Trans-Atlantic genomic differentiation and parallel environmental and allelic variation in lumpfish (cyclopterus lumpus)

Authors: LANGILLE, BARBARA - Department Of Fisheries And Oceans Canada; KESS, TONY - Department Of Fisheries And Oceans Canada; NUGENT, CAMERON - Fisheries & Oceans; MESSMER, AMBER - Fisheries & Oceans; DUFFY, STEVEN - Fisheries & Oceans; KNUTSEN, TIM MARTIN - Aquagen; KENT, MATTHEW - Norwegian University Of Life Sciences; BOYCE, DANNY - Memorial University Of Newfounland; GREGORY, ROBERT - Fisheries & Oceans; GAUTHIER, JOHANNE - Fisheries & Oceans; FAIRCHILD, ELIZABETH - University Of New Hampshire; Pietrak, Michael; EDDY, STEPHEN - University Of Maine; GARCIA DE LEANIZ, CARLOS - Swansea University; CONSUEGRA, SOFIA - Swansea University; WHITTAKER, BEN - Swansea University; BENTZEN, PAUL - Dalhousie University; BRADBURY, IAN - Department Of Fisheries And Oceans Canada

Submitted to: ICES Journal of Marine Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/15/2024
Publication Date: 4/15/2024
Citation: Langille, B.L., Kess, T., Nugent, C.M., Messmer, A., Duffy, S.J., Knutsen, T., Kent, M., Boyce, D., Gregory, R.S., Gauthier, J., Fairchild, E.A., Pietrak, M.R., Eddy, S., Garcia De Leaniz, C., Consuegra, S., Whittaker, B., Bentzen, P., Bradbury, I.R. 2024. Trans-Atlantic genomic differentiation and parallel environmental and allelic variation in lumpfish (cyclopterus lumpus). ICES Journal of Marine Science. 81(6):1025-1038. https://doi.org/10.1093/icesjms/fsae057.
DOI: https://doi.org/10.1093/icesjms/fsae057

Interpretive Summary: Lumpfish are common across the north Atlantic Ocean and native to both the North American (Northwest Atlantic) and European (Northeast Atlantic) waters. This makes them an interesting species to study in order to determine the role that genetics and environment have on population structure and evolution. Evaluation of lumpfish genetics shows a strong genetic basis for separation between the Northwest and Northeast Atlantic populations. These two regions display additional sub-populations which can be associated with adaptation of local environmental conditions. Overall, this suggests that adaptations to local environmental conditions will likely be increasingly important for this species.

Technical Abstract: In marine species with large populations and high dispersal potential, large-scale genetic differences and clinal trends in allele frequency can provide valuable insight into the evolutionary processes that shape diversity. The Lumpfish, Cyclopterus lumpus, is a globiform marine fish found throughout the North Atlantic which has traditionally been harvested for roe and more recently for application as a cleaner fish in salmon aquaculture. We used a 70K SNP array to evaluate population structure, clinal variation, and environmental drivers of structuring across the North Atlantic. Basin-scale structuring between the Northeast and Northwest Atlantic was significant and evident genome wide, with enrichment for loci associated with developmental or mitochondrial function. We identified a putative structural variant on chromosome 2 which was ~492 kilobase pairs, likely contributing to differentiation between Northeast and Northwest Atlantic Lumpfish, and consistent with post-glacial trans-Atlantic secondary contact. Regional structuring was also evident with Northwest Atlantic Lumpfish splitting into northern and southern groups, and Northeast Atlantic Lumpfish subdividing into four regional groups (1-Iceland/Faroe Islands, 2-English Channel, 3-Baltic Sea, 4- Norway/Iceland/Scotland). Clinal patterns in allele frequencies were observed in some loci (15% in the Northwest and 5% in the Northeast) of which 708 loci were shared and involved with growth, developmental processes, and locomotion. Within these loci, Redundancy Analysis identified climate associations both in the east (n=88 loci) and west (n=50 loci), with one shared locus. The combined evidence of trans-Atlantic differentiation, environmental associations, and clinal loci, suggests that the observed stock differences may be adaptive in this increasingly important species.