Evidence for selection and spatially distinct patterns found in a putative zona pellucida gene in Pacific cod, and implications for management

Abstract

Genetic differentiation has been observed in marine species even when no obvious barriers to gene flow exist, and understanding such differentiation is essential for effective fisheries management. Highly differentiated outlier loci can provide information on how genetic variation might not only contribute to local adaptation but may also be affected by historical demographic events. A locus which aligned to a predicted zona pellucida sperm-binding protein 3 gene (ZP3) in Atlantic cod (Gadus morhua) was previously identified as the highest outlier based on F ST in a RADseq study of Pacific cod (Gadus macrocephalus) across the West Coast of North America.However, because of the limited length of the RAD sequence and restricted geographic area of sampling, no conclusion on the functional significance of the observed variation was possible. In other marine species, ZP3 is involved in reproductive isolation, local adaptation, and has neofunctionalized as an antifreeze gene, and so it may provide important insights in functional population structure of Pacific cod. Here, we sequenced a 544-bp region of ZP3 in 230 Pacific cod collected from throughout their geographic range. We observed striking patterns of spatial structuring of ZP3 haplotypes, with a sharp break near Kodiak, Alaska, USA where populations within ~200 km of each other are nearly fixed for different haplotypes, contrasting a pattern of isolation by distance at other genetic markers in this region (F ST = 0.003).Phylogenetic analysis of ZP3 haplotypes revealed that the more southern haplotypes appear to be ancestral, with the northern haplotype evolving more recently, potentially in response to a novel selective pressure as Pacific cod recolonized northern latitudes after glaciation. The sharp break in haplotype frequencies suggests strong selective pressures are operating on small spatial scales and illustrates that selection can create high divergence even in marine species with ample opportunities for gene flow.

Genomic differentiation in Pacific cod using Pool‐Seq

“…Cod recolonized the North Pacific as glaciers receded, as recently as 14–15 kyr before present (Mann & Hamilton, 1995 ; Menounos et al, 2009 ). Analysis of the putative zona pellucida gene is consistent with this scenario, as the present‐day southern populations are more closely related to Atlantic cod and more northerly populations are more derived at this locus (Spies et al, 2021 ).…”

“…In Alaska, Pacific cod are managed in three management units corresponding to the Gulf of Alaska, Aleutian Islands, and eastern Bering Sea. A general pattern of isolation by distance among spawning groups of Pacific cod (Cunningham et al, 2009 ; Drinan et al, 2018 ; Spies, 2012 ) is punctuated by locally pronounced genetic differentiation between the Aleutian Islands and eastern Bering Sea (Spies, 2012 ) and between the western and eastern Gulf of Alaska (Drinan et al, 2018 ; Spies et al, 2021 ). However, divergence across the genome between Aleutian Islands and eastern Bering Sea cod has not been examined.…”

Pacific cod in the Anthropocene: An early life history perspective under changing thermal habitats

“…These include increased schooling behavior (Laurel et al, 2007) or shifts in metabolic thermal performance; that is, ‘reaction norms’ (Hutchings et al, 2007; Neubauer & Andersen, 2019). For example, cohorts of age‐0 Pacific cod collected in warm years grow faster at warmer temperature than age‐0 cohorts collected in colder years (Hurst et al, 2012), and recent genetic studies suggest strong directional selection among the ZP3 haplotype which has functional links to antifreeze glycoproteins and low‐thermal tolerance (Spies et al, 2021). These and other potential thermal adaptations are significant knowledge gaps for Pacific cod at every life stage and will have important bearing on how shifting thermal habitats affect Pacific cod under future climate change.…”

“…Increased spatial coverage is also necessary to span genetic breaks recently discovered in the Central GOA region (Spies et al, 2021).…”

“…Temperatures reflect the 145-160 °W Gulf of Alaska shelf domain. Size data for juveniles were based on collections from two bay locations (hence two values per year reported).directional selection among the ZP3 haplotype which has functional links to antifreeze glycoproteins and low-thermal tolerance(Spies et al, 2021). These and other potential thermal adaptations are significant knowledge gaps for Pacific cod at every life stage and will have important bearing on how shifting thermal habitats affect Pacific cod under future climate change.…”