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. 2023 Jul 6;16(7):1359-1376.
doi: 10.1111/eva.13575. eCollection 2023 Jul.

Evidence of hybridization between genetically distinct Baltic cod stocks during peak population abundance(s)

Cecilia Helmerson  1 , Peggy Weist  2 , Marine Servane Ono Brieuc  1   3 , Marius F Maurstad  1 , Franziska Maria Schade  4 , Jan Dierking  5 , Christoph Petereit  6 , Halvor Knutsen  3   7 , Julian Metcalfe  8 , David Righton  8 , Carl André  9 , Uwe Krumme  4 , Sissel Jentoft  1 , Reinhold Hanel  2
Affiliations

Evidence of hybridization between genetically distinct Baltic cod stocks during peak population abundance(s)

Cecilia Helmerson et al. Evol Appl. .

Abstract

Range expansions can lead to increased contact of divergent populations, thus increasing the potential of hybridization events. Whether viable hybrids are produced will most likely depend on the level of genomic divergence and associated genomic incompatibilities between the different entities as well as environmental conditions. By taking advantage of historical Baltic cod (Gadus morhua) otolith samples combined with genotyping and whole genome sequencing, we here investigate the genetic impact of the increased spawning stock biomass of the eastern Baltic cod stock in the mid 1980s. The eastern Baltic cod is genetically highly differentiated from the adjacent western Baltic cod and locally adapted to the brackish environmental conditions in the deeper Eastern basins of the Baltic Sea unsuitable for its marine counterparts. Our genotyping results show an increased proportion of eastern Baltic cod in western Baltic areas (Mecklenburg Bay and Arkona Basin)-indicative of a range expansion westwards-during the peak population abundance in the 1980s. Additionally, we detect high frequencies of potential hybrids (including F1, F2 and backcrosses), verified by whole genome sequencing data for a subset of individuals. Analysis of mitochondrial genomes further indicates directional gene flow from eastern Baltic cod males to western Baltic cod females. Our findings unravel that increased overlap in distribution can promote hybridization between highly divergent populations and that the hybrids can be viable and survive under specific and favourable environmental conditions. However, the observed hybridization had seemingly no long-lasting impact on the continuous separation and genetic differentiation between the unique Baltic cod stocks.

Keywords: Baltic Sea; Gadus morhua; contact zone; hybridization; inversions; population genetics.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

FIGURE 1
FIGURE 1
(a) Atlantic cod and sagittal otolith (whole and broken). Illustration: Cecilia Helmerson. Otoliths were used for genetic material and provision of age information. (b) Sampling sites in the Western Atlantic for individuals used in the WGS data‐set (displayed with dots): Celtic Sea (CEL), North Sea (NOR), the transition area into the Baltic Sea, including Oresund (ORE), Kiel Bight (KIE), Mecklenburg Bight (MEC), as well as Bornholm Basin (BOR) and Gdansk Deep (GDA). (c) Sampling areas of the southern part of the Baltic Sea for the individuals genotyped with the diagnostic SNP‐panel (displayed as rectangles): SDs are marked with bold lines and map show SD 22–25 and partially SD 21 and 26. Striped rectangles marking historical sampling sites (H) (1979–1989), grey rectangles marking modern (M) (2016) sampling areas. Grey and striped showing areas with both modern and historical samples (M + H). KIE = Kiel Bight, MEC = Mecklenburg Bight, ARK = Arkona Basin and BOR = Bornholm Basin.
FIGURE 2
FIGURE 2
PCA for individual cod in SNP dataset (N = 539). PCA is split per sampling location and coloured by genotype. Genotype scoring is divided into WBC (western Baltic cod), HYB (putative hybrids) and EBC (eastern Baltic cod). Modern samples from KIE and BOR used for projection are shown in background regardless of sampling area.
FIGURE 3
FIGURE 3
STRUCTURE plots showing fractions (f Structure ) for K = 2, split by area (vertical) of Western (purple) and Eastern (orange) genetic signal over time (horizontal). Samples are sorted according to fraction of western signal. Potential hybrids are shadowed as having fractions between 0.3 and 0.7. Samples selected for WGS are marked by purple dot for WBC (western Baltic cod), orange dot for EBC (eastern Baltic cod) and blue triangle for HYB (putative hybrids).
FIGURE 4
FIGURE 4
STRUCTURE plots showing fractions (f Structure ) for K = 2, of Western (purple) and Eastern (orange) genetic signal for theoretical hybrids and backcrosses as obtained with hybrid simulation tool. WBC is the western parents, B3 is the third‐generation backcrosses, B2 is the second‐generation backcrosses, F1 is the first‐generation hybrids, F2 is the second‐generation hybrids and EBC is the eastern parents. Hybrids within fraction 0.3–0.7 are shadowed and fraction of simulated hybrids picked up given below f HYB.
FIGURE 5
FIGURE 5
(a) PCA for individuals in WGS dataset (N = 53), coloured by sampling area. Point size is larger for historical samples from the SNP set and coloured by assigned population from Structure analysis. (b) Phylogenetic tree based on Protein coding genes (PCGs) Maximum likelihood tree for individuals undergoing WGS (same individuals as in PCA). Modern samples have grey text, historical WBC have purple text, historical EBC have black text and hybrids have blue text. Black points on branches represent bootstrap support values >95. Tree branching separating historical WBC and HYB is purple, branch with historical EBC is marked in yellow.
FIGURE 6
FIGURE 6
Fractions of heterozygosity (fHET) in SNP dataset (N = 436, 20 SNPs). Plots coloured by cod type scoring. Significantly different groups are marked with a,b and c.
FIGURE 7
FIGURE 7
Inversion proportions (fGenotype) for inversions at LG02 and LG12, for all historical samples. Proportions split per cod genotype (WBC, HYB, EBC) (pie‐charts) and genotype+sampling area (bar‐plots). Statistical groups are marked with a,b,c. Groups not significantly different are marked with the same letters. NA indicating groups not tested, due to few observations.
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