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

Authors
  • Montes, Iratxe1
  • Zarraonaindia, Iratxe1
  • Iriondo, Mikel1
  • Grant, W. Stewart2
  • Manzano, Carmen1
  • Cotano, Unai3
  • Conklin, Darrell4, 5
  • Irigoien, Xabier6
  • Estonba, Andone1
  • 1 University of the Basque Country (UPV/EHU), Department of Genetics, Physical Anthropology and Animal Physiology, Leioa, Spain , Leioa (Spain)
  • 2 Commercial Fisheries Division, Alaska Department of Fish and Game, Anchorage, AK, USA , Anchorage (United States)
  • 3 AZTI-Tecnalia, Marine Research Division, Pasaia, Spain , Pasaia (Spain)
  • 4 University of the Basque Country UPV/EHU, Department of Computer Science and Artificial Intelligence, San Sebastián, Spain , San Sebastián (Spain)
  • 5 IKERBASQUE, Basque Foundation for Science, Bilbao, Spain , Bilbao (Spain)
  • 6 King Abdullah University of Science and Technology, Red Sea Research Center, Thuwal, Saudi Arabia , Thuwal (Saudi Arabia)
Type
Published Article
Journal
Marine Biology
Publisher
Springer-Verlag
Publication Date
Sep 13, 2016
Volume
163
Issue
10
Identifiers
DOI: 10.1007/s00227-016-2979-7
Source
Springer Nature
Keywords
License
Yellow

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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