title: Parallel adaptive evolution of geographically distant herring populations on both sides of the North Atlantic Ocean.
abstract: Atlantic herring is an excellent species for studying the genetic basis of adaptation in geographically distant populations because of its characteristically large population sizes and low genetic drift. In this study we compared whole-genome resequencing data of Atlantic herring populations from both sides of the Atlantic Ocean. An important finding was the very low degree of genetic differentiation among geographically distant populations (fixation index = 0.026), suggesting lack of reproductive isolation across the ocean. This feature of the Atlantic herring facilitates the detection of genetic factors affecting adaptation because of the sharp contrast between loci showing genetic differentiation resulting from natural selection and the low background noise resulting from genetic drift. We show that genetic factors associated with timing of reproduction are shared between genetically distinct and geographically distant populations. The genes for thyroid-stimulating hormone receptor (TSHR), the SOX11 transcription factor (SOX11), calmodulin (CALM), and estrogen receptor 2 (ESR2A), all with a significant role in reproductive biology, were among the loci that showed the most consistent association with spawning time throughout the species range. In fact, the same two SNPs located at the 5' end ofTSHRshowed the most significant association with spawning time in both the east and west Atlantic. We also identified unexpected haplotype sharing between spring-spawning oceanic herring and autumn-spawning populations across the Atlantic Ocean and the Baltic Sea. The genomic regions showing this pattern are unlikely to control spawning time but may be involved in adaptation to ecological factor(s) shared among these populations.
authors.affiliation: Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, 752 36 Uppsala, Sweden.
authors.forename: Sangeet
authors.initials: S
authors.lastname: Lamichhaney
authors.affiliation: Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada.
authors.forename: Angela P
authors.initials: AP
authors.lastname: Fuentes-Pardo
authors.affiliation: Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, 752 36 Uppsala, Sweden.
authors.forename: Nima
authors.initials: N
authors.lastname: Rafati
authors.affiliation: Department of Zoology, Stockholm University, 106 91 Stockholm, Sweden.
authors.forename: Nils
authors.initials: N
authors.lastname: Ryman
authors.affiliation: Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada.
authors.forename: Gregory R
authors.initials: GR
authors.lastname: McCracken
authors.affiliation: Fisheries and Oceans Canada, Northwest Atlantic Fisheries Centre, St John's, Newfoundland A1C 5X1, Canada.
authors.forename: Christina
authors.initials: C
authors.lastname: Bourne
authors.affiliation: Fisheries and Oceans Canada, St. Andrews Biological Station, St. Andrews, New Brunswick E5B 2L9, Canada.
authors.forename: Rabindra
authors.initials: R
authors.lastname: Singh
authors.affiliation: Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada.
authors.forename: Daniel E
authors.initials: DE
authors.lastname: Ruzzante
authors.affiliation: Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, 752 36 Uppsala, Sweden; leif.andersson@imbim.uu.se.|Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, 750 07 Uppsala, Sweden.|Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, TX 77843.
authors.forename: Leif
authors.initials: L
authors.lastname: Andersson
mesh_terms: D000222:Adaptation, Physiological; D000818:Animals; D001267:Atlantic Ocean; D019143:Evolution, Molecular; D029941:Fish Proteins / Q000235:genetics*; D005399:Fishes / Q000235:genetics*; D055106:Genome-Wide Association Study; D011989:Receptors, Thyrotropin / Q000235:genetics*
chemical_list: D029941:Fish Proteins; D011989:Receptors, Thyrotropin
keywords: Atlantic herring; genetic adaptation; parallel evolution; reproductive strategies; whole-genome resequencing