Abstract
The ballan wrasse (Labrus bergylta) is a marine fish belonging to the family Labridae characterized by 2 main morphotypes that occur in sympatry: spotty and plain. Previous studies have revealed differences in their life‐history traits, such as growth and maturation; however, the genetic relationship between forms is presently unknown. Using 20 recently developed microsatellite markers, we conducted a genetic analysis of 41 and 48 spotty and plain ballan wrasse collected in Galicia (northwest Spain). The 2 morphotypes displayed highly significant genetic differences to each other (F ST = 0.018, P < 0.0001). A similar degree of genetic differentiation (F ST = 0.025, P < 0.0001) was shown using the STRUCTURE clustering approach with no priors at K = 2. In this case, the frequency of spotty and plain morphotypes was significantly different (χ2 = 9.46, P = 0.002). It is concluded that there is significant genetic heterogeneity within this species, which appears to be highly associated with the spotty and plain forms, but not completely explained by them. Given the previously demonstrated biological differences between morphotypes, and the present genetic analyses, we speculate about the convenience of a taxonomic re‐evaluation of this species.
Keywords: ballan wrasse, color morphotypes, Labrus bergylta, microsatellites, speciation
Cite this article as:
Quintela M, Danielsen E, Lopez L et al. (2016). Is the ballan wrasse (Labrus bergylta) two species? Genetic analysis reveals within‐species divergence associated with plain and spotted morphotype frequencies. Integrative Zoology 11, 162–72.
REFERENCES
- Antao T, Lopes A, Lopes R, Beja‐Pereira A, Luikart G (2008). LOSITAN: A workbench to detect molecular adaptation based on a FST-outlier method. BMC Bioinformatics 9, 323. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004). GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations.
- Corander J, Marttinen P (2006). Bayesian identification of admixture events using multilocus molecular markers. Molecular Ecology 15, 2833–43. [DOI] [PubMed] [Google Scholar]
- Corander J, Waldmann P, Marttinen P, Sillanpaa MJ (2004). BAPS 2: Enhanced possibilities for the analysis of genetic population structure. Bioinformatics 20, 2363–9. [DOI] [PubMed] [Google Scholar]
- D'Arcy J, Mirimin L, Fitzgerald R (2013). Phylogeographic structure of a protogynous hermaphrodite species, the ballan wrasse Labrus bergylta, in Ireland, Scotland, and Norway, using mitochondrial DNA sequence data. ICES Journal of Marine Science: Journal du Conseil 70, 685–93. [Google Scholar]
- D'Arcy J, Dunaevskaya E, Treasurer JW et al. (2012). Embryonic development in ballan wrasse Labrus bergylta . Journal of Fish Biology 81, 1101–10. [DOI] [PubMed] [Google Scholar]
- Earl DA, von Holdt BM (2012). STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–61. [Google Scholar]
- Evanno G, Regnaut S, Goudet J (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology 14, 2611–20. [DOI] [PubMed] [Google Scholar]
- Excoffier L, Laval G, Schneider S (2005). Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50. [PMC free article] [PubMed] [Google Scholar]
- Foll M, Gaggiotti O (2008). A genome‐scan method to identify selected loci appropriate for both dominant and codominant markers: A Bayesian perspective. Genetics 180, 977–93. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–9. [PubMed] [Google Scholar]
- Gray SM, McKinnon JS (2007). Linking color polymorphism maintenance and speciation. Trends in Ecology & Evolution 22, 71–9. [DOI] [PubMed] [Google Scholar]
- Hoekstra, Hopi E , Drumm, Kristen E , Nachman, Michael W (2004). Ecological genetics of adaptive color polymorphism in pocket mice: Geographic variation in selected and neutral genes. Evolution 58, 1329–41. [DOI] [PubMed] [Google Scholar]
- Hutchinson WF (2008). The dangers of ignoring stock complexity in fishery management: The case of the North Sea cod. Biology Letters 4, 693–5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jakobsson M, Rosenberg NA (2007). CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–6. [DOI] [PubMed] [Google Scholar]
- Knutsen H, Jorde PE, Blanco González E, Robalo J, Albretsen J, Almada V (2013). Climate change and genetic structure of leading edge and rear end populations in a northwards shifting marine fish species, the corkwing wrasse (Symphodus melops). PLoS ONE 8, e67492. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knutsen H, Olsen EM, Jorde PE, Espeland SH, AndrÉ C, Stenseth NC (2011). Are low but statistically significant levels of genetic differentiation in marine fishes ‘biologically meaningful’? A case study of coastal Atlantic cod. Molecular Ecology 20, 768–83. [DOI] [PubMed] [Google Scholar]
- McGinnity P, Prodöhl P, Ferguson A et al. (2003). Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proceedings of the Royal Society of London. Series B: Biological Sciences 270, 2443–50. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peakall R, Smouse PE (2006). GenAlEx 6: Genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–95. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pritchard JK, Stephens M, Donnelly P (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–59. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Quintela M, Danielsen EA, Svåsand T, Knutsen H, Skiftesvik AB, Glover KA (2014). Isolation and characterization of twenty microsatellite loci for the ballan wrasse, Labrus bergylta. Conservation Genetics Resources, 1–4.
- Rousset F (2008). GENEPOP′007: A complete re‐implementation of the genepop software for Windows and Linux. Molecular Ecology Resources 8, 103–6. [DOI] [PubMed] [Google Scholar]
- Skiftesvik AB, Bjelland RM, Durif CMF, Johansen IS, Browman HI (2013). Delousing of Atlantic salmon (Salmo salar) by cultured vs. wild ballan wrasse (Labrus bergylta). Aquaculture 402–3, 113–8. [Google Scholar]
- Venerus LA, Ciancio JE, Riva‐Rossi C, Gilbert‐Horvath EA, Gosztonyi AE, Garza JC (2013). Genetic structure and different color morphotypes suggest the occurrence and bathymetric segregation of two incipient species of Sebastes off Argentina. Naturwissenschaften 100, 645–58. [DOI] [PubMed] [Google Scholar]
- Villegas‐Ríos D (2013). Life‐history and behaviour of Labrus bergylta in Galicia. Department of Ecology and Marine Biodiversity, PhD thesis, 228. [Google Scholar]
- Villegas‐Ríos D, Alonso‐Fernández A, Domínguez‐Petit R, Saborido‐Rey F (2013a). Intraspecific variability in reproductive patterns in the temperate hermaphrodite fish, Labrus bergylta . Marine and Freshwater Research 64, 1156–68. [Google Scholar]
- Villegas‐Ríos D, Alonso‐Fernández A, Domínguez‐Petit R, Saborido‐Rey F (2014). Energy allocation and reproductive investment in a temperate protogynous hermaphrodite, the ballan wrasse Labrus bergylta . Journal of Sea Research 86, 76–85. [Google Scholar]
- Villegas‐Ríos D, Alonso‐Fernández A, Fabeiro M, Bañón R, Saborido‐Rey F (2013b). Demographic variation between colour patterns in a temperate protogynous hermaphrodite, the ballan wrasse Labrus bergylta . PLoS ONE 8, e71591. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Villegas‐Ríos D, Alós J, March D, Palmer M, Mucientes G, Saborido‐Rey F (2013c). Home range and diel behavior of the ballan wrasse, Labrus bergylta, determined by acoustic telemetry. Journal of Sea Research 80, 61–70. [Google Scholar]
- Weir BS, Cockerham CC (1984). Estimating F‐statistics for the analysis of population structure. Evolution 38, 1358–70. [DOI] [PubMed] [Google Scholar]
- Westgaard JI, Klemetsen A, Knudsen R (2004). Genetic differences between two sympatric morphs of Arctic charr confirmed by microsatellite DNA. Journal of Fish Biology 65, 1185–91. [Google Scholar]
- Wilson GA, Rannala B (2003). Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163, 1177–91. [DOI] [PMC free article] [PubMed] [Google Scholar]