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How Important Are Structural Variants for Speciation?

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How Important Are Structural Variants for Speciation? G C A T T A C G G C A T genes Review How Important Are Structural Variants for Speciation? Linyi Zhang 1,*, Radka Reifová 2, Zuzana Halenková 2 and Zachariah Gompert 1 1 Department of Biology, Utah State University, Logan, UT 84322, USA; [email protected] 2 Department of Zoology, Faculty of Science, Charles University, 12800 Prague, Czech Republic; [email protected] (R.R.); [email protected] (Z.H.) * Correspondence: [email protected] 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 contribu- tion 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. Citation: Zhang, L.; Reifová, R.; Keywords: reproductive isolation; hybridization; suppressed recombination Halenková, Z.; Gompert, Z. How Important Are Structural Variants for Speciation? Genes 2021, 12, 1084. https://doi.org/10.3390/ genes12071084 1. Introduction Identifying the genetic basis of reproductive isolation (RI) is important for understand- Academic Editors: Arcadi Navarro ing the speciation process, including how speciation begins and is completed [1–4]. Various Cuartiellas, Karel Janko and genetic changes can contribute to RI and promote speciation. In some cases, mutations Peter Mikulíˇcek in a few genes are known to contribute substantially to RI, suggesting a relatively simple genetic basis for speciation. Such speciation genes have been linked to hybrid inviability Received: 15 June 2021 in Drosophila (Hmr)[5], melanoma formation in Xiphophorus (Xmrk-2)[6], and changes in Accepted: 14 July 2021 the mating system in Solanum spp. (STYLE2.1) (reviewed by [7–9]). However, speciation Published: 17 July 2021 often involves many genes [10], and details of the genetic architecture of RI, including the types of mutations involved, could be critical for understanding the speciation process. Publisher’s Note: MDPI stays neutral The theory suggests that structural variants (see Figure1A); that is, a type of mutation with regard to jurisdictional claims in that cause a change in chromosomal location (translocation), orientation (inversion), or published maps and institutional affil- copy numbers (deletion, insertion and duplication) might be particularly important for iations. speciation, especially in preventing species from merging upon secondary contact [11–13]. Here, we review this body of theory about the ways in which structural variants can contribute to RI, evaluate evidence in support of or against this theory, and discuss future avenues of productive research on the role of structural variants in speciation, with an Copyright: © 2021 by the authors. emphasis on advances made possible by new molecular and statistical tools for detecting Licensee MDPI, Basel, Switzerland. and analyzing structural mutations. Although SVs are highly variable in size, we focus on This article is an open access article SVs greater than 50 bp in length [11]. distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Genes 2021, 12, 1084. https://doi.org/10.3390/genes12071084 https://www.mdpi.com/journal/genes Genes 2021, 12, 1084 2 of 17 Genes 2021, 12, x FOR PEER REVIEW 2 of 18 Figure 1. (A) Types of structural variants. (B) Underdominance of heterozygotes due to structural variants. Red Xs in (1) Figure 1. (A) Types of structural variants. (B) Underdominance of heterozygotes due to structural variants. Red Xs in and (2) suggested meiotic pairing failure, while red Xs in (3) indicate reduced fitness of the individual. (C) Structural C (1)variants and (2) suppress suggested recombination meiotic pairing as a mechanism failure, while to prevent red Xs sp inecies (3) indicate from hybridizing. reduced fitness Allele ofa and the b individual. would cause ( hybrid) Structural variantsinviability/sterility suppress recombination when present in as th ae mechanism same genetic to background. prevent species Without from an hybridizing. inversion, recombination Allele a and bcan would break cause up the hybrid inviability/sterilitylink between alleles when at locus present A and in locus the same B and genetic then selection background. can purge Without alleles an a inversion, and b (see recombination [14]). Red crosses can indicate break up the linkreduced between fitness alleles of the at individual. locus A and (D) locusGene duplications B and then selectionas a mechanism can purge for DMI alleles (Dobzhansky–Muller a and b (see [14]). Incompatibilities). Red crosses indicate reducedThe 0 stands fitness for of loss the of individual. function at (theD) Genelocus. duplicationsRed crosses indicate as a mechanism reduced fitness for DMI of the (Dobzhansky–Muller individual. Incompatibilities). The 0 stands for loss of function at the locus. Red crosses indicate reduced fitness of the individual. The study of structural variants dates back to the early 1920s, when Alfred Sturtevant identifiedThe studyan inversion of structural while variantscomparing dates the backchromosomes to the early of 1920s,D. simulans when with Alfred its sister Sturtevant speciesidentified D. melanogaster an inversion [15]. while Since comparing then, large the structural chromosomes variants ofhaveD. been simulans identifiedwith itsus- sister ingspecies cytologicD. melanogaster techniques in[15 various]. Since species, then, including large structural Drosophila variants [16], grasshoppers have been identified[17], and corn [18]. Due to the prevalence of structural variants in Drosophila and their easy using cytologic techniques in various species, including Drosophila [16], grasshoppers [17], identification with cytogenetic techniques, structural variants were among the first ge- and corn [18]. Due to the prevalence of structural variants in Drosophila and their easy netic markers used in population genetics [19]. Biologists in the 1930s–1960s hypothesized identification with cytogenetic techniques, structural variants were among the first genetic that these chromosome-level changes drove speciation based on the observation that markers used in population genetics [19]. Biologists in the 1930s–1960s hypothesized that many different structural variants were fixed between closely related species [17,20,21]. However,these chromosome-level with the advent of changes other molecular drove speciation markers (first based allozymes, on the observation and then later that mi- many crosatellitesdifferent structural and single variants nucleotide were polymorphisms fixed between closely[SNPs]) related and an species increased [17 focus,20,21 on]. However, the rolewith of the changes advent in of gene other expression molecular versus markers protein (first sequences allozymes, of individual and then latergenes, microsatellites the em- phasisand single on structural nucleotide variants polymorphisms decreased some [SNPs]) from and the an 1970 increased to the 1990s focus [1]. on the role of changes in geneRecent expression advances versus in molecular protein and sequences statistical of individualmethods have genes, brought the emphasis a renaissance on structural in thevariants study decreased of structural some variants, from theas these 1970 totechniques the 1990s can [1]. readily identify and genotype structuralRecent variants advances [22–27]. in molecular Recent evidence and statistical shows that methods large-scale have broughtstructural a renaissancevariants, es- in the peciallystudy of inversions, structural variants,are associated as these with techniques adaptive cantrait readily variation: identify including and genotype phenology structural in Rhagoletisvariants [fruit22–27 flies]. Recent[3], mimetic evidence wing showspatterns that in Heliconius large-scale butterflies structural [28,29], variants, cryptic especially col- orationinversions, in Timema are associated stick insects with [30], adaptive the repeated trait variation: evolution includingof distinct phenologymarine and in fresh-Rhagoletis waterfruit fliesecotypes [3], mimetic of three-spined wing patterns sticklebacks in Heliconius [31], andbutterflies ecotypes of [28 Helianthus,29], cryptic sunflowers coloration in [26].Timema However,stick insects in most [30 cases,], the it repeated is unclear evolution whether of the distinct SVs associated marine and with freshwater local adapta- ecotypes tionof three-spined represent balanced sticklebacks polymorphisms [31], and ecotypesversus the of earlyHelianthus stages ofsunflowers speciation
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