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The Paradox of Pollinating Floral Parasites

Extreme floral scent divergence and pollination
Extreme floral scent divergence and pollination

Studies of the chemical interactions between plants and insects have been particularly useful in showing the breadth of traits that may be involved in the evolution of interactions. Many of the thousands of chemicals produced by plants are thought to have evolved as defences against insects, microbes, or a combination of these enemies. These compounds can act as defences, repellents or attractants as plants evolve suites of chemicals that attract mutualistic taxa such as pollinators while also repelling others. Whether as defences or attractants, the chemical compounds affecting interactions with other species usually occur as chemical cocktails derived from multiple chemical pathways rather than as isolated chemicals. Proliferation of these compounds has contributed to specialization and diversification on both sides of these interactions.

The interactions between plants and pollinating floral parasites provide a particularly intriguing problem for the evolution of chemical traits in plants. These insects lay their eggs in the same flowers they pollinate, which means that their relationship to the plants has both antagonistic and mutualistic components. Close interactions with pollinating floral parasites have been suggested to favour the evolution of a highly specific plant–insect communication system, in the form of unique compounds that represent ‘private channels’ for exclusive attraction of specific pollinators. If so, then plant species pollinated by a single or a few obligate pollinators should include unique signal compounds or blends that diverge strongly from those produced by plants in more generalized pollination systems and, potentially, also from closely related plant species involved in specific interactions with other species of pollinating floral parasites. So far, however, there is limited evidence for the use of private channels in plants attracting these kinds of pollinator. For example, in the plant genus Yucca, which is involved in an obligate interaction with yucca moths, the three allopatric species analysed thus far show very similar floral scent profiles. Pollinating yucca moths are attracted to yucca floral scent, but the specific role of the novel floral volatiles in pollinator attraction awaits further examination.

Alternatively, growing evidence suggests that flower-pollinator specificity might be accomplished by way of specific blends of otherwise generic floral volatiles. Among the species that have been studied within Glochidion, Breynia and Ficus (for which bioassays have demonstrated olfactory attraction of pollinators), most show strong biosynthetic conservatism among related species, and emit floral scent cocktails composed of common floral compounds. In these cases, floral scent, combined with physical barriers (e.g. size-limiting ostioles in figs), limited visual display and finely tuned temporal dynamics of scent emission may constitute multi-modal ‘floral filters’ whose net result is pollinator-specificity. In other cases, differences in the relative contributions of the different compounds between close relatives, or potential hidden chiral variation in certain compounds, are sufficient to allow the pollinators to discriminate among these species in experimental trials.

A new paper in Annals of Botany describes striking floral scent variation within and between plant lineages, and determines whether these differences are genetically or environmentally based, then investigates the extent to which floral scent is temporally variable at the single flower level and also at the whole plant level as the plant ages, and tests whether visits by the pollinating floral parasite Greya politella alters floral scent production.

 

Extreme divergence in floral scent among woodland star species (Lithophragma spp.) pollinated by floral parasites. (2013) Annals of Botany Volume 111(4): 539-550. doi: 10.1093/aob/mct007
Abstract
A current challenge in coevolutionary biology is to understand how suites of traits vary as coevolving lineages diverge. Floral scent is often a complex, variable trait that attracts a suite of generalized pollinators, but may be highly specific in plants specialized on attracting coevolved pollinating floral parasites. In this study, floral scent variation was investigated in four species of woodland stars (Lithophragma spp.) that share the same major pollinator (the moth Greya politella, a floral parasite). Three specific hypotheses were tested: (1) sharing the same specific major pollinator favours conservation of floral scent among close relatives; (2) selection favours ‘private channels’ of rare compounds particularly aimed at the specialist pollinator; or (3) selection from rare, less-specialized co-pollinators mitigates the conservation of floral scent and occurrence of private channels. Dynamic headspace sampling and solid-phase microextraction were applied to greenhouse-grown plants from a common garden as well as to field samples from natural populations in a series of experiments aiming to disentangle the genetic and environmental basis of floral scent variation. Striking floral scent divergence was discovered among species. Only one of 69 compounds was shared among all four species. Scent variation was largely genetically based, because it was consistent across field and greenhouse treatments, and was not affected by visits from the pollinating floral parasite. The strong divergence in floral scents among Lithophragma species contrasts with the pattern of conserved floral scent composition found in other plant genera involved in mutualisms with pollinating floral parasites. Unlike some of these other obligate pollination mutualisms, Lithophragma plants in some populations are occasionally visited by generalist pollinators from other insect taxa. This additional complexity may contribute to the diversification in floral scent found among the Lithophragma species pollinated by Greya moths.

 

AJ Cann
Alan Cann is a Senior Lecturer in the School of Biological Sciences at the University of Leicester and formerly Internet Consulting Editor for AoB.

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