Disentangling structural genomic and behavioral barriers in a sea of connectivity

Genetic divergence among populations arises through natural selection or drift and is counteracted by high 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 gained attention as an important mechanism to maintain isolating barriers by protecting co-adapted alleles from breakdown through recombination. Yet, their relative role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question whether inversions play a role in ecotype divergence of highly connected populations of the marine fish Atlantic cod, by exploring a unique dataset combining whole-genome sequencing and behavioral data obtained with acoustic telemetry. Within a confined fjord environment, we find three genetically differentiated types of Atlantic cod belonging to the oceanic North Sea population, the western Baltic population, and a locally occurring fjord-type cod. Continuous behavioral tracking of the most common types North Sea and fjord-type cod over four years revealed temporally stable sympatry within the fjord. Despite overall weak genetic differentiation among all types, consistent with high levels of gene flow, we detect significant frequency shifts of three previously identified inversions. Nonetheless, the lack of fixed inversion differences indicates that inversions are unlikely to contribute strong postzygotic barriers, instead prezygotic isolating mechanisms may constitute additional barriers to gene flow. Behavioral data show that North Sea and fjord-type cod occupy different habitat depths, which may contribute to reproductive isolation and a behavioral barrier to gene flow. Our results provide the first insights into a complex interplay of genomic and behavioral barriers in Atlantic cod and establish a new model system towards an understanding of the role of genomic structural variants in adaptation and diversification.