Implications for speciation
Karyotype diversity is directly associated with diversification rates and species richness in angiosperms (Carta & Escudero, 2023) which suggests a key role of chromosome evolution in the plant diversification process. Chromosome evolution has been hypothesized as a major driver of diversification in the Mediterranean Basin (Escudero et al., 2018; Thompson, 2020). In addition, chromosome evolution has been suggested to play a major role in species diversification in holocentrics (de Vos et al., 2020; Escudero et al., 2010, 2013b; Hipp et al., 2010). Finally, chromosome evolution may also have an indirect role reinforcing geographical or ecological speciation (Coyne & Orr, 2004).
There are two overarching models for chromosomal speciation, hybrid dysfunction and recombination suppression (Ayala & Coluzzi, 2005). They are not mutually exclusive and they can both play a partial role in the process of chromosomal speciation, especially in holocentric chromosomes where hybrid dysfunction is better supported theoretically than in monocentrics (Lucek et al., 2022). The suggested adaptive chromosomal speciation here could be helpful to support both models of chromosomal speciation. On one hand, strong selection towards new chromosomal variants may help them to become established in the populations which can ameliorate one of the strongest critics against the hybrid dysfunction model (the minority cytotype exclusion; Levin, 1975). On the other hand, recombination suppression models already suggest locally adapted genes in which recombination is protected by chromosome rearrangements (Ayala & Coluzzi, 2005). Accordingly, under this chromosomal speciation model, we certainly expect that different karyotypes are locally adapted. Our landscape genomics analyses suggest that karyotypes are locally adapted in our study group. In addition, the phylogenetic placement of sampled populations suggests multiple origins of different chromosome numbers (e.g. 2n = 72, 76), which is congruent with recurrent chromosome fission and fusion processes in relatively short time periods (Escudero et al., under review) and further support its adaptive value. We hypothesize here that clusters of locally adapted genes in C. gr. laevigata may have been protected for recombination by the fission and fusion rearrangements. In fact, fissions and fusions in holocentric have been observed to suppress recombination in holocentrics in a study of comparative genomics (whole sequence genome vs. linkage map, Escudero et al., 2023). For instance, in C. laevigata , this would have allowed different karyotypes (and, consequently, gene combinations) to either disperse northwards after the last glacial period or remain in the progressively warmer habitats in the southern Iberian Peninsula, further contributing to lineage divergence.