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Zamia integrifolia L.f. (Cycadales), a threatened cycad native to Florida, depends on 2 native beetle species for pollination: Rhopalotria slossoni (Chevrolat; Coleoptera: Belidae) and Pharaxanotha floridana (Casey; Coleoptera: Erotylidae). Both insects are brood-site pollina- tion mutualists, known to live and feed within the pollen (male) cone. However, for pollination to occur, beetles must also visit ovulate (fe- male) cones, which have been assumed to offer no benefits to them as food or nurseries. We tested the potential for beetle pollinator use of ovulate cones by performing no-choice behavior and feeding trials for adults of both beetle species on both ovulate cones and pollen cones of Z. integrifolia. Rhopalotria slossoni beetles showed greater survival on ovulate cone tissues despite showing no significant difference in to- tal tissue mass consumed between cone sexes. Conversely, P. floridana consumed more tissue mass from ovulate cone scales yet showed no difference in survivorship on ovulate vs. pollen cone scales. Although neither beetle species is found in large numbers on ovulate cones in the field, our laboratory study suggests that both species could po- tentially benefit from feeding on ovulate cone tissues, questioning the standing hypothesis that Z. integrifolia pollination occurs by deceit. 

Studies of pollination biology often focus on visual and olfactory aspects of attraction, with few studies ad- dressing behavioral responses and morphological adaptation to primary metabolic attributes. As part of an in-depth study of obligate nursery pollination of cycads, we find that Rhopalotria furfuracea weevils show a strong physiological response and behavioral orientation to the cone humidity of the host plant Zamia furfur- acea in an equally sensitive manner to their responses to Z. furfuracea-produced cone volatiles. Our results demonstrate that weevils can perceive fine-scale differences in relative humidity (RH) and that individuals exhibit a strong behavioral preference for higher RH in binary choice assays. Host plant Z. furfuracea pro- duces a localized cloud of higher than ambient humidity around both pollen and ovulate cones, and R. furfuracea weevils preferentially land at the zone of maximum humidity on ovulate cones, i.e., the cracks between rows of megasporophylls that provide access to the ovules. Moreover, R. furfuracea weevils exhibit striking antennal morphological traits associated with RH perception, suggesting the importance of humidity sensing in the evolution of this insect lineage. Results from this study suggest that humidity functions in a signal-like fashion in this highly specialized pollination system and help to characterize a key pollination- mediating trait in an ancient plant lineage. 

Coevolution between plants and insects is thought to be responsible for generating biodiversity. Extensive research has focused largely on antagonistic herbivorous relationships, but mutualistic pollination systems also likely contribute to diversification. Here we describe an example of chemically-mediated mutualistic species interactions affecting trait evolution and lineage diversification. We show that volatile compounds produced by closely related species of Zamia cycads are more strikingly different from each other than are other phenotypic characters, and that two distantly related pollinating weevil species have specialized responses only to volatiles from their specific host Zamia species. Plant transcriptomes show that approximately a fifth of genes related to volatile production are evolving under positive selection, but we find no differences in the relative proportion of genes under positive selection in different categories. The importance of phenotypic divergence coupled with chemical communication for the maintenance of this obligate mutualism highlights chemical signaling as a key mechanism of coevolution between cycads and their weevil pollinators. 

Most cycads engage in brood-site pollination mutualisms, yet the mechanism by which the Cycadales entice pollination services from diverse insect mutualists remains unknown. Here, we characterize a push-pull pollination mechanism between a New World cycad and its weevil pollinators that mirrors the mechanism between a distantly related Old World cycad and its thrips pollinators. The behavioral convergence between weevils and thrips, combined with molecular phylogenetic dating and a meta-analysis of thermogenesis and coordinated patterns of volatile attraction and repulsion suggest that a push-pull pollination mutualism strategy is ancestral in this ancient, dioecious plant group. Hence, it may represent one of the earliest insect/plant pollination mechanisms, arising long before the evolution of visual floral signaling commonly used by flowering plants. 

Abstract Cycads are an ancient group of tropical gymnosperms that are toxic to most animals – including humans – though the larvae of many moths and butterflies (order: Lepidoptera) feed on cycads with apparent immunity. These insects belong to distinct lineages with varying degrees of specialisation and diverse feeding ecologies, presenting numerous opportunities for comparative studies of chemically mediated eco‐evolutionary dynamics. This review presents the first evolutionary evaluation of cycad‐feeding among Lepidoptera along with a comprehensive review of their ecology. Our analysis suggests that multiple lineages have independently colonised cycads from angiosperm hosts, yet only a few clades appear to have radiated following their transitions to cycads. Defensive traits are likely important for diversification, as many cycad specialists are warningly coloured and sequester cycad toxins. The butterfly family Lycaenidae appears to be particularly predisposed to cycad‐feeding and several cycadivorous lycaenids are warningly coloured and chemically defended. Cycad–herbivore interactions provide a promising but underutilised study system for investigating plant–insect coevolution, convergent and divergent adaptations, and the multi‐trophic significance of defensive traits; therefore the review ends by suggesting specific research gaps that would be fruitfully addressed in Lepidoptera and other cycad‐feeding insects.