Parallel evolution and adaptation to environmental factors in a marine flatfish: Implications for fisheries and aquaculture management of the turbot (Scophthalmus maximus).

Fernanda Dotti Do Prado,Manuel Vera,Adrian Carr,Carmen Bouza,Carlos Fernández,Filip A M Volckaert,Román Vilas,Einar Eg Nielsen,Belén G Pardo,Cemal Turan,Paulino Martínez,The Aquatrace Consortium ,Miguel Hermida,Rob Ogden,Andrés Blanco,John B Taggart,Francesco Maroso,Gregory E Maes

doi:10.1111/eva.12628

Abstract

Unraveling adaptive genetic variation represents, in addition to the estimate of population demographic parameters, a cornerstone for the management of aquatic natural living resources, which, in turn, represent the raw material for breeding programs. The turbot (Scophthalmus maximus) is a marine flatfish of high commercial value living on the European continental shelf. While wild populations are declining, aquaculture is flourishing in southern Europe. We evaluated the genetic structure of turbot throughout its natural distribution range (672 individuals; 20 populations) by analyzing allele frequency data from 755 single nucleotide polymorphism discovered and genotyped by double‐digest RAD sequencing. The species was structured into four main regions: Baltic Sea, Atlantic Ocean, Adriatic Sea, and Black Sea, with subtle differentiation apparent at the distribution margins of the Atlantic region. Genetic diversity and effective population size estimates were highest in the Atlantic populations, the area of greatest occurrence, while turbot from other regions showed lower levels, reflecting geographical isolation and reduced abundance. Divergent selection was detected within and between the Atlantic Ocean and Baltic Sea regions, and also when comparing these two regions with the Black Sea. Evidence of parallel evolution was detected between the two low salinity regions, the Baltic and Black seas. Correlation between genetic and environmental variation indicated that temperature and salinity were probably the main environmental drivers of selection. Mining around the four genomic regions consistently inferred to be under selection identified candidate genes related to osmoregulation, growth, and resistance to diseases. The new insights are useful for the management of turbot fisheries and aquaculture by providing the baseline for evaluating the consequences of turbot releases from restocking and farming.

Highlights

The detection of genetic structure in marine species represents a challenge due to generally high effective population sizes and high gene flow facilitated by the absence of physical barriers, which lead to genomic homogenization across populations (Danancher & Garcia-Vazquez, 2011; Vandamme et al, 2014; Vilas et al, 2015)
Results from STRUCTURE were processed with the program STRUCTURE HARVESTER v0.3 (Earl & vonHoldt, 2012) to estimate the best-fitted number of clusters K based on the ΔK method described by Evanno, Regnaut, and Goudet (2005)
Because STRUCTURE inference may be affected by uneven sampling (Puechmaille, 2016), as in our case due to the extensive sampling of the Atlantic area compared to other areas such as Adriatic and Black Sea, more restricted analyses including only Atlantic samples were performed to detect subtle genetic structuring

Summary

| INTRODUCTION

The detection of genetic structure in marine species represents a challenge due to generally high effective population sizes and high gene flow facilitated by the absence of physical barriers, which lead to genomic homogenization across populations (Danancher & Garcia-Vazquez, 2011; Vandamme et al, 2014; Vilas et al, 2015). Reproductive success and growth differences in turbot between the Atlantic Ocean and the Baltic Sea have been associated with salinity (Nissling, Johansson, & Jacobsson, 2006) and have been explained either by phenotypic plasticity (Florin & Höglund, 2007) or divergent selection (Vilas et al, 2010, 2015). An earlier study identified different hemoglobin genotypes, which suggested that turbot populations in the Northern Atlantic Ocean might not be entirely homogeneous (Imsland, Scanu, & Nævdal, 2003) These data highlight the need for more detailed studies using larger genomic coverage to clearly elucidate both neutral and adaptive genetic differentiation. The information gathered is useful for a sustainable management of genetic resources in the wild and for guiding selection of genetic raw material for the growing turbot aquaculture

| MATERIALS AND METHODS

| DISCUSSION

CONFLICT OF INTEREST