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      Fine-tuned Bee-Flower Coevolutionary State Hidden within Multiple Pollination Interactions

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          Abstract

          Relationships between flowers and pollinators are generally considered cases of mutualism since both agents gain benefits. Fine-tuned adaptations are usually found in the form of strict one-to-one coevolution between species. Many insect pollinators are, however, considered generalists, visiting numerous kinds of flowers, and many flower species (angiosperms) are also considered generalists, visited by many insect pollinators. We here describe a fine-tuned coevolutionary state of a flower-visiting bee that collects both nectar and pollen from an early spring flower visited by multiple pollinators. Detailed morphology of the bee proboscis is shown to be finely adjusted to the floral morphology and nectar production of the flower. Behavioral observations also confirm the precision of this mutualism. Our results suggest that a fine-tuned one-to-one coevolutionary state between a flower species and a pollinator species might be common, but frequently overlooked, in multiple flower-pollinator interactions.

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          Pollinator shifts drive increasingly long nectar spurs in columbine flowers.

          Directional evolutionary trends have long garnered interest because they suggest that evolution can be predictable. However, the identification of the trends themselves and the underlying processes that may produce them have often been controversial. In 1862, in explaining the exceptionally long nectar spur of Angraecum sesquipedale, Darwin proposed that a coevolutionary 'race' had driven the directional increase in length of a plant's spur and its pollinator's tongue. Thus he predicted the existence of an exceptionally long-tongued moth. Though the discovery of Xanthopan morgani ssp. praedicta in 1903 with a tongue length of 22 cm validated Darwin's prediction, his 'race' model for the evolution of long-spurred flowers remains contentious. Spurs may also evolve to exceptional lengths by way of pollinator shifts as plants adapt to a series of unrelated pollinators, each with a greater tongue length. Here, using a species-level phylogeny of the columbine genus, Aquilegia, we show a significant evolutionary trend for increasing spur length during directional shifts to pollinators with longer tongues. In addition, we find evidence for 'punctuated' change in spur length during speciation events, suggesting that Aquilegia nectar spurs rapidly evolve to fit adaptive peaks predefined by pollinator morphology. These findings show that evolution may proceed in predictable pathways without reversals and that change may be concentrated during speciation.
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            An Extreme Case of Plant–Insect Codiversification: Figs and Fig-Pollinating Wasps

            It is thought that speciation in phytophagous insects is often due to colonization of novel host plants, because radiations of plant and insect lineages are typically asynchronous. Recent phylogenetic comparisons have supported this model of diversification for both insect herbivores and specialized pollinators. An exceptional case where contemporaneous plant–insect diversification might be expected is the obligate mutualism between fig trees (Ficus species, Moraceae) and their pollinating wasps (Agaonidae, Hymenoptera). The ubiquity and ecological significance of this mutualism in tropical and subtropical ecosystems has long intrigued biologists, but the systematic challenge posed by >750 interacting species pairs has hindered progress toward understanding its evolutionary history. In particular, taxon sampling and analytical tools have been insufficient for large-scale cophylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on an average, wasps had sequences from 77% of 6 genes (5.6 kb), figs had sequences from 60% of 5 genes (5.5 kb), and overall 850 new DNA sequences were generated for this study. We also developed a new analytical tool, Jane 2, for event-based phylogenetic reconciliation analysis of very large data sets. Separate Bayesian phylogenetic analyses for figs and fig wasps under relaxed molecular clock assumptions indicate Cretaceous diversification of crown groups and contemporaneous divergence for nearly half of all fig and pollinator lineages. Event-based cophylogenetic analyses further support the codiversification hypothesis. Biogeographic analyses indicate that the present-day distribution of fig and pollinator lineages is consistent with a Eurasian origin and subsequent dispersal, rather than with Gondwanan vicariance. Overall, our findings indicate that the fig-pollinator mutualism represents an extreme case among plant–insect interactions of coordinated dispersal and long-term codiversification. [Biogeography; coevolution; cospeciation; host switching; long-branch attraction; phylogeny.]
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              The geographical mosaic of coevolution in a plant-pollinator mutualism.

              Although coevolution is widely accepted as a concept, its importance as a driving factor in biological diversification is still being debated. Because coevolution operates mainly at the population level, reciprocal coadaptations should result in trait covariation among populations of strongly interacting species. A long-tongued fly (Prosoeca ganglbaueri) and its primary floral food plant (Zaluzianskya microsiphon) were studied across both of their geographical ranges. The dimensions of the fly's proboscis and the flower's corolla tube length varied significantly among sites and were strongly correlated with each other. In addition, the match between tube length of flowers and tongue length of flies was found to affect plant fitness. The relationship between flower tube length and fly proboscis length remained significant in models that included various alternative environmental (altitude, longitude, latitude) and allometric (fly body size, flower diameter) predictor variables. We conclude that coevolution is a compelling explanation for the geographical covariation in flower depth and fly proboscis length.
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                Author and article information

                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group
                2045-2322
                05 February 2014
                2014
                : 4
                : 3988
                Affiliations
                [1 ]Department of Biological Sciences, Graduate School of Science and Engineering, Tokyo Metropolitan University , Hachioji, Tokyo, 192-0397 Japan
                [2 ]Department of Environmental Sciences, Tokyo Gakugei University , Tokyo, 184-8501 Japan
                [3 ]Department of Biology, University of California , Riverside, CA, 92521 USA
                [4 ]Department of Biological Sciences and Center for Water and the Environment, California State University , Chico, CA, 95929 USA
                [5 ]Department of Zoology, Graduate School of Science, Kyoto University , Kyoto, 606-8502 Japan
                [6 ]Graduate School of Arts and Sciences, University of Tokyo , Japan
                [7 ]Department of Mathematical and Systems Engineering, Shizuoka University , Hamamatsu, 432-8561 Japan
                [8 ]Department of Environmental and Forest Biology, State University of New York College of Environmental Science and Forestry , Syracuse, New York, 13210 USA
                [9 ]Marine Biosystems Research Center, Chiba University , 1 Uchiura, Kamogawa, Chiba-ken, 299-5502 Japan
                Author notes
                Article
                srep03988
                10.1038/srep03988
                3913927
                7e2647eb-59bd-4d38-aff6-988066e37613
                Copyright © 2014, Macmillan Publishers Limited. All rights reserved

                This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/

                History
                : 23 July 2013
                : 20 January 2014
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