Differences in female reproductive success between female and hermaphrodite individuals in the subdioecious shrub Eurya japonica (Theaceae)

Abstract

Subdioecy is thought to occupy a transitional position in the gynodioecy-dioecy pathway, explaining one of the evolutionary routes from hermaphroditism to dioecy. Quantifying any female reproductive advantage of females versus hermaphrodites is fundamental to examining the spectrum between subdioecy and dioecy; however, this is challenging, as multiple interacting factors, such as pollen limitation and resource availability, affect plant reproduction. We compared the female reproductive success of females and hermaphrodites via a field experiment in which we hand-pollinated individuals of the subdioecious shrub Eurya japonica of similar size growing under similar light conditions. Effects of pollen limitation and seed quality were also evaluated through comparing the results of hand- and natural-pollination treatments and performing additional laboratory and greenhouse experiments. Overall, females had higher fruit set and produced heavier fruit and more seeds than hermaphrodites, and these results were more pronounced for hand-pollinated than for natural-pollinated plants of both sexes. We also found that seeds naturally produced by females had a higher mean germination rate. These results indicate that females had a pronounced advantage in female reproductive success under conditions of no pollen limitation. The sexual difference in the degree of pollen limitation suggests a pollinator-mediated interaction, whereas the higher female reproductive success of females even under natural conditions implies that E. japonica is a good model species for elucidating the later stages of the gynodioecy-dioecy pathway.

High male fertility in males of a subdioecious shrub in hand-pollinated crosses

“…Previous work showed that trioecy (subdiocy) can be maintained under pollen limitation of female seed production because pollen limitation reduces the fitness of females but not self-fertile hermaphrodites, counteracting the seed fertility advantage of females in subdioecious population (Maurice and Fleming 1995; Fleming et al 1998; Wolf and Takebayashi 2004). However, in self-incompatible E. japonica , considering the weakened reproductive advantage of females against hermaphrodites under natural conditions (Wang et al 2015), although E. japonica is transitioning toward dioecy, pollinator-mediated pollen limitation may suppress enhanced fertility of females and males, thereby promoting the persistence of hermaphrodites in this E. japonica population (i.e. stable subdioecy).…”

“…Hand-pollination treatments also revealed that seeds sired with pollen from male individuals exhibited better performance. Given that the female reproductive success of female individuals is higher than that of hermaphrodites and that hermaphrodites are self-incompatible in E. japonica (Wang et al 2015), pollen limitation may inhibit the shift and permit the persistence of hermaphrodites in this E. japonica population.…”

“…; for details of the study site, see Wang et al 2015). Although the proportion of hermaphrodites including all sexual types in other populations is usually low (<1–10 %), but sometimes high (>10 %, reaching 38 %, Murata et al 1991; Higo 1994; Manabe 1996; Suzuki 2005; Tsuji and Sota 2010), the sex ratio of E. japonica flowering individuals was M: 30.1 %; F: 33.2 %; H: 5.1 %; HF: 22.6 %; HM: 4.0 % and HFM: 2.4 % at our study site.…”

Sex change in the subdioecious shrub Eurya japonica (Pentaphylacaceae)

“…However, it is inconsistent with our previous results that male individuals have an advantage in male fertility over hermaphrodites in hand‐pollinated crosses (Wang, Matsushita, Tomaru, & Nakagawa, 2016). Considering the weakened reproductive success of females versus hermaphrodites under natural conditions in this  E. japonica population (Wang et al., 2015), pollinator‐mediated interaction and reproductive success through male and female functions may be related to the gradual change in the sex ratio of E. japonica .…”

“…; for details of the study site, see Wang, Matsushita, Tomaru, & Nakagawa, 2015). Plot 1 was destroyed for construction of a building in May 2012, and we added one plot (Plot 4, 20 × 20 m) at the Higashiyama Zoo and Botanical Gardens, Nagoya, Japan (35°09′N, 136°58′E, 79–86 m a.s.l.)…”