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Incipient speciation within a subgenus of rockfish (Sebastosomus) provides evidence of recent radiations within an ancient species flock

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Abstract

The high frequency of speciation events associated with species flocks (i.e., radiations of closely related species) provides invaluable insight into the speciation process. Investigations of the speciation process in the marine environment are rare, and therefore, the genetic analysis of the rockfish genus Sebastes, considered an ancient marine species flock, provides an opportunity to investigate this process in the sea. Using both mitochondrial and nuclear markers, we analyzed five closely related species within the rockfish subgenus Sebastosomus. Our goal was to understand the evolutionary history and genetic relationships among species within this group and to provide evidence of recent speciation events within the subgenus. In the genetic analysis of the subgenus, we found different stages of the speciation process, with greater genetic divergences among three of the five species, evidence of recent divergence between two of the five species, Sebastes entomelas and S. mystinus, and significant genetic divergence between two lineages within S. mystinus revealing a signature of incipient speciation. We also found frequency differences of the two S. mystinus lineages among sample locations and found no evidence of introgression between the lineages at the location where both coexist. Although Sebastes is an example of an ancient species flock, this study provides evidence of ongoing speciation within the genus and reveals stages of this process from incipient to distinct species.

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References

  • Alesandrini S, Bernardi G (1999) Ancient species flocks and recent speciation events: what can rockfish teach us about cichlids (and vice versa)? J Mol Evol 49:814–818

    PubMed  CAS  Google Scholar 

  • Avise JC, Neigel JE, Arnold J (1984) Demographic influences on mitochondrial-DNA lineage survivorship in animal populations. J Mol Evol 20:99–105

    Article  PubMed  CAS  Google Scholar 

  • Barluenga M, Stolting KN, Salzburger W, Muschick M, Meyer A (2006) Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439:719–723

    Article  PubMed  CAS  Google Scholar 

  • Briggs JC (1995) Global Biogeography. Elsevier, Amsterdam

    Book  Google Scholar 

  • Buonaccorsi VP, Kimbrell CA, Lynn EA, Vetter RD (2002) Population structure of copper rockfish (Sebastes caurinus) reflects postglacial colonization and contemporary patterns of larval dispersal. Can J Fish Aquat Sci 59:1374–1384

    Article  CAS  Google Scholar 

  • Buonaccorsi VP, Kimbrell CA, Lynn EA, Vetter RD (2005) Limited realized dispersal and introgressive hybridization influence genetic structure and conservation strategies for brown rockfish, Sebastes auriculatus. Conserv Genet 6:697–713

    Article  Google Scholar 

  • Buonaccorsi VP, Westerman M, Stannard J, Kimbrell C, Lynn E, Vetter RD (2004) Molecular genetic structure suggests limited larval dispersal in grass rockfish, Sebastes rastrelliger. Mar Biol 145:779–788

    Google Scholar 

  • Burford MO, Larson RJ (2007) Genetic heterogeneity in a single year-class from a panmictic population of adult blue rockfish (Sebastes mystinus). Mar Biol 151:451–465

    Article  Google Scholar 

  • Cope JM (2004) Population genetics and phylogeography of the blue rockfish (Sebastes mystinus) from Washington to California. Can J Fish Aquat Sci 61:332–342

    Article  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland

    Google Scholar 

  • Eastman JT, McCune AR (2000) Fishes of the Antarctic continental shelf: evolution of a marine species flock? J Fish Biol 57:84–102

    Google Scholar 

  • Edwards SV, Beerli P (2000) Gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution 54:1839–1854

    PubMed  CAS  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin v.3.0: An integreated software package for population genetics data analysis. Evol Bioinf Online 1:47–50

    CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes—application to human mitochondrial-DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Gill T (1864) Critical remarks on the genera Sebastes and Sebastodes of Ayres. Proc Acad Nat Sci 16:145–147

    Google Scholar 

  • Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  PubMed  CAS  Google Scholar 

  • Hickerson MJ, Cunningham CW (2005) Contrasting quaternary histories in an ecologically divergent sister pair of low-dispersing intertidal fish (Xiphister) revealed by multilocus DNA analysis. Evolution 59:344–360

    PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Hyde JR, Vetter RD (2007) The origin, evolution, and diversification of rockfishes of the genus Sebastes (Cuvier). Mol Phylogenet Evol 44:790–811

    Article  PubMed  CAS  Google Scholar 

  • Johns GC, Avise JC (1998) Tests for ancient species flocks based on molecular phylogenetic appraisals of Sebastes rockfishes and other marine fishes. Evolution 52:1135–1146

    Article  Google Scholar 

  • Jorgensen SJ, Kaplan DM, Klimley AP, Morgan SG, O’Farrell MR, Botsford LW (2006) Limited movement in blue rockfish Sebastes mystinus: internal structure of home range. Mar Ecol Prog Ser 327:157–170

    Article  Google Scholar 

  • Kendall AW (2000) An historical review of Sebastes taxonomy and systematics. Mar Fish Rev 62:1–23

    Google Scholar 

  • Knowlton N (1993) Sibling species in the Sea. Annu Rev Ecol Syst 24:189–216

    Article  Google Scholar 

  • Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90

    Article  CAS  Google Scholar 

  • Kuhner MK, Yamato J, Felsenstein J (1998) Maximum likelihood estimation of population growth rates based on the coalescent. Genetics 149:429

    PubMed  CAS  Google Scholar 

  • Larson RJ (1980) Territorial behavior of the black and yellow rockfish and gopher rockfish (Scorpaenidae, Sebastes). Mar Biol 58:111–122

    Article  Google Scholar 

  • Lee WJ, Conroy J, Howell WH, Kocher TD (1995) Structure and evolution of teleost mitochondrial control regions. J Mol Evol 41:54–66

    Article  PubMed  CAS  Google Scholar 

  • Leet WS, Dewees CM, Klingbeil R, Larson EJ (2001) California’s living marine resources: status report. California Department of Fish and Game

  • Love MS, Yoklavich M, Thorsteinson L (2002) The rockfishes of the northeast Pacific. University of California Press, Berkeley

    Google Scholar 

  • Marko PB (2004) ‘What’s larvae got to do with it?’ Disparate patterns of post-glacial population structure in two benthic marine gastropods with identical dispersal potential. Mol Ecol 13:597–611

    Article  PubMed  CAS  Google Scholar 

  • McCartney MA, Acevdo J, Heredia C, Rico C, Quenouille B, Bermingham E, McMillan WO (2003) Genetic mosaic in a marine species flock. Mol Ecol 12:2963–2973

    Article  PubMed  CAS  Google Scholar 

  • McCune AR, Lovejoy NR (1998) The relative rate of sympatric and allopatric speciation in fishes. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 172–185

    Google Scholar 

  • Miller DJ, Geibel JJ (1973) Summary of blue rockfish and lingcod life histories; a reef ecology study; and giant kelp, Macrocystis pyrifera, experiments in Monterey Bay, California. Fish Bull 158:1–137

    Google Scholar 

  • Miller JA, Banks MA, Gomez-Uchida D, Shanks AL (2005) A comparison of population structure in black rockfish (Sebastes melanops) as determined with otolith microchemistry and microsatellite DNA. Can J Fish Aquat Sci 62:2189–2198

    Article  CAS  Google Scholar 

  • Narum SR, Buonaccorsi VP, Kimbrell CA, Vetter RD (2004) Genetic divergence between gopher rockfish (Sebastes carnatus) and black and yellow rockfish (Sebastes chrysomelas). Copeia: 926–931

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273

    Article  PubMed  CAS  Google Scholar 

  • Nylander JAA (2004) MrModeltest v.2. Program distributed by the author

  • Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67

    Article  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Quenouille B, Bermingham E, Planes S (2004) Molecular systematics of the damselfishes (Teleostei: Pomacentridae): Bayesian phylogenetic analyses of mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol 31:66–88

    Article  PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995a) An exact test for population differentiation. Evolution 49:1280–1283

    Article  Google Scholar 

  • Raymond M, Rousset F (1995b) Genepop (Version-1.2)—population-genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rice W (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Riginos C, Cunningham CW (2005) Local adaptation and species segregation in two mussel (Mytilus edulis × Mytilus trossulus) hybrid zones. Mol Ecol 14:381–400

    Article  PubMed  CAS  Google Scholar 

  • Rocha-Olivares A, Kimbrell CA, Eitner BJ, Vetter RD (1999a) Evolution of a mitochondrial cytochrome b gene sequence in the species-rich genus Sebastes (Teleostei, Scorpaenidae) and its utility in testing the monophyly of the subgenus Sebastomus. Mol Phylogenet Evol 11:426–440

    Article  PubMed  CAS  Google Scholar 

  • Rocha-Olivares A, Rosenblatt RH, Vetter RD (1999b) Molecular evolution, systematics, and zoogeography of the rockfish subgenus Sebastomus (Sebastes, Scorpaenidae) based on mitochondrial cytochrome b and control region sequences. Mol Phylogenet Evol 11:441–458

    Article  PubMed  CAS  Google Scholar 

  • Rocha-Olivares A, Vetter RD (1999) Effects of oceanographic circulation on the gene flow, genetic structure, and phylogeography of the rosethorn rockfish (Sebastes helvomaculatus). Can J Fish Aquat Sci 56:803–813

    Article  Google Scholar 

  • Roques S, Sevigny JM, Bernatchez L (2002) Genetic structure of deep-water redfish, Sebastes mentella, populations across the North Atlantic. Mar Biol 140:297–307

    Article  Google Scholar 

  • Schliewen U, Rassmann K, Markmann M, Markert J, Kocher T, Tautz D (2001) Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon. Mol Ecol 10:1471–1488

    Article  PubMed  CAS  Google Scholar 

  • Schluter D (2000) Ecological character displacement in adaptive radiation. Am Nat 156:S4–S16

    Article  Google Scholar 

  • Seeb LW (1998) Gene flow and introgression within and among three species of rockfishes, Sebastes auriculatus, S. caurinus, and S. maliger. J Hered 89:393–403

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. W·H. Freeman, New York

    Google Scholar 

  • Sorenson MD, Ast JC, Dimcheff DE, Yuri T, Mindell DP (1999) Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. Mol Phylogenet Evol 12:105–114

    Article  PubMed  CAS  Google Scholar 

  • Sotka EE, Wares JP, Barth JA, Grosberg RK, Palumbi SR (2004) Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Mol Ecol 13:2143–2156

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (1998) PAUP* Phylogenetic analysis using parsimony (*and other methods). Sinauer, Sunderland

    Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Vermeij GJ (1991) Anatomy of an invasion: the trans-arctic interchange. Paleobiology 17:281–307

    Google Scholar 

  • Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55:2455–2469

    PubMed  CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Westerman ME, Buonaccorsi VP, Stannard JA, Galver L, Taylor C, Lynn EA, Kimbrell CA, Vetter RD (2005) Cloning and characterization of novel microsatellite DNA markers for the grass rockfish, Sebastes rastrelliger, and cross-species amplification in 10 related Sebastes spp. Mol Ecol Notes 5:74–76

    Article  CAS  Google Scholar 

  • Wyllie-Echeverria T (1987) Thirty-four species of California rockfishes: maturity and seasonality of reproduction. Fish Bull 85:229–250

    Google Scholar 

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Acknowledgments

We could not have completed this research without assistance in both the field and the lab. For their assistance with samples we thank, K. Gordon, S. Parker, A. Chapelle, D. Bondemiller, J. Hyde, M. Ramon, R. Buckley, M. McCrea, and J. Barr. We would like to thank Vince Buonaccorsi, Mark Carr, Ralph Larson, Stephen Palumbi, and Peter Raimondi for comments on an earlier version of this manuscript. Anonymous reviewer’s comments greatly improved this manuscript. The project was funded by grants to M.O. Burford from the PADI Foundation, Myers Trust Grant, The ASIH Raney Fund, Friends of the Long Marine Lab Fellowship, California Environmental Quality Initiative (CEQI) Graduate Fellowship, the Marilyn C. Davis Grant, and from the Packard Foundation’s Partnership for the Interdisciplinary Study of Coastal Oceans (PISCO). This is contribution number 290 from PISCO, funded primarily by the Gordon and Betty Moore Foundation and the David and Lucile Packard Foundation.

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Correspondence to Martha O. Burford.

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Communicated by T. Reusch.

Appendices

Appendix A

Table 5

Table 5 Adult sample locations and summary statistics for Sebastes mystinus, S. entomelas, S. serranoides, and S. melanops

Appendix B

Table 6

Table 6 Microsatellite summary statistics for Sebastes mystinus

Appendix C

Table 7

Table 7 Results of the grouping analysis for Sebastes mystinus using six microsatellite loci

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Burford, M.O., Bernardi, G. Incipient speciation within a subgenus of rockfish (Sebastosomus) provides evidence of recent radiations within an ancient species flock. Mar Biol 154, 701–717 (2008). https://doi.org/10.1007/s00227-008-0963-6

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