Selection and inertia in the evolution of holocentric chromosomes in sedges (Carex, Cyperaceae)

Abstract

Summary• Changes in chromosome number as a result of fission and fusion in holocentrics have direct and immediate effects on the recombination rate. We investigate the support for the classic hypothesis that environmental stability selects for increased recombination rates.• We employed a phylogenetic and cytogenetic data set from one of the most diverse angiosperm genera in the world, which has the largest nonpolyploid chromosome radiation (Carex, Cyperaceae; 2n = 12-124; 2100 spp.). We evaluated alternative Ornstein-Uhlenbeck models of chromosome number adaptation to the environment in an information-theoretic framework.• We found moderate support for a positive influence of lateral inflorescence unit size on chromosome number, which may be selected in a stable environment in which resources for reproductive investment are larger. We found weak support for a positive influence on chromosome number of water-saturated soils and among-month temperature constancy, which would be expected to be negatively select for pioneering species. Chromosome number showed a strong phylogenetic signal.• We argue that our finding of small but significant effects of life history and ecology is compatible with our original hypothesis regarding selection of optima in recombination rates: low recombination rate is optimal when inmediate fitness is required. By contrast, high recombination rate is optimal when stable environments allow for evolutionary innovation.

RAD‐seq linkage mapping and patterns of segregation distortion in sedges: meiosis as a driver of karyotypic evolution in organisms with holocentric chromosomes

“…We predicted that we would find non‐Mendelian segregation of whole linkage groups or contiguous blocks within them, evidence of nonrandom segregation of chromosome variants that differ by a small number of fissions and/or fusions. This study thus complements previous work on the role of selection in chromosome number variation in this diverse holocentric genus (Hipp, ; Escudero et al ., , b), adding meiotic drive to environmental selection.…”

“…The holocentric chromosome structure has been proposed to promote rapid chromosome differentiation and thus genetic differentiation (Mola & Papeschi, ; Hipp et al ., , ; Bureš et al ., ). High rates of holocentric chromosome evolution have been demonstrated in the Lepidoptera (Lukhtanov et al ., , ; Kandul et al ., ; Dinca et al ., ; Joron et al ., ) and in Carex (Hipp, ; Escudero et al ., , , b, , b). There is neither agreement on how these rearrangements become fixed in populations, nor how they promote speciation (recombination suppression vs. hybrid dysfunction; Rieseberg, ; Butlin, ).…”

Flow cytometry may allow microscope-independent detection of holocentric chromosomes in plants

“…These features, and the absence of a centromere, substantially affect genome and karyotype evolution10111213141516 and make holocentric lineages useful model systems for studying various evolutionary phenomena, such as recombination rates and adaptability17, meiotic drive1819, sex-chromosome evolution202122 and homoploid hybridization232425.…”

Evolution of genome size and genomic GC content in carnivorous holokinetics (Droseraceae)

“…In contrast to monocentric chromosomes, whose kinetochore formation is restricted to the small areas of the centromeres, holokinetic chromosomes lack primary constrictions and their kinetochores are formed along their poleward surfaces (Bure s et al, 2013;Cuacos et al, 2015). Holokinetic chromosomes, therefore, tolerate chromosomal fissions or fusions and do not allow more than two crossovers in meiosis (reviewed in Bure s et al, 2013;Heckmann and Houben, 2013) which may substantially affect genome and karyotype evolution of their bearers (Escudero et al, 2012;Bure s et al, 2013;Bure s and Zedek, 2014;Lukhtanov et al, 2015;S ıchov a et al, 2016). One such effect may be a negative correlation between genome size and chromosome number in holokinetic lineages (Nishikawa et al, 1984;Roalson et al, 2007; Z avesk a Dr abkov a and Vl cek, 2010;Bure s et al, 2013;Lipnerov a et al, 2013;Bure s and Zedek, 2014).…”