Achiasmatic meiosis in the unisexual Amazon molly, Poecilia formosa

Abstract

Unisexual reproduction, which generates clonal offspring, is an alternative strategy to sexual breeding and occurs even in vertebrates. A wide range of non-sexual reproductive modes have been described, and one of the least understood questions is how such pathways emerged and how they mechanistically proceed. The Amazon molly, Poecilia formosa, needs sperm from males of related species to trigger the parthenogenetic development of diploid eggs. However, the mechanism, of how the unreduced female gametes are produced, remains unclear. Cytological analyses revealed that the chromosomes of primary oocytes initiate pachytene but do not proceed to bivalent formation and meiotic crossovers. Comparing ovary transcriptomes of P. formosa and its sexual parental species revealed expression levels of meiosis-specific genes deviating from P. mexicana but not from P. latipinna. Furthermore, several meiosis genes show biased expression towards one of the two alleles from the parental genomes. We infer from our data that in the Amazon molly diploid oocytes are generated by apomixis due to a failure in the synapsis of homologous chromosomes. The fact that this failure is not reflected in the differential expression of known meiosis genes suggests the underlying molecular mechanism may be dysregulation on the protein level or misexpression of a so far unknown meiosis gene, and/or hybrid dysgenesis because of compromised interaction of proteins from diverged genomes.

From asexuality to sexual reproduction: cyclical switch of gametogenic pathways in hybrids depends on ploidy level

“…For instance, clonal gametogenesis may be achieved by premeiotic endoreplication that causes ploidy elevation during gonocyte proliferation e.g., in diploid hybrids, the chromosome set of gonocytes becomes tetraploid (Cimino, 1972b Macgregor and Uzzell, 1964). A contrasting mechanism involves achiasmatic meiosis, as in hybrid Poecilia formosa, where the ploidy level of gonocytes remains unmodified but chromosomes exist as univalents during the first meiotic prophase with no sign of recombination (Dedukh et al, 2022b;Monaco et al, 1984). Hypothetically, the reductional division is skipped, but the equational division is normal again resulting in the same type of clonal progeny (Dedukh et al, 2022b;Monaco et al, 1984).…”

Genetic and karyotype divergence between parents affect clonality and sterility in hybrids

“…However, hybridization is also known to give rise to fertile, yet asexually reproducing hybrids in various animal and plant taxa. Asexual hybrids exhibit a broad spectrum of cytological mechanisms for the production of unreduced, often clonal, gametes, which range from entirely ameiotic processes (apomixis) to those involving more or less distorted meiosis (automixis) 10,11 .…”

From asexuality to sexual reproduction: a cyclical switch of gametogenic pathways in hybrids depends on ploidy level

“…A contrasting mechanism involves achiasmatic meiosis, as in hybrid Poecilia formosa, where the ploidy level of gonocytes remains unmodi ed but chromosomes exist as univalents during the rst meiotic prophase with no sign of recombination 21,30 . Hypothetically, the reductional division is skipped, but the equational division is normal again resulting in the same type of clonal progeny 21,30 .…”