The role of genome structural variation on plastic and constitutive phenotypic divergence in multifarious environments

The ubiquity of structural variants in the genomes of model organisms has become apparent. Although some of these variants are associated with disorders, some studies documented their adaptive advantage. In particular, copy number variable regions have been suggested to mediate adaptive response to rapidly changing environments. However, little is known about the evolutionary role of genome structural variation in human-induced environmental change.
We apply high throughput sequencing and phenotyping to dense geographic samples of the ecological model species and keystone aquatic crustacean Daphnia magna to investigate mechanisms of adaptation to multifarious environments. We measure fitness-linked traits in control and stressful conditions, as well as genome-wide polymorphism and structural variation on 19 populations distributed along three orthogonal gradients of selection. We identify genome variants underpinning plastic and constitutive phenotypic responses to each of the stressors in the landscape as well as to multiple stressors. Genes and pathways shared among populations experiencing the same stressor underpin local adaptation, whereas a very small proportion of alleles is shared among these populations. Daphnia shows a high number of structural variants linked to stress response. The high number of structural variants and repeatable patterns of standing genetic variation at gene and pathway, rather than allele level indicate that selection operates at high hierarchical levels in this species, enabling a fast adjustment to rapid environmental changes. Our findings have important implications for the impact of purifying selection on structural genome variants and their role in adaptive responses to anthropogenic stress. Further, they provide a conceptual framework of how genes might interact with the environment and evolve toward the development of plastic traits. Finally, our findings suggest that the effective population size of this species may be smaller than allele frequency estimates suggest as the target of natural selection are gene networks rather than single alleles.