Natural selection drives genome-wide evolution via chance genetic associations

Understanding selection's impact on the genome is a major theme in
biology. Functionally-neutral genetic regions can be affected indirectly
by natural selection, via their statistical association with genes under
direct selection. The genomic extent of such indirect selection,
particularly across loci not physically linked to those under direct
selection, remains poorly understood, as does the time scale at which
indirect selection occurs. Here we use field experiments and genomic data
in stick insects, deer mice and stickleback fish to show that widespread
statistical associations with genes known to affect fitness cause many
genetic loci across the genome to be impacted indirectly by selection.
This includes regions physically distant from those directly under
selection. Then, focusing on the stick insect system, we show that
statistical associations between SNPs and other unknown, causal variants
result in additional indirect selection in general and specifically within
genomic regions of physically linked loci. This widespread indirect
selection necessarily makes aspects of evolution more predictable. Thus,
natural selection combines with chance genetic associations to affect
genome-wide evolution across linked and unlinked loci and even in
modest-sized populations. This process has implications for the
application of evolutionary principles in basic and applied science.