Structural Variants and Speciation: Multiple Processes at Play

Abstract

Research on the genomic architecture of speciation has increasingly revealed the importance of structural variants (SVs) that affect the presence, abundance, position, and/or direction of a nucleotide sequence. SVs include large chromosomal rearrangements such as fusion/fissions, inversions and translocations, as well as smaller variants such as duplications, insertions, and deletions (CNVs). Although we have ample evidence that SVs play a key role in speciation, the underlying mechanisms differ depending on the type and length of the SV, as well as the ecological, demographic and historical context. We review predictions and empirical evidence for classic processes such as underdominance due to meiotic aberrations and the coupling effect of recombination suppression before exploring how recent sequencing methodologies illuminate the prevalence and diversity of SVs. We discuss specific properties of SVs and their impact throughout the genome, highlighting that multiple processes are at play, and possibly interacting, in the relationship between SVs and speciation.

The Impact of Chromosomal Rearrangements in Speciation: From Micro- to Macroevolution

“…These differences may or may not have been instrumental in the evolution of RI, and could have evolved after speciation was completed. Nevertheless, if CRs play a role in speciation as suggested by different theoretical models and supported by empirical microevolutionary studies (see Berdan et al 2023), wewould expect a positive correlation between chromosomal change and rates of speciation (see below), even though this relationship might be hard to detect due to the influence of various other factors. Conversely, the absence of such a correlation could highlight that CRs are primarily involved in intraspecific divergence, but rarely lead to different species and increased speciation rates.…”

“…A more recent line of theory focuses on the effects of CRs on recombination, especially in scenarios where speciation occurs in the presence of gene flow (Rieseberg 2001;Navarro and Barton 2003;Faria and Navarro 2010;Guerrero and Kirkpatrick 2014). Under these models, the frequency of a new CR may increase when recombination suppression strengthens linkage disequilibrium (LD) between two or more locally advantageous alleles located within a rearranged genomic region (see Berdan et al 2023). This will reduce effective recombination within the rearranged region in heterokaryotypes, whereby additional barrier loci (e.g., alleles involved in incompatibilities) can accumulate, enhancing RI (Lande 1985;Navarro and Barton 2003;Kirkpatrick and Barton 2006;Guerrero and Kirkpatrick 2014;Connallon and Olito 2022).…”

“…2). While the prediction that CRs between populations contribute to RI is supported by many empirical studies (see Berdan et al 2023), the association of rates of chromosomal evolution and speciation has been tested less frequently but is a focus of this work.…”

“…1). These rearranged chromosomes can impact organismal phenotype and reshape the evolutionary trajectories of populations, potentially resulting in speciation (see Berdan et al 2023).…”

“…Various theoretical models have explored how chromosomal rearrangements (CRs) can be involved in speciation by reducing gene flow between populations and contributing to reproductive isolation (RI), and these have garnered empirical support (see Berdan et al 2023). For instance, CRs can contribute to phenotypic adaptive divergence and/or lead to the accumulation of genetic incompatibilities, reducing gene flow between populations (e.g., Navarro and Barton 2003;Lowry and Willis 2010).…”