Dataset Information

Modularity increases rate of floral evolution and adaptive success for functionally specialized pollination systems.

ABSTRACT: Angiosperm flowers have diversified in adaptation to pollinators, but are also shaped by developmental and genetic histories. The relative importance of these factors in structuring floral diversity remains unknown. We assess the effects of development, function and evolutionary history by testing competing hypotheses on floral modularity and shape evolution in Merianieae (Melastomataceae). Merianieae are characterized by different pollinator selection regimes and a developmental constraint: tubular anthers adapted to specialized buzz-pollination. Our analyses of tomography-based 3-dimensional flower models show that pollinators selected for functional modules across developmental units and that patterns of floral modularity changed during pollinator shifts. Further, we show that modularity was crucial for Merianieae to overcome the constraint of their tubular anthers through increased rates of evolution in other flower parts. We conclude that modularity may be key to the adaptive success of functionally specialized pollination systems by making flowers flexible (evolvable) for adaptation to changing selection regimes.

SUBMITTER: Dellinger AS

PROVIDER: S-EPMC6895197 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Modularity increases rate of floral evolution and adaptive success for functionally specialized pollination systems.

Dellinger Agnes S AS Artuso Silvia S Pamperl Susanne S Michelangeli Fabián A FA Penneys Darin S DS Fernández-Fernández Diana M DM Alvear Marcela M Almeda Frank F Scott Armbruster W W Staedler Yannick Y Schönenberger Jürg J

Communications biology 20191205

Angiosperm flowers have diversified in adaptation to pollinators, but are also shaped by developmental and genetic histories. The relative importance of these factors in structuring floral diversity remains unknown. We assess the effects of development, function and evolutionary history by testing competing hypotheses on floral modularity and shape evolution in Merianieae (Melastomataceae). Merianieae are characterized by different pollinator selection regimes and a developmental constraint: tub ...[more]

PMID: 31872071

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Project description:BackgroundAnimals fertilize thousands of angiosperm species whose floral-display sizes can significantly influence pollinator behavior and plant reproductive success. Many studies have measured the interactions among pollinator behavior, floral-display size, and plant reproductive success, but few studies have been able to separate the effects of pollinator behavior and post-pollination processes on angiosperm sexual reproduction. In this study, we utilized the highly self-incompatible pollinium-pollination system of Asclepias syriaca (Common Milkweed) to quantify how insect visitors influenced male reproductive success measured as pollen removal, female reproductive success measured as pollen deposition, and self-pollination rate. We also determined how floral-display size impacts both visitor behavior and self-pollination rate.ResultsFour insect taxonomic orders visited A. syriaca: Coleoptera, Diptera, Hymenoptera, and Lepidoptera. We focused on three groups of visitor taxa within two orders (Hymenoptera and Lepidoptera) with sample sizes large enough for quantitative analysis: Apis mellifera (Western Honey Bee), Bombus spp. (bumble bees) and lepidopterans (butterflies and moths). Qualitatively, lepidopterans had the highest pollinator importance values, but the large variability in the lepidopteran data precluded meaningful interpretation of much of their behavior. The introduced A. mellifera was the most effective and most important diurnal pollinator with regard to both pollen removal and pollen deposition. However, when considering the self-incompatibility of A. syriaca, A. mellifera was not the most important pollinator because of its high self-pollination rate as compared to Bombus spp. Additionally, the rate of self-pollination increased more rapidly with the number of flowers per inflorescence in A. mellifera than in the native Bombus spp.ConclusionsApis mellifera's high rate of self-pollination may have significant negative effects on both male and female reproductive successes in A. syriaca, causing different selection on floral-display size than native pollinators.

Project description:BackgroundPlant-pollinator mutualistic networks show non-random structural properties that promote species coexistence. However, these networks show high variability in the interacting species and their connections. Mismatch between plant and pollinator attributes can prevent interactions, while trait matching can enable exclusive access, promoting pollinators' niche partitioning and, ultimately, modularity. Thus, plants belonging to specialized modules should integrate their floral traits to optimize the pollination function. Herein, we aimed to analyze the biological processes involved in the structuring of plant-hummingbird networks by linking network morphological constraints, specialization, modularity and phenotypic floral integration.MethodsWe investigated the understory plant-hummingbird network of two adjacent habitats in the Lacandona rainforest of Mexico, one characterized by lowland rainforest and the other by savanna-like vegetation. We performed monthly censuses to record plant-hummingbird interactions for 2 years (2018-2020). We also took hummingbird bill measurements and floral and nectar measurements. We summarized the interactions in a bipartite matrix and estimated three network descriptors: connectance, complementary specialization (H2'), and nestedness. We also analyzed the modularity and average phenotypic floral integration index of each module.ResultsBoth habitats showed strong differences in the plant assemblage and network dynamics but were interconnected by the same four hummingbird species, two Hermits and two Emeralds, forming a single network of interaction. The whole network showed low levels of connectance (0.35) and high specialization (H2' = 0.87). Flower morphologies ranged from generalized to specialized, but trait matching was an important network structurer. Modularity was associated with morphological specialization. The Hermits Phaethornis longirostris and P. striigularis each formed a module by themselves, and a third module was formed by the less-specialized Emeralds: Chlorestes candida and Amazilia tzacatl. The floral integration values were higher in specialized modules but not significantly higher than that formed by generalist species.ConclusionsOur findings suggest that biological processes derived from both trait matching and "forbidden" links, or nonmatched morphological attributes, might be important network drivers in tropical plant-hummingbird systems while morphological specialization plays a minor role in the phenotypic floral integration. The broad variety of corolla and bill shapes promoted niche partitioning, resulting in the modular organization of the assemblage according to morphological specialization. However, more research adding larger datasets of both the number of modules and pollination networks for a wider region is needed to conclude whether phenotypic floral integration increases with morphological specialization in plant-hummingbird systems.

Dataset Information

Modularity increases rate of floral evolution and adaptive success for functionally specialized pollination systems.

Publications

Modularity increases rate of floral evolution and adaptive success for functionally specialized pollination systems.

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