The genetic architecture underlying ecological adaptation in Atlantic herring is not consistent with the infinitesimal model

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 the herring is in conflict with the infinitesimal model for complex traits because of the large shifts in allele frequencies at hundreds of loci under selection.

[1]  L. Andersson,et al.  A combination of genetic and phenotypic characterization of spring- and autumn-spawning herring suggests gene flow between populations , 2020, ICES Journal of Marine Science.

[2]  S. Tischkau.  Mechanisms of circadian clock interactions with aryl hydrocarbon receptor signalling , 2020, The European journal of neuroscience.

[3]  X. Jiao,et al.  Thyroid hormone receptor beta mutations alter photoreceptor development and function in Danio rerio (zebrafish) , 2019, bioRxiv.

[4]  Mats E. Pettersson,et al.  Recurrent convergent evolution at amino acid residue 261 in fish rhodopsin , 2019, Proceedings of the National Academy of Sciences.

[5]  Li Xuejiao,et al.  Asymmetrical methyltransferase PRMT3 regulates human mesenchymal stem cell osteogenesis via miR-3648 , 2019, Cell Death & Disease.

[6]  He Zhang,et al.  A chromosome-level assembly of the Atlantic herring genome—detection of a supergene and other signals of selection , 2019, Genome Research.

[7]  A. Whitehead,et al.  Adaptive introgression enables evolutionary rescue from extreme environmental pollution , 2019, Science.

[8]  L. Andersson,et al.  Adaptation to seasonal reproduction and temperature-associated factors drive temporal and spatial differentiation in northwest Atlantic herring despite gene flow , 2019, bioRxiv.

[9]  T. Yoshimura,et al.  Photoperiodic Regulation of Reproduction in Vertebrates. , 2019, Annual review of animal biosciences.

[10]  L. Bernatchez,et al.  Eco-Evolutionary Genomics of Chromosomal Inversions. , 2018, Trends in ecology & evolution.

[11]  Heng Li,et al.  Minimap2: pairwise alignment for nucleotide sequences , 2017, Bioinform..

[12]  Michael C. Schatz,et al.  Accurate detection of complex structural variations using single molecule sequencing , 2017, Nature Methods.

[13]  O. Daumke,et al.  Structural Basis for Aryl Hydrocarbon Receptor-Mediated Gene Activation. , 2017, Structure.

[14]  Mats E. Pettersson,et al.  Moderate nucleotide diversity in the Atlantic herring is associated with a low mutation rate , 2017, bioRxiv.

[15]  L. Andersson,et al.  Parallel adaptive evolution of geographically distant herring populations on both sides of the North Atlantic Ocean , 2017, Proceedings of the National Academy of Sciences.

[16]  Michael C. Schatz,et al.  Ribbon: Visualizing complex genome alignments and structural variation , 2016, bioRxiv.

[17]  M. Goddard,et al.  Genetics of complex traits: prediction of phenotype, identification of causal polymorphisms and genetic architecture , 2016, Proceedings of the Royal Society B: Biological Sciences.

[18]  Mats E. Pettersson,et al.  The genetic basis for ecological adaptation of the Atlantic herring revealed by genome sequencing , 2016, eLife.

[19]  C. Antunes,et al.  Effects of salinity on upstream-migrating, spawning sea lamprey, Petromyzon marinus , 2016, Conservation physiology.

[20]  J. Naggert,et al.  A Mutation in Syne2 Causes Early Retinal Defects in Photoreceptors, Secondary Neurons, and Müller Glia. , 2015, Investigative ophthalmology & visual science.

[21]  N. Hintzen,et al.  Managing a complex population structure: exploring the importance of information from fisheries-independent sources , 2015 .

[22]  R. Nash,et al.  Seasonal Dynamics of Atlantic Herring (Clupea harengus L.) Populations Spawning in the Vicinity of Marginal Habitats , 2014, PloS one.

[23]  Ross M. Fraser,et al.  Defining the role of common variation in the genomic and biological architecture of adult human height , 2014, Nature Genetics.

[24]  D. Petrov,et al.  Genomic Evidence of Rapid and Stable Adaptive Oscillations over Seasonal Time Scales in Drosophila , 2013, PLoS genetics.

[25]  H. Ono,et al.  The saccus vasculosus of fish is a sensor of seasonal changes in day length , 2013, Nature Communications.

[26]  Heng Li.  Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[27]  L. Pnueli,et al.  Gonadotrophin‐Releasing Hormone Signalling Downstream of Calmodulin , 2012, Journal of neuroendocrinology.

[28]  M. Grabherr,et al.  Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring , 2012, Proceedings of the National Academy of Sciences.

[29]  Martin I. Taylor,et al.  Environmental selection on transcriptome‐derived SNPs in a high gene flow marine fish, the Atlantic herring (Clupea harengus) , 2012, Molecular ecology.

[30]  R. Weiss,et al.  Homozygous thyroid hormone receptor β-gene mutations in resistance to thyroid hormone: three new cases and review of the literature. , 2012, The Journal of clinical endocrinology and metabolism.

[31]  Robert Kofler,et al.  PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq) , 2011, Bioinform..

[32]  Gonçalo R. Abecasis,et al.  The variant call format and VCFtools , 2011, Bioinform..

[33]  Helga Thorvaldsdóttir,et al.  Integrative Genomics Viewer , 2011, Nature Biotechnology.

[34]  D. Conley,et al.  The Development of the Baltic Sea Basin During the Last 130 ka , 2011 .

[35]  A. Punt,et al.  Reconciling stock assessment and management scales under conditions of spatially varying catch histories , 2011 .

[36]  M. DePristo,et al.  The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. , 2010, Genome research.

[37]  N. Ryman,et al.  Temporally stable genetic structure of heavily exploited Atlantic herring (Clupea harengus) in Swedish waters , 2010, Heredity.

[38]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[39]  L. Andersson,et al.  Genetic variability in Atlantic herring (Clupea harengus harengus): description of protein loci and population data , 2009 .

[40]  B. Browning,et al.  Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. , 2007, American journal of human genetics.

[41]  Manuel A. R. Ferreira,et al.  PLINK: a tool set for whole-genome association and population-based linkage analyses. , 2007, American journal of human genetics.

[42]  K. V. Van Look,et al.  Molecular basis of sex and reproductive status in breeding zebrafish. , 2007, Physiological genomics.

[43]  Stefano Mariani,et al.  Divergent origins of sympatric herring population components determined using genetic mixture analysis , 2007 .

[44]  L. Clausen,et al.  Application and validation of otolith microstructure as a stock identification method in mixed Atlantic herring (Clupea harengus) stocks in the North Sea and western Baltic , 2007 .

[45]  I. McQuinn,et al.  Metapopulations and the Atlantic herring , 1997, Reviews in Fish Biology and Fisheries.

[46]  S. Salzberg,et al.  Fast algorithms for large-scale genome alignment and comparison. , 2002, Nucleic acids research.

[47]  Lori A. Manzon.  The role of prolactin in fish osmoregulation: a review. , 2002, General and comparative endocrinology.

[48]  I. Johnston,et al.  Functional consequences and population differences in the developmental plasticity of muscle to temperature in Atlantic herring Clupea harengus , 2001 .

[49]  Øyvind Ulltang,et al.  Varlation in migration and abundance of norwegian spring spawning herring (Clupea harengus L.) , 1997 .

[50]  L. Andersson,et al.  Lack of correspondence between genetic and morphologic variability patterns in Atlantic herring (Clupea harengus) , 1984, Heredity.

[51]  M. Bulmer,et al.  The Effect of Selection on Genetic Variability , 1971, The American Naturalist.

[52]  R. C. Macridis.  A review , 1963 .

[53]  R. Fisher.  XV.—The Correlation between Relatives on the Supposition of Mendelian Inheritance. , 1919, Transactions of the Royal Society of Edinburgh.

[54]  L. Penrose,et al.  THE CORRELATION BETWEEN RELATIVES ON THE SUPPOSITION OF MENDELIAN INHERITANCE , 2022 .