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      Environmental metagenetics unveil novel plant‐pollinator interactions

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          Abstract

          Honey bees are efficient pollinators of flowering plants, aiding in the plant reproductive cycle and acting as vehicles for evolutionary processes. Their role as agents of selection and drivers of gene flow is instrumental to the structure of plant populations, but historically, our understanding of their influence has been limited to predominantly insect‐dispersed flowering species. Recent metagenetic work has provided evidence that honey bees also forage on pollen from anemophilous species, suggesting that their role as vectors for transmission of plant genetic material is not confined to groups designated as entomophilous, and leading us to ask: could honey bees act as dispersal agents for non‐flowering plant taxa? Using an extensive pollen metabarcoding dataset from Canada, we discovered that honey bees may serve as dispersal agents for an array of sporophytes ( Anchistea, Claytosmunda, Dryopteris, Osmunda, Osmundastrum, Equisetum) and bryophytes ( Funaria, Orthotrichum, Sphagnum, Ulota). Our findings also suggest that honey bees may occasionally act as vectors for the dispersal of aquatic phototrophs, specifically Coccomyxa and Protosiphon, species of green algae. Our work has shed light on the broad resource‐access patterns that guide plant‐pollinator interactions and suggests that bees could act as vectors of gene flow, and potentially even agents of selection, across Plantae.

          Abstract

          We used pollen metabarcoding to investigate if honey bees interact with and disperse cells from non‐flowering plants. We discovered that honey bees may serve as dispersal agents for an array of sporophytes ( Anchistea, Claytosmunda, Dryopteris, Osmunda, Osmundastrum, Equisetum) and bryophytes ( Funaria, Orthotrichum, Sphagnum, Ulota). Our findings also suggest that honey bees may occasionally act as vectors for dispersal of aquatic phototrophs, specifically Coccomyxa and Protosiphon, species of green algae. These findings, though preliminary, open up a new field of research.

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          Most cited references58

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          DADA2: High resolution sample inference from Illumina amplicon data

          We present DADA2, a software package that models and corrects Illumina-sequenced amplicon errors. DADA2 infers sample sequences exactly, without coarse-graining into OTUs, and resolves differences of as little as one nucleotide. In several mock communities DADA2 identified more real variants and output fewer spurious sequences than other methods. We applied DADA2 to vaginal samples from a cohort of pregnant women, revealing a diversity of previously undetected Lactobacillus crispatus variants.
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            Importance of pollinators in changing landscapes for world crops.

            The extent of our reliance on animal pollination for world crop production for human food has not previously been evaluated and the previous estimates for countries or continents have seldom used primary data. In this review, we expand the previous estimates using novel primary data from 200 countries and found that fruit, vegetable or seed production from 87 of the leading global food crops is dependent upon animal pollination, while 28 crops do not rely upon animal pollination. However, global production volumes give a contrasting perspective, since 60% of global production comes from crops that do not depend on animal pollination, 35% from crops that depend on pollinators, and 5% are unevaluated. Using all crops traded on the world market and setting aside crops that are solely passively self-pollinated, wind-pollinated or parthenocarpic, we then evaluated the level of dependence on animal-mediated pollination for crops that are directly consumed by humans. We found that pollinators are essential for 13 crops, production is highly pollinator dependent for 30, moderately for 27, slightly for 21, unimportant for 7, and is of unknown significance for the remaining 9. We further evaluated whether local and landscape-wide management for natural pollination services could help to sustain crop diversity and production. Case studies for nine crops on four continents revealed that agricultural intensification jeopardizes wild bee communities and their stabilizing effect on pollination services at the landscape scale.
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              Long-distance dispersal: a framework for hypothesis testing.

              Tests of hypotheses about the biogeographical consequences of long-distance dispersal have long eluded biologists, largely because of the rarity and presumed unpredictability of such events. Here, we examine data for terrestrial (including littoral) organisms in the Pacific to show that knowledge of dispersal by wind, birds and oceanic drift or rafting, coupled with information about the natural environment and biology of the organisms, can be used to generate broad biogeographic predictions. We then examine the predictions in the context of the origin, frequency of arrival and location of establishment of dispersed organisms, as well as subsequent patterns of endemism and diversification on remote islands. The predicted patterns are being increasingly supported by phylogenetic data for both terrestrial and littoral organisms. Copyright © 2011 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                zayed@yorku.ca
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                07 November 2023
                November 2023
                : 13
                : 11 ( doiID: 10.1002/ece3.v13.11 )
                : e10645
                Affiliations
                [ 1 ] Department of Biology York University Toronto Ontario Canada
                [ 2 ] Appalachian Laboratory University of Maryland Center for Environmental Science Frostburg Maryland USA
                [ 3 ] Ontario Beekeepers' Association Tech‐Transfer Program, Orchard Park Office Centre Guelph Ontario Canada
                [ 4 ] Beaverlodge Research Farm, Agriculture and Agri‐Food Canada Beaverlodge Alberta Canada
                [ 5 ] School of Environmental Sciences University of Guelph Guelph Ontario Canada
                [ 6 ] Department of Biochemistry & Molecular Biology and Michael Smith Laboratories Vancouver British Columbia Canada
                Author notes
                [*] [* ] Correspondence

                Amro Zayed, Department of Biology, York University, 4700 Keele St., Toronto, ON M2J1P3, Canada.

                Email: zayed@ 123456yorku.ca

                Author information
                https://orcid.org/0009-0007-4989-2424
                https://orcid.org/0000-0003-3233-4585
                Article
                ECE310645 ECE-2023-08-01333.R1
                10.1002/ece3.10645
                10630067
                37941738
                adf563bd-a0a7-4f2f-b095-1730d32a38ec
                © 2023 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 05 October 2023
                : 04 August 2023
                : 09 October 2023
                Page count
                Figures: 5, Tables: 2, Pages: 8, Words: 5827
                Funding
                Funded by: Genome Canada , doi 10.13039/100008762;
                Funded by: Ontario Genomics Institute , doi 10.13039/501100000092;
                Award ID: OGI‐185
                Funded by: Ontario Research Fund
                Award ID: 16420
                Categories
                Applied Ecology
                Nature Notes
                Nature Notes
                Custom metadata
                2.0
                November 2023
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.3.4 mode:remove_FC converted:07.11.2023

                Evolutionary Biology
                bees,metabarcoding,metagenomics,pollen,pollination
                Evolutionary Biology
                bees, metabarcoding, metagenomics, pollen, pollination

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