Skip to main content

Advertisement

SpringerLink
Log in

Analysis of individual year-classes of a marine fish reveals little evidence of first-generation hybrids between cryptic species in sympatric regions

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

As settled juveniles and adults, blue rockfish (Sebastes mystinus) are nonmigratory inhabitants of kelp and rocky reef habitats along the California coast, USA, and prior to settlement, they possess a pelagic larval and juvenile stage lasting 3–5 months. A previous study of adults revealed two cryptic species within S. mystinus and evidence of reproductive isolation in a region where both cryptic adults co-occur. Given this pattern of reproductive isolation, we investigated the degree of hybridization or introgression in individual year-classes shortly after juvenile settlement in two different years (2001 and 2002). Using microsatellite markers, we found little indication of hybridization in new juvenile year-classes despite an adult population that comprised both cryptic species. However, we found an average of two percent of hybrid or introgressed individuals in regions with a low frequency of one of the two species. Therefore, while the lack of hybrids or introgression supports the hypothesis of reproductive isolation between the cryptic species within S. mystinus, the age-structured analysis also revealed a spatial pattern of low-frequency differences in the number of introgressed individuals. These results suggest that reproductive barriers may breakdown when one of the two species predominates the regional adult gene pool.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ammann AJ (2004) SMURFs: standard monitoring units for the recruitment of temperate reef fishes. J Exp Mar Biol Ecol 299:135–154

    Article  Google Scholar 

  • Anderson TW, Carr MH (1998) BINCKE: a highly efficient net for collecting reef fishes. Environ Biol Fish 51:111–115

    Article  Google Scholar 

  • Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229

    CAS  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, 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 (2009) Demographic history, geographic 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

    Article  Google Scholar 

  • Burford MO, Bernardi G (2008) Incipient speciation within a subgenus of rockfish (Sebastosomus) provides evidence of recent radiations within an ancient species flock. Mar Biol 154:701–717

    Article  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

    Google Scholar 

  • Butlin RK, Galindo J, Grahame JW (2008) Sympatric, parapatric or allopatric: the most important way to classify speciation? Phil Trans Roy Soc B 363:2997–3007

    Article  Google Scholar 

  • Crow KD, Munehara H, Bernardi G (2010) Sympatric speciation in a genus of marine fishes. Mol Ecol 19:2089–2105

    Article  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  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

    CAS  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  CAS  Google Scholar 

  • Hyde JR, Kimbrell CA, Burdick JE, Lynn EA, Vetter RD (2008) Cryptic speciation in the vermilion rockfish (Sebastes miniatus) and the role of bathymetry in the speciation process. Mol Ecol 17:1122–1136

    Article  CAS  Google Scholar 

  • Johannesson K (2009) Inverting the null-hypothesis of speciation: a marine snail perspective. Evol Ecol 23:5–16

    Article  Google Scholar 

  • Johannesson K, Johannesson B, Lundgren U (1995) Strong natural-selection causes microscale allozyme variation in a marine snail. Proc Nat Acad Sci USA 92:2602–2606

    Article  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 

  • Laroche WA, Richardson SL (1981) Development of larvae and juveniles of the rockfishes Sebastes entomelas and S. zacentrus (family Scorpaenidae) and occurrence off Oregon, with notes on head spines S. mystinus, S. flavidus, and S. melanops. Fish Bull 79:215–230

    Google Scholar 

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

    Google Scholar 

  • Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York

    Google Scholar 

  • Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge

    Google Scholar 

  • McCafferty S, Bermingham E, Quenouille B, Planes S, Hoelzer G, Asoh K (2002) Historical biogeography and molecular systematics of the Indo- Pacific genus Dascyllus (Teleostei: Pomacentridae). Mol Ecol 11:1377–1392

    Article  CAS  Google Scholar 

  • Miller DJ, Lea RN (1972) Guide to coastal marine fishes of California. Fish Bull 157:1–235

    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 

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

    Google Scholar 

  • Palumbi SR, Lessios HA (2005) Evolutionary animation: how do molecular phylogenies compare to Mayr’s reconstruction of speciation patterns in the sea? Proc Nat Acad Sci USA 102:6566–6572

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Rawson PD, Agrawal V, Hilbish TJ (1999) Hybridization between the blue mussels Mytilus galloprovincialis and M. trossulus along the Pacific coast of North America: evidence for limited introgression. Mar Biol 134:201–211

    Article  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 

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

    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  CAS  Google Scholar 

  • Waples RS (1987) A multispecies approach to the analysis of gene flow in marine shore fishes. Evolution 41:385–400

    Article  Google Scholar 

  • Wares JP, Gaines SD, Cunningham CW (2001) A comparative study of asymmetric migration events across a marine biogeographic boundary. Evolution 55:295–306

    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 

  • Wing SR, Botsford LW, Largier JL, Morgan LE (1995) Spatial structure of relaxation events and crab settlement in the northern California upwelling system. Mar Ecol Prog Ser 128:199–211

    Article  Google Scholar 

Download references

Acknowledgments

For their assistance with sample collections, we thank the Oregon and Washington Department of Fish and Wildlife and the California Department of Fish and Game, and R. Buckley, D. Bondemiller, K. Gordon, J. Headlee, D. VenTresca, P. Gundelfinger, R. Larson, T. Laidig, S. Parker, A. Chapelle, J. Barlow, M. O’Farrell, P. Tompkins, J. Fugurski, J. Grover, R. Nakamura, T. Olive, J. Hyde, M. Ramon, G. Bernardi, N. Crane, M. McCrea, and J. Barr. We would also like to thank M. Reiskind, R. Larson, S. Palumbi, and P. Raimondi for comments on an earlier version of this manuscript. Finally, we would like to acknowledge two anonymous reviewers who provided comments that greatly improved this manuscript. The project was funded by grants 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 393 from PISCO, funded primarily by the Gordon and Betty Moore Foundation and the David and Lucile Packard Foundation.

Author information

Author notes

  1. Martha O. Burford

    Present address: Department of Biology, University of Central Oklahoma, 100 North University Drive, Edmond, OK, 73034, USA

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 100 Shaffer Road, Santa Cruz, CA, 95060, USA

    Martha O. Burford, Giacomo Bernardi & Mark H. Carr

Authors
  1. Martha O. Burford
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Giacomo Bernardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark H. Carr
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martha O. Burford.

Additional information

Communicated by T. Reusch.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 13 kb)

Appendices

Appendix 1

See Table 5.

Table 5 Adult Sebastes mystinus sample locations summarized from Burford (2009)
Full size table

Appendix 2

See Table 6.

Table 6 Results of parameter estimates in the STRUCTURE assignment model using groupings (K) of 1–5, average log-likelihood, variance, data estimates for K, and estimates of ∆K
Full size table

Appendix 3

See Table 7.

Table 7 Standard error of the combined 5 runs of STRUCTURE analysis of juvenile Sebastes mystinus
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Burford, M.O., Bernardi, G. & Carr, M.H. Analysis of individual year-classes of a marine fish reveals little evidence of first-generation hybrids between cryptic species in sympatric regions. Mar Biol 158, 1815–1827 (2011). https://doi.org/10.1007/s00227-011-1694-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-011-1694-7

Keywords

Search

Navigation