Figure 1. Schematic model of meiosis in species with monocentric chromosomes and of meiotic adaptations in species with holocentric chromosomes.

(a) Monocentric chromosomes: Sister chromatids mono-orient at metaphase I via fused sister kinetochores, allowing homologous chromosome segregation, whereas at metaphase II sister chromatids bi-orient and segregate from each other. Note a ring bivalent configuration of metacentric chromosomes. (b–e) Holocentric chromosomes: Several options exist to deal with a holocentric chromosome architecture and meiosis: (b,c) chromosome remodelling, (d) functional monocentric chromosomes and (e) ‘inverted chromatid segregation’. Note that rod-shaped bivalents are shown (b–e), recombination events are not indicated (a–e) and sister chromatids are of the same colour. (b,c) One typically off-centred crossover leads to a cruciform bivalent with a short and a long arm. Owing to progressive condensation, bivalents occur ‘rod-shaped’ at metaphase I (short and long arms are not indicated in b,c). The crossover location triggers a distinct spatiotemporal protein distribution, for example, proteins including Aurora B or chromokinesin KLP-19 form a ring around the mid-bivalent, and (outer) kinetochore proteins encase each homologue. This distribution conditions cohesion loss at the mid-bivalent and retention at long arms during anaphase I enabling homologue separation. During meiosis II, proteins including KLP-19 surround the ring-shaped sister chromatid interface while (outer) kinetochore proteins encase individual sisters. At anaphase II, cohesion gets lost at the sister chromatid interface allowing sister chromatid separation. (b) KLP-19 mediates a pushing force from the mid-bivalent supported by lateral microtubules ensheathing bivalents during meiosis I and linked sister chromatids during meiosis II. (c) Bivalent ends facing polewards are attached by microtubules. (d) Microtubule attachment to a restricted terminal chromosomal region. Holocentric chromosomes become functional monocentric (‘telokinetic‘) enabling separation of homologues during meiosis I and of sister chromatids during meiosis II. Active sister kinetochores can form even at opposite metaphase II chromosome termini. (e) Homologous sister chromatids, attached by microtubules along nearly their entire lengths, face opposite poles during metaphase I and separate from each other at anaphase I. Homologous non-sister chromatids are joined by metaphase II and separate at anaphase II. Hence, an inverted meiotic chromatid segregation sequence compared to the typical meiotic segregation pattern in monocentric chromosome species occurs.