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Title: Evolutionary Diversification in Insect Vector–Phytoplasma–Plant Associations
Abstract The association between insect herbivores and vascular plants represents one of the greatest success stories in terrestrial evolution. Specific mechanisms generating diversity in the association remain poorly understood, but it has become increasingly clear that microbes play important roles in mediating plant–insect interactions. Previous research on phytoplasmas (Acholeplasmatales: Acholeplasmataceae), a diverse group of plant-pathogenic bacteria, and their hemipteran insect vectors suggests that this system provides a new model for understanding how interactions among distantly related but ecologically associated groups of organisms can drive evolutionary diversification. Phytoplasma infections affect the phenotypes of both plants and vectors, altering functional traits (e.g., diet breadth) and mediating host shifts which may, in turn, alter genetic and phylogenetic patterns. This review highlights previous research on the functional ecology and phylogenetic components of phytoplasma-plant-vector (PPV) associations relevant to the evolutionary diversification of this system. Although phytoplasmas and their hosts occur in most terrestrial biomes and have evolved together over the past 300+ million years, major gaps in knowledge of PPV associations remain because most prior research on the system focused on strategies for mitigating effects of phytoplasma diseases in agroecosystems. Study of this system within a broader evolutionary context could help elucidate mechanisms by which interactions between insect herbivores, microbes, and plants drive biological diversification and also help predict the emergence of diseases affecting agriculture. Future research should more thoroughly document PPV associations in natural habitats, examine the relative prevalence of cospeciation versus host shifts in this system, and test possible macroevolutionary consequences of host manipulation by phytoplasmas.  more » « less
Award ID(s):
1639601
NSF-PAR ID:
10312163
Author(s) / Creator(s):
;
Editor(s):
Reddy, Gadi V
Date Published:
Journal Name:
Annals of the Entomological Society of America
Volume:
114
Issue:
2
ISSN:
0013-8746
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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  1. Phytoplasmas are phloem-limited plant pathogenic bacteria in the class Mollicutes transmitted by sap-feeding insect vectors of the Order Hemiptera. Vectors still have not yet been identified for about half of the 33 known phytoplasma groups and this has greatly hindered efforts to control the spread of diseases affecting important crops. Extensive gaps of knowledge on actual phytoplasma vectors and on the plant disease epidemiology prevent our understanding of the basic underlying biological mechanisms that facilitate interactions between insects, phytoplasmas and their host plants. This paper presents a complete online database of Hemiptera-Phytoplasma-Plant (HPP) biological interactions worldwide, searchable via an online interface. The raw data are available through Zenodo at https://doi.org/10.5281/zenodo.2532738. The online database search interface was created using the 3I software (Dmitriev 2006) which enhances data usability by providing a customised web interface (http://trivellone.speciesfile.org/) that provides an overview of the recorded biological interactions and ability to discover particular interactions by searching for one or more phytoplasma, insect or plant taxa. The database will facilitate synthesis of all available and relevant data on the observed associations between phytoplasmas and their insect and plant hosts and will provide useful data to generate and test ecological and evolutionary hypotheses. 
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  2. Abstract

    Phytoplasmas (Mollicutes,Acholeplasmataceae), vector‐borne obligate bacterial plant parasites, infect nearly 1,000 plant species and unknown numbers of insects, mainly leafhoppers (Hemiptera, Deltocephalinae), which play a key role in transmission and epidemiology. Although the plant–phytoplasma–insect association has been evolving for >300 million years, nearly all known phytoplasmas have been discovered as a result of the damage inflicted by phytoplasma diseases on crops. Few efforts have been made to study phytoplasmas occurring in noneconomically important plants in natural habitats. In this study, a subsample of leafhopper specimens preserved in a large museum biorepository was analyzed to unveil potential new associations. PCR screening for phytoplasmas performed on 227 phloem‐feeding leafhoppers collected worldwide from natural habitats revealed the presence of 6 different previously unknown phytoplasma strains. This indicates that museum collections of herbivorous insects represent a rich and largely untapped resource for discovery of new plant pathogens, that natural areas worldwide harbor a diverse but largely undiscovered diversity of phytoplasmas and potential insect vectors, and that independent epidemiological cycles occur in such habitats, posing a potential threat of disease spillover into agricultural systems. Larger‐scale future investigations will contribute to a better understanding of phytoplasma genetic diversity, insect host range, and insect‐borne phytoplasma transmission and provide an early warning for the emergence of new phytoplasma diseases across global agroecosystems.

     
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  3. PLEASE CONTACT AUTHORS IF YOU CONTRIBUTE AND WOULD LIKE TO BE LISTED AS A CO-AUTHOR. (this message will be removed some time weeks/months after the first publication)

    Terrestrial Parasite Tracker indexed biotic interactions and review summary.

    The Terrestrial Parasite Tracker (TPT) project began in 2019 and is funded by the National Science foundation to mobilize data from vector and ectoparasite collections to data aggregators (e.g., iDigBio, GBIF) to help build a comprehensive picture of arthropod host-association evolution, distributions, and the ecological interactions of disease vectors which will assist scientists, educators, land managers, and policy makers. Arthropod parasites often are important to human and wildlife health and safety as vectors of pathogens, and it is critical to digitize these specimens so that they, and their biotic interaction data, will be available to help understand and predict the spread of human and wildlife disease.

    This data publication contains versioned TPT associated datasets and related data products that were tracked, reviewed and indexed by Global Biotic Interactions (GloBI) and associated tools. GloBI provides open access to finding species interaction data (e.g., predator-prey, pollinator-plant, pathogen-host, parasite-host) by combining existing open datasets using open source software.

    If you have questions or comments about this publication, please open an issue at https://github.com/ParasiteTracker/tpt-reporting or contact the authors by email.

    Funding:
    The creation of this archive was made possible by the National Science Foundation award "Collaborative Research: Digitization TCN: Digitizing collections to trace parasite-host associations and predict the spread of vector-borne disease," Award numbers DBI:1901932 and DBI:1901926

    References:
    Jorrit H. Poelen, James D. Simons and Chris J. Mungall. (2014). Global Biotic Interactions: An open infrastructure to share and analyze species-interaction datasets. Ecological Informatics. https://doi.org/10.1016/j.ecoinf.2014.08.005.

    GloBI Data Review Report

    Datasets under review:
     - University of Michigan Museum of Zoology Insect Division. Full Database Export 2020-11-20 provided by Erika Tucker and Barry Oconner. accessed via https://github.com/EMTuckerLabUMMZ/ummzi/archive/6731357a377e9c2748fc931faa2ff3dc0ce3ea7a.zip on 2022-06-24T14:02:48.801Z
     - Academy of Natural Sciences Entomology Collection for the Parasite Tracker Project accessed via https://github.com/globalbioticinteractions/ansp-para/archive/5e6592ad09ec89ba7958266ad71ec9d5d21d1a44.zip on 2022-06-24T14:04:22.091Z
     - Bernice Pauahi Bishop Museum, J. Linsley Gressitt Center for Research in Entomology accessed via https://github.com/globalbioticinteractions/bpbm-ent/archive/c085398dddd36f8a1169b9cf57de2a572229341b.zip on 2022-06-24T14:04:37.692Z
     - Texas A&M University, Biodiversity Teaching and Research Collections accessed via https://github.com/globalbioticinteractions/brtc-para/archive/f0a718145b05ed484c4d88947ff712d5f6395446.zip on 2022-06-24T14:06:40.154Z
     - Brigham Young University Arthropod Museum accessed via https://github.com/globalbioticinteractions/byu-byuc/archive/4a609ac6a9a03425e2720b6cdebca6438488f029.zip on 2022-06-24T14:06:51.420Z
     - California Academy of Sciences Entomology accessed via https://github.com/globalbioticinteractions/cas-ent/archive/562aea232ec74ab615f771239451e57b057dc7c0.zip on 2022-06-24T14:07:16.371Z
     - Clemson University Arthropod Collection accessed via https://github.com/globalbioticinteractions/cu-cuac/archive/6cdcbbaa4f7cec8e1eac705be3a999bc5259e00f.zip on 2022-06-24T14:07:40.925Z
     - Denver Museum of Nature and Science (DMNS) Parasite specimens (DMNS:Para) accessed via https://github.com/globalbioticinteractions/dmns-para/archive/a037beb816226eb8196533489ee5f98a6dfda452.zip on 2022-06-24T14:08:00.730Z
     - Field Museum of Natural History IPT accessed via https://github.com/globalbioticinteractions/fmnh/archive/6bfc1b7e46140e93f5561c4e837826204adb3c2f.zip on 2022-06-24T14:18:51.995Z
     - Illinois Natural History Survey Insect Collection accessed via https://github.com/globalbioticinteractions/inhs-insects/archive/38692496f590577074c7cecf8ea37f85d0594ae1.zip on 2022-06-24T14:19:37.563Z
     - UMSP / University of Minnesota / University of Minnesota Insect Collection accessed via https://github.com/globalbioticinteractions/min-umsp/archive/3f1b9d32f947dcb80b9aaab50523e097f0e8776e.zip on 2022-06-24T14:20:27.232Z
     - Milwaukee Public Museum Biological Collections Data Portal accessed via https://github.com/globalbioticinteractions/mpm/archive/9f44e99c49ec5aba3f8592cfced07c38d3223dcd.zip on 2022-06-24T14:20:46.185Z
     - Museum for Southern Biology (MSB) Parasite Collection accessed via https://github.com/globalbioticinteractions/msb-para/archive/178a0b7aa0a8e14b3fe953e770703fe331eadacc.zip on 2022-06-24T15:16:07.223Z
     - The Albert J. Cook Arthropod Research Collection accessed via https://github.com/globalbioticinteractions/msu-msuc/archive/38960906380443bd8108c9e44aeff4590d8d0b50.zip on 2022-06-24T16:09:40.702Z
     - Ohio State University Acarology Laboratory accessed via https://github.com/globalbioticinteractions/osal-ar/archive/876269d66a6a94175dbb6b9a604897f8032b93dd.zip on 2022-06-24T16:10:00.281Z
     - Frost Entomological Museum, Pennsylvania State University accessed via https://github.com/globalbioticinteractions/psuc-ento/archive/30b1f96619a6e9f10da18b42fb93ff22cc4f72e2.zip on 2022-06-24T16:10:07.741Z
     - Purdue Entomological Research Collection accessed via https://github.com/globalbioticinteractions/pu-perc/archive/e0909a7ca0a8df5effccb288ba64b28141e388ba.zip on 2022-06-24T16:10:26.654Z
     - Texas A&M University Insect Collection accessed via https://github.com/globalbioticinteractions/tamuic-ent/archive/f261a8c192021408da67c39626a4aac56e3bac41.zip on 2022-06-24T16:10:58.496Z
     - University of California Santa Barbara Invertebrate Zoology Collection accessed via https://github.com/globalbioticinteractions/ucsb-izc/archive/825678ad02df93f6d4469f9d8b7cc30151b9aa45.zip on 2022-06-24T16:12:29.854Z
     - University of Hawaii Insect Museum accessed via https://github.com/globalbioticinteractions/uhim/archive/53fa790309e48f25685e41ded78ce6a51bafde76.zip on 2022-06-24T16:12:41.408Z
     - University of New Hampshire Collection of Insects and other Arthropods UNHC-UNHC accessed via https://github.com/globalbioticinteractions/unhc/archive/f72575a72edda8a4e6126de79b4681b25593d434.zip on 2022-06-24T16:12:59.500Z
     - Scott L. Gardner and Gabor R. Racz (2021). University of Nebraska State Museum - Parasitology. Harold W. Manter Laboratory of Parasitology. University of Nebraska State Museum. accessed via https://github.com/globalbioticinteractions/unl-nsm/archive/6bcd8aec22e4309b7f4e8be1afe8191d391e73c6.zip on 2022-06-24T16:13:06.914Z
     - Data were obtained from specimens belonging to the United States National Museum of Natural History (USNM), Smithsonian Institution, Washington DC and digitized by the Walter Reed Biosystematics Unit (WRBU). accessed via https://github.com/globalbioticinteractions/usnmentflea/archive/ce5cb1ed2bbc13ee10062b6f75a158fd465ce9bb.zip on 2022-06-24T16:13:38.013Z
     - US National Museum of Natural History Ixodes Records accessed via https://github.com/globalbioticinteractions/usnm-ixodes/archive/c5fcd5f34ce412002783544afb628a33db7f47a6.zip on 2022-06-24T16:13:45.666Z
     - Price Institute of Parasite Research, School of Biological Sciences, University of Utah accessed via https://github.com/globalbioticinteractions/utah-piper/archive/43da8db550b5776c1e3d17803831c696fe9b8285.zip on 2022-06-24T16:13:54.724Z
     - University of Wisconsin Stevens Point, Stephen J. Taft Parasitological Collection accessed via https://github.com/globalbioticinteractions/uwsp-para/archive/f9d0d52cd671731c7f002325e84187979bca4a5b.zip on 2022-06-24T16:14:04.745Z
     - Giraldo-Calderón, G. I., Emrich, S. J., MacCallum, R. M., Maslen, G., Dialynas, E., Topalis, P., … Lawson, D. (2015). VectorBase: an updated bioinformatics resource for invertebrate vectors and other organisms related with human diseases. Nucleic acids research, 43(Database issue), D707–D713. doi:10.1093/nar/gku1117. accessed via https://github.com/globalbioticinteractions/vectorbase/archive/00d6285cd4e9f4edd18cb2778624ab31b34b23b8.zip on 2022-06-24T16:14:11.965Z
     - WIRC / University of Wisconsin Madison WIS-IH / Wisconsin Insect Research Collection accessed via https://github.com/globalbioticinteractions/wis-ih-wirc/archive/34162b86c0ade4b493471543231ae017cc84816e.zip on 2022-06-24T16:14:29.743Z
     - Yale University Peabody Museum Collections Data Portal accessed via https://github.com/globalbioticinteractions/yale-peabody/archive/43be869f17749d71d26fc820c8bd931d6149fe8e.zip on 2022-06-24T16:23:29.289Z

    Generated on:
    2022-06-24

    by:
    GloBI's Elton 0.12.4 
    (see https://github.com/globalbioticinteractions/elton).

    Note that all files ending with .tsv are files formatted 
    as UTF8 encoded tab-separated values files.

    https://www.iana.org/assignments/media-types/text/tab-separated-values


    Included in this review archive are:

    README:
      This file.

    review_summary.tsv:
      Summary across all reviewed collections of total number of distinct review comments.

    review_summary_by_collection.tsv:
      Summary by reviewed collection of total number of distinct review comments.

    indexed_interactions_by_collection.tsv: 
      Summary of number of indexed interaction records by institutionCode and collectionCode.

    review_comments.tsv.gz:
      All review comments by collection.

    indexed_interactions_full.tsv.gz:
      All indexed interactions for all reviewed collections.

    indexed_interactions_simple.tsv.gz:
      All indexed interactions for all reviewed collections selecting only sourceInstitutionCode, sourceCollectionCode, sourceCatalogNumber, sourceTaxonName, interactionTypeName and targetTaxonName.

    datasets_under_review.tsv:
      Details on the datasets under review.

    elton.jar: 
      Program used to update datasets and generate the review reports and associated indexed interactions.

    datasets.zip:
      Source datasets used by elton.jar in process of executing the generate_report.sh script.

    generate_report.sh:
      Program used to generate the report

    generate_report.log:
      Log file generated as part of running the generate_report.sh script
     

     
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  4. Phytoplasmas are obligate transkingdom bacterial parasites that infect a variety of plant species and replicate in phloem-feeding insects in the order Hemiptera, mainly leafhoppers (Cicadellidae). The insect capacity in acquisition, transmission, survival, and host range directly determines the epidemiology of phytoplasmas. However, due to the difficulty of insect sampling and the lack of follow-up transmission trials, the confirmed phytoplasma insect hosts are still limited compared with the identified plant hosts. Recently, quantitative polymerase chain reaction (qPCR)-based quick screening of 227 leafhoppers collected in natural habitats unveiled the presence of previously unknown phytoplasmas in six samples. In the present study, 76 leafhoppers, including the six prescreened positive samples, were further examined to identify and characterize the phytoplasma strains by semi-nested PCR. A total of ten phytoplasma strains were identified in leafhoppers from four countries including South Africa, Kyrgyzstan, Australia, and China. Based on virtual restriction fragment length polymorphism (RFLP) analysis, these ten phytoplasma strains were classified into four distinct ribosomal (16Sr) groups (16SrI, 16SrIII, 16SrXIV, and 16SrXV), representing five new subgroups (16SrI-AO, 16SrXIV-D, 16SrXIV-E, 16SrXIV-F, and 16SrXV-C). The results strongly suggest that the newly identified phytoplasma strains not only represent new genetic subgroup lineages, but also extend previously undiscovered geographical distributions. In addition, ten phytoplasma-harboring leafhoppers belonged to seven known leafhopper species, none of which were previously reported insect vectors of phytoplasmas. The findings from this study provide fresh insight into genetic diversity, geographical distribution, and insect host range of phytoplasmas. Further transmission trials and screening of new potential host plants and weed reservoirs in areas adjacent to collection sites of phytoplasma harboring leafhoppers will contribute to a better understanding of phytoplasma transmission and epidemiology. 
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  5. Abstract

    Plants and their insect herbivores have been a dominant component of the terrestrial ecological landscape for the past 410 million years and feature intricate evolutionary patterns and co‐dependencies. A complex systems perspective allows for both detailed resolution of these evolutionary relationships as well as comparison and synthesis across systems. Using proxy data of insect herbivore damage (denoted by the damage type or DT) preserved on fossil leaves, functional bipartite network representations provide insights into how plant–insect associations depend on geological time, paleogeographical space, and environmental variables such as temperature and precipitation. However, the metrics measured from such networks are prone to sampling bias. Such sensitivity is of special concern for plant–DT association networks in paleontological settings where sampling effort is often severely limited. Here, we explore the sensitivity of functional bipartite network metrics to sampling intensity and identify sampling thresholds above which metrics appear robust to sampling effort. Across a broad range of sampling efforts, we find network metrics to be less affected by sampling bias and/or sample size than richness metrics, which are routinely used in studies of fossil plant–DT interactions. These results provide reassurance that cross‐comparisons of plant–DT networks offer insights into network structure and function and support their widespread use in paleoecology. Moreover, these findings suggest novel opportunities for using plant–DT networks in neontological terrestrial ecology to understand functional aspects of insect herbivory across geological time, environmental perturbations, and geographic space.

     
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