Cost limitation through constrained oviposition site in a plant‐pollinator/seed predator mutualism

Abstract

Summary1. Mutualism often involves reciprocal exploitation due to individual selection for increased benefits even at the expense of the partner. Therefore, stability and outcomes of such interactions crucially depend on cost limitation mechanisms. 2. In the plant, pollinator /seed predator interaction between Silene latifolia (Caryophyllaceae) and Hadena bicruris (Lepidoptera: Noctuidae), moths generate pollination benefits as adults but impose seed predation costs as larvae. We examined whether floral morphology limits over-exploitation by constraining oviposition site. Oviposition site varies naturally inside vs. outside the corolla tube, but neither its determinants nor its effect on the interaction have been investigated. 3. In a common garden with plants originating from eight populations, corolla tube length predicted oviposition site, but not egg presence or pollination efficiency, suggesting that long corolla tubes constrain the moth to lay eggs on petals. Egg position was also predicted by the combined effect of corolla tube and moth ovipositor lengths, with shorter ovipositor than corolla tube resulting in higher probability for eggs outside. Egg position on a given plant was repeatable over different exposure nights. 4. When egg position was experimentally manipulated, eggs placed on the petal resulted in significantly fewer successful fruit attacks compared with eggs placed inside the corolla tube, suggesting differences in egg/larval mortality. Egg position also differently affected larval mass, fruit mass and fruit development. 5. Our results indicate that constraining oviposition site through a long corolla tube reduces seed predation costs suffered by the plant without negatively affecting pollination efficiency and, hence may act to limit over-exploitation. However, the net effects of corolla tube depth variation on this interaction may fluctuate with extrinsic factors affecting egg mortality, and with patterns of gene flow affecting trait matching between the interacting species. 6. The intermediate fitness costs incurred by both plant and insect associated with the different egg positions may reduce selective pressures for this interaction to evolve towards antagonism, favouring instead a mutualistic outcome. While a role for oviposition site variation in cost limitation is a novel finding in this system, it may apply more generally also to other mutualisms involving pollinating seed predators.

Diversification through multitrait evolution in a coevolving interaction

“…Parasitism of flowers or seeds is common among insects, but many plant linages have flowers poorly suited to pollination by ovipositing insects (25). Interactions between some plant and insect lineages, such as Silene plants and Hadena moths, seem to remain at the interface between parasitism and mutualism; however, like Lithophragma and Greya, they may possibly vary in ecological outcome among populations (4,29). It is likely, though, that more plants are pollinated by floral parasites than is currently known.…”

Choices and consequences of oviposition by a pollinating seed predator,Hadena ectypa(Noctuidae), on its host plant,Silene stellata(Caryophyllaceae)

“…An additional possible moth benefit of oviposition into flowers with longer corolla tubes may be protection for larvae. Egg mortality from desiccation due to exposure can be high (Zimmerman and Brody, 1998), and deeper corolla tubes may provide a more humid environment, which may increase larval survival (Brantjes, 1976b; Wilson et al, 1982; Labouche and Bernasconi, 2013). In addition, parasitoids likely pose a potential major threat to Hadena larval survival (Elzinga et al, 2003), and Hadena larvae from eggs that are laid where exposure to parasitoid attack is minimized may have higher survival (Chen and Welter, 2007).…”

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

“…Although some research has addressed host plant selection in frugivorous and seed predator insects that also pollinate sexually dimorphic plants (Collin et al, 2002;Parachnowitsch & Caruso, 2008;Burkhardt et al, 2009;LaBouche & Bernasconi, 2013;Tzeng et al, 2014;Wang et al, 2014), we know of only two studies to have quantified traits used by strict antagonists that consume reproductive parts (Ashman et al, 2004;Ashman & Penet, 2007). We know of none to have addressed how sessile, pre-dispersal seed predators select host plants in a sexually dimorphic plant.…”

“…Sexually dimorphic plants provide ideal systems to examine cues that may drive female choice of oviposition sites because the sexes often differ in traits that could be important to florivores, frugivores, and pre-dispersal seed predators (e.g. Shykoff et al, 2003;Asikainen & Mutikainen, 2005;LaBouche & Bernasconi, 2013). In the sexually dimorphic dioecious Silene latifolia Poir., female plants are attacked by the seed predator moth Hadena bicruris Hufnagel and recent work has shown that, among female plants, variation in floral shape influences oviposition and, in turn, larval survival (LaBouche & Bernasconi, 2013).…”

“…Shykoff et al, 2003;Asikainen & Mutikainen, 2005;LaBouche & Bernasconi, 2013). In the sexually dimorphic dioecious Silene latifolia Poir., female plants are attacked by the seed predator moth Hadena bicruris Hufnagel and recent work has shown that, among female plants, variation in floral shape influences oviposition and, in turn, larval survival (LaBouche & Bernasconi, 2013). However, H. bicruris moths pollinate S. latifolia plants while ovipositing.…”