Frequency and maintenance of unreduced gametes in natural plant populations: associations with reproductive mode, life history and genome size

Abstract

Fertilization involving unreduced (2n) gametes is considered the dominant mechanism of polyploid formation in angiosperms; however, our knowledge of the prevalence of and evolutionary mechanisms maintaining 2n gametes in natural populations is limited. We hypothesize that 2n gametes are deleterious consequences of meiotic errors maintained by mutation-selection balance and should increase in species with relaxed opportunities for selection on sexual processes (asexuality), reduced efficacy of selection (asexuality, selfing) and increased genome instability (high chromosome number). We used flow cytometry to estimate male 2n gamete production in 60 populations from 24 species of Brassicaceae. We quantified variation in 2n gamete production within and among species, and examined associations with life history, reproductive mode, genome size and chromosomal number while accounting for phylogeny. Most individuals produced < 2% 2n male gametes, whereas a small number had > 5% (up to 85%) production. Variation in 2n gamete production was significant among species and related to reproductive system; asexual species produced significantly more 2n gametes than mixed-mating and outcrossing species. Our results, unique in their multi-species perspective, are consistent with 2n gametes being deleterious but maintained when opportunities for selection are limited. Rare individuals with elevated 2n gamete production may be key contributors to polyploid formation.

Pure polyploidy: Closing the gaps in autopolyploid research

“…The effects of environmental factors (particularly extreme heat and cold) and genotype on unreduced gamete formation are well characterized (reviewed in Mason & Pires, 2015), and researchers have also identified many specific genes that either directly or indirectly impact meiotic reduction (reviewed in Brownfield & K€ ohler, 2011;Crismani et al, 2013). Unreduced gamete production also increases in cases of relaxed selection of gametic viability, as in organisms with asexual reproductive strategies (Kreiner et al, 2017).…”

Polyploidy promotes species diversification of Allium through ecological shifts

“…A high intraspecific frequency of polyploidy can be achieved by various mechanisms, including recurrent origins (Soltis & Soltis, ), triploid mediation (Köhler et al ., ), or mating‐system transition to asexuality (Freeling, ). Interactions among these factors can overcome MCE‐related disadvantages and promote polyploid speciation (Ramsey & Schemske, ; Husband, ; Kreiner et al ., ). Additionally, a high intraspecific polyploid frequency will increase the population size as well as contacts within or among populations (Fowler & Levin, ; Levin, ).…”

Polyspermy in angiosperms: Its contribution to polyploid formation and speciation

“…Polyploids can arise through a somatic doubling in plant sporophytic tissues and by the fusion of unreduced gametes, which occurs because of meiotic or mitotic failures during gametogenesis (Ramsey & Schemske, ). The fusion of a reduced gamete with an unreduced one results in the emergence of a triploid progeny (Brownfield & Köhler, ; Kreiner, Kron, & Husband, ; Ramsey & Schemske, ). For the composition of the subsequent generations, a triploid plant can contribute to producing the swarms of gametes with different ploidy (Henry et al, ), suggesting that tetraploids can be produced from triploids via self‐fertilization or backcrossing to diploids (Ramsey & Schemske, ).…”