Oceanographic connectivity and environmental correlates of genetic structuring in Atlantic herring in the Baltic Sea

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 (F ST % 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 (F ST = 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 (F ST = 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.

Genetic biodiversity in the Baltic Sea: species-specific patterns challenge management

“…For example, the free-floating larval stage in Atlantic herring and a later pelagic life stage mediate potential for long distance dispersal and is a likely explanation for the lack of genetic structuring for herring within the Baltic Sea shown here, as well as in previous studies using neutral genetic markers Jørgensen et al 2005). Genetic divergence among herring populations has indeed been shown to be affected more by ocean currents than geographic distance (Teacher et al 2013). Ocean currents are more likely to affect species with freefloating life stages, such as herring, or bladderwrack, for which dispersal of eggs are limited, but detached adults have the potential for dispersal by means of rafting (Tatarenkov et al 2007).…”

“…The observed pattern of isolation by distance found in whitefish and pike in the present study as well as previous studies (Laikre et al 2005b;Olsson et al 2012a) is consistent with such limited dispersal and suggests that migration predominantly takes place between geographically proximate populations. It should be noted that recent studies have detected isolation by distance also in herring (Teacher et al 2013) and three-spined and nine-spined stickleback (DeFaveri et al 2012). Those studies included larger sample sizes and/or more genetic markers than examined here, however, and may thus have been characterized by higher statistical power for detection of isolation by distance.…”

“…For example, salinity has been correlated with genetic differentiation in Atlantic herring and three-spined stickleback, using both selected and neutral loci Lamichhaney et al 2012;Limborg et al 2012;; ocean connectivity has been correlated with genetic divergence in herring (Teacher et al 2013) as has temperature for herring and three-spined stickleback (Limborg et al 2012;.…”

“…This shared genetic barrier is now supported by a wide range of fish species, such as the sand goby (Larmuseau et al 2009), sprat (Limborg et al 2009), herring (Limborg et al 2012;Lamichhaney et al 2012), whitefish (Olsson et al 2012a) and sticklebacks (Shikano et al 2010;. The relatively large genetic differentiation in this region has generally been attributed to selection for the low saline environment followed by adaptive divergence and subsequent reduced gene flow which affect selected as well as Biodivers Conserv (2013) 22:3045-3065 3059 putatively neutral genetic markers, in species with a marine background (Limborg et al 2012;Teacher et al 2013;. However, it is important to note that demographic rather than non-adaptive forces, such as secondary contact between divergent lineages, or the formation of hybrid zones, have also generated similar patterns of genetic discontinuities in this region.…”

Selective exploitation of spatially structured coastal fish populations by recreational anglers may lead to evolutionary downsizing of adults

“…However, coastal currents may create barriers to dispersal (Cowen et al 2006). Recent studies that combined genetics and oceanography have suggested that marine fish populations are not as open as expected (Palumbi & Warner 2003, Teacher et al 2013. Even at spatial scales of a few kilometres, meta-populations with limited gene flow can emerge in the marine environment (e.g.…”