Parallel adaptive evolution of geographically distant PNAS PLUS herring populations on both sides of the North Atlantic Ocean Sangeet Lamichhaneya,1, Angela P. Fuentes-Pardob,1, Nima Rafatia, Nils Rymanc, Gregory R. McCrackenb, Christina Bourned, Rabindra Singhe, Daniel E. Ruzzanteb, and Leif Anderssona,f,g,2 aScience for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, 752 36 Uppsala, Sweden; bDepartment of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada; cDepartment of Zoology, Stockholm University, 106 91 Stockholm, Sweden; dFisheries and Oceans Canada, Northwest Atlantic Fisheries Centre, St John’s, Newfoundland A1C 5X1, Canada; eFisheries and Oceans Canada, St. Andrews Biological Station, St. Andrews, New Brunswick E5B 2L9, Canada; fDepartment of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, 750 07 Uppsala, Sweden; and gDepartment of Veterinary Integrative Biosciences, Texas A&M University, College Station, TX 77843 Contributed by Leif Andersson, February 24, 2017 (sent for review October 27, 2016; reviewed by Dorte Bekkevold and Craig R. Primmer) Atlantic herring is an excellent species for studying the genetic basis with traditional genome scans, and adaptive changes can often of adaptation in geographically distant populations because of its be confounded with demographic history effects such as pop- characteristically large population sizes and low genetic drift. In this ulation structure and genetic drift (10), making the dissection of study we compared whole-genome resequencing data of Atlantic such genetic differentiations challenging. herring populations from both sides of the Atlantic Ocean. An Our recent population-scale genomic study on Atlantic her- important finding was the very low degree of genetic differen- ring has demonstrated that this species is an ideal model for the tiation among geographically distant populations (fixation index = detection of signatures of selection (11, 12). The large effective 0.026), suggesting lack of reproductive isolation across the ocean. population size (Atlantic herring is one of the most abundant fish This feature of the Atlantic herring facilitates the detection of ge- species on earth) probably combined with gene flow between netic factors affecting adaptation because of the sharp contrast populations results in extremely low levels of genetic differenti- GENETICS between loci showing genetic differentiation resulting from ation at selectively neutral loci across populations exposed to natural selection and the low background noise resulting from different ecological conditions. These factors allowed us to genetic drift. We show that genetic factors associated with tim- identify about 500 independent loci associated with local adap- ing of reproduction are shared between genetically distinct and geographically distant populations. The genes for thyroid- tation as regards the colonization of the brackish Baltic Sea and stimulating hormone receptor (TSHR), the SOX11 transcription timing of reproduction in Northeast (NE) Atlantic herring factor (SOX11), calmodulin (CALM), and estrogen receptor 2 populations (11). (ESR2A), all with a significant role in reproductive biology, were Atlantic herring is a schooling pelagic fish distributed throughout among the loci that showed the most consistent association with the North Atlantic Ocean and adjacent waters, including the Baltic spawning time throughout the species range. In fact, the same Sea (Fig. 1). The population structure of Atlantic herring is con- two SNPs located at the 5′ end of TSHR showed the most signif- sidered to be one of the most complex of any marine fish, and there icant association with spawning time in both the east and west is a long history of attempts to describe it (13). Traditionally, herring Atlantic. We also identified unexpected haplotype sharing be- tween spring-spawning oceanic herring and autumn-spawning Significance populations across the Atlantic Ocean and the Baltic Sea. The genomic regions showing this pattern are unlikely to control Identification of genetic changes that allow a species to adapt spawning time but may be involved in adaptation to ecological to different environmental conditions is an important topic in factor(s) shared among these populations. evolutionary biology. In this study we analyzed whole-genome resequencing data of Atlantic herring populations from both genetic adaptation | Atlantic herring | parallel evolution | reproductive sides of the Atlantic Ocean and identified a number of loci that strategies | whole-genome resequencing show consistent associations with spawning time (spring or autumn). Several of these loci, such as thyroid-stimulating hor- idely dispersed and abundant species generally exhibit mone receptor (TSHR), have a well-established role in reproduc- Wpopulations inhabiting divergent habitats. Such pop- tive biology, whereas others have never been implicated in ulations need to adapt to local biotic and abiotic factors, a controlling reproduction. Genetic variants associated with adap- process that results in higher fitness in the local environment and tation to spring or autumn spawning are shared to a large extent leads to genetic and phenotypic differentiation among subpop- among populations across the Atlantic Ocean and the Baltic Sea, ulations (1, 2). In addition to such local adaptation, if a trait providing evidence for parallel adaptive evolution. responds to similar forces of natural selection independently Author contributions: D.E.R. and L.A. conceived the study; S.L., A.P.F.-P., N. Rafati, and across multiple populations or species, parallel evolution will N. Ryman performed research; G.R.M., C.B., and R.S. contributed critical samples for the lead to similar adaptive changes among geographically distant study; and S.L., A.P.F.-P., D.E.R., and L.A. wrote the paper. populations (3). Such parallel adaptation may be caused by Reviewers: D.B., Technical University of Denmark; and C.R.P., University of Turku. convergent evolution or by the sharing of similar (or identical) The authors declare no conflict of interest. – genetic changes across populations (4 6). Identification of the Freely available online through the PNAS open access option. genetic basis for ecological adaptation is a fundamental goal in Data deposition: The Illumina reads reported in this article have been submitted to the evolutionary biology (7), and current technological advances in Short Reads Archive (https://www.ncbi.nlm.nih.gov/sra) (accession no. PRJNA338612). population-scale high-throughput sequencing provide powerful 1S.L. and A.P.F.-P. contributed equally to this work. tools to explore these processes at a genomic scale (8). However, 2To whom correspondence should be addressed. Email: [email protected]. many adaptive traits are expected to have a highly polygenic This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. background (9) in which genes of small effect are hard to detect 1073/pnas.1617728114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1617728114 PNAS Early Edition | 1of10 Downloaded by guest on September 24, 2021 Canada 35‰ WInB WBoB 35‰ WFB NW Atlantic Ocean WNsS WNsF 35‰ WGeB United States Baltic Sea Kattegat Skagerrak North Sea NE Atlantic Ocean NW Atlantic Ocean NE Atlantic Ocean BK AB1 3‰ Iceland Sweden AI Finland BU 6‰ BÄV Norway BH BÄH 35‰ BÄS BV SH 7‰ North Sea SB KB BG NS 32‰ KT 20‰ BA BR Baltic Sea 12‰ BC Fig. 1. Sampling sites. Geographic location of all BF population samples. Abbreviations for localities are given in Table 1. The relative locations of pop- ulations sampled from the NW and NE Atlantic Ocean are indicated in the inserted globe. Maps were created using ArcGIS (Esri). stocks have been described based on morphology and life history Northwest (NW) Atlantic (17), where the species is recognized traits such as spawning time and location (13–15). Populations are for the complexity and plasticity of its stocks (13, 18). Similar to known to spawn in different seasons, with some spawning in the the NE Atlantic populations, herring in the NW Atlantic un- spring, others in the autumn, and still others at intermediate times. dergo north–south and inshore–offshore migrations for feeding In each case, spawning generally takes place over a protracted pe- and reproduction (19), with spawning taking place mostly during riod of a few weeks. The optimal spawning time is generally linked spring and autumn (20) from Cape Cod to northern New- to environmental conditions associated with plankton blooms (16). foundland (14). Previous genetic studies based on a small num- Our recent study revealed highly significant genetic differentiation ber of microsatellite markers reported weak but significant between spring- and autumn-spawning herring in the NE Atlantic, genetic structuring between NW and NE Atlantic populations as with some of the loci involved in this differentiation likely control- well as among spawning aggregations within the NW Atlantic ling the timing of reproduction (11). (21, 22). Our previous genome-scale studies of Atlantic herring were The presence of spring- and autumn-spawning herring pop- restricted to population samples from the NE Atlantic, but this ulations on both sides of the North Atlantic provides an excep- species is ecologically important throughout the North Atlantic. tional opportunity to explore whether the same or similar genetic In fact, herring support a commercially important