Pollination efficiency and the pollen-ovule ratio.

Pollination presents a risky journey for pollen grains. Pollen loss is sometimes thought to favour greater pollen investment to compensate for the inefficiency of transport. Sex allocation theory, to the contrary, has consistently concluded that postdispersal loss should have no selective effect on investment in either sex function. But the intuitively appealing compensation idea continues to be raised despite the lack of theoretical endorsement. We address the theoretical issue with a model that directly represents pollen loss (and ovule loss through floral demise or loss of receptivity) as rate-dependent dynamical processes. These loss rates can be varied to examine the effect of pollination efficiency on optimal sex allocation. Pollen-ovule ratios follow from the sex allocation based on the resource costs of pollen and ovule production. This model confirms conventional findings that pollen loss should have essentially no effect on sexual resource allocation in large, panmictic populations. Pollen limitation of seed set does not alter this conclusion. These results force us to rethink the empirical association of pollination efficiency with low pollen-ovule ratios. This pattern could arise if efficient pollen transport commonly results in stigmatic deposition of cohorts of related pollen. Empirical evidence of correlated paternity supports this explanation.

Why the Shaw-Mohler equation works and when it doesn't.

Fitness gain curves were introduced into the framework of the Shaw-Mohler equation, the foundation of sex allocation theory. I return to the Shaw-Mohler equation to consider how it embodies the rare-sex advantage underlying frequency-dependent selection on the sex ratio. The Shaw-Mohler formulation is based on the numbers of males and females randomly mating in a panmictic population. Gain curves are meant to describe reproductive success through male and female functions in hermaphrodites and have been inserted in place of male and female numbers in the Shaw-Mohler equation. In doing so, gain curves bypass consideration of the implicit mating process in the Shaw-Mohler argument and can lead to anomalies like unequal total male and female fitness in a population. If gain curves truly represent fitness gain, equality of total male and female fitness requires a constant sex allocation of equal resource investment into male and female functions. The blurring of input with fitness outcome has led to misinterpretation of what gain curves mean in reproductive ecology. They can describe a particular reproductive ecology, such as diminishing fitness returns on resource investment, but lack causal efficacy with respect to sex allocation.

Ancient insect vision tuned for flight among rocks and plants underpins natural flower colour diversity.

Understanding the origins of flower colour signalling to pollinators is fundamental to evolutionary biology and ecology. Flower colour evolves under pressure from visual systems of pollinators, like birds and insects, to establish global signatures among flowers with similar pollinators. However, an understanding of the ancient origins of this relationship remains elusive. Here, we employ computer simulations to generate artificial flower backgrounds assembled from real material sample spectra of rocks, leaves and dead plant materials, against which to test flowers' visibility to birds and bees. Our results indicate how flower colours differ from their backgrounds in strength, and the distributions of salient reflectance features when perceived by these key pollinators, to reveal the possible origins of their colours. Since Hymenopteran visual perception evolved before flowers, the terrestrial chromatic context for its evolution to facilitate flight and orientation consisted of rocks, leaves, sticks and bark. Flowers exploited these pre-evolved visual capacities of their visitors, in response evolving chromatic features to signal to bees, and differently to birds, against a backdrop of other natural materials. Consequently, it appears that today's flower colours may be an evolutionary response to the vision of diurnal pollinators navigating their world millennia prior to the first flowers.

Fly pollination drives convergence of flower coloration.

Plant-pollinator interactions provide a natural experiment in signal evolution. Flowers are known to have evolved colour signals that maximise their ease of detection by the visual systems of important pollinators such as bees. Whilst most angiosperms are bee pollinated, our understanding on how the second largest group of pollinating insects, flies, may influence flower colour evolution is limited to the use of categorical models of colour discrimination that do not reflect the small colour differences commonly observed between and within flower species. Here we show by comparing flower signals that occur in different environments including total absence of bees, a mixture of bee and fly pollination within one plant family (Orchidaceae) from a single community, and typical flowers from a broad taxonomic sampling of the same geographic region, that perceptually different colours, empirically measured, do evolve in response to different types of insect pollinators. We show evidence of both convergence among fly-pollinated floral colours but also of divergence and displacement of colour signals in the absence of bee pollinators. Our findings give an insight into how both ecological and agricultural systems may be affected by changes in pollinator distributions around the world.

The Effect of Pollen Limitation on the Evolution of Mating System and Seed Size in Hermaphroditic Plants.

Pollen limitation, when inadequate pollen receipt results in a plant setting fewer seeds and fruits, can reduce plant reproductive success and promote the evolution of self-fertilization as a mechanism of reproductive assurance. However, the effect of pollen limitation on the joint evolution of mating system and seed size is not known. Using an evolutionarily stable strategy resource allocation model, we show that where moderate pollen limitation and strong inbreeding depression select for complete outcrossing, pollen limitation should also increase the optimal seed size. In contrast, pollen limitation should not affect the optimal seed size under complete selfing, in which case ovule fertilization is certain. Under intermediate conditions, a mixed mating system evolves if the probability of ovule fertilization declines as more ovules are produced, so that a selfed seed with inbreeding depression provides equal marginal fitness returns to a larger outcrossed seed that may result from pollen limitation. Under mixed mating, outcrossed seeds should be larger than selfed seeds, and pollen limitation should not affect the optimal size of either outcrossed or selfed seeds. Our results identify a novel pathway through which pollen limitation selects for mixed mating and provide an adaptive explanation as to why selfed seeds are often smaller than outcrossed seeds.

Infrastructure construction without information exchange: the trail clearing mechanism in Atta leafcutter ants.

A wide range of group-living animals construct tangible infrastructure networks, often of remarkable size and complexity. In ant colonies, infrastructure construction may require tens of thousands of work hours distributed among many thousand individuals. What are the individual behaviours involved in the construction and what level of complexity in inter-individual interaction is required to organize this effort? We investigate this question in one of the most sophisticated trail builders in the animal world: the leafcutter ants, which remove leaf litter, cut through overhangs and shift soil to level the path of trail networks that may cumulatively extend for kilometres. Based on obstruction experiments in the field and the laboratory, we identify and quantify different individual trail clearing behaviours. Via a computational model, we further investigate the presence of recruitment, which-through direct or indirect information transfer between individuals-is one of the main organizing mechanisms of many collective behaviours in ants. We show that large-scale transport networks can emerge purely from the stochastic process of workers encountering obstructions and subsequently engaging in removal behaviour with a fixed probability. In addition to such incidental removal, we describe a dedicated clearing behaviour in which workers remove additional obstructions independent of chance encounters. We show that to explain the dynamics observed in the experiments, no information exchange (e.g. via recruitment) is required, and propose that large-scale infrastructure construction of this type can be achieved without coordination between individuals.

Plant traits moderate pollen limitation of introduced and native plants: a phylogenetic meta-analysis of global scale.

The role of pollination in the success of invasive plants needs to be understood because invasives have substantial effects on species interactions and ecosystem functions. Previous research has shown both that reproduction of invasive plants is often pollen limited and that invasive plants can have high seed production, motivating the questions: How do invasive populations maintain reproductive success in spite of pollen limitation? What species traits moderate pollen limitation for invaders? We conducted a phylogenetic meta-analysis with 68 invasive, 50 introduced noninvasive and 1931 native plant populations, across 1249 species. We found that invasive populations with generalist pollination or pollinator dependence were less pollen limited than natives, but invasives and introduced noninvasives did not differ. Invasive species produced 3× fewer ovules/flower and >250× more flowers per plant, compared with their native relatives. While these traits were negatively correlated, consistent with a tradeoff, this did not differ with invasion status. Invasive plants that produce many flowers and have floral generalisation are able to compensate for or avoid pollen limitation, potentially helping to explain the invaders' reproductive successes.

Floral colour structure in two Australian herbaceous communities: it depends on who is looking.

BACKGROUND AND AIMS: Pollinator-mediated interactions between plant species may affect the composition of angiosperm communities. Floral colour signals should play a role in these interactions, but the role will arise from the visual perceptions and behavioural responses of multiple pollinators. Recent advances in the visual sciences can be used to inform our understanding of these perceptions and responses. We outline the application of appropriate visual principles to the analysis of the annual cycle of floral colour structure in two Australian herbaceous communities. METHODS: We used spectrographic measurements of petal reflectance to determine the location of flowers in a model of hymenopteran colour vision. These representations of colour perception were then translated to a behaviourally relevant metric of colour differences using empirically calibrated colour discrimination functions for four hymenopteran species. We then analysed the pattern of colour similarity in terms of this metric in samples of co-flowering plants over the course of a year. We used the same method to analyse the annual pattern of phylogenetic relatedness of co-flowering plants in order to compare colour structure and phylogenetic structure. KEY RESULTS: Co-flowering communities at any given date seldom had colour assemblages significantly different from random. Non-random structure, both dispersion and clustering, occurred occasionally, but depended on which bee observer is considered. The degree of colour similarity was unrelated to phylogenetic similarity within a co-flowering community. CONCLUSIONS: Perceived floral colour structure varied with the sensory capabilities of the observer. The lack of colour structure at most sample dates, particularly the rarity of strong dispersion, suggests that plants do not use chromatic signals primarily to enable bees to discriminate between co-flowering species. It is more likely that colours make plants detectable in a complex landscape.

The enigma of sex allocation in Selaginella.

Background and Aims: The division of resource investment between male and female functions is poorly known for land plants other than angiosperms. The ancient lycophyte genus Selaginella is similar in some ways to angiosperms (in heterospory and in having sex allocation occur in the sporophyte generation, for example) but lacks the post-fertilization maternal investments that angiosperms make via fruit and seed tissues. One would therefore expect Selaginella to have sex allocation values less female-biased than in flowering plants and closer to the theoretical prediction of equal investment in male and female functions. Nothing is currently known of sex allocation in the genus, so even the simplest predictions have not been tested. Methods: Volumetric measurements of microsporangial and megasporangial investment were made in 14 species of Selaginella from four continents. In five of these species the length of the main above-ground axis of each plant was measured to determine whether sex allocation is related to plant size. Key Results: Of the 14 species, 13 showed male-biased allocations, often extreme, in population means and among the great majority of individual plants. There was some indication from the five species with axis length measurements that relative male allocation might be related to the release height of spores, but this evidence is preliminary. Conclusions: Sex allocation in Selaginella provides a phylogenetic touchstone showing how the innovations of fruit and seed investment in the angiosperm life cycle lead to typically female-biased allocations in that lineage. Moreover, the male bias we found in Selaginella requires an evolutionary explanation. The bias was often greater than what would occur from the mere absence of seed and fruit investments, and thus poses a challenge to sex allocation theory. It is possible that differences between microspores and megaspores in their dispersal ecology create selective effects that favour male-biased sexual allocation. This hypothesis remains tentative.

Resource Allocation and Seed Size Selection in Perennial Plants under Pollen Limitation.

Pollen limitation may affect resource allocation patterns in plants, but its role in the selection of seed size is not known. Using an evolutionarily stable strategy model of resource allocation in perennial iteroparous plants, we show that under density-independent population growth, pollen limitation (i.e., a reduction in ovule fertilization rate) should increase the optimal seed size. At any level of pollen limitation (including none), the optimal seed size maximizes the ratio of juvenile survival rate to the resource investment needed to produce one seed (including both ovule production and seed provisioning); that is, the optimum maximizes the fitness effect per unit cost. Seed investment may affect allocation to postbreeding adult survival. In our model, pollen limitation increases individual seed size but decreases overall reproductive allocation, so that pollen limitation should also increase the optimal allocation to postbreeding adult survival. Under density-dependent population growth, the optimal seed size is inversely proportional to ovule fertilization rate. However, pollen limitation does not affect the optimal allocation to postbreeding adult survival and ovule production. These results highlight the importance of allocation trade-offs in the effect pollen limitation has on the ecology and evolution of seed size and postbreeding adult survival in perennial plants.

Self-compatibility is over-represented on islands.

Because establishing a new population often depends critically on finding mates, individuals capable of uniparental reproduction may have a colonization advantage. Accordingly, there should be an over-representation of colonizing species in which individuals can reproduce without a mate, particularly in isolated locales such as oceanic islands. Despite the intuitive appeal of this colonization filter hypothesis (known as Baker's law), more than six decades of analyses have yielded mixed findings. We assembled a dataset of island and mainland plant breeding systems, focusing on the presence or absence of self-incompatibility. Because this trait enforces outcrossing and is unlikely to re-evolve on short timescales if it is lost, breeding system is especially likely to reflect the colonization filter. We found significantly more self-compatible species on islands than mainlands across a sample of > 1500 species from three widely distributed flowering plant families (Asteraceae, Brassicaceae and Solanaceae). Overall, 66% of island species were self-compatible, compared with 41% of mainland species. Our results demonstrate that the presence or absence of self-incompatibility has strong explanatory power for plant geographical patterns. Island floras around the world thus reflect the role of a key reproductive trait in filtering potential colonizing species in these three plant families.

Why background colour matters to bees and flowers.

Flowers are often viewed by bee pollinators against a variety of different backgrounds. On the Australian continent, backgrounds are very diverse and include surface examples of all major geological stages of the Earth's history, which have been present during the entire evolutionary period of Angiosperms. Flower signals in Australia are also representative of typical worldwide evolutionary spectral adaptations that enable successful pollination. We measured the spectral properties of 581 natural surfaces, including rocks, sand, green leaves, and dry plant materials, sampled from tropical Cairns through to the southern tip of mainland Australia. We modelled in a hexagon colour space, how interactions between background spectra and flower-like colour stimuli affect reliable discrimination and detection in bee pollinators. We calculated the extent to which a given locus would be conflated with the loci of a different flower-colour stimulus using empirically determined colour discrimination regions for bee vision. Our results reveal that whilst colour signals are robust in homogeneous background viewing conditions, there could be significant pressure on plant flowers to evolve saliently-different colours to overcome background spectral noise. We thus show that perceptual noise has a large influence on how colour information can be used in natural conditions.

Pollen Limitation Is Common--Should It Be?

Although several meta-analyses have indicated that pollen limitation of seed output is widespread and often severe in flowering plants, a theoretical model of Rosenheim et al. published in 2014 predicts otherwise. Their predictions of infrequent pollen limitation were based on estimated ratios between prefertilization and postfertilization costs that are likely to be unrealistically low and on an assumption about variance in ovule fertilization among plants that is likely to be unrealistically narrow. I show that the predictions of the model of Rosenheim et al. are sensitive to these assumptions. In particular, more realistic distributions of pollination variation yield predictions that are in better accord with empirical data. Pervasive pollen limitation therefore remains unsurprising, although the extent of lifetime pollen limitation remains an important frontier for research.

Coevolutionary elaboration of pollination-related traits in an alpine ginger (Roscoea purpurea) and a tabanid fly in the Nepalese Himalayas.

Geographical variation in the interacting traits of plant-pollinator mutualism can lead to local adaptive differentiation. We tested Darwin's hypothesis of reciprocal selection as a key driving force for the evolution of floral traits of an alpine ginger (Roscoea purpurea) and proboscis length of a tabanid fly (Philoliche longirostris). We documented the pattern of trait variation in R. purpurea and P. longirostris across five populations. At each site, we quantified pollinator-mediated selection on floral display area, inflorescence height and corolla length of R. purpurea by comparing selection gradients for flowers exposed to natural pollination and to supplemental hand pollination. Reciprocal selection between plant and fly was examined at two sites via the relationship between proboscis length and nectar consumption (fly benefit) and corolla length and pollen deposition (plant benefit). Local corolla tube length was correlated with local fly proboscis length among the five sites. We found strong linear selection imposed by pollinators on corolla tube length at all sites, but there was no consistent relationship of fitness to inflorescence height or floral display area. Selection between corolla length and proboscis length was reciprocal at the two experimental sites examined. The geographical pattern of trait variation and the evidence of selection is consistent with a mosaic of local, species-specific reciprocal selection acting as the major driving force for the evolution of corolla length of R. purpurea and proboscis length of P. longirostris.

The scope of Baker's law.

Baker's law refers to the tendency for species that establish on islands by long-distance dispersal to show an increased capacity for self-fertilization because of the advantage of self-compatibility when colonizing new habitat. Despite its intuitive appeal and broad empirical support, it has received substantial criticism over the years since it was proclaimed in the 1950s, not least because it seemed to be contradicted by the high frequency of dioecy on islands. Recent theoretical work has again questioned the generality and scope of Baker's law. Here, we attempt to discern where the idea is useful to apply and where it is not. We conclude that several of the perceived problems with Baker's law fall away when a narrower perspective is adopted on how it should be circumscribed. We emphasize that Baker's law should be read in terms of an enrichment of a capacity for uniparental reproduction in colonizing situations, rather than of high selfing rates. We suggest that Baker's law might be tested in four different contexts, which set the breadth of its scope: the colonization of oceanic islands, metapopulation dynamics with recurrent colonization, range expansions with recurrent colonization, and colonization through species invasions.

Multitasking in a plant-ant interaction: how does Acacia myrtifolia manage both ants and pollinators?

Plant associations with protective ants are widespread among angiosperms, but carry the risk that ants will deter pollinators as well as herbivores. Such conflict, and adaptations to ameliorate or prevent the conflict, have been documented in African and neotropical acacias. Ant-acacia associations occur in Australia, but little is known of their ecology. Moreover, recent phylogenetic evidence indicates that Australian acacias are only distantly related to African and American acacias, providing an intercontinental natural experiment in the management of ant-pollinator conflict. We examined four populations of Acacia myrtifolia over a 400-km environmental gradient in southeastern Australia using ant and pollinator exclusion as well as direct observation of ants and pollinators to assess the potential for ant-pollinator conflict to affect seed set. Native bees were the only group of floral visitors whose visitation rates were a significant predictor of fruiting success, although beetles and wasps may play an important role as "insurance" pollinators. We found no increase in pollinator visitation or fruiting success following ant exclusion, even with large sample sizes and effective exclusion. Because ants are facultative visitors to A. myrtifolia plants, their presence may be insufficient to interfere greatly with floral visitors. It is also likely that the morphological location of extrafloral nectaries tends to draw ants away from reproductive parts, although we commonly observed ants on inflorescences, so the spatial separation is not strict. A. myrtifolia appears to maintain a generalized mutualism over a wide geographic range without the need for elaborate adaptations to resolve ant-pollinator conflict.

Distinctive convergence in Australian floral colours seen through the eyes of Australian birds.

We used a colour-space model of avian vision to assess whether a distinctive bird pollination syndrome exists for floral colour among Australian angiosperms. We also used a novel phylogenetically based method to assess whether such a syndrome represents a significant degree of convergent evolution. About half of the 80 species in our sample that attract nectarivorous birds had floral colours in a small, isolated region of colour space characterized by an emphasis on long-wavelength reflection. The distinctiveness of this 'red arm' region was much greater when colours were modelled for violet-sensitive (VS) avian vision than for the ultraviolet-sensitive visual system. Honeyeaters (Meliphagidae) are the dominant avian nectarivores in Australia and have VS vision. Ancestral state reconstructions suggest that 31 lineages evolved into the red arm region, whereas simulations indicate that an average of five or six lineages and a maximum of 22 are likely to have entered in the absence of selection. Thus, significant evolutionary convergence on a distinctive floral colour syndrome for bird pollination has occurred in Australia, although only a subset of bird-pollinated taxa belongs to this syndrome. The visual system of honeyeaters has been the apparent driver of this convergence.

Shades of red: bird-pollinated flowers target the specific colour discrimination abilities of avian vision.

Colour signals are a major cue in putative pollination syndromes. There is evidence that the reflectance spectra of many flowers target the distinctive visual discrimination abilities of hymenopteran insects, but far less is known about bird-pollinated flowers. Birds are hypothesized to exert different selective pressures on floral colour compared with hymenopterans because of differences in their visual systems. We measured the floral reflectance spectra of 206 Australian angiosperm species whose floral visitors are known from direct observation rather than inferred from floral characteristics. We quantified the match between these spectra and the hue discrimination abilities of hymenopteran and avian vision, and analysed these metrics in a phylogenetically informed comparison of flowers in different pollination groups. We show that bird-visited flowers and insect-visited flowers differ significantly from each other in the chromatic cues they provide, and that the differences are concentrated near wavelengths of optimal colour discrimination by whichever class of pollinator visits the flowers. Our results indicate that angiosperms have evolved the spectral signals most likely to reinforce their pollinators' floral constancy (the tendency of individual pollinators to visit flowers of the same species) in communities of similarly coloured floral competitors.