A Roadmap for Understanding the Evolutionary Significance of Structural Genomic Variation

Structural genomic variants (SVs) take diverse forms and are ubiquitous drivers of ecological and evolutionary processes. Most studies of SVs focus on the adaptive significance of gene duplications and large inversions. Future studies should catalog SVs of all types and sizes and systematically test their evolutionary implications. We propose a roadmap and definitions for the study of SVs in ecological and evolutionary genomics. Best practices for SV detection are needed to facilitate comparisons across studies. Integrating population genomic, theoretical, and experimental approaches to SVs will more comprehensively characterize genomic variation, uncover the adaptive and neutral processes shaping the evolutionary trajectory of SVs, and identify the mechanisms by which SVs impact adaptation and speciation. Structural genomic variants (SVs) are ubiquitous and play a major role in adaptation and speciation. Yet, comparative and population genomics have focused predominantly on gene duplications and large-effect inversions. The lack of a common framework for studying all SVs is hampering progress towards a more systematic assessment of their evolutionary significance. Here we (i) review how different types of SVs affect ecological and evolutionary processes; (ii) suggest unifying definitions and recommendations for future studies; and (iii) provide a roadmap for the integration of SVs in ecoevolutionary studies. In doing so, we lay the foundation for population genomics, theoretical, and experimental approaches to understand how the full spectrum of SVs impacts ecological and evolutionary processes. Structural genomic variants (SVs) are ubiquitous and play a major role in adaptation and speciation. Yet, comparative and population genomics have focused predominantly on gene duplications and large-effect inversions. The lack of a common framework for studying all SVs is hampering progress towards a more systematic assessment of their evolutionary significance. Here we (i) review how different types of SVs affect ecological and evolutionary processes; (ii) suggest unifying definitions and recommendations for future studies; and (iii) provide a roadmap for the integration of SVs in ecoevolutionary studies. In doing so, we lay the foundation for population genomics, theoretical, and experimental approaches to understand how the full spectrum of SVs impacts ecological and evolutionary processes. genomic marker obtained by amplification of a short fragment of DNA cut by restriction enzymes. Polymorphism is characterized by variable lengths. a genomic structural variant in which a segment of DNA is reversed end-to-end relative to a reference sequence. a genomic structural variant in which a segment of DNA is represented in different numbers of copies. The segment can be absent (deletion) or present in two or more copies [duplication(s)] relative to a reference. a genomic region that explains variation in mRNA transcript abundance. process by which one DNA sequence replaces a homologous sequence such that the sequences become identical after the conversion event. a genomic structural variant, example of CNV, in which a region of DNA that contains a gene is duplicated. region of reduced recombination, characterized by high LD, and often associated with high local differentiation between genetic groups. individuals that are heterozygous/homozygous for a structural variant when it is considered as a single locus. The alleles are the different possible haplotypes (e.g., the inverted and noninverted states for an inversion). a genomic structural variant in which a segment of DNA varies in presence or absence relative to a reference. Indels include CNVs and nonreciprocal translocations. nonrandom association of alleles at different loci. a genomic structural variant, example of CNV, constituted by a tract of DNA motifs (1–10 bp for micro-, 10–60 bp for mini-) repeated 10–50 times. Also referred to as tandem repeats and simple sequence repeats. a form of homologous recombination that occurs between two lengths of DNA that have high sequence similarity, but are not alternate alleles, such as TE copies. a model in which an inversion is indirectly favored by natural selection because it suppresses recombination between sets of alleles, whereby alleles within a set are favored in similar contexts and each set is favored in a different context. genomic variant affecting a single base pair, including SNPs and single base-pair indels. a single base-pair substitution. genomic variation between individuals affecting the presence, abundance, position, and/or direction of a nucleotide sequence (Figure 1). a genomic structural variant in which a segment of DNA is in a different position relative to a reference. Translocations can be either reciprocal or non-reciprocal (generating indels) and affect whole chromosome arms, such as in whole-arm reciprocal translocations. The translocation of a segment of chromosome can result in a change in the total number of chromosomes, either by joining two chromosomes in one (fusion) or splitting a chromosome into two (fission). When fusions/fissions and translocations occur at the centromeres, they are called Robertsonian. a segment of DNA that can change its position in the genome by either a cut-and-paste mechanism (DNA transposons) or a copy-and-paste mechanism (retrotransposons). TEs are a form of translocation, indel, and/or duplication.