Forbidden links, trait matching and modularity in plant-hummingbird networks: Are specialized modules characterized by higher phenotypic floral integration?

BACKGROUND: Plant-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. METHODS: We 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. RESULTS: Both 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. CONCLUSIONS: Our 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.

Variation in floral morphology and plant reproductive success in four Ipomoea species (Convolvulaceae) with contrasting breeding systems.

This study tested the hypothesis that self-compatibility would be associated with floral traits that facilitate autonomous self-pollination to ensure reproduction under low pollinator visitation. In a comparison of two pairs of Ipomoea species with contrasting breeding systems, we predicted that self-compatible (SC) species would have smaller, less variable flowers, reduced herkogamy, lower pollinator visitation and higher reproductive success than their self-incompatible (SI) congeners. We studied sympatric species pairs, I. hederacea (SC)- I. mitchellae (SI) and I. purpurea (SC)-I. indica (SI), in Mexico, over two years. We quantified variation in floral traits and nectar production, documented pollinator visitation, and determined natural fruit and seed set. Hand-pollination and bagging experiments were conducted to determine potential for autonomous self-pollination and apomixis. Self-compatible Ipomoea species had smaller flowers and lower nectar production than SI species; however, floral variation and integration did not vary according to breeding system. Bees were primary pollinators of all species, but visitation rates were seven times lower in SC than SI species. SC species had a high capacity for autonomous self-pollination due to reduced herkogamy at the highest anther levels. Self-compatible species had two to six times higher fruit set than SI species. Results generally support the hypothesis that self-compatibility and autonomous self-pollination ensure reproduction under low pollinator visitation. However, high variation in morphological traits of SC Ipomoea species suggests they maintain variation through outcrossing. Furthermore, reduced herkogamy was associated with high potential for autonomous self-pollination, providing a reproductive advantage that possibly underlies transitions to self-compatibility in Ipomoea.

The search for Pleiades in trait constellations: functional integration and phenotypic selection in the complex flowers of Morrenia brachystephana (Apocynaceae).

Pollinator-mediated natural selection on single traits, such as corolla tube or spur length, has been well documented. However, flower phenotypes are usually complex, and selection is expected to act on several traits that functionally interact rather than on a single isolated trait. Despite the fact that selection on complex phenotypes is expectedly widespread, multivariate selection modelling on such phenotypes still remains under-explored in plants. Species of the subfamily Asclepiadoideae (Apocynaceae) provide an opportunity to study such complex flower contrivances integrated by fine-scaled organs from disparate developmental origin. We studied the correlation structure among linear floral traits (i) by testing a priori morphological, functional or developmental hypotheses among traits and (ii) by exploring the organization of flower covariation, considering alternative expectations of modular organization or whole flower integration through conditional dependence analysis (CDA) and integration matrices. The phenotypic selection approach was applied to determine whether floral traits involved in the functioning of the pollination mechanism were affected by natural selection. Floral integration was low, suggesting that flowers are organized in more than just one correlation pleiad; our hypothetical functional correlation matrix was significantly correlated with the empirical matrix, and the CDA revealed three putative modules. Analyses of phenotypic selection showed significant linear and correlational gradients, lending support to expectations of functional interactions between floral traits. Significant correlational selection gradients found involved traits of different floral whorls, providing evidence for the existence of functional integration across developmental domains.