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      Untangling the Hypogeococcus pungens species complex (Hemiptera: Pseudococcidae) for Argentina, Australia, and Puerto Rico based on host plant associations and genetic evidence

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          Abstract

          Hypogeococcus pungens, a mealybug native of southern South America, is devastating native cacti in Puerto Rico and threatening cactus diversity in the Caribbean, and potentially in Central and North America. The taxonomic status of H. pungens is controversial since it has been reported feeding not only on Cactaceae but also on other plant families throughout its distribution range. However, in Australia, where the species had been exported from Argentina to control weedy American cacti, it was never found on host plants other than Cactaceae. These conflicting pieces of evidence not only cast doubt on the species identity that invaded Puerto Rico, but also have a negative impact on the search for natural enemies to be used in biological control programs against this pest. Here we present reproductive incompatibility and phylogenetic evidences that give support to the hypothesis that H. pungens is a species complex in which divergence appears to be driven by the host plants. The nuclear EF1α and 18S and the mitochondrial COI genes were used as markers to evaluate the phylogenetic relationships among H. pungens populations collected in Argentina, Australia and Puerto Rico feeding on Cactaceae and/or Amaranthaceae. Additionally, we conducted reciprocal crosses between mealybugs from both hosts. Species delimitation analysis revealed two well-supported putative species within H. pungens, one including mealybugs feeding on Amaranthaceae ( H. pungens sensu stricto), and a new undescribed species using Cactaceae as hosts. Additionally, we found asymmetric reproductive incompatibility between these putative species suggesting recent reproductive isolation. The Bayesian species delimitation also suggested that the Australian mealybug population may derive from another undescribed species. Overall, the patterns of genetic differentiation may be interpreted as the result of recent speciation events prompted by host plant shifts. Finally, the finding of a single haplotype in the Puerto Rico population suggests only one invasive event. We still need to identify the geographical origin of the pest in order to enable the use of biological control to reduce the threat to cacti diversity in the Caribbean.

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          Most cited references 43

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          Revisiting the insect mitochondrial molecular clock: the mid-Aegean trench calibration.

          Phylogenetic trees in insects are frequently dated by applying a "standard" mitochondrial DNA (mtDNA) clock estimated at 2.3% My(-1), but despite its wide use reliable calibration points have been lacking. Here, we used a well-established biogeographic barrier, the mid-Aegean trench separating the western and eastern Aegean archipelago, to estimate substitution rates in tenebrionid beetles. Cytochrome oxidase I (cox1) for six codistributed genera across 28 islands (444 individuals) on both sides of the mid-Aegean trench revealed 60 independently coalescing entities delimited with a mixed Yule-coalescent model. One representative per entity was used for phylogenetic analysis of mitochondrial (cox1, 16S rRNA) and nuclear (Mp20, 28S rRNA) genes. Six nodes marked geographically congruent east-west splits whose separation was largely contemporaneous and likely to reflect the formation of the mid-Aegean trench at 9-12 Mya. Based on these "known" dates, a divergence rate of 3.54% My(-1) for the cox1 gene (2.69% when combined with the 16S rRNA gene) was obtained under the preferred partitioning scheme and substitution model selected using Bayes factors. An extensive survey suggests that discrepancies in mtDNA substitution rates in the entomological literature can be attributed to the use of different substitution models, the use of different mitochondrial gene regions, mixing of intraspecific with interspecific data, and not accounting for variance in coalescent times or postseparation gene flow. Different treatments of these factors in the literature confound estimates of mtDNA substitution rates in opposing directions and obscure lineage-specific differences in rates when comparing data from various sources.
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            An index of substitution saturation and its application.

            We introduce a new index to measure substitution saturation in a set of aligned nucleotide sequences. The index is based on the notion of entropy in information theory. We derive the critical values of the index based on computer simulation with different sequence lengths, different number of OTUs and different topologies. The critical value enables researchers to quickly judge whether a set of aligned sequences is useful in phylogenetics. We illustrate the index by applying it to an analysis of the aligned sequences of the elongation factor-1alpha gene originally used to resolve the deep phylogeny of major arthropod groups. The method has been implemented in DAMBE.
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              Host races in plant-feeding insects and their importance in sympatric speciation.

               James Mallet,  M Dres (2002)
              The existence of a continuous array of sympatric biotypes - from polymorphisms, through ecological or host races with increasing reproductive isolation, to good species - can provide strong evidence for a continuous route to sympatric speciation via natural selection. Host races in plant-feeding insects, in particular, have often been used as evidence for the probability of sympatric speciation. Here, we provide verifiable criteria to distinguish host races from other biotypes: in brief, host races are genetically differentiated, sympatric populations of parasites that use different hosts and between which there is appreciable gene flow. We recognize host races as kinds of species that regularly exchange genes with other species at a rate of more than ca. 1% per generation, rather than as fundamentally distinct taxa. Host races provide a convenient, although admittedly somewhat arbitrary intermediate stage along the speciation continuum. They are a heuristic device to aid in evaluating the probability of speciation by natural selection, particularly in sympatry. Speciation is thereby envisaged as having two phases: (i) the evolution of host races from within polymorphic, panmictic populations; and (ii) further reduction of gene flow between host races until the diverging populations can become generally accepted as species. We apply this criterion to 21 putative host race systems. Of these, only three are unambiguously classified as host races, but a further eight are strong candidates that merely lack accurate information on rates of hybridization or gene flow. Thus, over one-half of the cases that we review are probably or certainly host races, under our definition. Our review of the data favours the idea of sympatric speciation via host shift for three major reasons: (i) the evolution of assortative mating as a pleiotropic by-product of adaptation to a new host seems likely, even in cases where mating occurs away from the host; (ii) stable genetic differences in half of the cases attest to the power of natural selection to maintain multilocus polymorphisms with substantial linkage disequilibrium, in spite of probable gene flow; and (iii) this linkage disequilibrium should permit additional host adaptation, leading to further reproductive isolation via pleiotropy, and also provides conditions suitable for adaptive evolution of mate choice (reinforcement) to cause still further reductions in gene flow. Current data are too sparse to rule out a cryptic discontinuity in the apparently stable sympatric route from host-associated polymorphism to host-associated species, but such a hiatus seems unlikely on present evidence. Finally, we discuss applications of an understanding of host races in conservation and in managing adaptation by pests to control strategies, including those involving biological control or transgenic parasite-resistant plants.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: Visualization
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: InvestigationRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: VisualizationRole: 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
                25 July 2019
                2019
                : 14
                : 7
                Affiliations
                [1 ] Fundación para el Estudio de Especies Invasivas (FuEDEI), Hurlingham, Buenos Aires, Argentina
                [2 ] Instituto de Ecología Genética y Evolución de Buenos Aires (IEGEBA), Departamento de Ecología Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
                [3 ] Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Ciudad Autónoma de Buenos Aires, Argentina
                [4 ] Grupo de investigación en Evolución, Ecología y Conservación (EECO), Universidad del Quindío, Armenia, Colombia
                [5 ] U.S. Department of Agriculture-ARS, Tallahassee, Florida, United States of America
                [6 ] Department of Entomology, University of California, Riverside, California, United States of America
                [7 ] Caribbean Advisor to the APHIS Administrator, USDA, San Juan, Puerto Rico
                National Cheng Kung University, TAIWAN
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                [¤]

                Current address: Instituto de Biología Agrícola de Mendoza (IBAM), Mendoza, Argentina.

                Article
                PONE-D-19-10795
                10.1371/journal.pone.0220366
                6657911
                31344099

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                Page count
                Figures: 2, Tables: 2, Pages: 17
                Product
                Funding
                Funded by: USDA-APHIS Invasive Species Coordination Program
                Award ID: APH-HQ-16-0181
                Award Recipient :
                Funded by: USDA-APHIS Farm Bill
                Award ID: Farm Bill FY 17: 6.0385.01
                Award Recipient :
                This study was supported by the USDA-APHIS Invasive Species Coordination Program from 2014 to 2016 (APH-HQ-16-0181), and USDA-APHIS Farm Bill funding for fiscal year 2017 (Farm Bill FY 17: 6.0385.01). 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
                Evolutionary Biology
                Evolutionary Processes
                Speciation
                Species Delimitation
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Biology and Life Sciences
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Computer and Information Sciences
                Data Management
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                People and places
                Geographical locations
                North America
                Caribbean
                Puerto Rico
                Biology and Life Sciences
                Agriculture
                Pest Control
                People and places
                Geographical locations
                South America
                Argentina
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                People and Places
                Geographical Locations
                Oceania
                Australia
                Ecology and Environmental Sciences
                Species Colonization
                Invasive Species
                Custom metadata
                All sequences were deposited in GenBank under accession numbers MN013440 - MN013743.

                Uncategorized

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