Disentangling structural genomic and behavioural barriers in a sea of connectivity

Abstract

Genetic divergence among populations arises through natural selection or drift and is counteracted by connectivity and gene flow. In sympatric populations, isolating mechanisms are thus needed to limit the homogenizing effects of gene flow to allow for adaptation and speciation. Chromosomal inversions act as an important mechanism maintaining isolating barriers, yet their role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question of whether inversions play a role in the divergence of connected populations of the marine fish Atlantic cod (Gadus morhua), by exploring a unique data set combining whole-genome sequencing data and behavioural data obtained with acoustic telemetry. Within a confined fjord environment, we find three genetically differentiated Atlantic cod types belonging to the oceanic North Sea population, the western Baltic population and a local fjord-type cod. Continuous behavioural tracking over 4 year revealed temporally stable sympatry of these types within the fjord. Despite overall weak genetic differentiation consistent with high levels of gene flow, we detected significant frequency shifts of three previously identified inversions, indicating an adaptive barrier to gene flow. In addition, behavioural data indicated that North Sea cod and individuals homozygous for the LG12 inversion had lower fitness in the fjord environment. However, North Sea and fjord-type cod also occupy different depths, possibly contributing to prezygotic reproductive isolation and representing a behavioural barrier to gene flow. Our results provide the first insights into a complex interplay of genomic and behavioural isolating barriers in Atlantic cod and establish a new model system towards an understanding of the role of genomic structural variants in adaptation and diversification.

Keywords: Atlantic cod; adaptation; behavioural traits; chromosomal rearrangements; gene flow; sympatric divergence.

Figure 1

Genomic variation and population relationships. (a) Map of the study area with sampling sites depicted as coloured points: AVE: Averøya; LOW: Lowestoft; NOR: North Sea; TVE: Tvedestrand; ORE: Öresund; KIE: Kiel Bight; BOR: Bornholm. Colours match sampling sites in all figures. (b) Principal components analysis of genotypes excluding linkage groups LG01, 02, 07, and 12. Shown are the two main principal component axes (PC1, PC2); main clusters are identified as belonging to the North Sea, eastern Baltic Sea, western Baltic Sea and fjord‐type cod. (c) Phylogenetic relationships inferred using the multispecies coalescence model. Canadian individuals (CAN) were used to root the tree; the Tvedestrand sample was divided into North Sea‐type individuals (TVEn) and fjord‐type individuals (TVEf, see inset). Node support is shown as Bayesian posterior probabilities (PP), estimated population sizes are shown by point size (theta), the white line follows the maximum clade credibility summary tree, and thin coloured lines show a subsample of all inferred trees

Figure 2

Barriers to gene flow in the genomic landscape. (a) Windowed measurements of linkage disequilibrium (LD, genotype correlation, r ²), pairwise population divergence (fixation index, F_ST), pairwise between population sequence divergence (d _xy) and nucleotide diversity (π) for linkage groups LG02, 07, and 12. Grey boxes outline the regions of large inversions. (b) Principal components analyses of variants within the inversions. Shown are the two main axes (PC1, PC2); main clusters are outlined by grey circles depicting individuals homozygous for the ancestral arrangement (anc), heterozygous (het) or homozygous for the inverted arrangement (inv). (c) Maximum likelihood trees of homozygous sequences within the inversions. The grey outline indicates placement of fjord‐type (TVEf) specimens. The grey double bar signifies discontinuation of the branch connecting ancestral (left) and inverted (right) arrangements. (d) Frequency of homozygous ancestral (white), homozygous inverted (black), and heterozygous (grey) individuals per sampling site, as well as within fjord‐type (TVEf) and North Sea‐type (TVEn) fish. * significantly overrepresented ancestral or inverted arrangements. Colours match sampling sites in Figure 1

Figure 3

Survival and behavioural barriers to gene flow. Mean predictions (black lines) from models describing cod behaviour (a–c) and survival (d), also showing the 95% confidence bands (grey fields) and partial residuals (dots). For each model, the predictions are scaled against a reference level (zero). Survival is estimated as relative longevity (days survived/mean days survived). anc: ancestral; F: female; het: heterozygous; inv: inverted; M: male; TVEf: fjord‐type; TVEn: North Sea‐type