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1.
  • Bekkevold, Dorte, et al. (author)
  • Mixed-stock analysis of Atlantic herring (Clupea harengus) : a tool for identifying management units and complex migration dynamics
  • 2023
  • In: ICES Journal of Marine Science. - : Oxford University Press. - 1054-3139 .- 1095-9289. ; 80:1, s. 173-184
  • Journal article (peer-reviewed)abstract
    • We developed and validated a mixed-stock analysis (MSA) method with 59 single-nucleotide polymorphisms selected from genome-wide data to assign individuals to populations in mixed-stock samples of Atlantic herring from the North and Baltic seas. We analysed 3734 herring from spawning locations and scientific catches of mixed feeding stocks to demonstrate a "one-fits-all" tool with unprecedented accuracy for monitoring spatio-temporal dynamics throughout a large geographical range with complex stock mixing. We re-analysed time-series data (2002-2021) and compared inferences about stock composition with estimates from morphological data. We show that contributions from the western Baltic spring-spawning stock complex, which is under management concern, have likely been overestimated. We also show that a genetically distinctive population of western Baltic autumn spawners, ascribed low fisheries importance, contributes non-negligible and potentially temporally increasing proportions to mixed-stock aggregations, calling for a re-evaluation of stock definitions. MSA data can be implemented in stock assessment and in a variety of applications, including marine ecosystem description, impact assessment of specific fleets, and stock-rebuilding plans.
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2.
  • Berg, Florian, et al. (author)
  • A combination of genetic and phenotypic characterization of spring- and autumn-spawning herring suggests gene flow between populations
  • 2021
  • In: ICES Journal of Marine Science. - : Oxford University Press. - 1054-3139 .- 1095-9289. ; 78:2, s. 694-703
  • Journal article (peer-reviewed)abstract
    • Atlantic herring (Clupea harengus) has complex population structure and dynamics including diverse life histories and spawning times with spring and autumn spawning as the most common modes. Originally, spawning herring were phenotypically identified based on their maturity development or otolith microstructure by determining seasonal specific larval growth patterns. Recently, genetic markers have revealed clear genetic differentiation between spring- and autumn-spawning populations. All three methods were applied to herring caught at the same locations during spring and autumn to determine the coherence of methods. In a selected subset, most herring (similar to 77%) had an otolith microstructure and genetic assignment coinciding with the phenotypically assigned spawning season. Non-spawning herring (<5%) that were classified as belonging to the current spawning season using genotyping and otolith-typing were assigned as skipped spawners. For similar to 8% of spawning herring, the genetic and otolith assignment contradicted the phenotypically assigned spawning season, characteristic of straying individuals. Otolith-typing contradicted the genetic and phenotypical assignment in similar to 7% of the cases, potentially representing individuals reuniting back to the spawning season favoured by their genotype. Although the viability of offspring from these individuals remains undocumented, it is suggested that the observed switching of spawning season may contribute to gene flow between herring populations.
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3.
  • Berg, Florian, et al. (author)
  • Genetic factors have a major effect on growth, number of vertebrae and otolith shape in Atlantic herring (Clupea harengus)
  • 2018
  • In: PLOS ONE. - : Public Library of Science (PLoS). - 1932-6203. ; 13:1
  • Journal article (peer-reviewed)abstract
    • 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.
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4.
  • Berg, Florian, et al. (author)
  • Genetic origin and salinity history influence the reproductive success of Atlantic herring
  • 2019
  • In: Marine Ecology Progress Series. - : Inter-Research Science Center. - 0171-8630 .- 1616-1599. ; 617, s. 81-94
  • Journal article (peer-reviewed)abstract
    • Atlantic herring populations inhabit environments ranging in salinity from fully marine to nearly freshwater, but their relative reproductive success in these respective environments remains unclear. We conducted factorial crossing experiments using parents from 3 wild populations associated with different salinity environments: the Baltic Sea (similar to 6 psu), an inland brackish lake in Norway (Landvikvannet, similar to 16 psu), and the Atlantic (similar to 30 to 35 psu). Further experiments used crosses within and between Atlantic purebreds and Atlantic/Baltic hybrids reared until first maturity at 3 yr of age. Crossing experiments were conducted at 6, 16 and 35 psu. Fertilization and hatching rates were estimated, and egg sizes were measured. Fertilization rates were highest at 16 psu for all combinations. The paternal genetic and salinity origin influenced fertilization rates at 6 and 35 psu, indicating a genetic adaptation to their original environment. Fertilization rates for males originating from 16 psu were low at 35 psu. Atlantic/Baltic hybrids had lower fertilization rates than Atlantic purebreds at 35 psu. Hatching rates were not influenced by any parental factors or salinity. Maternal effects and salinity influenced egg size. Atlantic females had significantly larger eggs than the Atlantic/Baltic hybrid females. For all genetic groups, egg size decreased with increasing salinity at incubation mainly due to osmotic effects. The observed lower fertilization success at salinities other than those of the parental fish habitat would have evolutionary consequences when herring colonize new habitats with different salinities or if interbreeding occurred between populations originating from different salinity habitats.
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5.
  • Berg, Florian, et al. (author)
  • Respiration rates of herring larvae at different salinities, and effects of previous environmental history
  • 2020
  • In: Marine Ecology Progress Series. - : INTER-RESEARCH. - 0171-8630 .- 1616-1599. ; 650, s. 141-152
  • Journal article (peer-reviewed)abstract
    • Metabolic rates of early life history stages of marine fishes show considerable interindividual differences, and are highly influenced by extrinsic factors like temperature or food availability. Measuring oxygen uptake rates is a proxy for estimating metabolic rates. Still, the relationship between respiration rates and ambient or previous salinity conditions as well as parental and developmental acclimation to changes in salinity remains largely unexplored. In the present study, we conducted experiments to investigate the effects of salinity on the routine metabolic rates (RMR) of euryhaline Atlantic herring Clupea harengus larvae at 3 levels of salinity: low (6 psu), intermediate (16 psu) and high (35 psu), reflecting ecologically relevant conditions for herring populations in the Atlantic Ocean and Baltic Sea. The larvae originated from different genetic backgrounds and salinity adaptations to account for cross-generation effects on metabolic rates. Closed respirometry carried out over 24 h on individual fish larvae generally confirmed near isometric respiration rates at all salinity regimes, with rates being 15.4% higher at 6 psu and 7.5% higher at 35 psu compared to 16 psu conditions. However, transgenerational acclimation to different salinity regimes of the parents had no effect on the salinity-specific metabolic rates of their offspring. Our study demonstrates the ability of herring to cope with a wide range of salinity conditions, irrespective of parental environmental history and genetic origin. This phenotypic plasticity is considered to be one of the main contributing factors to the success of herring as a widely distributed fish species in the North Atlantic and adjacent waters.
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6.
  • Farrell, Edward D. D., et al. (author)
  • A baseline for the genetic stock identification of Atlantic herring, Clupea harengus, in ICES Divisions 6.a, 7.b-c
  • 2022
  • In: Royal Society Open Science. - : The Royal Society. - 2054-5703. ; 9:9
  • Journal article (peer-reviewed)abstract
    • Atlantic herring in International Council for Exploration of the Sea (ICES) Divisions 6.a, 7.b-c comprises at least three populations, distinguished by temporal and spatial differences in spawning, which have until recently been managed as two stocks defined by geographical delineators. Outside of spawning the populations form mixed aggregations, which are the subject of acoustic surveys. The inability to distinguish the populations has prevented the development of separate survey indices and separate stock assessments. A panel of 45 single-nucleotide polymorphisms, derived from whole-genome sequencing, were used to genotype 3480 baseline spawning samples (2014-2021). A temporally stable baseline comprising 2316 herring from populations known to inhabit Division 6.a was used to develop a genetic assignment method, with a self-assignment accuracy greater than 90%. The long-term temporal stability of the assignment model was validated by assigning archive (2003-2004) baseline samples (270 individuals) with a high level of accuracy. Assignment of non-baseline samples (1514 individuals) from Divisions 6.a, 7.b-c indicated previously unrecognized levels of mixing of populations outside of the spawning season. The genetic markers and assignment models presented constitute a 'toolbox' that can be used for the assignment of herring caught in mixed survey and commercial catches in Division 6.a into their population of origin with a high level of accuracy.
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7.
  • Feng, Chungang, et al. (author)
  • Moderate nucleotide diversity in the Atlantic herring is associated with a low mutation rate
  • 2017
  • In: eLIFE. - : ELIFE SCIENCES PUBLICATIONS LTD. - 2050-084X. ; 6
  • Journal article (peer-reviewed)abstract
    • The Atlantic herring is one of the most abundant vertebrates on earth but its nucleotide diversity is moderate (pi = 0.3%), only three-fold higher than in human. Here, we present a pedigree-based estimation of the mutation rate in this species. Based on whole-genome sequencing of four parents and 12 offspring, the estimated mutation rate is 2.0 x 10(-9) per base per generation. We observed a high degree of parental mosaicism indicating that a large fraction of these de novo mutations occurred during early germ cell development. The estimated mutation rate the lowest among vertebrates analyzed to date - partially explains the discrepancy between the rather low nucleotide diversity in herring and its huge census population size. But a species like the herring will never reach its expected nucleotide diversity because of fluctuations in population size over the millions of years it takes to build up high nucleotide diversity.
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8.
  • Han, Fan, et al. (author)
  • Ecological adaptation in Atlantic herring is associated with large shifts in allele frequencies at hundreds of loci
  • 2020
  • In: eLIFE. - : ELIFE SCIENCES PUBLICATIONS LTD. - 2050-084X. ; 9
  • Journal article (peer-reviewed)abstract
    • Atlantic herring is widespread in North Atlantic and adjacent waters and is one of the most abundant vertebrates on earth. This species is well suited to explore genetic adaptation due to minute genetic differentiation at selectively neutral loci. Here, we report hundreds of loci underlying ecological adaptation to different geographic areas and spawning conditions. Four of these represent megabase inversions confirmed by long read sequencing. The genetic architecture underlying ecological adaptation in herring deviates from expectation under a classical infinitesimal model for complex traits because of large shifts in allele frequencies at hundreds of loci under selection.
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9.
  • Hill, Jason, et al. (author)
  • Recurrent convergent evolution at amino acid residue 261 in fish rhodopsin
  • 2019
  • In: Proceedings of the National Academy of Sciences of the United States of America. - : Proceedings of the National Academy of Sciences. - 0027-8424 .- 1091-6490. ; 116:37, s. 18473-18478
  • Journal article (peer-reviewed)abstract
    • The evolutionary process that occurs when a species colonizes a new environment provides an opportunity to explore the mechanisms underlying genetic adaptation, which is essential knowledge for understanding evolution and the maintenance of biodiversity. Atlantic herring has an estimated total breeding stock of about 1 trillion (10(12)) and has colonized the brackish Baltic Sea within the last 10,000 y. Minute genetic differentiation between Atlantic and Baltic herring populations at selectively neutral loci combined with this rapid adaptation to a new environment facilitated the identification of hundreds of loci underlying ecological adaptation. A major question in the field of evolutionary biology is to what extent such an adaptive process involves selection of novel mutations with large effects or genetic changes at many loci, each with a small effect on phenotype (i.e., selection on standing genetic variation). Here we show that a missense mutation in rhodopsin (Phe261Tyr) is an adaptation to the red-shifted Baltic Sea light environment. The transition from phenylalanine to tyrosine differs only by the presence of a hydroxyl moiety in the latter, but this results in an up to 10-nm red-shifted light absorbance of the receptor. Remarkably, an examination of the rhodopsin sequences from 2,056 species of fish revealed that the same missense mutation has occurred independently and been selected for during at least 20 transitions between light environments across all fish. Our results provide a spectacular example of convergent evolution and how a single amino acid change can have a major effect on ecological adaptation.
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10.
  • Martínez Barrio, Álvaro, et al. (author)
  • The genetic basis for ecological adaptation of the Atlantic herring revealed by genome sequencing
  • 2016
  • In: eLIFE. - 2050-084X. ; 5
  • Journal article (peer-reviewed)abstract
    • Ecological adaptation is of major relevance to speciation and sustainable population management, but the underlying genetic factors are typically hard to study in natural populations due to genetic differentiation caused by natural selection being confounded with genetic drift in subdivided populations. Here, we use whole genome population sequencing of Atlantic and Baltic herring to reveal the underlying genetic architecture at an unprecedented detailed resolution for both adaptation to a new niche environment and timing of reproduction. We identify almost 500 independent loci associated with a recent niche expansion from marine (Atlantic Ocean) to brackish waters (Baltic Sea), and more than 100 independent loci showing genetic differentiation between spring- and autumn-spawning populations irrespective of geographic origin. Our results show that both coding and non-coding changes contribute to adaptation. Haplotype blocks, often spanning multiple genes and maintained by selection, are associated with genetic differentiation.
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