in the Old World leaf warblers. Nature 355, 817–821.doi:10.1038/355817a0 (doi:10.1038/355817a0). Crossref, PubMed, Web of Science, Google Scholar - 11
Seehausen O., 2008 Speciation through sensory drive in cichlid fish. Nature 455, 620–626.doi:10.1038/nature07285 (doi:10.1038/nature07285). Crossref, PubMed, Web of Science, Google Scholar - 12
Dieckmann U.& Doebeli M. . 1999 On the origin of species by sympatric speciation. Nature 400, 354–357.doi:10.1038/22521 (doi:10.1038/22521). Crossref, PubMed, Web of Science, Google Scholar - 13
Van Doorn G. S., Edelaar P.& Weissing F. J. . 2009 On the origin of species by natural and sexual selection. Science 326, 1704–1707.doi:10.1126/science.1181661 (doi:10.1126/science.1181661). Crossref, PubMed, Web of Science, Google Scholar - 14
Barluenga M., Stölting K. N., Salzburger W., Muschick M.& Meyer A. . 2006 Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439, 719–723.doi:10.1038/nature04325 (doi:10.1038/nature04325). Crossref, PubMed, Web of Science, Google Scholar - 15
Bokma F. . 2008 Detection of ‘punctuated equilibrium’ by Bayesian estimation of speciation and extinction rates, ancestral character states, and rates of anagenetic and cladogenetic evolution on a molecular phylogeny. Evolution 62, 2718–2726.doi:10.1111/j.1558-5646.2008.00492.x (doi:10.1111/j.1558-5646.2008.00492.x). Crossref, PubMed, Web of Science, Google Scholar - 16
Hyde J. R.& Vetter R. D. . 2007 The origin, evolution, an diversification of rockfishes of the genus Sebastes (Cuvier). Mol. Phylogenet. Evol. 44, 790–811.doi:10.1016/j.ympev.2006.12.026 (doi:10.1016/j.ympev.2006.12.026). Crossref, PubMed, Web of Science, Google Scholar - 17
Love M. S., Yaklovich M.& Thorsteinson L. . 2002 The rockfishes of the northeast Pacific. Berkeley, CA: University of California Press. Google Scholar - 18
Hyde J. R., Kimbrell C. A., Budrick J. E., Lynn E. A.& Vetter R. D. . 2008 Cryptic speciation in the vermillion rockfish (Sebates miniatus) and the role of bathymetry in the speciation process. Mol. Ecol. 17, 1122–1136.doi:10.1111/j.1365-294X.2007.03653.x (doi:10.1111/j.1365-294X.2007.03653.x). Crossref, PubMed, Web of Science, Google Scholar - 19
Burford M. O. . 2009 Demographic history, geographical distribution and reproductive isolation of distinct lineages of blue rockfish (Sebastes mystinus), a marine fish with a high dispersal potential. J. Evol. Biol. 22, 1471–1486.doi:10.1111/j.1420-9101.2009.01760.x (doi:10.1111/j.1420-9101.2009.01760.x). Crossref, PubMed, Web of Science, Google Scholar - 20
Mangel M., Kindsvater H. K.& Bonsall M. B. . 2007 Evolutionary analysis of life span, competition, and adaptive radiation, motivated by the Pacific rockfishes (Sebastes). Evolution 61, 1208–1224.doi:10.1111/j.1558-5646.2007.00094.x (doi:10.1111/j.1558-5646.2007.00094.x). Crossref, PubMed, Web of Science, Google Scholar - 21
Johansson M. L., Banks M. A., Glunt K. D., Hassel-Finnegan H. M.& Buonaccorsi V. P. . 2008 Influence of habitat discontinuity, geographical distance, and oceanography on fine-scale population genetic structure of copper rockfish (Sebastes caurinus). Mol. Ecol. 17, 3051–3061.doi:10.1111/j.1365-294X.2008.03814.x (doi:10.1111/j.1365-294X.2008.03814.x). Crossref, PubMed, Web of Science, Google Scholar - 22
Barraclough T. G.& Vogler A. P. . 2000 Detecting the geographical pattern of speciation from species-level phylogenies. Am. Nat. 155, 419–434.doi:10.1086/303332 (doi:10.1086/303332). Crossref, PubMed, Web of Science, Google Scholar - 23
Hallacher L. E.& Roberts D. A. . 1985 Differential utilization of space and food by the inshore rockfishes (Scorpaenidae: Sebastes) of Carmel Bay, California. Environ. Biol. Fish. 12, 91–110.doi:10.1007/BF00002762 (doi:10.1007/BF00002762). Crossref, Web of Science, Google Scholar - 24
Ingram T.& Shurin J. B. . 2009 Trait-based assembly and phylogenetic structure in northeast Pacific rockfish assemblages. Ecology 90, 2444–2453.doi:10.1890/08-1841.1 (doi:10.1890/08-1841.1). Crossref, PubMed, Web of Science, Google Scholar - 25
Helvey M. . 1982 First observations of courtship behavior in rockfish, genus Sebastes. Copeia 1982, 763–770.doi:10.2307/1444084 (doi:10.2307/1444084). Crossref, Google Scholar - 26
Post D. M. . 2002 Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.doi:10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2 (doi:10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2). Crossref, Web of Science, Google Scholar - 27
Felsenstein J. . 1985 Phylogenies and the comparative method. Am. Nat. 125, 1–15.doi:10.1086/284325 (doi:10.1086/284325). Crossref, Web of Science, Google Scholar - 28
Felsenstein J. . 2008 Comparative methods with sampling error and within-species variation: contrasts revisited and revised. Am. Nat. 171, 713–725.doi:10.1086/587525 (doi:10.1086/587525). Crossref, PubMed, Web of Science, Google Scholar - 29
Freckleton R. P., Harvey P. H.& Pagel M. . 2002 Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712–726.doi:10.1086/343873 (doi:10.1086/343873). Crossref, PubMed, Web of Science, Google Scholar - 30
Harmon L. J., Weir J. T., Brock C. D., Glor R. E.& Challenger W. . 2008 GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129–131.doi:10.1093/bioinformatics/btm538 (doi:10.1093/bioinformatics/btm538). Crossref, PubMed, Web of Science, Google Scholar - 31
Pagel M. . 1997 Inferring evolutionary processes from phylogenies. Zool. Scripta 26, 331–348.doi:10.1111/j.1463-6409.1997.tb00423.x (doi:10.1111/j.1463-6409.1997.tb00423.x). Crossref, Web of Science, Google Scholar - 32
Nee S., Holmes E. C., May R. M.& Harvey P. H. . 1994 Extinction rates can be estimated from molecular phylogenies. Phil. Trans. R. Soc. Lond. B 344, 77–82.doi:10.1098/rstb.1994.0054 (doi:10.1098/rstb.1994.0054). Link, Web of Science, Google Scholar - 33
Rabosky D. L. . 2006 LASER: a maximum-likelihood toolkit for detecting temporal shifts in diversification rates. Evol. Bioinform. Online 2, 257–260. Crossref, Web of Science, Google Scholar - 34
Rabosky D. L. . 2010 Extinction rates should not be estimated from molecular phylogenies. Evolution 64, 1816–1824. Crossref, PubMed, Web of Science, Google Scholar - 35
O'Meara B. C., Ané C., Sanderson M. J.& Wainwright P. C. . 2006 Testing for different rates of continuous trait evolution using likelihood. Evolution 60, 922–933. Crossref, PubMed, Web of Science, Google Scholar - 36
R Development Core Team. 2008 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Google Scholar
- 37
Anderson D. R., Burnham K. P.& Thompson W. L. . 2000 Null hypothesis testing: problems, prevalence, and an alternative. J. Wildl. Manage. 64, 912–923. Crossref, Web of Science, Google Scholar - 38
Warrant E.& Locket N. A. . 2004 Vision in the deep sea. Biol. Rev. 79, 671–712.doi:10.1017/S1464793103006420 (doi:10.1017/S1464793103006420). Crossref, PubMed, Web of Science, Google Scholar - 39
Glor R. E., Kolbe J. T., Powell R., Larson A.& Losos J. B. . 2003 Phylogenetic analysis of ecological and morphological diversification in Hispaniolan trunk-ground anoles (Anolis cybotes group). Evolution 57, 2383–2397. Crossref, PubMed, Web of Science, Google Scholar - 40
Johns G. C.& Avise J. C. . 1998 Tests for ancient species flocks based on molecular phylogenetic appraisals of Sebastes rockfishes and other marine fishes. Evolution 52, 1135–1146.doi:10.2307/2411243 (doi:10.2307/2411243). Crossref, PubMed, Web of Science, Google Scholar - 41
Sivasundar A.& Palumbi S. R. . 2010 Parallel amino acid replacements in the rhodopsins of the rockfishes (Sebastes spp.) associated with shifts in habitat depth. J. Evol. Biol. 23, 1159–1169.doi:10.1111/j.1420-9101.2010.01977.x (doi:10.1111/j.1420-9101.2010.01977.x). Crossref, PubMed, Web of Science, Google Scholar