Gender inequality in predispersal seed predation contributes to female seed set advantage in a gynodioecious species

Abstract

Most flowering plants are hermaphrodites. However, in gynodioecious species, some members of the population are male-sterile and reproduce only by setting seed, while others gain fitness through both male and female function. How females compensate for the loss of male function remains unresolved for most gynodioecious species. Here, as with many plants, fitness differences may be influenced by interactions with multiple species. However, whether multiple species interactions result in gender-specific fitness differences remains unknown. Using observational data from 2009-2010, we quantified seed set of the two sex morphs of Polemonium foliosissimu and asked how it is affected by pollination, and seed predation from a dipteran predispersal seed predator (Anthomyiidae: Hylemya sp.). We assessed seed production and losses to predation in 27 populations for one year and in six populations for a second year. Females set significantly more seed than did hermaphrodites in both years. Of the fitness components we assessed, including the number of flowers per plant, fruit set, seeds/fruit, and proportion of fruits destroyed by Hylemya, only fruit destruction differed significantly between the sexes. In one year, seeds/fruit and predation had a stronger effect on seed set for hermaphrodites than for females. Because predispersal seed predators do not pollinate flowers, their effects may depend on successful pollination of flowers on which they oviposit. To examine if genders differed in pollen limitation and seed predation and/or their interactive effects, in 2011 we hand-pollinated flowers and removed seed predator eggs in a fully factorial design. Both sexes were pollen limited, but their degree of pollen limitation did not differ. However, predation reduced.seed set more for hermaphrodites than for females. We found no significant interaction between hand pollen and seed predation, and no interaction between hand pollination and gender. Our results suggest that while interactions with both pollinators and seed predators affect reproductive success, floral enemies can cause inequality in seed set between genders. The next step is to understand how the seed set advantage affects long-term fitness and persistence of females in gynodioecious populations.

The role of infectious disease in the evolution of females: Evidence from anther‐smut disease on a gynodioecious alpine carnation*

“…However, the majority of this work has focused on the impacts of herbivores (Marshall and Ganders ; Ashman et al. ; Clarke and Brody ) and we know far less about the effects of disease (reviewed in Vega‐Frutis et al. ).…”

“…A plurality of studies have now found that herbivores, particularly florivores (Ashman et al. ; Tsuji and Sota ), and predispersal seed predators (Marshall and Ganders ; Collin and Shykoff ; Clarke and Brody ; Miyake et al. ) preferentially favor hermaphrodites over females.…”

Prolonged stigma and flower lifespan in females of the gynodioecious plant Geranium sylvaticum

“…Bai et al, 2011;Barr and Fishman, 2011;Cuevas and López, 2011;Griffin and Byers, 2012;Blank et al, 2014;Cuevas et al, 2014) and/or they produce less nectar and pollen, leading to lower pollinator visitation rates (Delph, 1996;Ashman, 2000;Bai et al, 2011). On the other hand, the smaller size and number of flowers of female plants may also render them less attractive to enemies like florivores or seed herbivores, leading to a relatively higher seed output in females than hermaphrodites (Marshall and Ganders, 2001;Ashman, 2002;Asikainen and Mutikainen, 2005a;Collin and Shykoff, 2009;Clarke and Brody, 2015).…”

Wise flies: a pre‐dispersal seed predator prefers hermaphrodites over females in the gynodioecious Polemonium foliosissimum

“…We can exclude some of these: the thickness of the carpel wall did not differ between the sex morphs ( t 124 = 0.838, d.f. = 124, P = 0.404), nor did fruit set or seeds/fruit (Clarke & Brody, ). We also found no significant difference in phenology that could drive a mismatch between oviposition and food provisioning (Hilker & Meiners, ).…”

“…Thompson & Pellmyr, 1992). Prior work in this system established that hermaphrodites lose more fruits to Hylemya, but did not investigate if fruit destruction was as a result of female preference for hermaphrodites, higher larval performance on hermaphrodites, or both (Clarke & Brody, 2015). The exposure of Hyleyma eggs from underneath the sepals on which they are laid is a source of significant egg mortality within and among host plants (Zimmerman, 1980c;Zimmerman & Brody, 1998).…”