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      Production of Early Diploid Males by European Colonies of the Invasive Hornet Vespa velutina nigrithorax

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          Abstract

          The invasive yellow-legged hornet Vespa velutina nigrithorax was accidentally introduced in Europe in the early 2000s. As is the case in colonies of other wasp and hornet species, V. velutina colonies are known to produce sexuals (males and new queens) at the end of the summer. We show that early-stage colonies in French populations frequently produce males well before the usual reproductive period. The vast majority of the males produced are diploid, which is consistent with the loss of genetic diversity previously reported in introduced populations in France. Since males do not participate in colony activities, the production of early diploid males at the expense of workers is expected to hamper colony growth and, ultimately, decrease the expansion of the species in its invasive range in Europe.

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          Most cited references21

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          The genetics of inbreeding depression.

          Inbreeding depression - the reduced survival and fertility of offspring of related individuals - occurs in wild animal and plant populations as well as in humans, indicating that genetic variation in fitness traits exists in natural populations. Inbreeding depression is important in the evolution of outcrossing mating systems and, because intercrossing inbred strains improves yield (heterosis), which is important in crop breeding, the genetic basis of these effects has been debated since the early twentieth century. Classical genetic studies and modern molecular evolutionary approaches now suggest that inbreeding depression and heterosis are predominantly caused by the presence of recessive deleterious mutations in populations.
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            The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein.

            Haplodiploid organisms comprise about 20% of animals. Males develop from unfertilized eggs while females are derived from fertilized eggs. The underlying mechanisms of sex determination, however, appear to be diverse and are poorly understood. We have dissected the complementary sex determiner (csd) locus in the honeybee to understand its molecular basis. In this species, csd acts as the primary sex-determining signal with several alleles segregating in populations. Males are hemizygous and females are heterozygous at this locus; nonreproducing diploid males occur when the locus is homozygous. We have characterized csd by positional cloning and repression analysis. csd alleles are highly variable and no transcription differences were found between sexes. These results establish csd as a primary signal that governs sexual development by its allelic composition. Structural similarity of csd with tra genes of Dipteran insects suggests some functional relation of what would otherwise appear to be unrelated sex-determination mechanisms.
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              Sex determination in the hymenoptera.

              The dominant and ancestral mode of sex determination in the Hymenoptera is arrhenotokous parthenogenesis, in which diploid females develop from fertilized eggs and haploid males develop from unfertilized eggs. We discuss recent progress in the understanding of the genetic and cytoplasmic mechanisms that make arrhenotoky possible. The best-understood mode of sex determination in the Hymenoptera is complementary sex determination (CSD), in which diploid males are produced under conditions of inbreeding. The gene mediating CSD has recently been cloned in the honey bee and has been named the complementary sex determiner. However, CSD is only known from 4 of 21 hymenopteran superfamilies, with some taxa showing clear evidence of the absence of CSD. Sex determination in the model hymenopteran Nasonia vitripennis does not involve CSD, but it is consistent with a form of genomic imprinting in which activation of the female developmental pathway requires paternally derived genes. Some other hymenopterans are not arrhenotokous but instead exhibit thelytoky or paternal genome elimination.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                28 September 2015
                2015
                : 10
                : 9
                : e0136680
                Affiliations
                [1 ]IRBI, UMR CNRS 7261, University of Tours, Faculty of Sciences, Parc de Grandmont, 37200 Tours, France
                [2 ]Evolution Biologique & Ecologie, Université Libre de Bruxelles, 1050 Brussels, Belgium
                Universidade de São Paulo, Faculdade de Filosofia Ciências e Letras de Ribeirão Preto, BRAZIL
                Author notes

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

                Conceived and designed the experiments: ED. Performed the experiments: ED JG QG SA. Analyzed the data: ED SA. Contributed reagents/materials/analysis tools: ED JG QG SA. Wrote the paper: ED SA. Collection of colonies in the field: ED JG QG.

                Article
                PONE-D-15-15185
                10.1371/journal.pone.0136680
                4586377
                26414951
                8f4a720e-8222-4ff7-96de-ef6aae7b35ee
                Copyright @ 2015

                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
                : 23 April 2015
                : 6 August 2015
                Page count
                Figures: 1, Tables: 1, Pages: 9
                Funding
                This work was funded by the local government (Région Centre, France) (ED) and several grants from Belgium’s National Fund for Scientific Research (SA).
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                Research Article
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                All relevant data are within the paper.

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