Beyond Simple Reproductive Assurance: Cleistogamy Allows Adaptive Plastic Responses to Pollen Limitation

Abstract

Historically, the persistence of mixed mating (reproduction via both self-and cross-fertilization) has presented a puzzle because classic theory predicts that mixed mating should be evolutionarily unstable. One mechanism that could contribute to the maintenance of mixed mating in cleistogamous species is the ability to invest in the appropriate type of reproduction (outcrossing vs. selfing) for a given pollination environment. We tested whether Collomia grandiflora plants responded to pollen limitation by plastically shifting relative investment in cleistogamous (obligately self-fertilizing) versus chasmogamous (potentially outcrossing) reproduction. We estimated reproductive effort (seed production) for chasmogamous and cleistogamous reproductive modes in hand-pollinated and unpollinated plants. We also investigated whether plastic responses to pollen limitation could be constrained by water availability or early nutrient fertilization. Pollen limitation significantly increased cleistogamous reproductive effort, and responses were consistent across gradients of water availability and soil fertility. Our results suggest that dimorphic cleistogamy can provide more than a fixed level of reproductive assurance, as plasticity in allocation to cleistogamy versus chasmogamy can simultaneously enable outcrossing when pollinators are abundant and increase selfing when pollinators are scarce. We argue that such plasticity could be a factor in the evolutionary maintenance of mixed mating in cleistogamous plants.

Season‐dependent effect of cleistogamy in Lamium amplexicaule: flower type origin versus inbreeding status

“…Our results do not support the hypothesis that plastic cleistogamy is an adaptation to resource availability, a postulation in which smaller plants should favor closed over open flowers due to the supposedly higher production cost of open flowers (Schemske, ; Waller, ). Nevertheless, the observed patterns of plasticity of CH proportion across seasons are consistent with the reproductive assurance hypothesis (sensu Lloyd, ): namely, that closed flowers, being independent of pollinator activity for fertilization, should be favored when pollinators are scarce, e.g., in autumn (Berg and Redbo‐Torstensson, ; Albert et al., ). Indeed, our findings showed that CH pollination success for the progeny of open flowers was higher in spring than in autumn, which coincided with a higher proportion of CH, whereas CL pollination success did not substantially vary across seasons.…”

Patterns of chasmogamy and cleistogamy, a mixed-mating strategy in an endangered perennial

“…Plant size has been shown to be a limiting factor for reproductive effort (Jasieniuk and Lechowicz 1987; Diaz and MacNair 1998; Munguía-Rosas et al 2015) with some studies demonstrating that manipulations of above-ground vegetation can significantly reduce CL alone (Diaz and MacNair 1998) or both floral morphs (Munguía-Rosas et al 2015). Resource limitations that negatively impact CL may be induced by environmental stresses such as soil moisture or soil fertility gradients (Schoen and Lloyd 1984; Bell and Quinn 1987; Albert et al 2011). However, in a review by Campbell et al (1983), two-thirds of perennial non-ruderal grass species expressed CL in response to stochastic environmental conditions.…”

Enhanced leaky sex expression is an adaptive plastic response to pollen limitation in the dioecious plantMercurialis annua

“…Our results provide evidence for a plastic component to the expression of sex inconstancy in M. annua, with a slight tendency for more leaky females in populations lacking males and, significantly, females that on average produced more than twice as many male flowers in the absence of males than in their presence. Plastic responses to pollen limitation in plants have been recorded previously, in the context of the increased production of cleistogamous flowers and corresponding selfing rates in Viola praemorsa (Jones et al 2013) and Collomia grandiflora (Albert et al 2011). However, although leaky sex expression is a common feature of the reproduction of dioecious plants (Lloyd and Bawa 1984;Korpelainen 1998;Ehlers and Bataillon 2007;Cossard and Pannell 2019), our study provides demonstrates that such leakiness may be plastic and sensitive to mating opportunities.…”