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.