Skipping sex: A nonrecombinant genomic assemblage of complementary reproductive modules

Abstract

The unusual occurrence and developmental diversity of asexual eukaryotes remain a puzzle. De novo formation of a functioning asexual genome requires a unique assembly of sets of genes or gene states to disrupt cellular mechanisms of meiosis and gametogenesis, and to affect discrete components of sexuality and produce clonal or hemiclonal offspring. We highlight two usually overlooked but essential conditions to understand the molecular nature of clonal organisms, that is, a nonrecombinant genomic assemblage retaining modifiers of the sexual program, and a complementation between altered reproductive components. These subtle conditions are the basis for physiologically viable and genetically balanced transitions between generations. Genomic and developmental evidence from asexual animals and plants indicates the lack of complementation of molecular changes in the sexual reproductive program is likely the main cause of asexuals' rarity, and can provide an explanatory frame for the developmental diversity and lability of developmental patterns in some asexuals as well as for the discordant time to extinction estimations.

Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the ‘extended speciation continuum'

“…It states that the formation of ‘asexually' reproducing hybrids ( box 1 ) is particularly likely when the genetic divergence between parental genomes is large enough to distort hybrid gametogenesis towards producing a high proportion of unreduced gametes, but not too large to significantly affect hybrid viability or fertility. Discussing the balance hypothesis, Stöck et al ([ 148 ], supported by [ 149 , 150 ]), also emphasized that ‘asexual' vertebrates are very rarely formed (e.g. 0.5% of reptile species [ 39 , 151 , 152 ]) since both sufficient divergence and generally complex genetic preconditions are necessary to naturally produce viable and fertile clonal genomes and phenotypes (‘rare formation hypothesis' [ 148 ]).…”

Variation of Residual Sexuality Rates along Reproductive Development in Apomictic Tetraploids of Paspalum

“…Apomixis is assumed to result from temporal and spatial changes in important stages of sexual development, caused by mutations or epigenetic modifications that arise after hybridization and polyploidization events [2,14,15]. As apomixis and sexuality coexist in the same plant or even in the same ovule [1,4,16], it has been proposed that apomixis emerged from the rearrangement of sexual developmental programs [17][18][19][20]. Contrary to this, other authors indicate that the main molecular components associated with apomixis (apomeiosis and parthenogenesis) may have emerged before sex [21,22].…”

Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex

“…However, the switch between sexuality and unisexuality occurs from one generation to another in the polyploid Carassius complex, suggesting that it might be based on genetic machinery present in the direct ancestors of the clones. Recently, Hojsgaard and Schartl (2021) proposed that a nonrecombinant genetic assemblage might be an essential condition for the occurrence of a unisexual lineage. In this study, we observed the suppression of synapsis and the first meiotic division during oogenesis of C. gibelio clone A + and wild clone H ( figs.…”

“…Over 100 species or biotypes across around 22 genera of fish, amphibians, and reptiles are able to reproduce via parthenogenesis, gynogenesis, or hybridogenesis ( Gui and Zhou 2010 ; Avise 2015 ; Zhou and Gui 2017 ). However, as an evolutionary genetic paradox, the unusual evolutionary persistence, clonal diversity, and reproductive strategy of unisexual vertebrates remain a puzzle ( Hojsgaard and Schartl 2021 ).…”

“…Traditionally, unisexual lineages have been predicted to be evolutionarily short-lived by classical theories, such as the Red Queen hypothesis ( Bell 1982 ) and Muller’s ratchet model ( Muller 1964 ). Due to the absence of normal meiosis, clonal lineages lack recombinational genetic variation and accumulate deleterious mutations, which inevitably lead to genomic decay ( Gui and Zhou 2010 ; Avise 2015 ; Hojsgaard and Schartl 2021 ). However, some well-known unisexual vertebrates have evolved for more than several hundred thousand years and have successfully colonized wider and harsher habitats than their sexual relatives ( Spolsky et al 1992 ; Lampert and Schartl 2008 ; Loewe and Lamatsch 2008 ; Pellino et al 2013 ; Brunes et al 2019 ).…”