Chromosomal speciation through holocentric lenses

Inés Gómez-Ramos , Rogelio Sánchez-Villegas, Ana Valdés-Florido, Carmen Benítez-Benítez, Lucía Laynez-Puyana, Kjetil Lysne Voje, František Zedek, Enrique Maguilla, Kohta Yoshida, Kay Lucek, Marcial Escudero

Chromosomal rearrangements (CRs) can trigger speciation by acting as barriers to gene flow. Two main theoretical frameworks were developed on how they contribute to speciation: causing infertility in heterokaryotypes (hybrid dysfunction) or creating islands of divergence through recombination suppression. However, these theories were developed with monocentric chromosomes in mind. Species with holocentric chromosomes, which lack a localized centromere, account for 15-20 % of the eukaryote biodiversity in terms of species richness. These organisms have a higher tolerance for large CRs but the number of chiasmata (recombination) is more restricted, defying assumptions for both types of chromosomal speciation models. This highlights the need to look at chromosomal speciation through holocentric lenses.
Here, we synthesize how holocentricity redefines these frameworks across diverse lineages, shedding light into the diverse patterns in both karyotypic diversity and their impact on speciation. We further show that the effects of CRs depend on interactions among meiotic mechanisms, genome organization, reproductive barriers, and demographic history. Rather than producing a single evolutionary outcome, holocentricity generates a diversity of pathways through which chromosome evolution can influence speciation.