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      When taxonomy and biological control researchers unite: Species delimitation of Eadya parasitoids (Braconidae) and consequences for classical biological control of invasive paropsine pests of Eucalyptus

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          Abstract

          The invasive eucalyptus tortoise beetle, Paropsis charybdis, defoliates plantations of Eucalyptus nitens in New Zealand. Recent efforts to identify host specific biological control agents (parasitoids) from Tasmania, Australia, have focused on the larval parasitoid wasp, Eadya paropsidis (Braconidae), first described in 1978. In Tasmania, Eadya has been reared from Paropsisterna agricola (genus abbreviated Pst.), a smaller paropsine that feeds as a larva on juvenile rather than adult foliage of Eucalyptus nitens. To determine which of the many paropsine beetle hosts native to Tasmania are utilized by E. paropsidis, and to rule out the presence of cryptic species, a molecular phylogenetic approach was combined with host data from rearing experiments from multiple locations across six years. Sampling included 188 wasps and 94 beetles for molecular data alone. Two mitochondrial genes ( COI and Cytb) and one nuclear gene ( 28S) were analyzed to assess the species limits in the parasitoid wasps. The mitochondrial genes were congruent in delimiting four separate phylogenetic species, all supported by morphological examinations of Eadya specimens collected throughout Tasmania. Eadya paropsidis was true to the type description, and was almost exclusively associated with P. tasmanica. A new cryptic species similar to E. paropsidis, Eadya sp. 3, was readily reared from Pst. agricola and P. charybdis from all sites and all years. Eadya sp. 3 represents the best candidate for biological control of P. charybdis and was determined as the species undergoing host range testing in New Zealand for its potential as a biological control agent. Another new species, Eadya sp. 1, was morphologically distinctive and attacked multiple hosts. The most common host was Pst. variicollis, but was also reared from Pst. nobilitata and Pst. selmani. Eadya sp. 1 may have potential for control against Pst. variicollis, a new incursion in New Zealand, and possibly Pst. selmani in Ireland. Our molecular data suggests that Pst. variicollis is in need of taxonomic revision and the geographic source of the beetle in New Zealand may not be Tasmania. Eadya sp. 2 was rarely collected and attacked P. aegrota elliotti and P. charybdis. Most species of Eadya present in Tasmania are not host specific to one beetle species alone, but demonstrate some host plasticity across the genera Paropsisterna and Paropsis. This study is an excellent example of collaborative phylogenetic and biological control research prior to the release of prospective biological control agents, and has important implications for the Eucalyptus industry worldwide.

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          Cryptic species as a window on diversity and conservation.

          The taxonomic challenge posed by cryptic species (two or more distinct species classified as a single species) has been recognized for nearly 300 years, but the advent of relatively inexpensive and rapid DNA sequencing has given biologists a new tool for detecting and differentiating morphologically similar species. Here, we synthesize the literature on cryptic and sibling species and discuss trends in their discovery. However, a lack of systematic studies leaves many questions open, such as whether cryptic species are more common in particular habitats, latitudes or taxonomic groups. The discovery of cryptic species is likely to be non-random with regard to taxon and biome and, hence, could have profound implications for evolutionary theory, biogeography and conservation planning.
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              DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae).

              Insect parasitoids are a major component of global biodiversity and affect the population dynamics of their hosts. However, identification of insect parasitoids is often difficult, and they are suspected to contain many cryptic species. Here, we ask whether the cytochrome c oxidase I DNA barcode could function as a tool for species identification and discovery for the 20 morphospecies of Belvosia parasitoid flies (Diptera: Tachinidae) that have been reared from caterpillars (Lepidoptera) in Area de Conservación Guanacaste (ACG), northwestern Costa Rica. Barcoding not only discriminates among all 17 highly host-specific morphospecies of ACG Belvosia, but it also raises the species count to 32 by revealing that each of the three generalist species are actually arrays of highly host-specific cryptic species. We also identified likely hybridization among Belvosia by using a variable internal transcribed spacer region 1 nuclear rDNA sequence as a genetic covariate in addition to the strategy of overlaying barcode clusters with ecological information. If general, these results will increase estimates of global species richness and imply that tropical conservation and host-parasite interactions may be more complex than expected.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                16 August 2018
                2018
                : 13
                : 8
                : e0201276
                Affiliations
                [1 ] University of Central Florida, Department of Biology, Orlando, FL, United States of Amrica
                [2 ] Aarhus University, Department of Agroecology, Aarhus, Denmark
                [3 ] Tasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS, Australia
                [4 ] Scion, Rotorua, New Zealand
                Nanjing Agricultural University, CHINA
                Author notes

                Competing Interests: Co-funding of this project (to T. Withers) was provided by the New Zealand Ministry for Primary Industries Sustainable Farming Fund, NZ Farm Forestry Association, Southwood Exports Ltd, Oji Fibre Solutions NZ Ltd, the Forest Owners Association, and Ministry for Business Innovation and Employment Strategic Science Investment Funding to Scion. Co-funding of this project (to B. Sharanowski) was provided by National Science Engineering and Research Council (NSERC), Canada Discovery Grant ( http://www.nserc-crsng.gc.ca/Professors-Professeurs/Grants-Subs/DGIGP-PSIGP_eng.asp) and start-up funds from the Department of Biology, College of Sciences, University of Central Florida. The funders had no role in study design, data collection and analysis, interpretation of results, decision to publish, or preparation of the manuscript. This funding does not alter our adherence to PLOS ONE policies on sharing data and materials.

                Author information
                http://orcid.org/0000-0002-8085-5900
                Article
                PONE-D-17-32806
                10.1371/journal.pone.0201276
                6095507
                30114194
                da8680b2-f083-4eec-974f-6fb52e8968bd
                © 2018 Peixoto et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 7 September 2017
                : 12 July 2018
                Page count
                Figures: 5, Tables: 6, Pages: 28
                Funding
                Funded by: New Zealand MPI Sustainable Farming Fund
                Award Recipient :
                Funded by: NZ Farm Forestry Association
                Award Recipient :
                Funded by: Southwood Export Ltd
                Award Recipient :
                Funded by: Natural Sciences Engineering and Research Council (NSERC) Discovery
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100007900, University of Central Florida;
                Award Recipient :
                Co-funding of this project (to T. Withers) was provided by the New Zealand MPI Sustainable Farming Fund, NZ Farm Forestry Association, Southwood Export Ltd, Oji Fibre Solutions, the Forest Owners Association, and Scion MBIE core funding. Co-funding of this project (to B. Sharanowski) was provided by National Science Engineering and Research Council (NSERC), Canada Discovery Grant ( http://www.nserc-crsng.gc.ca/Professors-Professeurs/Grants-Subs/DGIGP-PSIGP_eng.asp) and start-up funds from the Department of Biology, College of Sciences, University of Central Florida. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Beetles
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Speciation
                Cryptic Speciation
                Biology and Life Sciences
                Agriculture
                Pest Control
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Speciation
                Species Delimitation
                Ecology and Environmental Sciences
                Species Colonization
                Invasive Species
                Biology and Life Sciences
                Species Interactions
                Parasitism
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                People and places
                Geographical locations
                Oceania
                New Zealand
                Custom metadata
                Genetic data is submitted to Genbank (under accessions KX989891-KX990220, KY031346-KY031518, MH107809-MH107817 and MH237732-MH237825). Data sets for all gene alignments were deposited in Figshare ( https://figshare.com/): 10.6084/m9.figshare.6149219. All other data is available in Supporting Information.

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                Uncategorized

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