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Concern for pollinator health often focuses on social bees and their agricultural importance at the expense of other pollinators and their ecosystem services. When pollinating herbivores use the same plants as nectar sources and larval hosts, ecological conflicts emerge for both parties, as the pollinator's services are mitigated by herbivory and its larvae are harmed by plant defences. We tracked individual-level metrics of pollinator health-growth, survivorship, fecundity-across the life cycle of a pollinating herbivore, the common hawkmoth, Hyles lineata , interacting with a rare plant, Oenothera harringtonii , that is polymorphic for the common floral volatile ( R )-(-)-linalool. Linalool had no impact on floral attraction, but its experimental addition suppressed oviposition on plants lacking linalool. Plants showed robust resistance against herbivory from leaf-disc to whole-plant scales, through poor larval growth and survivorship. Higher larval performance on other Oenothera species indicates that constitutive herbivore resistance by O. harringtonii is not a genus-wide trait. Leaf volatiles differed among populations of O. harringtonii but were not induced by larval herbivory. Similarly, elagitannins and other phenolics varied among plant tissues but were not herbivore-induced. Our findings highlight asymmetric plant-pollinator interactions and the importance of third parties, including alternative larval host plants, in maintaining pollinator health. This article is part of the theme issue 'Natural processes influencing pollinator health: from chemistry to landscapes'.

Premise of the Study: Land-use change is cited as a primary driver of global biodiversity loss, with myriad consequences for species, populations, and ecosystems. However, few studies have examined its impact on species interactions, particularly pollination. Furthermore, when the effects of land-use change on pollination have been studied, the focus has largely been on species pollinated by diurnal pollinators, namely, bees and butterflies. Here, we focus on Oenothera harringtonii, a night-flowering, disturbance-adapted species that has experienced a range-wide gradient of land-use change. We tested the hypothesis that the negative impacts of land-use change are mitigated by long-distance pollination., Methods: Our study included both temporal (4 yr) and spatial (19 populations range-wide, and 1, 2, and 5 km from the population center) data, providing a comprehensive understanding of the role of land-use change on pollination biology and reproduction., Key Results: We first confirmed that O. harringtonii is self-incompatible and reliant on pollinators for reproduction. We then showed that hawkmoths (primarily Hyles lineata) are highly reliable and effective pollinators in both space and time. Unlike other studies, we did not detect an effect of population size, increased isolation, or a reduction in suitable habitat in areas with evidence of land-use change on pollination (visitation, pollen removal and deposition). Furthermore, the proportion of suitable habitat and other fragmentation metrics examined were not associated with population size or density in this plant species., Conclusions: We conclude that nocturnal pollination of Oenothera harringtonii via hawkmoths is robust to the negative impacts of land-use change., (© 2016 Skogen et al. Published by the Botanical Society of America. This work is licensed under a Creative Commons Attribution License (CC-BY).)

Heteranthery, the presence of two or more anther types in the same flower, is taxonomically widespread among bee-pollinated angiosperms, yet has puzzled botanists since Darwin. We test two competing hypotheses for its evolution: the long-standing 'division of labour' hypothesis, which posits that some anthers are specialized as food rewards for bees whereas others are specialized for surreptitious pollination, and our new hypothesis that heteranthery is a way to gradually release pollen that maximizes pollen delivery. We examine the evolution of heteranthery and associated traits across the genus Clarkia (Onagraceae) and study plant-pollinator interactions in two heterantherous Clarkia species. Across species, heteranthery is associated with bee pollination, delayed dehiscence and colour crypsis of one anther whorl, and movement of that anther whorl upon dehiscence. Our mechanistic studies in heterantherous species show that bees notice, forage on and export pollen from each anther whorl when it is dehiscing, and that heteranthery promotes pollen export. We find no support for division of labour, but multifarious evidence that heteranthery is a mechanism for gradual pollen presentation that probably evolved through indirect male-male competition for siring success.

Background: Plant volatiles play an important role in both plant-pollinator and plant-herbivore interactions. Intraspecific polymorphisms in volatile production are ubiquitous, but studies that explore underlying differential gene expression are rare. Oenothera harringtonii populations are polymorphic in floral emission of the monoterpene (R)-(−)-linalool; some plants emit (R)-(−)-linalool (linalool+ plants) while others do not (linalool- plants). However, the genes associated with differential production of this floral volatile in Oenothera are unknown. We used RNA-Seq to broadly characterize differential gene expression involved in (R)-(−)-linalool biosynthesis. To identify genes that may be associated with the polymorphism for this trait, we used RNA-Seq to compare gene expression in six different Oenothera harringtonii tissues from each of three linalool+ and linalool- plants. Results: Three clusters of differentially expressed genes were enriched for terpene synthase activity: two were characterized by tissue-specific upregulation and one by upregulation only in plants with flowers that produce (R)-(−)-linalool. A molecular phylogeny of all terpene synthases identified two putative (R)-(−)-linalool synthase transcripts in Oenothera harringtonii, a single allele of which is found exclusively in linalool+ plants. Conclusions: By using a naturally occurring polymorphism and comparing different tissues, we were able to identify candidate genes putatively involved in the biosynthesis of (R)-(−)-linalool. Expression of these genes in linalool- plants, while low, suggests a regulatory polymorphism, rather than a population-specific loss-of-function allele. Additional terpene biosynthesis-related genes that are up-regulated in plants that emit (R)-(−)-linalool may be associated with herbivore defense, suggesting a potential economy of scale between plant reproduction and defense. [ABSTRACT FROM AUTHOR]

Heteranthery, the presence of two or more anther types in the same flower, is taxonomically widespread among bee-pollinated angiosperms, yet has puzzled botanists since Darwin. We test two competing hypotheses for its evolution: the long-standing 'division of labour' hypothesis, which posits that some anthers are specialized as food rewards for bees whereas others are specialized for surreptitious pollination, and our new hypothesis that heteranthery is a way to gradually release pollen that maximizes pollen delivery. We examine the evolution of heteranthery and associated traits across the genus Clarkia (Onagraceae) and study plant–pollinator interactions in two heterantherous Clarkia species. Across species, heteranthery is associated with bee pollination, delayed dehiscence and colour crypsis of one anther whorl, and movement of that anther whorl upon dehiscence. Our mechanistic studies in heterantherous species show that bees notice, forage on and export pollen from each anther whorl when it is dehiscing, and that heteranthery promotes pollen export. We find no support for division of labour, but multifarious evidence that heteranthery is a mechanism for gradual pollen presentation that probably evolved through indirect male–male competition for siring success. [ABSTRACT FROM AUTHOR]

The study of floral trait diversity has a long history due to its role in angiosperm diversification. While many studies have focused on visual traits including morphology and color, few have included floral scent despite its importance in pollination. Of the studies that have included floral scent, sampling has been limited and rarely explores variation at the population level. We studied geographic variation in the flowers of Oenothera harringtonii , a rare plant endemic to a vulnerable shortgrass prairie habitat, whose population structure and conservation status are well studied. The self-incompatible flowers of O. harringtonii open at dusk, produce nectar and a strong fragrance, and are pollinated by hawkmoths. We collected floral trait (morphology, scent chemistry and emission rates) data from 650 individuals from 19 wild populations to survey floral variation across the entire range of this species. Similarly, we collected floral data from 49 individuals grown in a greenhouse common garden, to assess whether variation observed in the field is consistent when environment factors (temperature, watering regime, soil) are standardized. We identified 35 floral volatiles representing 5 biosynthetic classes. Population differentiation was stronger for floral scent chemistry than floral morphology. (R)-(−)-linalool was the most important floral trait differentiating populations, exhibiting clinal variation across the distribution of O. harringtonii without any correlated shifts in floral morphology. Populations in the north and west produced (R)-(−)-linalool consistently, those in the east and south largely lacked it, and populations at the center of the distribution were polymorphic. Floral scent emissions in wild populations varied across four years but chemical composition was largely consistent over time. Similarly, volatile emission rates and chemical composition in greenhouse-grown plants were consistent with those of wild populations of origin. Our data set, which represents the most extensive population-level survey of floral scent to date, indicates that such sampling may be needed to capture potentially adaptive geographic variation in wild populations. [Display omitted] • Extensive sampling captured the nature of floral trait variation in wild populations. • Population differentiation was stronger for floral scent chemistry than morphology. • (R)-(−)-linalool was the most important floral trait differentiating populations. • (R)-(−)-linalool production exhibits a geographic cline with no shifts in morphology. [ABSTRACT FROM AUTHOR]