Introduction
Chromosome evolution is one of the most important drivers of
biodiversity (Stebbins, 1950; Butlin, 2005; Ayala & Coluzzi, 2005;
Hoffmann & Rieseberg, 2008). Chromosomal rearrangements are often
associated with speciation (Rieseberg, 2001), as they have the potential
to reduce gene flow between diverging populations (Grant, 1963). In
angiosperms, karyotypic diversity is significantly associated with both
clade species richness and diversification rates, which suggests
chromosomal rearrangements promote or reinforce the speciation process
(Carta & Escudero, 2023). Much research into chromosome evolution in
plants has focused on the physiological and ecological implications of
polyploidy (e.g. Otto & Whitton, 2000; Otto, 2007), while the
evolutionary consequences of dysploidy have received comparatively much
less attention (Escudero et al., 2014).
Speciation mediated by chromosome evolution has been explained by two
models. First, the hybrid-dysfunction model of chromosomal speciation
presumes reduced fitness of hybrids between chromosome races. This model
is undermined by the fact that strong selection against structural
heterozygotes (underdominance) would make new cytotypes extremely
difficult to succeed, meaning that underdominant mutations are not
likely to cause speciation (Coyne & Orr, 2004). The alternative model,
the suppressed recombination model of chromosomal speciation is better
supported theoretically as it does not involve underdominance. In this
case, chromosomal rearrangements promote divergence between populations
by preventing recombination in clusters of locally coadapted gene
complexes (supergenes; Schwander et al., 2014; Black & Shuker, 2019).
These rearrangements may facilitate species divergence even in the
presence of ongoing gene flow between chromosomatically differentiated
populations (Navarro & Barton, 2003; Ortiz-Barrientos et al., 2002;
Noor et al., 2001; Lowry & Willis, 2010).
In holocentric chromosomes, centromeric regions are distributed along
the entire length of the chromosome, which may therefore attach to
microtubules during mitosis and meiosis (Márquez-Corro et al., 2019a).
In contrast, monocentric chromosomes have microtubule attachments
localized exclusively in a single centromeric region. Holocentric
chromosome organization has been described for ca. 20 lineages in three
of the six kingdoms in the domain Eukarya (the Eukaryotes): plants
(angiosperms and green algae); animals (at least six species-rich
arthropod clades, plus velvet worms and nematodes); and Rhizaria
(Escudero et al., 2016; Márquez-Corro et al., 2018). As a consequence,
approximately, ca. 20% of all Eukaryotes have holocentric chromosomes
(Márquez-Corro et al., 2018). The evolutionary implications of
holocentricity are potentially profound but largely misunderstood.
Because of these special features of holocentric chromosomes, they have
been suggested as ideal systems to test the proposed models of
chromosomal speciation (Lucek et al., 2022).
Chromosome fragments from fissions that would be lost in monocentric
chromosomes may be inherited and become fixed in organisms with
holocentric chromosomes (Márquez-Corro et al., 2019a). Likewise,
enlarged chromosomes from fusion events can align and segregate
correctly in holocentric chromosomes. Conversely, in organisms with
monocentric chromosomes fusions usually result in the formation of
dicentric chromosomes that fail to segregate properly (Márquez-Corro et
al., 2019a). Consequently, large series of chromosome numbers and high
rates of karyotype evolution are found in holocentric lineages
(i.e. , butterflies and moths –Lepidoptera– 2n = 10 to
250, sedges –Cyperaceae– 2n = 4 to 226; de Vos et al. 2020;
Márquez-Corro et al., 2019b, 2021). In Lepidoptera, phylogenetic
comparative evidence suggests that chromosome fission and fusion drive
cladogenesis (de Vos et al. 2020; Augustijnen et al., 2023). In the
sedge genus Carex (Cyperaceae), chromosome rearrangements
contribute to genetic diversity within species (Hipp et al., 2010;
Escudero et al., 2013a) and the karyotype diversity is positively
associated with the time of coalescence of the species (Escudero et al.,
2010). Finally, chromosome number changes from fission and fusion are
related to linkage groups and, in holocentrics, they also determine
recombination rates as the number of chiasmata during meiosis is
directly proportional to chromosome number (Nokkala et al., 2004). As a
consequence, linkage groups and recombination rates (chromosome numbers)
have been positively associated with adaptive speciation towards
different environmental conditions in holocentric sedges (Escudero et
al., 2012, 2013b; Spalink et al., 2018; Márquez-Corro et al., 2021).
Some of the patterns of chromosome number association with environmental
conditions are rather weak at the macroevolutionary level (Escudero et
al., 2012; Spalink et al., 2018; Márquez-Corro et al., 2021), probably
based on the fact that chromosome evolution is much faster than
speciation rates in sedges (Márquez-Corro et al., 2021).
We hypothesize that holocentric chromosomes may be playing an important
role in species’ ability to adapt and colonize new environments.
Therefore, having a direct impact on niche expansion for some of the
most widespread species of the study group. Karyotype rearrangements may
leave a traceable signature in the different individuals’ genomes,
probably linked to specific loci in the linkage groups. Landscape
genomics constitutes a currently developing approach that may help to
identify specific genetic markers, including chromosome number
variation, associated with environmental variables and therefore
involved in local adaptation processes (Rellstab et al., 2015; Hoban et
al, 2016; Ahrens et al., 2018). To our knowledge, no study using
landscape genomics has addressed this topic in organisms with
holocentric chromosomes.
The goals of this study are: (i) to infer patterns of holocentric
chromosome evolution at phylogeography scale in a lineage of four
closely related and recently diversified Carex species, (ii) to
identify genomic signatures of adaptive evolution and investigate the
associations between chromosome numbers and local environmental
conditions, (iii) to elucidate the role of cytogenetic evolution on the
diversification of the group and specifically the model of chromosomal
speciation.