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"HARDER, LAWRENCE D."
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The Ecology of Mating and Its Evolutionary Consequences in Seed Plants
Mating in seed plants arises from interactions between plant traits and the environmental and demographic context in which individuals reside. These interactions commonly cause nonrandom mating, including selfing and promiscuous outcrossing within local neighborhoods. Shared features of seed plants, specifically immobility, hermaphroditism, and modularity, shape the essential character of mating mediated by animals, wind, and water. In addition, diverse floral strategies promote cross- and self-mating, depending on environmental circumstances. Extrinsic ecological factors influence all stages of the mating process-pollination, pollen-tube growth, ovule fertilization-as well as seed development, determining offspring quantity and quality. Traditionally, measures of plant mating systems have focused on a single axis of variation, the maternal outcrossing rate. Instead, we argue for an expanded perspective encompassing mating portfolios, which include all offspring to which individuals contribute genetically as maternal or paternal parents. This approach should expose key ecological determinants of mating-system variation and their evolutionary consequences.
Journal Article
Darwin's beautiful contrivances: evolutionary and functional evidence for floral adaptation
Summary 530 I. Introduction 530 II. The process of floral and inflorescence adaptation 532 III. Experimental studies of flowers as adaptations 538 IV. Floral diversification: microevolution writ large? 539 V. Concluding comments 541 Acknowledgements 542 References 542 Although not 'a professed botanist', Charles Darwin made seminal contributions to understanding of floral and inflorescence function while seeking evidence of adaptation by natural selection. This review considers the legacy of Darwin's ideas from three perspectives. First, we examine the process of floral and inflorescence adaptation by surveying studies of phenotypic selection, heritability and selection responses. Despite widespread phenotypic and genetic capacity for natural selection, only one-third of estimates indicate phenotypic selection. Second, we evaluate experimental studies of floral and inflorescence function and find that they usually demonstrate that reproductive traits represent adaptations. Finally, we consider the role of adaptation in floral diversification. Despite different diversification modes (coevolution, divergent use of the same pollen vector, pollinator shifts), evidence of pollination ecotypes and phylogenetic patterns suggests that adaptation commonly contributes to floral diversity. Thus, this review reveals a contrast between the inconsistent occurrence of phenotypic selection and convincing experimental and comparative evidence that floral traits are adaptations. Rather than rejecting Darwin's hypotheses about floral evolution, this contrast suggests that the tempo of creative selection varies, with strong, consistent selection during episodes of diversification, but relatively weak and inconsistent selection during longer, 'normal' periods of relative phenotypic stasis.
Journal Article
Floral adaptation and diversification under pollen limitation
Pollen limitation (PL) of seed production creates unique conditions for reproductive adaptation by angiosperms, in part because, unlike under ovule or resource limitation, floral interactions with pollen vectors can contribute to variation in female success. Although the ecological and conservation consequences of PL have received considerable attention in recent times, its evolutionary implications are poorly appreciated. To identify general influences of PL on reproductive adaptation compared with those under other seed-production limits and their implications for evolution in altered environments, we derive a model that incorporates pollination and post-pollination aspects of PL. Because PL always favours increased ovule fertilization, even when population dynamics are not seed limited, it should pervasively influence selection on reproductive traits. Significantly, under PL the intensity of inbreeding does not determine whether outcrossing or autonomous selfing can evolve, although it can affect which response is most likely. Because the causes of PL are multifaceted in both natural and anthropogenically altered environments, the possible outcrossing solutions are diverse and context dependent, which may contribute to the extensive variety of angiosperm reproductive characteristics. Finally, the increased adaptive options available under PL may be responsible for positive global associations between it and angiosperm diversity.
Journal Article
Global growth and stability of agricultural yield decrease with pollinator dependence
Human welfare depends on the amount and stability of agricultural production, as determined by crop yield and cultivated area. Yield increases asymptotically with the resources provided by farmers' inputs and environmentally sensitive ecosystem services. Declining yield growth with increased inputs prompts conversion of more land to cultivation, but at the risk of eroding ecosystem services. To explore the interdependence of agricultural production and its stability on ecosystem services, we present and test a general graphical model, based on Jensen's inequality, of yield-resource relations and consider implications for land conversion. For the case of animal pollination as a resource influencing crop yield, this model predicts that incomplete and variable pollen delivery reduces yield mean and stability (inverse of variability) more for crops with greater dependence on pollinators. Data collected by the Food and Agriculture Organization of the United Nations during 1961-2008 support these predictions. Specifically, crops with greater pollinator dependence had lower mean and stability in relative yield and yield growth, despite global yield increases for most crops. Lower yield growth was compensated by increased land cultivation to enhance production of pollinator-dependent crops. Area stability also decreased with pollinator dependence, as it correlated positively with yield stability among crops. These results reveal that pollen limitation hinders yield growth of pollinator-dependent crops, decreasing temporal stability of global agricultural production, while promoting compensatory land conversion to agriculture. Although we examined crop pollination, our model applies to other ecosystem services for which the benefits to human welfare decelerate as the maximum is approached.
Journal Article
Diverse mating consequences of the evolutionary breakdown of the sexual polymorphism heterostyly
Reproductive systems of flowering plants are evolutionarily fluid, with mating patterns changing in response to shifts in abiotic conditions, pollination systems, and population characteristics. Changes in mating should be particularly evident in species with sexual polymorphisms that become ecologically destabilized, promoting transitions to alternative reproductive systems. Here, we decompose female mating portfolios (incidence of selfing, outcross mate number, and intermorph mating) in eight populations of Primula oreodoxa, a self-compatible insect-pollinated herb. This species is ancestrally distylous, with populations subdivided into two floral morphs that usually mate with each other (disassortative mating). Stages in the breakdown of polymorphism also occur, including “mixed” populations of distylous and homostylous (self-pollinating) morphs and purely homostylous populations. Population morph ratios vary with elevation in association with differences in pollinator availability, providing an unusual opportunity to investigate changes in mating patterns accompanying transitions in reproductive systems. Unexpectedly, individuals mostly outcrossed randomly, with substantial disassortative mating in at most two distylous populations. As predicted, mixed populations had higher selfing rates than distylous populations, within mixed populations, homostyles selfed almost twice as much as the distylous morphs, and homostylous populations exhibited the highest selfing rates. Populations with homostyles outcrossed with fewer mates and mate number varied negatively with population selfing rates. These differences indicate maintenance of distyly at low elevation, transition to monomorphic selfing at high elevation, and uncertain, possibly variable fates at intermediate elevation. By quantifying the earliest changes in mating that initiate reproductive transitions, our study highlights the key role of mating in promoting evolutionary divergence.
Journal Article
Evolution and Development of Inflorescence Architectures
To understand the constraints on biological diversity, we analyzed how selection and development interact to control the evolution of inflorescences, the branching structures that bear flowers. We show that a single developmental model accounts for the restricted range of inflorescence types observed in nature and that this model is supported by molecular genetic studies. The model predicts associations between inflorescence architecture, climate, and life history, which we validated empirically. Paths, or evolutionary wormholes, link different architectures in a multidimensional fitness space, but the rate of evolution along these paths is constrained by genetic and environmental factors, which explains why some evolutionary transitions are rare between closely related plant taxa.
Journal Article
Non-equilibrium dynamics and floral trait interactions shape extant angiosperm diversity
Why are some traits and trait combinations exceptionally common across the tree of life, whereas others are vanishingly rare? The distribution of trait diversity across a clade at any time depends on the ancestral state of the clade, the rate at which new phenotypes evolve, the differences in speciation and extinction rates across lineages, and whether an equilibrium has been reached. Here we examine the role of transition rates, differential diversification (speciation minus extinction) and non-equilibrium dynamics on the evolutionary history of angiosperms, a clade well known for the abundance of some trait combinations and the rarity of others. Our analysis reveals that three character states (corolla present, bilateral symmetry, reduced stamen number) act synergistically as a key innovation, doubling diversification rates for lineages in which this combination occurs. However, this combination is currently less common than predicted at equilibrium because the individual characters evolve infrequently. Simulations suggest that angiosperms will remain far from the equilibrium frequencies of character states well into the future. Such non-equilibrium dynamics may be common when major innovations evolve rarely, allowing lineages with ancestral forms to persist, and even outnumber those with diversification-enhancing states, for tens of millions of years.
Journal Article
Function and evolution of aggregated pollen in angiosperms
The evolution of different forms of pollen aggregation (tetrads, polyads, pollen threads, pollinia) from individual monads is a recurring transition in angiosperm history, having occurred independently at least 39 times. Aggregation should evolve only under special circumstances, because diminishing returns associated with pollen removal and receipt instead favor monads that act largely independently. All forms of aggregation result in sibling pollen grains acting together, but they seem to evolve to ease different limitations on siring success: tetrads may evolve most commonly when pollinators visit infrequently, pollen threads may be most beneficial when ovules become available synchronously, and pollinia greatly increase the probability that a pollen grain removed by a pollinator reaches a conspecific stigma. Once pollen aggregation evolves, its implications for gametophytic competition and the relatedness of seeds within fruits probably influence further reproductive evolution, especially the frequency with which pollen from a single donor sires all seeds in a fruit. This latter effect, rather than improvements in pollination efficiency, probably accounts for the common association of pollen aggregation with low pollen:ovule ratios. The ability of orchid pollinia to reduce diminishing returns during pollination may explain both the floral diversity and the widespread occurrence of deceit pollination in this clade.
Journal Article
Mammal pollinators lured by the scent of a parasitic plant
To communicate with animals, plants use signals that are distinct from their surroundings. Animals generally learn to use these signals through associative conditioning; however, signals are most effective when they elicit innate behavioural responses. Many plant species have flowers specialized for pollination by ground-dwelling mammals, but the signals used to attract these pollinators have not been elucidated. Here, we demonstrate the chemical basis for attraction of mammal pollinators to flowers of the dioecious parasitic plant Cytinus visseri (Cytinaceae). Two aliphatic ketones dominate the scent of this species; 3-hexanone, which elicits strong innate attraction in rodents, and 1-hexen-3-one, which repels them in isolation, but not in combination with 3-hexanone. The aliphatic ketone-dominated scent of C. visseri contrasts with those of insect-pollinated plants, which are typically dominated by terpenoids, aromatic or non-ketone aliphatic compounds. 3-hexanone is also known from some bat-pollinated species, suggesting independent evolution of plant signals in derived, highly specialized mammal-pollination systems.
Journal Article