Selection by higher-order effects of salinity and bacteria on early life-stages of Western Baltic spring-spawning herring.
ABSTRACT: Habitat stratification by abiotic and biotic factors initiates divergence of populations and leads to ecological speciation. In contrast to fully marine waters, the Baltic Sea is stratified by a salinity gradient that strongly affects fish physiology, distribution, diversity and virulence of important marine pathogens. Animals thus face the challenge to simultaneously adapt to the concurrent salinity and cope with the selection imposed by the changing pathogenic virulence. Western Baltic spring-spawning herring (Clupea harengus) migrate to spawning grounds characterized by different salinities to which herring are supposedly adapted. We hypothesized that herring populations do not only have to cope with different salinity levels but that they are simultaneously exposed to higher-order effects that accompany the shifts in salinity, that is induced pathogenicity of Vibrio bacteria in lower saline waters. To experimentally evaluate this, adults of two populations were caught in their spawning grounds and fully reciprocally crossed within and between populations. Larvae were reared at three salinity levels, representing the spawning ground salinity of each of the two populations, or Atlantic salinity conditions resembling the phylogenetic origin of Clupea harengus. In addition, larvae were exposed to a Vibrio spp. infection. Life-history traits and gene expression analysis served as response variables. Herring seem adapted to Baltic Sea conditions and cope better with low saline waters. However, upon a bacterial infection, herring larvae suffer more when kept at lower salinities implying reduced resistance against Vibrio or higher Vibrio virulence. In the context of recent climate change with less saline marine waters in the Baltic Sea, such interactions may constitute key future stressors.
Project description:Herring, Clupea harengus, is one of the ecologically and commercially most important species in European northern seas, where two distinct ecotypes have been described based on spawning time; spring and autumn. To date, it is unknown if these spring and autumn spawning herring constitute genetically distinct units. We assessed levels of genetic divergence between spring and autumn spawning herring in the Baltic Sea using two types of DNA markers, microsatellites and Single Nucleotide Polymorphisms, and compared the results with data for autumn spawning North Sea herring. Temporally replicated analyses reveal clear genetic differences between ecotypes and hence support reproductive isolation. Loci showing non-neutral behaviour, so-called outlier loci, show convergence between autumn spawning herring from demographically disjoint populations, potentially reflecting selective processes associated with autumn spawning ecotypes. The abundance and exploitation of the two ecotypes have varied strongly over space and time in the Baltic Sea, where autumn spawners have faced strong depression for decades. The results therefore have practical implications by highlighting the need for specific management of these co-occurring ecotypes to meet requirements for sustainable exploitation and ensure optimal livelihood for coastal communities.
Project description:The population structure of Atlantic herring (Clupea harengus) from 13 local, coastal and offshore areas of the North Sea, Skagerrak, Kattegat and western Baltic (northeast Atlantic) was studied using biological and environmental data from 1970-2015. The objective was to identify distinct populations by comparing variability in the temporal and spatial phenotypic characteristics and evaluate the potential for mixing of populations in time and space. The populations varied in biological characteristics such as mean vertebral counts (VS), growth and maturity ogives. Generalized additive models indicated temporally stable VS in the North Sea and western Baltic, whereas intra-annual temporal variation of VS occurred in other areas. High variability of VS within a population was not affected by environmental factors such as temperature and salinity. Consequently, seasonal VS variability can be explained by the presence or absence of herring populations as they migrate between areas. The three main populations identified in this paper correspond to the three managed stocks in this area: Norwegian spring spawners (NSS), western Baltic spring spawners (WBSS) and North Sea autumn spawners (NSAS). In addition, several local populations were identified in fjords or lakes along the coast, but our analyses could not detect direct mixing of local populations with the three main populations. Our results highlight the importance of recognizing herring dynamics and understanding the mixing of populations as a challenge for management of herring.
Project description:Baltic herring (Clupea harengus membras) is a total spawner with a group-synchronous ovarian organization. Age polymodality in total spawners is considered an important factor in assuring that a strong population is sustainable under an intensive harvesting regime and different climatic conditions. In the present study, we investigated the seasonal and inter-annual variation in spawner age structure and the effect of preceding winter thermal conditions on the start of the herring spawning and larvae retention period. Herring spawning season in the Gulf of Riga starts up to six weeks later after colder winters compared to milder winters. Significantly older individuals dominated at the beginning of the spawning season, and thus herring mean age gradually decreased towards the end of the spawning season from 1999-2015. On an annual scale, this pattern was obvious after cold winters, while after mild winters the pattern did not continue, indicating a more homogenous maturation cycle and spawning period, despite the age and size of the herring population in mild winters. Further, herring condition factor was studied in relation to age and spawning season following different winter thermal conditions. Young, 2- and 3- year old first-spawning herring experienced significantly lower conditions after cold winters compared to older ages, indicating an age-dependent effect of preceding winter on herring maturation cycle, condition and spawning time.
Project description:Atlantic herring, Clupea harengus, have complex population structures. Mixing of populations is known, but the extent of connectivity is still unclear. Phenotypic plasticity results in divergent phenotypes in response to environmental factors. A marked salinity gradient occurs from Atlantic Ocean (salinity 35) into the Baltic Sea (salinity range 2-12). Herring from both habitats display phenotypic and genetic variability. To explore how genetic factors and salinity influence phenotypic traits like growth, number of vertebrae and otolith shape an experimental population consisting of Atlantic purebreds and Atlantic/Baltic F1 hybrids were incubated and co-reared at two different salinities, 16 and 35, for three years. The F1-generation was repeatedly sampled to evaluate temporal variation. A von Bertalanffy growth model indicated that reared Atlantic purebreds had a higher maximum length (26.2 cm) than Atlantic/Baltic hybrids (24.8 cm) at salinity 35, but not at salinity 16 (25.0 and 24.8 cm, respectively). In contrast, Atlantic/Baltic hybrids achieved larger size-at-age than the wild caught Baltic parental group. Mean vertebral counts and otolith aspect ratios were higher for reared Atlantic purebreds than Atlantic/Baltic hybrids, consistent with the differences between parental groups. There were no significant differences in vertebral counts and otolith aspect ratios between herring with the same genotype but raised in different salinities. A Canonical Analysis of Principal Coordinates was applied to analyze the variation in wavelet coefficients that described otolith shape. The first discriminating axis identified the differences between Atlantic purebreds and Atlantic/Baltic hybrids, while the second axis represented salinity differences. Assigning otoliths based on genetic groups (Atlantic purebreds vs. Atlantic/Baltic hybrids) yielded higher classification success (~90%) than based on salinities (16 vs. 35; ~60%). Our results demonstrate that otolith shape and vertebral counts have a significant genetic component and are therefore useful for studies on population dynamics and connectivity.
Project description: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.
Project description:BACKGROUND: Marine fish, such as the Atlantic herring (Clupea harengus), often show a low degree of differentiation over large geographical regions. Despite strong environmental gradients (salinity and temperature) in the Baltic Sea, population genetic studies have shown little genetic differentiation among herring in this area, but some evidence for environmentally-induced selection has been uncovered. The mitochondrial genome is a likely target for selection in this system due to its functional role in metabolism. RESULTS: We sequenced whole mitochondrial genomes for herring from throughout the Baltic region (n=98) in order to investigate evidence for geographical structuring, selection, and associations between genetic and environmental variation. Three well-supported clades that predate the formation of the Baltic Sea were identified, but geographic structuring of this variation was weak (?ST = 0.036). There was evidence for significant positive selection, particularly in the ND2, ND4 and ND5 genes, and amino acids under significant selection in these genes explained some of the clade formation. Despite uncovering evidence for selection, correlations between genetic diversity or differentiation with environmental factors (temperature, salinity, latitude) were weak. CONCLUSIONS: The results indicate that most of the current mtDNA diversity in herring predates the formation of the Baltic Sea, and that little structuring has evolved since. Thus, fisheries management units in this region cannot be determined on the basis of mtDNA variability. Preliminary evidence for selection underlying clade formation indicates that the NADH complex may be useful for examining adaptation and population structuring at a broader geographical scale.
Project description:The existence of biologically differentiated populations has been credited with a major role in conferring sustainability and in buffering overall productivity of anadromous fish population complexes where evidence for spatial structure is uncontroversial. Here, we describe evidence of correlated genetic and life history (spawning season linked to spawning location) differentiation in an abundant and highly migratory pelagic fish, Atlantic herring, Clupea harengus, in the North Sea (NS) and adjacent areas. The existence of genetically and phenotypically diverse stocks in this region despite intense seasonal mixing strongly implicates natal homing in this species. Based on information from genetic markers and otolith morphology, we estimate the proportional contribution by NS, Skagerrak (SKG) and Kattegat and western Baltic (WBS) fish to mixed aggregations targeted by the NS fishery. We use these estimates to identify spatial and temporal differences in life history (migratory behaviour) and habitat use among genetically differentiated migratory populations that mix seasonally. Our study suggests the existence of more complex patterns of intraspecific diversity than was previously recognized. Sustainability may be compromised if such complex patterns are reduced through generalized management (e.g. area closures) that overlooks population differences in spatial use throughout the life cycle.
Project description:Norwegian Spring Spawning herring (NSSH) Clupea harengus L. spawn on coastal banks along the west coast of Norway. The larvae are generally transported northward in the Norwegian Coastal Current (NCC) with many individuals utilizing nursery grounds in the Barents Sea. The recruitment to this stock is highly variable with a few years having exceptionally good recruitment. The principal causes of recruitment variability of this herring population have been elusive. Here we undertake an event analysis using data between 1948 and 2010 to gain insight into the physical conditions in the NCC that coincide with years of high recruitment. In contrast to a typical year when northerly upwelling winds are prominent during spring, the years with high recruitment coincide with predominantly southwesterly winds and weak upwelling in spring and summer, which lead to an enhanced northward coastal current during the larval drift period. Also in most peak recruitment years, low-salinity anomalies are observed to propagate northward during the spring and summer. It is suggested that consistent southwesterly (downwelling) winds and propagating low-salinity anomalies, both leading to an enhanced northward transport of larvae, are important factors for elevated recruitment. At the same time, these conditions stabilize the coastal waters, possibly leading to enhanced production and improved feeding potential along the drift route to Barents Sea. Further studies on the drivers of early life history mortality can now be undertaken with a better understanding of the physical conditions that prevail during years when elevated recruitment occurs in this herring stock.
Project description:Thiamine (vitamin B1) deficiency in salmonids related to a lipid-rich fish diet causes offspring mortality in the yolk-sac fry phase. A low free thiamine (THIAM) concentration in eggs is an indication of this syndrome. Thiamine deficiency of salmon (Salmo salar) feeding in the Baltic Sea, called M74, was connected to the principal prey fish and feeding area using fatty acid (FA) signature analysis. The FAs of feeding salmon from two areas of the Baltic Sea, the Baltic Proper (57°10' 19°30') and the Bothnian Sea (61°30' 20°00') in 2004, reflected the principal prey species in these areas, sprat (Sprattus sprattus) and herring (Clupea harengus), respectively. Arachidonic acid (ARA, 20:4n-6) and 18:1n-7 indicated dietary herring, 18:1n-9 dietary sprat and 14:0 feeding in the Baltic Proper. The muscle FA profile of non-M74 female spawners of the River Simojoki in a year (1998) with a moderate M74 incidence and salmon of a non-M74 year (2004) reflected herring FAs, whereas the FAs in the M74 year and specifically in M74 females displayed characteristics of sprat. In the M74 year, the THIAM concentration had the strongest positive correlation with the proportion of muscle ARA, and the strongest negative correlations with 14:0 and the ratios 18:1n-9/ARA and 14:0/ARA. Thus, ARA along with 14:0 and these ratios were the most sensitive FA indicators of the dietary species and origin of the M74 syndrome. Despite the pre-spawning fasting, tissue FA signatures were consequently able to connect dietary sprat in the Baltic Proper with thiamine deficiency in Baltic salmon.
Project description:Atlantic herring (Clupea harengus), a vital ecosystem component and target of the largest Northwest Atlantic pelagic fishery, undergo seasonal spawning migrations that result in elusive sympatric population structure. Herring spawn mostly in fall or spring, and genomic differentiation was recently detected between these groups. Here we used a subset of this differentiation, 66 single nucleotide polymorphisms (SNPs) to analyze the temporal dynamics of this local adaptation and the applicability of SNP subsets in stock assessment. We showed remarkable temporal stability of genomic differentiation corresponding to spawning season, between samples taken a decade apart (2005 N = 90 vs. 2014 N = 71) in the Gulf of St. Lawrence, and new evidence of limited interbreeding between spawning components. We also examined an understudied and overexploited herring population in Bras d'Or lake (N = 97); using highly reduced SNP panels (N SNPs > 6), we verified little-known sympatric spawning populations within this unique inland sea. These results describe consistent local adaptation, arising from asynchronous reproduction in a migratory and dynamic marine species. Our research demonstrates the efficiency and precision of SNP-based assessments of sympatric subpopulations; and indeed, this temporally stable local adaptation underlines the importance of such fine-scale management practices.