How Important Are Structural Variants for Speciation?

Abstract

Understanding the genetic basis of reproductive isolation is a central issue in the study of speciation. Structural variants (SVs); that is, structural changes in DNA, including inversions, translocations, insertions, deletions, and duplications, are common in a broad range of organisms and have been hypothesized to play a central role in speciation. Recent advances in molecular and statistical methods have identified structural variants, especially inversions, underlying ecologically important traits; thus, suggesting these mutations contribute to adaptation. However, the contribution of structural variants to reproductive isolation between species-and the underlying mechanism by which structural variants most often contribute to speciation-remain unclear. Here, we review (i) different mechanisms by which structural variants can generate or maintain reproductive isolation; (ii) patterns expected with these different mechanisms; and (iii) relevant empirical examples of each. We also summarize the available sequencing and bioinformatic methods to detect structural variants. Lastly, we suggest empirical approaches and new research directions to help obtain a more complete assessment of the role of structural variants in speciation.

Keywords: hybridization; reproductive isolation; suppressed recombination.

Figure 1

(A) Types of structural variants. (B) Underdominance of heterozygotes due to structural variants. Red Xs in (1) and (2) suggested meiotic pairing failure, while red Xs in (3) indicate reduced fitness of the individual. (C) Structural variants suppress recombination as a mechanism to prevent species from hybridizing. Allele a and b would cause hybrid inviability/sterility when present in the same genetic background. Without an inversion, recombination can break up the link between alleles at locus A and locus B and then selection can purge alleles a and b (see [14]). Red crosses indicate reduced fitness of the individual. (D) Gene duplications as a mechanism for DMI (Dobzhansky–Muller Incompatibilities). The 0 stands for loss of function at the locus. Red crosses indicate reduced fitness of the individual.

Figure 2

Example cases of structural variants involved in reproductive isolation. (A) Loci associated with female preference and male hybrid sterility located within an inversion in Drosophila pseudoobscura [14]. Blue color represents genomic region from D. pseudoobscura, and orange color represents genomic region from D. persimilis. (B) Loss of function in duplicated genes lead to hybrid lethality between Mimulus guttatus and M. nasutus [57]. Black crosses indicate the loss of the gene function, while the red cross represents the reduced fitness of the hybrid individual. (C) Deletion and inversion act as large mutation leads to color morph variation among Timema species both increasing (melanic morph) and decreasing (green versus striped morphs) RI between hosts [30]. Drawings of Drosophila, Mimulus and Timema credit to Rosa Marin Ribas.

Figure 3

Summary of studies of structural variants involved in reproductive isolation. TSL, INV, DEL, INS and DUP stand for translocation, inversion, deletion, insertion and duplication, respectively.