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, Miguel Hermida, Carmen Bouza, Belén G. Pardo, Román Vilas, Andrés Blanco, Carlos Fernández, Francesco Maroso, Gregory E. Maes, Cemal Turan, Filip A.M. Volckaert, John B. Taggart, Adrian Carr, Rob Ogden, Einar Eg Nielsen, Paulino Martínez*

*Corresponding author for this work

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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.

Original languageEnglish
JournalEvolutionary Applications
Volume11
Issue number8
Pages (from-to)1322-1341
ISSN1752-4563
DOIs
Publication statusPublished - 2018

Keywords

  • Adaptive variation
  • Conservation genetics
  • Population structure
  • RAD sequencing

Cite this

do Prado, Fernanda Dotti ; Vera, Manuel ; Hermida, Miguel ; Bouza, Carmen ; Pardo, Belén G. ; Vilas, Román ; Blanco, Andrés ; Fernández, Carlos ; Maroso, Francesco ; Maes, Gregory E. ; Turan, Cemal ; Volckaert, Filip A.M. ; Taggart, John B. ; Carr, Adrian ; Ogden, Rob ; Nielsen, Einar Eg ; Martínez, Paulino. / Parallel evolution and adaptation to environmental factors in a marine flatfish : Implications for fisheries and aquaculture management of the turbot (Scophthalmus maximus). In: Evolutionary Applications. 2018 ; Vol. 11, No. 8. pp. 1322-1341.
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title = "Parallel evolution and adaptation to environmental factors in a marine flatfish: Implications for fisheries and aquaculture management of the turbot (Scophthalmus maximus)",
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.",
keywords = "Adaptive variation, Conservation genetics, Population structure, RAD sequencing",
author = "{do Prado}, {Fernanda Dotti} and Manuel Vera and Miguel Hermida and Carmen Bouza and Pardo, {Bel{\'e}n G.} and Rom{\'a}n Vilas and Andr{\'e}s Blanco and Carlos Fern{\'a}ndez and Francesco Maroso and Maes, {Gregory E.} and Cemal Turan and Volckaert, {Filip A.M.} and Taggart, {John B.} and Adrian Carr and Rob Ogden and Nielsen, {Einar Eg} and Paulino Mart{\'i}nez",
year = "2018",
doi = "10.1111/eva.12628",
language = "English",
volume = "11",
pages = "1322--1341",
journal = "Evolutionary Applications (Online)",
issn = "1752-4563",
publisher = "Wiley-Blackwell",
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}

do Prado, FD, Vera, M, Hermida, M, Bouza, C, Pardo, BG, Vilas, R, Blanco, A, Fernández, C, Maroso, F, Maes, GE, Turan, C, Volckaert, FAM, Taggart, JB, Carr, A, Ogden, R, Nielsen, EE & Martínez, P 2018, 'Parallel evolution and adaptation to environmental factors in a marine flatfish: Implications for fisheries and aquaculture management of the turbot (Scophthalmus maximus)', Evolutionary Applications, vol. 11, no. 8, pp. 1322-1341. https://doi.org/10.1111/eva.12628

Parallel evolution and adaptation to environmental factors in a marine flatfish : Implications for fisheries and aquaculture management of the turbot (Scophthalmus maximus). / do Prado, Fernanda Dotti; Vera, Manuel; Hermida, Miguel; Bouza, Carmen; Pardo, Belén G.; Vilas, Román; Blanco, Andrés; Fernández, Carlos; Maroso, Francesco; Maes, Gregory E.; Turan, Cemal; Volckaert, Filip A.M.; Taggart, John B.; Carr, Adrian; Ogden, Rob; Nielsen, Einar Eg; Martínez, Paulino.

In: Evolutionary Applications, Vol. 11, No. 8, 2018, p. 1322-1341.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Parallel evolution and adaptation to environmental factors in a marine flatfish

T2 - Implications for fisheries and aquaculture management of the turbot (Scophthalmus maximus)

AU - do Prado, Fernanda Dotti

AU - Vera, Manuel

AU - Hermida, Miguel

AU - Bouza, Carmen

AU - Pardo, Belén G.

AU - Vilas, Román

AU - Blanco, Andrés

AU - Fernández, Carlos

AU - Maroso, Francesco

AU - Maes, Gregory E.

AU - Turan, Cemal

AU - Volckaert, Filip A.M.

AU - Taggart, John B.

AU - Carr, Adrian

AU - Ogden, Rob

AU - Nielsen, Einar Eg

AU - Martínez, Paulino

PY - 2018

Y1 - 2018

N2 - 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.

AB - 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.

KW - Adaptive variation

KW - Conservation genetics

KW - Population structure

KW - RAD sequencing

U2 - 10.1111/eva.12628

DO - 10.1111/eva.12628

M3 - Journal article

C2 - 30151043

AN - SCOPUS:85044871119

VL - 11

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EP - 1341

JO - Evolutionary Applications (Online)

JF - Evolutionary Applications (Online)

SN - 1752-4563

IS - 8

ER -