Shifting balancing selection on a chromosomal inversion in island populations

Chromosomal inversions often underlie local adaptation and differentiation between populations. However, little is known about how selection acting on a balanced inversion shifts in different environments in the context of demographic events. Here, we combine population genomic approaches with extensive simulations to show that split events of island populations shifted a parameter of balancing selection on a polymorphic inversion. In Eurasian blackcaps (Sylvia atricapilla), an 8 Mb-long inversion has been maintained polymorphic in most populations across the species distribution range by long-term balancing selection. The frequency of this inversion is consistently lower in island resident and continental resident populations compared to behaviourally ancestral continental migrant populations. Inference of population history shows that at least four groups of residents, specifically one continental population and three sets of populations on different island systems, originate from independent and simultaneous split events from one ancestral population. Such a demographic history indicates that the consistent reduction in the inversion frequency among these independent resident populations is unlikely due to shared stochastic events. Approximate Bayesian computation (ABC) applied to simulations of balancing selection under the blackcap demography indicates that the optimal frequency of the inversion in the regime of negative frequency-dependent selection, a type of balancing selection, became lower in island populations. These results highlight how parallel shifts in selection parameters in similar environments can contribute to genetic differentiation among populations at inversion loci.