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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’.

To avoid inbreeding depression, plants have evolved diverse breeding systems to favor outcrossing, such as self-incompatibility. However, changes in biotic and abiotic conditions can result in selective pressures that lead to a breakdown in self-incompatibility. The shift to increased selfing is commonly associated with reduced floral features, lower attractiveness to pollinators, and increased inbreeding. We tested the hypothesis that the loss of self-incompatibility, a shift to self-fertilization (autogamy), and concomitant evolution of the selfing syndrome (reduction in floral traits associated with cross-fertilization) will lead to increased inbreeding and population differentiation in Oenothera primiveris. Across its range, this species exhibits a shift in its breeding system and floral traits from a self-incompatible population with large flowers to self-compatible populations with smaller flowers.We conducted a breeding system assessment, evaluated floral traits in the field and under controlled conditions, and measured population genetic parameters using RADseq data.Our results reveal a bimodal transition to the selfing syndrome from the west to the east of the range of O. primiveris. This shift includes variation in the breeding system and the mating system, a reduction in floral traits (flower diameter, herkogamy, and scent production), a shift to greater autogamy, reduced genetic diversity, and increased inbreeding.The observed variation highlights the importance of range-wide studies to understand breeding system variation and the evolution of the selfing syndrome within populations and species.

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.

BackgroundPlant 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.ResultsThree 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.ConclusionsBy using a naturally occurring polymorphism and comparing different tissues, we were able to identify genes putatively involved in the biosynthesis of (R)-(-)-linalool. Expression of these genes in linalool-plants 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.

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.

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.

Wild parsnip is an invasive species with a global distribution in temperate climates. Parsnips are native to Eurasia and have been cultivated for more than five centuries. It is unclear whether the global invasion of this species is a consequence of escape from cultivation or the accidental introduction of a Eurasian wild subspecies. In this study, we used nuclear ribosomal DNA internal transcribed spacer (ITS) and chloroplast DNA (cpDNA) markers to evaluate the genetic structure of wild parsnip in its native range (Europe) and in three distinct geographic regions where it is considered invasive: eastern North America, western North America, and New Zealand. We also compared wild and cultivated parsnips to determine whether they are genetically distinct. From 112 individuals, we recovered 14 ITS and 27 cpDNA haplotypes. One ITS haplotype was widespread; few haplotypes were rare singletons. In contrast, at least two lineages of cpDNA haplotypes were recovered, with several novel haplotypes restricted to Europe. Cultivated parsnips were not genetically distinct from wild parsnips, and numerous wild parsnip populations shared haplotypes with cultivars. High genetic diversity was recovered in all three regions, suggesting multiple introductions.

Insect herbivores and their hostplants constitute much of Earth’s described diversity, but how these often-specialized associations evolve and generate biodiversity is still not fully understood. We combined detailed hostplant data and comparative phylogenetic analyses of the lepidopteran family Momphidae to explore how shifts in the use of hostplant resources, not just hostplant taxonomy, contribute to the diversification of phytophagous insect lineages. We generated two phylogenies primarily from momphid species in the nominate genus,MomphaHübner. A six-gene phylogeny was constructed with exemplars from Onagraceae hosts in western and southwestern USA and a cytochromecoxidase subunit 1 (COI) phylogeny utilized both our collected sequences and publicly available accessions from the Barcode of Life Data System. Coalescent-based analyses combined with morphological data revealed ca. 56 undescribedMomphaspecies-level taxa, many of which are hostplant specialists on southwestern USA Onagraceae. Our phylogenetic reconstructions identified four major momphid clades: 1) an Onagraceae flower- and fruit-feeding clade, 2) a Melastomataceae galling clade, 3) an Onagraceae and Rubiaceae leafmining clade, and 4) a heterogeneous clade associated with multiple hostplant families, plant tissues, and larval feeding modes. Ancestral trait reconstructions on the COI tree identified leafmining on Onagraceae as the ancestral state for Momphidae. Cophylogenetic analyses detected loose phylogenetic tracking of hostplant taxa. Our study finds that shifts along three hostplant resource axes (hostplant taxon, plant tissue type, and larval feeding mode) contributed to the evolutionary success and diversification ofMompha. More transitions between exploited host tissue types than between hostplant families indicated that exploited host tissue (without a change in host) played an unexpectedly large role in the diversification of these moths.

When plant species invade new areas, they can escape from specialist enemies and thereby reduce investment in chemical defense. Enemy release may have other impacts on plant chemistry; in the absence of specialists, plants may be able to increase production of volatiles that enhance attractiveness to pollinators. In the United States (US), the introduced Eurasian wild parsnip, Pastinaca sativa, has long been subject to attack by an introduced coevolved florivore, Depressaria pastinacella, the parsnip webworm. In 2004, webworms were found for the first time attacking parsnips in New Zealand (NZ). Relative to US P. sativa, NZ P. sativa produces lower levels of defenses but higher levels of certain floral volatiles, suggesting that escape from its specialist florivore may have resulted in changes in volatile profiles to increase pollinator attraction.In this study, we examined the influence of wild parsnip floral volatiles on pollinator attraction and seed production in NZ and the US. While many insect groups were observed on parsnip umbels, the percentage of flowers that set seed could significantly be predicted by the occurrence of large calyptrate flies and small syrphids in both localities. In the US, β-pinene, γ-terpinene, hexyl butyrate, octyl butyrate, germacrene D and an unknown monoterpene were all positively correlated with visitation by large calyptrates and small syrphids. In NZ, trans- ocimene, carene and octyl butyrate were positively correlated with visitation. Remarkably, most compounds positively associated with visitation are produced in significantly higher proportions in NZ flowers, suggesting that NZ flowers, in the absence of specialized florivores, may be chemically better constituted to attract pollinators.

The diversity of floral forms in angiosperms is frequently attributed to pollinators but herbivores can be just as important. Here we examine the role of a flower-feeding caterpillar, Mompha, in driving floral trait evolution and subsequent pollinator-shifts in a recently radiated clade of flowering plants, Oenothera sect. Calylophus (Onagraceae). Longer-tubed, hawkmoth flowers had substantially greater damage compared to smaller bee-pollinated flowers. Mompha's preference for longer-tubed flowers, which is evident even within populations of some species, may have played an important role in driving the morphological changes associated with shifts from hawkmoth to bee pollination., Floral trait evolution is frequently attributed to pollinator-mediated selection but herbivores can play a key role in shaping plant reproductive biology. Here we examine the role of florivores in driving floral trait evolution and pollinator shifts in a recently radiated clade of flowering plants, Oenothera sect. Calylophus. We compare florivory by a specialist, internal feeder, Mompha, on closely related hawkmoth- and bee-pollinated species and document variation in damage based on floral traits within sites, species and among species. Our results show that flowers with longer floral tubes and decreased floral flare have increased Mompha damage. Bee-pollinated flowers, which have substantially smaller floral tubes, experience on average 13% less Mompha florivory than do hawkmoth-pollinated flowers. The positive association between tube length and Mompha damage is evident even within sites of some species, suggesting that Mompha can drive trait differentiation at microevolutionary scales. Given that there are at least two independent shifts from hawkmoth to bee pollination in this clade, florivore-mediated selection on floral traits may have played an important role in facilitating morphological changes associated with transitions from hawkmoth to bee pollination.

As a specialist on the reproductive structures of Pastinaca sativa and species in the related genus Heracleum, the parsnip webworm (Depressaria pastinacella) routinely encounters a distinctive suite of phytochemicals in hostplant tissues. Little is known, however, about the detoxification mechanisms upon which this species relies to metabolize these compounds. In this study, larval guts containing hostplant tissues were homogenized, and metabolism was determined by incubating reactions with and without NADPH and analyzing for substrate disappearance and product appearance by gas chromatography-mass spectrometry. Using this approach, we found indications of carboxylesterase activity, in the form of appropriate alcohol metabolites for three aliphatic esters in hostplant tissues-octyl acetate, octyl butyrate, and hexyl butyrate. Involvement of webworm esterases in hostplant detoxification subsequently was confirmed with metabolism assays with pure compounds. This study is the first to implicate esterases in lepidopteran larval midgut metabolism of aliphatic esters, ubiquitous constituents of flowers and fruits. In addition, this method confirmed that webworms detoxify furanocoumarins and myristicin in their hostplants via cytochrome P450-mediated metabolism, and demonstrated that these enzymes also metabolize the coumarin osthol and the fatty acid derivative palmitolactone.

The Enemy Release Hypothesis links exotic plant success to escape from enemies such as herbivores and pathogens. Recent work has shown that exotic plants that more fully escape herbivores and pathogens are more likely to become highly invasive, compared to plants with higher enemy loads in their novel ranges. We predicted that highly invasive plants from the Asteraceae and the Brassicaceae would be less acceptable, in laboratory no-choice feeding trials, to the generalist herbivore the American grasshopper, Schistocerca americana. We also compared herbivory on invasive and non-invasive plants from the genus Centaurea in no-choice feeding trials using the red-legged grasshopper Melanoplus femurrubrum and in a common garden in the field. In accordance with our predictions, highly invasive plants were fed on less by grasshoppers in the laboratory. They also received less damage in the field, suggesting that they contain feeding deterrents that render them less acceptable to generalist herbivores than non-invasive plants.

Although selection by herbivores for increased feeding deterrence in hostplants is well documented, selection for increased oviposition deterrence is rarely examined. We investigated chemical mediation of oviposition by the parsnip webworm (Depressaria pastinacella) on its principal hostplant Pastinaca sativa to determine whether ovipositing adults choose hostplants based on larval suitability and whether hostplants experience selection for increased oviposition deterrence. Webworms consume floral tissues and florivory selects for increased feeding deterrents; moths, however, oviposit on leaves of pre-bolting plants. Exclusive use of different plant parts for oviposition and larval feeding suggests oviposition should select for increased foliar deterrents. Recent webworm colonization of New Zealand (NZ) allowed us to assess phenotypic changes in foliar chemicals in response to webworm oviposition. In a common garden experiment, we compared NZ populations with and without a history of infestation from 2004 to 2006 for changes in leaf chemistry in response to oviposition. Three leaf volatiles, cis- and trans-ocimene, and β-farnesene, elicit strong responses in female moth antennae; these compounds were negatively associated with oviposition and are likely oviposition deterrents. Leaf β-farnesene was positively correlated with floral furanocoumarins that deter florivory; greater oviposition on plants with low floral furanocoumarins indicates that moths preferentially oviposit on parsnips most suitable for larval growth. Unlike florivory, high oviposition on leaves did not lower plant fitness, consistent with the fact that NZ parsnip foliar chemistry was unaffected by 3–6 years of webworm infestation. Thus, in this system, selection by ovipositing moths on foliar chemistry is weaker than selection by larvae on floral chemistry.