Transcriptome analysis deciphers evolutionary mechanisms underlying genetic differentiation between coastal and offshore anchovy populations in the Bay of Biscay
- 337 Downloads
Morphometry and otolith microchemistry point to the existence of two populations of the European anchovy (Engraulis encrasicolus) in the Bay of Biscay: one in open seawaters, and a yet unidentified population in coastal waters. To test this hypothesis, we assembled a large number of samples from the region, including 587 juveniles and spawning adults from offshore and coastal waters, and 264 fish from other locations covering most of the species’ European range. These samples were genotyped for 456 exonic SNPs that provide a robust way to decipher adaptive processes in these populations. Two genetically differentiated populations of anchovy inhabit the Bay of Biscay with different population dynamics: (1) a large offshore population associated with marine waters included in the wide-shelf group, and (2) a coastal metapopulation adapted to estuarine environments in the Bay of Biscay and North Sea included in the narrow-shelf group. Transcriptome analysis identified neutral and adaptive evolutionary processes underlying differentiation between these populations. Reduced gene flow between offshore and coastal populations in the Bay of Biscay appears to result from divergence between two previously isolated gene pools adapted to contrasting habitats and now in secondary contact. Eleven molecular markers appear to mark divergent selection between the ecotypes, and a majority of these markers are associated with salinity variability. Ecotype differences at two outlier genes, TSSK6 and basigin, may hinder gamete compatibility between the ecotypes and reinforce reproductive isolation. Additionally, possible convergent evolution between offshore and coastal populations in the Bay of Biscay has been detected for the syntaxin1B-otoferlin gene system, which is involved in the control of larval buoyancy. Further study of exonic markers opens the possibility of understanding the mechanisms of adaptive divergence between European anchovy populations.
KeywordsReproductive Isolation Coastal Population Adaptive Landscape Genetic Entity Gironde Estuary
We thank Aitor Albaina for deep discussions of our results and 2 reviewers for their constructive comments, which have helped to improve the article. Gary R. Carvalho and Dave Bembo provided the sample 17. Kristina Raab and Jeroen van der Kooij provided the sample from the IJsselmeer (sample 25). Cesar Vilas provided the two samples from Guadalquivir (samples 27 and 28). Jérôme Goudet kindly assisted with a beta version of Fstat 2.9.4 to handle large datasets. Finally, the authors thank for technical and human support provided by Sequencing and Genotyping SGIker unit of UPV/EHU and European funding (ERDF and ESF).
This study was funded by the Ministry of Science and Research of the Government of Spain through ECOGENBAY (MICINN CTM2009-13570-C02-02) and by a Research Grant (3571/2008) from the University of the Basque Country (UPV/EHU). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Compliance with ethical standards
Conflict of interest
All authors of this study declare that they have no conflict of interest.
All applicable international, national and institutional guidelines for the care and use of animals were followed.
- Aldanondo N, Cotano U, Tiepolo M, Boyra G et al (2010) Growth and movement patterns of early juvenile European anchovy (Engraulis encrasicolus L.) in the Bay of Biscay based on otolith microstructure and chemistry. Fish Oceanogr 19:196–208. doi: 10.1111/j.1365-2419.2010.00537.x CrossRefGoogle Scholar
- Braak CJF, Smilauer P (2002) CANOCO Reference Manual and CanoDraw for Windows user’s guide: software for Canonical Community Ordination (Version 4.5). Microcomputer PowerGoogle Scholar
- Chatterjee P, Padmanarayana M, Abdullah N, Holman CL, LaDu J, Tanguay RL, Johnson CP (2015) Otoferlin deficiency in zebrafish results in defects in balance and hearing: rescue of the balance and hearing phenotype with full-length and truncated forms of mouse otoferlin. Mol Cell Biol 35(6):1043–1054. doi: 10.1128/MCB.01439-14 CrossRefGoogle Scholar
- Dulzetto F (1947) L’Engraulis dei laghi di Ganzirri e del Faro. Mem Soc It Sci XL 3(26):5–28Google Scholar
- Ganias K (2014) Biology and ecology of sardines and anchovies. CRC Press, Boca Raton. ISBN: 978-1-4822-2854-0Google Scholar
- Guerault D, Avrilla J (1978) L’anchois du Golfe de Gascogne. Mise en évidence de l’existance de deux populations et bilan de nos connaissances sur la biologie de l’espèce. ICES CM 1978/H:24Google Scholar
- ICES (2008) Report of the Workshop on Small Pelagics (Sardina pilchardus, Engraulis encrasicolus) maturity stages (WKSPMAT), 10–14 November 2008, Mazara del Vallo, Italy. ICES CM 2008/ACOM:40Google Scholar
- Kada O, Abdellaoui S, Ramdani M, Nachit D (2009) Contribution à l’identification et à la caractérisation biologique et dynamique de l’anchois de la lagune de Nador (Maroc). Bull Inst Sci (Rabat), Sect Sci de la Vie 31:91–98Google Scholar
- Langella O (2002) POPULATIONS 1.2.28. Population genetic software (individuals or populations distances, phylogenetic trees). Available from http://bioinformatics.org/~tryphon/populations/
- Magoulas A, Castilho R, Caetano S, Marcato S, Partanello T (2006) Mitochondrial DNA reveals a mosaic pattern of phylogeographical structure in Atlantic and Mediterranean populations of anchovy (Engraulis encrasicolus). Mol Phylogenet Evol 39:734–746. doi: 10.1016/j.ympev.2006.01.016 CrossRefGoogle Scholar
- Messaoud H, Bouriga N, Daly Yahia MN, Boumaiza M et al (2011) Discrimination de trois populations d’anchois du genre Engraulis (Clupeiforme, Engraulidae) des côtes Tunisiennes par analyse de forme des otolithes. Bull Inst Natl Sci Tech Mer (Salambô) 38:21–27Google Scholar
- Molecular Ecology Resources Primer Development Consortium, Abreu AG, Albaina A, Alpermann TJ et al (2012) Permanent genetic resources added to molecular ecology resources database 1 October 2011–30 November 2011. Mol Ecol Resour 12:374–376. doi: 10.1111/j.1755-0998.2011.03109.x CrossRefGoogle Scholar
- Motos L, Uriarte A, Valencia V (1996) The spawning environment of the Bay of Biscay anchovy (Engraulis encrasicolus L.). Sci Mar 60(Suppl. 2):117–140Google Scholar
- Quignard JP, Hamdouni T, Zaouali J (1973) Donnees preliminaires sur les caracteres biometriques des anchois Engraulis encrasicolus (Linné, 1758) des cotes de Tunisie et du Lac Ichkeul. Rev Trav Inst Pêch Marit 37:191–196Google Scholar
- Reynolds J, Weir BS, Cockerham CC (1983) Estimation of the coancestry coefficient: basis for a short-term genetic distance. Genetics 105:767–779Google Scholar
- Rowe S, Hutchings JA (2003) Mating systems and the conservation of commercially exploited marine fish. TREE 18:567–572Google Scholar
- Santiago J, Eltink A (1988) Distribution and abundance of anchovy eggs in the Bay of Biscay in May 1987 in comparison to 1983 and 1986. ICES CM 1988/H:9Google Scholar
- Santiago J, Sanz A (1992) Egg production estimates of the Bay of Biscay anchovy, Engraulis encrasicholus (L.), spawning stock in 1987 and 1988 (Estimaciones de la producción de huevos del stock reproductor de anchoa, Engraulis encrasicholus (L.), del golfo de Vizcaya en 1987 y 1988). Bol Inst Esp Oceanogr 8:225–230Google Scholar
- Viñas J, Sanz N, Peñarrubia L, Araguas RM et al (2014) Genetic population structure of European anchovy in the Mediterranean Sea and the Northeast Atlantic Ocean using sequence analysis of the mitochondrial DNA control region. ICES J Mar Sci 71(2):391–397. doi: 10.1093/icesjms/fst132 CrossRefGoogle Scholar
- Warnes G, Gorjanc G, Leisch F, Man M (2012) genetics: population Genetics. R package version 1.3.8. https://cran.r-project.org/web/packages/genetics/index.html. Accessed 20 May 2015