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      Genetic Diversity and Wolbachia Infection Patterns in a Globally Distributed Invasive Ant

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          Abstract

          Understanding the phylogeographic history of an invasive species may facilitate reconstructing the history and routes of its invasion. The longhorn crazy ant, Paratrechina longicornis, is a ubiquitous agricultural and household pest throughout much of the tropics and subtropics, but little is known about the history of its spread. Here, we examine worldwide genetic variation in P. longicornis and its associated Wolbachia bacterial symbionts. Analyses of mtDNA sequences of 248 P. longicornis workers (one per colony) from 13 geographic regions reveal two highly diverged mtDNA clades that co-occur in most of the geographic regions. These two mtDNA clades are associated with different Wolbachia infection patterns, but are not congruent with patterns of nDNA (microsatellite) variation. Multilocus sequence typing reveals two distinct Wolbachia strains in P. longicornis, namely, wLonA and wLonF. The evolutionary histories of these two strains differ; wLonA appears to be primarily transmitted maternally, and patterns of mtDNA and nDNA variation and wLonA infection status are consistent with a relatively recent Wolbachia-induced selective sweep. In contrast, the observed patterns of mtDNA variation and wLonF infections suggest frequent horizontal transfer and losses of wLonF infections. The lack of nDNA structure among sampled geographic regions coupled with the finding that numerous mtDNA haplotypes are shared among regions implies that inadvertent long-distance movement through human commerce is common in P. longicornis and has shaped the genetic structure of this invasive ant worldwide.

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          Wolbachia: master manipulators of invertebrate biology.

          Wolbachia are common intracellular bacteria that are found in arthropods and nematodes. These alphaproteobacteria endosymbionts are transmitted vertically through host eggs and alter host biology in diverse ways, including the induction of reproductive manipulations, such as feminization, parthenogenesis, male killing and sperm-egg incompatibility. They can also move horizontally across species boundaries, resulting in a widespread and global distribution in diverse invertebrate hosts. Here, we review the basic biology of Wolbachia, with emphasis on recent advances in our understanding of these fascinating endosymbionts.
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            Environmental and Economic Costs of Nonindigenous Species in the United States

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              Wolbachia as a bacteriocyte-associated nutritional mutualist.

              Many insects are dependent on bacterial symbionts that provide essential nutrients (ex. aphid-Buchnera and tsetse-Wiglesworthia associations), wherein the symbionts are harbored in specific cells called bacteriocytes that constitute a symbiotic organ bacteriome. Facultative and parasitic bacterial symbionts like Wolbachia have been regarded as evolutionarily distinct from such obligate nutritional mutualists. However, we discovered that, in the bedbug Cimex lectularius, Wolbachia resides in a bacteriome and appears to be an obligate nutritional mutualist. Two bacterial symbionts, a Wolbachia strain and an unnamed gamma-proteobacterium, were identified from different strains of the bedbug. The Wolbachia symbiont was detected from all of the insects examined whereas the gamma-proteobacterium was found in a part of them. The Wolbachia symbiont was specifically localized in the bacteriomes and vertically transmitted via the somatic stem cell niche of germalia to oocytes, infecting the incipient symbiotic organ at an early stage of the embryogenesis. Elimination of the Wolbachia symbiont resulted in retarded growth and sterility of the host insect. These deficiencies were rescued by oral supplementation of B vitamins, confirming the essential nutritional role of the symbiont for the host. The estimated genome size of the Wolbachia symbiont was around 1.3 Mb, which was almost equivalent to the genome sizes of parasitic Wolbachia strains of other insects. These results indicate that bacteriocyte-associated nutritional mutualism can evolve from facultative and prevalent microbial associates like Wolbachia, highlighting a previously unknown aspect of the parasitism-mutualism evolutionary continuum.
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                Author and article information

                Contributors
                Journal
                Front Genet
                Front Genet
                Front. Genet.
                Frontiers in Genetics
                Frontiers Media S.A.
                1664-8021
                17 September 2019
                2019
                : 10
                : 838
                Affiliations
                [1] 1Research Institute for Sustainable Humanosphere, Kyoto University , Kyoto, Japan
                [2] 2Wilkes Honors College, Florida Atlantic University , Jupiter, FL, United States
                [3] 3Department of Evolution, Ecology and Behavior and Department of Entomology, University of Illinois Urbana-Champaign , IL, United States
                [4] 4Department of Entomology, University of California , Riverside, CA, United States
                [5] 5Entomology and Plant Pathology, University of Tennessee , Knoxville, TN, United States
                Author notes

                Edited by: Horacio Naveira, University of A Coruña, Spain

                Reviewed by: Hannes Schuler, Free University of Bozen-Bolzano, Italy; Dimitrios N. Avtzis, Hellenic Agricultural, Organization – ELGO, Greece

                *Correspondence: DeWayne Shoemaker, dewayne.shoemaker@ 123456utk.edu ; Chin-Cheng Scotty Yang, ccyang@ 123456rish.kyoto-u.ac.jp

                This article was submitted to Evolutionary and Population Genetics, a section of the journal Frontiers in Genetics

                Article
                10.3389/fgene.2019.00838
                6758599
                31608104
                cd18abd2-22c7-46f8-877d-4d60bee95009
                Copyright © 2019 Tseng, Wetterer, Suarez, Lee, Yoshimura, Shoemaker and Yang

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 27 April 2019
                : 13 August 2019
                Page count
                Figures: 7, Tables: 2, Equations: 0, References: 128, Pages: 15, Words: 7302
                Funding
                Funded by: Ministry of Science and Technology, Taiwan 10.13039/501100004663
                Funded by: Research Institute for Sustainable Humanosphere, Kyoto University 10.13039/501100009405
                Categories
                Genetics
                Original Research

                Genetics
                horizontal transfer,invasive species,phylogeography,selective sweep,wolbachia
                Genetics
                horizontal transfer, invasive species, phylogeography, selective sweep, wolbachia

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