Large-scale mutation in the evolution of a gene complex for cryptic coloration

Abstract

The types of mutations affecting adaptation in the wild are only beginning to be understood. In particular, whether structural changes shape adaptation by suppressing recombination or by creating new mutations is unresolved. Here, we show that multiple linked but recombining loci underlie cryptic color morphs of Timema chumash stick insects. In a related species, these loci are found in a region of suppressed recombination, forming a supergene. However, in seven species of Timema, we found that a megabase-size “supermutation” has deleted color loci in green morphs. Moreover, we found that balancing selection likely contributes more to maintaining this mutation than does introgression. Our results show how suppressed recombination and large-scale mutation can help to package gene complexes into discrete units of diversity such as morphs, ecotypes, or species.

The Genomic Architecture and Evolutionary Fates of Supergenes

“…For instance, large hemizygous regions, genomic fragments that are only present in one of the supergene haplotypes, have been implicated as the genomic architecture of supergenes. Examples of hemizygous supergenes are found in both plants (heterostyly in Primula ; Li et al 2016 ; see Genomic Architectures of Supergenes: Implications for Evolutionary Trajectories) and animals (pea aphid male wing dimorphism; Li et al 2020 ; cryptic coloration morphs in Timema stick insects; Villoutreix et al 2020 ) ( table 1 ). Such hemizygous supergenes may arise as a result of either duplication of genomic regions, deletion of a segment from one haplotype, or introgression.…”

How Important Are Structural Variants for Speciation?

“…In addition to the mechanisms described above, structural variants can have direct and immediate phenotypic effects that could contribute to speciation. The phenotypic effects of structural variants might be particularly large if 1) insertions or deletions encompass multiple genes affecting a trait; or 2) the breakpoints of structural variants, such as inversions, disrupt a reading frame or alter expression at a developmental switch gene [ 30 , 110 , 111 ]. Many insertions come from transposons, which carry strong promotors that may alter the expression of nearby genes.…”

“…Regardless of the effect on reproductive isolation per se, it is important to note that structural mutations can simultaneously affect traits by altering recombination and by altering gene expression or protein structure. This is especially true for inversions, as the mutational process, giving rise to inversions can also create deletions at the breakpoints [ 30 ]. This was likely the case for structural variants affecting cryptic color in Timema stick insects ( Figure 2 C).…”

“…In conclusion, we now know that structural variants can, in principle, contribute to reproductive isolation by various mechanisms, but we do not know which of these are most important or about the relative importance of structural variants versus point mutations. Even though some studies have mapped phenotypic traits underlying reproductive barriers to structural variants, such as inversions, very few studies have distinguished whether structural variants affect RI by suppressing recombination of multiple adaptive alleles, or large effect of mutations, or other genetic mechanisms (but see [ 30 , 98 ]). Fine-scale genomic mapping and functional manipulation and validation of genes are necessary to tease apart the effects, such as changes in gene expression via breaking points vs. carrying functional genes within the structural variant [ 149 ].…”

“…Recent advances in molecular and statistical methods have brought a renaissance in the study of structural variants, as these techniques can readily identify and genotype structural variants [ 22 , 23 , 24 , 25 , 26 , 27 ]. Recent evidence shows that large-scale structural variants, especially inversions, are associated with adaptive trait variation: including phenology in Rhagoletis fruit flies [ 3 ], mimetic wing patterns in Heliconius butterflies [ 28 , 29 ], cryptic coloration in Timema stick insects [ 30 ], the repeated evolution of distinct marine and freshwater ecotypes of three-spined sticklebacks [ 31 ], and ecotypes of Helianthus sunflowers [ 26 ]. However, in most cases, it is unclear whether the SVs associated with local adaptation represent balanced polymorphisms versus the early stages of speciation (or both).…”