Geographical matching of volatile signals and pollinator olfactory responses in a cycad brood-site mutualism

Abstract

Brood-site mutualisms represent extreme levels of reciprocal specialization between plants and insect pollinators, raising questions about whether these mutualisms are mediated by volatile signals and whether these signals and insect responses to them covary geographically in a manner expected from coevolution. Cycads are an ancient plant lineage in which almost all extant species are pollinated through brood-site mutualisms with insects. We investigated whether volatile emissions and insect olfactory responses are matched across the distribution range of the African cycad Encephalartos villosus. This cycad species is pollinated by the same beetle species across its distribution, but cone volatile emissions are dominated by alkenes in northern populations, and by monoterpenes and a pyrazine compound in southern populations. In reciprocal choice experiments, insects chose the scent of cones from the local region over that of cones from the other region. Antennae of beetles from northern populations responded mainly to alkenes, while those of beetles from southern populations responded mainly to pyrazine. In bioassay experiments, beetles were most strongly attracted to alkenes in northern populations and to the pyrazine compound in southern populations. Geographical matching of cone volatiles and pollinator olfactory preference is consistent with coevolution in this specialized mutualism.

Extreme diversification of floral volatiles within and among species ofLithophragma(Saxifragaceae)

“…In general, there are only a few examples of plant species scored for intraspecific floral scent variation among multiple populations (55), and most of these studies lack the broader phylogenetic and ecological context available for Lithophragma. In a South African cycad, Encephalartos villosus, scent variation has been tightly linked to geographic variation in the antennal sensitivity and behavioral preferences of the local weevil pollinators (32). Perhaps the most similar system to Lithophragma involves plants of the genus Silene (Caryophyllaceae), which are pollinated both by specialist noctuid moth seed predators of the genus Hadena and by generalized moth pollinators (56).…”

“…Hence, reproduction (and, as a consequence, fitness) of the insect and host plant is intimately linked. If floral scents and insect responses are locally coadapted, these chemical cues could function as important isolating traits among populations, and thus function as drivers of diversification (32).…”

2‐Alkyl‐3‐methoxypyrazines are potent attractants of florivorous scarabs (Melolonthidae, Cyclocephalini) associated with economically exploitable Neotropical palms (Arecaceae)

“…2‐Alkyl‐3‐methoxypyrazines (MPs) are nitrogen‐containing aromatic compounds known to participate in the chemical communication system of insects as deterrents, alarm pheromone components and synomones. They are also recognized in food science for their strong (often undesired) effect on human odor perception and very low detection thresholds (low ng L −1 air range) .…”

“…Another MP, 2‐isopropyl‐3‐methoxypyrazine (IPMP), has been isolated in high concentrations in headspace samples obtained from receptive male and female cones of Cycas and Zamia (Cycadales), and its selective attractiveness to pollinator amorphocerine weevils ( Porthetes sp. ; Curculionidae, Amorphocerini) has led to speculation of its possible function as a private channel of communication in cycad–weevil interactions …”

“…; Curculionidae, Amorphocerini) has led to speculation of its possible function as a private channel of communication in cycad-weevil interactions. 3 The diverse cyclocephaline scarabs (Melolonthidae, Cyclocephalini; ∼ 350 spp.) are noteworthy anthophilous insects in Neotropical ecosystems, where they are associated with no fewer than 1200 species of night-blooming angiosperms.…”