Allan G. Ellis

Floral Mimicry Enhances Pollen Export: The Evolution of Pollination by Sexual Deceit Outside of the Orchidaceae

Although the majority of flowering plants achieve pollination by exploiting the food‐seeking behavior of animals, some use alternative ploys that exploit their mate‐seeking behavior. Sexual deception is currently known only from the Orchidaceae and almost always involves pollination by male hymenoptera. An outstanding problem has been to identify the selective factors in plants that favor exploitation of mating versus feeding behaviors in pollinators. Here we show that the insectlike petal ornaments on inflorescences of the daisy Gorteria diffusa elicit copulation attempts from male bombyliid flies and that the intensity of the mating response varies across geographical floral morphotypes, suggesting a continuum in reliance on feeding through mating responses for pollination. Using pollen analogues applied to a morphotype with prominent insectlike petal ornaments, we demonstrate that mate‐seeking male flies are several‐fold more active and export significantly more pollen than females. These results suggest that selection for traits that exploit insect mating behavior can occur through the male component of plant fitness and conclusively demonstrates pollination by sexual deception in Gorteria, making this the first confirmed report of sexual deception outside of the Orchidaceae.

The evolution of floral variation without pollinator shifts in Gorteria diffusa (Asteraceae)

One of the most widely accepted explanations for floral diversification in angiosperms is the pollinator-shift model developed by Verne Grant and Ledyard Stebbins. According to this model, the most profound changes in floral traits (such as morphology, color, patterning and scent) occur when plants undergo adaptive shifts between pollinator classes. We tested this model through investigations of geographical variation in floral form and pollinator assemblages in the South African annual daisy Gorteria diffusa. This species has elaborate insect-like ornaments on the capitulum, which attract bee flies belonging to the genus Megapalpus. We found unprecedented levels of geographically structured intraspecific variation and identified 14 discrete forms that vary in the morphology and ornamentation of the capitulum. This variation is not due to phenotypic plasticity because differences among forms were maintained in plants grown from seed in a common garden experiment. Contrary to predictions from the pollinator-shift model, all populations, regardless of floral phenotype, were pollinated primarily by a single species of Megapalpus bee fly. Much of the extensive variation in floral form in G. diffusa therefore appears to have arisen without evolutionary shifts between pollinator types.

Do pollinators influence the assembly of flower colours within plant communities

The co-occurrence of plant species within a community is influenced by local deterministic or neutral processes as well as historical regional processes. Floral trait distributions of co-flowering species that share pollinators may reflect the impact of pollinator preference and constancy on their assembly within local communities. While pollinator sharing may lead to increased visitation rates for species with similar flowers, the receipt of foreign pollen via interspecific pollinator movements can decrease seed set. We investigated the pattern of community flower colour assembly as perceived by native honeybee pollinators within 24 local assemblages of co-flowering Oxalis species within the Greater Cape Floristic Region, South Africa. To explore the influence of pollinators on trait assembly, we assessed the impact of colour similarity on pollinator choices and the cost of heterospecific pollen receipt. We show that flower colour is significantly clustered within Oxalis communities and that this is not due to historical constraint, as flower colour is evolutionarily labile within Oxalis and communities are randomly structured with respect to phylogeny. Pollinator observations reveal that the likelihood of pollinators switching between co-flowering species is low and increases with flower colour similarity. Interspecific hand pollination significantly reduced seed set in the four Oxalis species we investigated, and all were dependant on pollinators for reproduction. Together these results imply that flower colour similarity carries a potential fitness cost. However, pollinators were highly flower constant, and remained so despite the extreme similarity of flower colour as perceived by honeybees. This suggests that other floral traits facilitate discrimination between similarly coloured species, thereby likely resulting in a low incidence of interspecific pollen transfer (IPT). If colour similarity promotes pollinator attraction at the community level, the observed clustering of flower colour within communities might result from indirect facilitative interactions.

Development of a complex floral trait: the pollinator-attracting petal spots of the beetle daisy, Gorteria diffusa (Asteraceae).

Angiosperms possess a variety of complex floral traits that attract animal pollinators. Dark petal spots have evolved independently many times across the angiosperm phylogeny and have been shown to attract insect pollinators from several lineages. Here we present new data on the ontogeny and morphological complexity of the elaborate insect-mimicking petal spots of the South African daisy species, Gorteria diffusa (Asteraceae), commonly known as the beetle daisy, although it is fly-pollinated. Using light and scanning electron microscopy and histology, we identified three distinct specialized cell types of the petal epidermis that compose the petal spot. Sophisticated patterning of pigments, cuticular elaborations, and multicellular papillate trichomes make the G. diffusa petal spot a uniquely complex three-dimensional floral ornament. Examination of young inflorescence meristems revealed that G. diffusa ray florets develop (and probably also initiate) basipetally, in the opposite direction to the disc florets-a developmental phenomenon that has been found in some other daisies, but which contradicts conventional theories of daisy inflorescence architecture. Using these ontogenetic and morphological data, we have identified the mechanism by which G. diffusa patterns its insect-mimicking petal spots, and we propose a testable model for the genetic regulation of petal spot identity.

Floral polymorphism and the fitness implications of attracting pollinating and florivorous insects.

BACKGROUND AND AIMS Floral polymorphism is frequently attributed to pollinator-mediated selection. Multiple studies, however, have revealed the importance of non-pollinating visitors in floral evolution. Using the polymorphic annual daisy Ursinia calenduliflora, this study investigated the importance of different insect visitors, and their effects on fitness, in the maintenance of floral polymorphism. METHODS The spatial structure of a discrete floral polymorphism was characterized based on the presence/absence of anthocyanin floret spots in U. calenduliflora. A 3-year observational study was then conducted in polymorphic populations to investigate differences in visitation rates of dominant visitors to floral morphs. Experiments were performed to explore the floral preference of male and female Megapalpus capensis (the dominant insect visitor) and their effectiveness as pollinators. Next, floral damage by antagonistic florivores and the reproductive success of the two floral morphs were surveyed in multiple populations and years. KEY RESULTS Floral polymorphism in U. calenduliflora was structured spatially, as were insect visitation patterns. Megapalpus capensis males were the dominant visitors and exhibited strong preference for the spotted morph in natural and experimental observations. While this may indicate potential fitness benefits for the spotted morph, female fitness did not differ between floral morphs. However, as M. capensis males are very efficient at exporting U. calenduliflora pollen, their preference may likely increase the reproductive fitness of the spotted morph through male fitness components. The spotted morph, however, also suffered significantly greater costs due to ovule predation by florivores than the spotless morph. CONCLUSIONS The results suggest that pollinators and florivores may potentially exert antagonistic selection that could contribute to the maintenance of floral polymorphism across the range of U. calenduliflora. The relative strength of selection imposed by each agent is potentially determined by insect community composition and abundance at each site, highlighting the importance of community context in the evolution of floral phenotypes.

Intraspecific divergence and convergence of floral tube length in specialized pollination interactions.

Floral tubes are often thought to be a consequence of adaptive specialization towards pollinator morphology. We explore floral tube length evolution within Tritoniopsis revoluta (Iridaceae), a species with considerable geographical tube length variation. We ask whether tube lengths of T. revoluta populations are associated with pollinator proboscis lengths, whether floral divergence occurs in the presence of different pollinators and whether floral convergence occurs between distantly related populations pollinated by the same pollinator. Finally, we ask whether tube length evolution is directional. Shifts between morphologically different pollinators were always associated with shifts in floral morphology, even when populations were very closely related. Distantly related populations had similar tube lengths when they were pollinated by the same pollinator. Shifts in tube length tended to be from short to long, although reversals were not infrequent. After correcting for the population-level phylogeny, there was a strong positive, linear relationship between floral tube length and pollinator proboscis length, suggesting that plants are functionally specialized on different pollinators at different sites. However, because tube length evolution in this system can be a bidirectional process, specialization to the local pollinator fauna is unlikely to result in evolutionary or ecological dead-ends such as canalization or range limitation.

The structure of legume–rhizobium interaction networks and their response to tree invasions

We provide data on how legume-rhizobia interaction webs react to invasions by exotic legumes. This is the first study of its kind and found that general hypotheses derived from above-ground mutualistic webs may not hold for below-ground counterparts. Specifically, we found that legume-rhizobia interactions at the community level are highly specialised resulting in strongly modular webs, which are not nested, and that invasive legumes do not infiltrate existing native webs but rather form unique and novel modules in webs.

Floral trait variation and integration as a function of sexual deception in Gorteria diffusa

Phenotypic integration, the coordinated covariance of suites of morphological traits, is critical for proper functioning of organisms. Angiosperm flowers are complex structures comprising suites of traits that function together to achieve effective pollen transfer. Floral integration could reflect shared genetic and developmental control of these traits, or could arise through pollinator-imposed stabilizing correlational selection on traits. We sought to expose mechanisms underlying floral trait integration in the sexually deceptive daisy, Gorteria diffusa, by testing the hypothesis that stabilizing selection imposed by male pollinators on floral traits involved in mimicry has resulted in tighter integration. To do this, we quantified patterns of floral trait variance and covariance in morphologically divergent G. diffusa floral forms representing a continuum in the levels of sexual deception. We show that integration of traits functioning in visual attraction of male pollinators increases with pollinator deception, and is stronger than integration of non-mimicry trait modules. Consistent patterns of within-population trait variance and covariance across floral forms suggest that integration has not been built by stabilizing correlational selection on genetically independent traits. Instead pollinator specialization has selected for tightened integration within modules of linked traits. Despite potentially strong constraint on morphological evolution imposed by developmental genetic linkages between traits, we demonstrate substantial divergence in traits across G. diffusa floral forms and show that divergence has often occurred without altering within-population patterns of trait correlations.

Costs of deception and learned resistance in deceptive interactions

The costs that species suffer when deceived are expected to drive learned resistance, although this relationship has seldom been studied experimentally. Flowers that elicit mating behaviour from male insects by mimicking conspecific females provide an ideal system for such investigation. Here, we explore interactions between a sexually deceptive daisy with multiple floral forms that vary in deceptiveness, and the male flies that pollinate it. We show that male pollinators are negatively impacted by the interaction, suffering potential mating costs in terms of their ability and time taken to locate genuine females within deceptive inflorescences. The severity of these costs is determined by the amount of mating behaviour elicited by deceptive inflorescences. However, inexperienced male flies exhibit the ability to learn to discriminate the most deceptive inflorescences as female mimics and subsequently reduce the amount of mating behaviour they exhibit on them with increased exposure. Experienced males, which interact with sexually deceptive forms naturally, exhibit similar patterns of reduced mating behaviour on deceptive inflorescences in multiple populations, indicating that pollinator learning is widespread. As sexually deceptive plants are typically dependent on the elicitation of mating behaviour from male pollinators for pollination, this may result in antagonistic coevolution within these systems.

Invariant antagonistic network structure despite high spatial and temporal turnover of interactions

Recent work has suggested that emergent ecological network structure exhibits very little spatial or temporal variance despite changes in community composition. However, the changes in network interactions associated with turnover in community composition have seldom been assessed. Here we examine whether changes in ecological networks are best detected by standard emergent network metrics or by assessing internal network changes (i.e. interaction and composition turnover). To eliminate possible spatial or phylogenetic effects, that in large-scale studies may obscure mechanisms structuring networks and interactions, we sampled multiple antagonistic (plant-herbivore) networks for a single diverse plant family (the Restionaceae) in the hyperdiverse Cape Floristic Region. These are the first plant-herbivore networks constructed for this global biodiversity hotspot. We found invariant emergent network structure despite considerable changes in insect and plant composition across communities over time and space. In contrast, there was high interaction turnover between networks. Seasonally, this was driven by turnover in insect species and insect host switching. Spatially, this was driven by simultaneous turnover in plant and insect species, suggesting that many insects are host specific or that both groups exhibit parallel responses to environmental gradients. Spatial interaction turnover was also driven by turnover in plants, showing that many insects can utilise multiple (possibly closely related) hosts and this may create divergent selection gradients that promote insect speciation. Thus we show highly variable interaction fidelity, despite invariant emergent network structure. We suggest that evaluating internal network changes may be more effective at elucidating the processes structuring networks, and many fine-scale changes may be obscured when only calculating emergent network metrics. This article is protected by copyright. All rights reserved.