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Transcriptome analysis deciphers evolutionary mechanisms underlying genetic differentiation between coastal and offshore anchovy populations in the Bay of Biscay

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Abstract

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.

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Acknowledgments

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).

Funding

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.

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    1. Department of Genetics, Physical Anthropology and Animal Physiology, University of the Basque Country (UPV/EHU), Leioa, Spain

      Iratxe Montes, Iratxe Zarraonaindia, Mikel Iriondo, Carmen Manzano & Andone Estonba

    2. Commercial Fisheries Division, Alaska Department of Fish and Game, Anchorage, AK, USA

      W. Stewart Grant

    3. Marine Research Division, AZTI-Tecnalia, Pasaia, Spain

      Unai Cotano

    4. Department of Computer Science and Artificial Intelligence, University of the Basque Country UPV/EHU, San Sebastián, Spain

      Darrell Conklin

    5. IKERBASQUE, Basque Foundation for Science, Bilbao, Spain

      Darrell Conklin

    6. Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia

      Xabier Irigoien

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    1. Iratxe Montes
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    Iratxe Montes and Iratxe Zarraonaindia have equally contributed to this work.

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    Montes, I., Zarraonaindia, I., Iriondo, M. et al. Transcriptome analysis deciphers evolutionary mechanisms underlying genetic differentiation between coastal and offshore anchovy populations in the Bay of Biscay. Mar Biol 163, 205 (2016). https://doi.org/10.1007/s00227-016-2979-7

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