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.
Highlights
How new species arise and adapt to their environments is a fundamental question in the field of evolutionary biology
Using a unique data set combining genomic with behavioural data of highly connected wild Atlantic cod populations within a fjord ecosystem, we here show that significant frequency shifts of chromosomal inversions among cod types exist, one of which was correlated with survival within the fjord environment, suggesting the existence of adaptive barriers to gene flow
Based on whole‐genome sequencing data, we demonstrated that the Atlantic cod community in the southern Norwegian fjord of Tvedestrand consists of three co‐ occurring genetically differentiated cod types, of which two types are associated with the adjacent Atlantic cod populations in the North Sea and the western Baltic Sea, while the third forms a distinct unit that was only detected within the fjord (Figure 1b)
Summary
How new species arise and adapt to their environments is a fundamental question in the field of evolutionary biology. In addition to structural rearrangements of the genome acting as postzygotic barriers to restrict gene flow between sympatric populations, prezygotic mechanisms including fitness advantages in the local environment, temporal, spatial or ecological shifts during the breeding season (causing allopatric reproduction), as well as behavioural differences (e.g., assortative mating) may play a role (Coyne & Orr, 2004; Jones, Brown, Pemberton, & Braithwaite, 2006). To investigate the relative roles of different barrier mechanisms for the potential of adaptation and diversification in sympatric populations characterized by homogenizing gene flow, here we focus on a topographically restricted coastal fjord ecosystem in which the occurrence of three genetically differentiated types of Atlantic cod, a resident fjord‐type, an oceanic North Sea‐type and a western Baltic‐type, have been reported (Barth, Berg, et al, 2017; Knutsen et al, 2018). We test whether behavioural differences, potentially acting as prezygotic barriers to gene flow, are present among the cod types and whether these are correlated with the inversion states
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