Variable and sexually conflicting selection onSilene stellatafloral traits by a putative moth pollinator selective agent

Abstract

Conflicting selection is an important evolutionary mechanism because it impedes directional evolution and helps to maintain phenotypic variation. It can arise when mutualistic and antagonistic selective agents exert opposing selection on the same trait and when distinct phenotypic optima are favored by different fitness components. In this study, we test for conflicting selection through different sexual functions of the hermaphroditic plant, Silene stellata during its early and late flowering season. We find selection is consistently stronger during the early flowering season, which aligns with the activity peak of the pollinating seed predator Hadena ectypa. Importantly, we observe sex‐specific selection on petal dimensions to have opposite signs. We propose that the observed sexually conflicting selection on petal design results from the negative selection through female function for the avoidance of oviposition and the subsequent fruit predation by H. ectypa larvae and the positive selection through male function for pollen export by H. ectypa adults. The Silene–Hadena interaction has previously been considered to be largely parasitic. Our findings suggest a trade‐off mechanism that could thwart the evolution of an “escape route” from the nocturnal pollination syndrome by Silene spp. and contribute to the long‐term maintenance of the Silene–Hadena system.

Quantitative genetic basis of floral design in a natural plant population

“…Importantly, in Zhou et al (2020), we also found conflicting selection pressures exerted on the petal dimensions through the two sexual functions. Remarkably, the floral trait under the strongest conflicting selection (petal length) is also found to have the highest heritability in this paper.…”

“…The Silene-Hadena interaction is further complicated by a guild of generalist pollinator moths, that are equally effective at pollen transfer (Reynolds et al ., 2012). In a previous study, we found that the parasitic and mutualistic interaction between H. ectypa leads to conflicting selection on the petal dimension through the two sexual functions of S. stellata (Zhou et al ., 2020). Furthermore, the transition between H. ectypa and the copollinating species across the flowering phenology also leads to temporally variable selection.…”

“…All study plants were within a 20-by-20-meter exclosure constructed in a natural S. stellata population near Mountain Lake Biological Station (37.348296°, - 80.544301°, elevation ≈ 1,100–1,300 m). The two cohorts within a year correspond to periods when H. ectypa or the copollinators were the dominant pollinator, respectively (Zhou, Dudash, and Fenster, 2016; Zhou et al ., 2020). Our sampling of genotypes to quantify patterns of genetic variation thus take into account potentially different selection pressures that plants in the early and late cohorts experience.…”

“…S. stellata is an emerging model organism for studying pollinator-plant interaction and the evolution of mutualism (Kephart et al ., 2006; Bernasconi et al ., 2009) due to its complex interaction with the pollinator/seed predator moth Hadena ectypa . A previous study has shown prevalent phenotypic selection on the S. stellata floral traits (Zhou et al ., 2020). Most notably, the petal dimensions of S. stellata were found to be under strong conflicting selection through the two sexual functions of the hermaphroditic plant, mediated by the positive and negative interaction with H. ectypa .…”

Paucity of natural history data impedes phylogenetic analyses of pollinator‐driven evolution

“…Syndromes are thought to indicate the selective agents that have driven convergent evolution of correlated floral traits (Fenster et al ., 2004). Tests of syndrome hypotheses by analyzing selection on floral traits by specific pollinator groups through male and female function are, however, rare (Reynolds et al ., 2010; Zhou et al ., 2020). Quantitative analyses of syndrome traits for species with known pollination systems (‘observed species’) can be used to identify clustering in trait space (Wilson et al ., 2004; Marten‐Rodriguez et al ., 2009; Armbruster et al ., 2011), and predict pollination systems of species for which traits could be measured, but for which pollinator data are lacking (‘unobserved species’) (Whittall & Hodges, 2007; Navarro‐Perez et al ., 2013).…”