Abstract

Marine fish often show little genetic structuring in neutral marker genes, and Atlantic herring (Clupea harengus) in the Baltic Sea are no exception; historically, very low levels of population differentiation (FST ≍ 0.002) have been found, despite a high degree of interpopulation environmental heterogeneity in salinity and temperature. Recent exome sequencing and SNP studies have however shown that many loci are under selection in this system. Here, we combined population genetic analyses of a large number of transcriptome-derived microsatellite markers with oceanographic modelling to investigate genetic differentiation and connectivity in Atlantic herring at a relatively fine scale within the Baltic Sea. We found evidence for weak but robust and significant genetic structuring (FST = 0.008) explainable by oceanographic connectivity. Genetic differentiation was also associated with site differences in temperature and salinity, with the result driven by the locus Her14 which appears to be under directional selection (FST = 0.08). The results show that Baltic herring are genetically structured within the Baltic Sea, and highlight the role of oceanography and environmental factors in explaining this structuring. The results also have implications for the management of herring fisheries, the most economically important fishery in the Baltic Sea, suggesting that the current fisheries management units may be in need of revision.

Highlights

  • Intraspecific biodiversity forms the basis for evolution and is important for the long-term viability of populations and thereby for sustainable harvesting of species of commercial importance (Frankham et al 2002; Avise 2008; Schindler et al 2010)

  • We address the following questions: (i) Is there evidence for population differentiation in the Baltic Sea, (ii) Is there an indication of outlier loci that may be under selection, (iii) Do gene-associated microsatellites show different patterns of population differentiation than random microsatellite markers, (iv) How well does population differentiation correlate with seascape connectivity and geographical distance, and (v) Is there any evidence for correlations between genetic differentiation or genetic diversity with environmental variables, including salinity, temperature, and fishing pressure

  • Outlier tests The loci detected as outliers by Lositan were the same under the Infinite Alleles and Stepwise mutation models. Those that fell outside the 95% confidence intervals were mostly in the direction of positive selection (High fixed between sites. Population differentiation (FST) relative to HE): CPA104, CPA107, CPA112, Her14, Her37, Her41, Her63, while locus CPA114 fell in the direction of putative balancing selection (Low FST relative to HE)

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Summary

Introduction

Intraspecific biodiversity forms the basis for evolution and is important for the long-term viability of populations and thereby for sustainable harvesting of species of commercial importance (Frankham et al 2002; Avise 2008; Schindler et al 2010). Gene flow by drifting larvae and migrating adults may be extensive, and local adaptation in marine fish has traditionally been viewed as rare, with weak population structuring (Waples 1998). Recent studies show that marine fish may be spatially structured into genetically distinct populations on both wide Concurrent variation in ecologically important traits (e.g. spawning time, migration patterns etc.) among populations may indicate adaptive differentiation, possibly affecting resilience to environmental change and exploitation (Hauser and Carvalho 2008). Genomic approaches have identified functional genes subjected to natural selection (e.g. Schulte et al 2000; Andersen et al 2009; Corander et al 2013; Lamichhaney et al 2012), the molecular mechanism underlying adaptations and the effects on fitness are as yet typically unknown (cf. Barrett and Hoekstra 2011)

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