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

Abstract

Chromosomal rearrangements (CRs) have been known since almost the beginning of genetics. While an important role for CRs in speciation has been suggested, evidence primarily stems from theoretical and empirical studies focusing on the microevolutionary level (i.e., on taxon pairs where speciation is often incomplete). Although the role of CRs in eukaryotic speciation at a macroevolutionary level has been supported by associations between species diversity and rates of evolution of CRs across phylogenies, these findings are limited to a restricted range of CRs and taxa. Now that more broadly applicable and precise CR detection approaches have become available, we address the challenges in filling some of the conceptual and empirical gaps between micro- and macroevolutionary studies on the role of CRs in speciation. We synthesize what is known about the macroevolutionary impact of CRs and suggest new research avenues to overcome the pitfalls of previous studies to gain a more comprehensive understanding of the evolutionary significance of CRs in speciation across the tree of life.

Figure 1.

Summary of commonly studied chromosomal rearrangements (CRs), including the deletion of small segments along a chromosome, as well as the duplication or the inversion of such chromosomal material, respectively. Larger CRs include the reciprocal translocation of chromosomal regions between chromosomes, as well as the fusion or the fission of entire chromosomes. The fusion and fission illustrated are Robertsonian rearrangements (i.e., they involve breakage at the centromere). (Figure created with BioRender.com.)

Figure 2.

From patterns to processes studying chromosomal rearrangements (CRs) in speciation. (A) The three different components discussed in this article: microevolutionary processes result in reproductive isolation (RI) (blue), which potentially lead to phylogenetic splits, increasing speciation rates on the macroevolutionary scale (red). The probability of this happening depends on different factors that influence the emergence of chromosomal mutations in the first place (green). (B) Methods to study the macroevolutionary implications of CRs in speciation primarily involve phylogenetic approaches. Shown is an example for character states such as the number of chromosomes that are inferred along a phylogeny (left) and boxplots summarizing the phylogenetic inferences to assess the impact of CR-associated karyotypic changes on, for example, rates of speciation (right). The example was modified from de Vos et al. (2020) and is based on ChromoSSE. (C) Interpreting the phylogenetic signal of CRs at the tip level is often not trivial as a direct implication of CRs during speciation may not be given. A link between CRs and speciation can be inferred if a mutation that leads to a CR is frequently followed by a speciation event within a short amount of time.

Figure 3.

The role of chromosomal rearrangements (CRs) during speciation at both a micro- and macroevolutionary level exemplified by some animal and plant systems. (A) For the house mouse (Mus musculus), chromosomal races are common and can cause strong, yet not complete reproductive isolation. (Panel A is modified from Grize et al. 2019 under the terms of the Creative Commons Attribution 4.0 International License.) (B) At a macroevolutionary level, CRs have been suggested to have contributed to the diversification in rock-wallabies of the genus Petrogale. (Panel B is modified from Potter et al. 2017 under the terms of the Creative Commons Attribution License (CC BY) and the authors, © 2017 Potter, Bragg, Blom, Deakin, Kirkpatrick, Eldridge, and Moritz.) (C) Similar patterns are observed in the order Lepidoptera, where, for example, the wood-white butterfly Leptidea sinapsis shows a high variation in chromosome numbers across a Eurasian geographic scale but does not appear to cause strong reproductive isolation. (MI) Metaphase I of meiosis, (MII) Metaphase II of meiosis. (Panel C is modified from Lukhtanov et al. 2011 under the terms of the Creative Commons Attribution License 2.0, © 2011 by Lukhtanov et al., licensee BioMed Central.) (D) However, in other genera, chromosomal changes occur primarily among species and have been suggested as a driver for speciation. (Panel D based on data in Talavera et al. 2013.) (E) Intraspecific variation in chromosome numbers also occurs in plants (e.g., in panel E—Carex scoparia) where the degree of reproductive isolation scales with the number of CRs (see Escudero et al. 2016). (Image in Panel E kindly provided by Marcial Escudero.) (F) The overall diversity in chromosome numbers has been similarly attributed to have driven diversification in this genus. (Panel F is reprinted from Marques-Corro et al. 2021, with permission from the Institute of Botany, Chinese Academy of Sciences © 2021.) Pictures of Carex by Modesto Luceño Garces, pictures of Carex methaphases by Marcial Escudero.