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      Florivory of Early Cretaceous flowers by functionally diverse insects: implications for early angiosperm pollination

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          Abstract

          Florivory (flower consumption) occurs worldwide in modern angiosperms, associated with pollen and nectar consumption. However, florivory remains unrecorded from fossil flowers since their Early Cretaceous appearance. We test hypotheses that earliest angiosperms were pollinated by a diverse insect fauna by evaluating 7858 plants from eight localities of the latest Albian Dakota Formation from midcontinental North America, in which 645 specimens (8.2%) were flowers or inflorescences. Well-preserved specimens were categorized into 32 morphotypes, nine of which displayed 207 instances of damage from 11 insect damage types (DTs) by four functional-feeding groups of hole feeding, margin feeding, surface feeding and piercing-and-sucking. We assessed the same DTs inflicted by known florivores on modern flowers that also are their pollinators, and associated insect mouthpart types causing such damage. The diverse, Dakota florivore–pollinator community showed a local pattern at Braun's Ranch of flower morphotypes 4 and 5 having piercing-and-sucking as dominant and margin feeding as minor interactions, whereas Dakotanthus cordiformis at Rose Creek I and II had an opposite pattern. We found no evidence for nectar robbing. These data support the rapid emergence of early angiosperms of florivore and associated pollinator guilds expressed at both the local and regional community levels.

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          A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity.

          The establishment of modern terrestrial life is indissociable from angiosperm evolution. While available molecular clock estimates of angiosperm age range from the Paleozoic to the Late Cretaceous, the fossil record is consistent with angiosperm diversification in the Early Cretaceous. The time-frame of angiosperm evolution is here estimated using a sample representing 87% of families and sequences of five plastid and nuclear markers, implementing penalized likelihood and Bayesian relaxed clocks. A literature-based review of the palaeontological record yielded calibrations for 137 phylogenetic nodes. The angiosperm crown age was bound within a confidence interval calculated with a method that considers the fossil record of the group. An Early Cretaceous crown angiosperm age was estimated with high confidence. Magnoliidae, Monocotyledoneae and Eudicotyledoneae diversified synchronously 135-130 million yr ago (Ma); Pentapetalae is 126-121 Ma; and Rosidae (123-115 Ma) preceded Asteridae (119-110 Ma). Family stem ages are continuously distributed between c. 140 and 20 Ma. This time-frame documents an early phylogenetic proliferation that led to the establishment of major angiosperm lineages, and the origin of over half of extant families, in the Cretaceous. While substantial amounts of angiosperm morphological and functional diversity have deep evolutionary roots, extant species richness was probably acquired later.
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            The origin and early diversification of angiosperms

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              The ancestral flower of angiosperms and its early diversification

              Recent advances in molecular phylogenetics and a series of important palaeobotanical discoveries have revolutionized our understanding of angiosperm diversification. Yet, the origin and early evolution of their most characteristic feature, the flower, remains poorly understood. In particular, the structure of the ancestral flower of all living angiosperms is still uncertain. Here we report model-based reconstructions for ancestral flowers at the deepest nodes in the phylogeny of angiosperms, using the largest data set of floral traits ever assembled. We reconstruct the ancestral angiosperm flower as bisexual and radially symmetric, with more than two whorls of three separate perianth organs each (undifferentiated tepals), more than two whorls of three separate stamens each, and more than five spirally arranged separate carpels. Although uncertainty remains for some of the characters, our reconstruction allows us to propose a new plausible scenario for the early diversification of flowers, leading to new testable hypotheses for future research on angiosperms.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SupervisionRole: ValidationRole: VisualizationRole: Writing-original draftRole: Writing-review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: VisualizationRole: Writing-original draftRole: Writing-review & editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing-original draftRole: Writing-review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing-original draftRole: Writing-review & editing
                Journal
                Proc Biol Sci
                RSPB
                royprsb
                Proceedings of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8452
                1471-2954
                June 30, 2021
                June 16, 2021
                June 16, 2021
                : 288
                : 1953
                : 20210320
                Affiliations
                [ 1 ]College of Life Science and Academy for Multidisciplinary Studies, Capital Normal University, , Beijing, People's Republic of China
                [ 2 ]Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, , Tenth Street and Constitution Avenue, Washington, DC, USA
                [ 3 ]Department of Entomology, University of Maryland, , College Park, MD, USA
                [ 4 ]Department of Geology, Indiana University, , 1001 Tenth Street, Bloomington, IN, USA
                Author notes

                Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.5448682.

                Author information
                http://orcid.org/0000-0002-6940-1473
                http://orcid.org/0000-0002-4838-5099
                http://orcid.org/0000-0001-7226-6703
                http://orcid.org/0000-0001-8660-0901
                Article
                rspb20210320
                10.1098/rspb.2021.0320
                8207559
                2c760c9a-0476-4e80-9e96-6b7648ffd41c
                © 2021 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : Feburary 8, 2021
                : May 20, 2021
                Funding
                Funded by: Project of High-level Teachers in Beijing Municipal Universities in the Period of 13th Five-year Plan, http://dx.doi.org/10.13039/501100012435;
                Award ID: Grant IDHT20180518
                Funded by: National Science Foundation of United States;
                Award ID: DEB 10720
                Award ID: DEB 75-02268
                Award ID: DEB 75-19849
                Award ID: DEB 77-04846
                Award ID: EAR 79-00898
                Funded by: National Natural Science Foundation of China, http://dx.doi.org/10.13039/501100001809;
                Award ID: Grants 31730087
                Award ID: Grants 32020103006
                Categories
                1001
                70
                144
                60
                Palaeobiology
                Research Articles
                Custom metadata
                June 30, 2021

                Life sciences
                florivory,fossil plant damage,functional-feeding group,generalist,nectar robbing,pollination

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