Asymmetric reproductive interference: The consequences of cross‐pollination on reproductive success in sexual–apomictic populations of Potentilla puberula (Rosaceae)

Abstract

Apomixis evolves from a sexual background and usually is linked to polyploidization. Pseudogamous gametophytic apomicts, which require a fertilization to initiate seed development, of various ploidy levels frequently co‐occur with their lower‐ploid sexual ancestors, but the stability of such mixed populations is affected by reproductive interferences mediated by cross‐pollination. Thereby, reproductive success of crosses depends on the difference in ploidy levels of mating partners, that is, on tolerance of deviation from the balanced ratio of maternal versus paternal genomes. Quality of pollen can further affect reproductive success in intercytotype pollinations. Cross‐fertilization, however, can be avoided by selfing which may be induced upon pollination with mixtures of self‐ and cross‐pollen (i.e., mentor effects). We tested for reproductive compatibility of naturally co‐occurring tetraploid sexuals and penta‐ to octoploid apomicts in the rosaceous species Potentilla puberula by means of controlled crosses. We estimated the role of selfing as a crossing barrier and effects of self‐ and cross‐pollen quality as well as maternal: paternal genomic ratios in the endosperm on reproductive success. Cross‐fertilization of sexuals by apomicts was not blocked by selfing, and seed set was reduced in hetero‐ compared to homoploid crosses. Thereby, seed set was negatively related to deviations from balanced parental genomic ratios in the endosperm. In contrast, seed set in the apomictic cytotypes was not reduced in hetero‐ compared to homoploid crosses. Thus, apomictic cytotypes either avoided intercytotype cross‐fertilization through selfing, tolerated intercytotype cross‐fertilizations without negative effects on reproductive success, or even benefitted from higher pollen quality in intercytotype pollinations. Our experiment provides evidence for asymmetric reproductive interference, in favor of the apomicts, with significantly reduced seed set of sexuals in cytologically mixed populations, whereas seed set in apomicts was not affected. Incompleteness of crossing barriers further indicated at least partial losses of a parental genomic endosperm balance requirement.

Ploidy-Dependent Effects of Light Stress on the Mode of Reproduction in the Ranunculus auricomus Complex (Ranunculaceae)

“…The current theory suggests that epigenetic mutation in polyploids creates relaxation on genomic imprinting during endosperm development (Kaushal et al, 2018). This could be the reason of higher seed set in hexaploid than in tetraploid cytotypes, similar to in hexaploid Potentilla puberula that had higher seed set than the tetraploids (Dobeš et al, 2018). These findings suggest the presence of a buffer effect on genomic imprinting in polyploids.…”

Difference in reproductive mode rather than ploidy explains niche differentiation in sympatric sexual and apomictic populations ofPotentilla puberula

“…Geographical range expansion of outcrossing sexuals, on the contrary, may be hindered by demographic dynamics (e.g., Allee effects, Allee, Emerson, Park, Park, & Schmidt, ) or pollinator dependence. Apomicts may thus have a priority effect (Levins & Culver, ; Shulman et al, ) in regions potentially suitable for sexuals and block their establishment by competitive exclusion and asymmetrical reproductive interference (Dobeš et al, ; Kyogoku, ; Mogie, ).…”

“…It exhibits a series of reproductively differentiated ploidy levels comprising tetra‐ ( x = 7; 2 n = 28), penta‐ (2 n = 35), hexa‐ (2 n = 42), hepta‐ (2 n = 49), and octoploids (2 n = 56; Dobeš, ). Tetraploid individuals reproduce almost exclusively sexually and are self‐incompatible, whereas higher ploids are predominantly self‐compatible and pseudogamous apomicts (Dobeš et al, ; Nardi et al, ). For hexaploids, both reproductive modes are documented, with apomictic individuals usually clustering with other apomictic cytotypes, and sexual individuals occurring in low frequencies within sexual tetraploid populations (which probably originate frequently de novo as autohexaploids, Nardi et al, ).…”

“…Given the strong correspondence between ploidy level and reproductive mode, with more than 90% of seeds by cytotype being derived by either reproductive mode (Dobeš et al, ; Nardi et al, ), we considered henceforth tetraploid individuals to be sexual and penta‐, hepta‐, and octoploids to be apomicts. According to Nardi et al (), hexaploids comprise sexual autohexaploids (ca.…”

“…Thereby, the probability of occurrence of a cytotype in a specific population (i.e., 0 or 1 in single‐cytotype populations and 0.5 in mixed populations) was related to ecological variables by means of logistic regressions. We used occurrences instead of frequencies (i.e., number of individuals) because of uneven sample sizes and to reduce the effects of possible reproductive interference among cytotypes (Dobeš et al, ), which may influence the relative frequencies of sexual and apomictic cytotypes in mixed populations. The Bonferroni correction was applied to the obtained p ‐values.…”