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      Possible Epigenetic Origin of a Recurrent Gynandromorph Pattern in Megachile Wild Bees

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          Abstract

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          Gynandromorphs, i.e., individuals with a mix of male and female body parts, are known for many species of insects and other animals with separate sexes. This anomaly is generally regarded as the result of localized genetic mutations in sex-determining genes. We analyzed the specific mix of male and female characters in naturally occurring gynandromorphs of 21 species of the wild bee genus Megachile and found a recurrent pattern. Based on the regularity of this pattern, and the current knowledge on sex determination and sex differentiation in the relatively closely-related honey bee, we argue that the origin of these composite phenotypes is possibly epigenetic, rather than genetic, i.e., produced by some defects in the maintenance of the regulatory signals that control sex differentiation at the level of single cell lineages, rather than triggered by genetic mutations.

          Abstract

          Gynandromorphs, i.e., individuals with a mix of male and female traits, are common in the wild bees of the genus Megachile (Hymenoptera, Apoidea). We described new transverse gynandromorphs in Megachile pilidens Alfkeen, 1924 and analyze the spatial distribution of body parts with male vs. female phenotype hitherto recorded in the transverse gynandromorphs of the genus Megachile. We identified 10 different arrangements, nine of which are minor variants of a very general pattern, with a combination of male and female traits largely shared by the gynandromorphs recorded in 20 out of 21 Megachile species in our dataset. Based on the recurrence of the same gynandromorph pattern, the current knowledge on sex determination and sex differentiation in the honey bee, and the results of recent gene-knockdown experiments in these insects, we suggest that these composite phenotypes are possibly epigenetic, rather than genetic, mosaics, with individual body parts of either male or female phenotype according to the locally expressed product of the alternative splicing of sex-determining gene transcripts.

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          Most cited references67

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          The Bees of the World

          In this extensive update of his definitive reference, Charles D. Michener reveals a diverse fauna that numbers more than 17,000 species and ranges from the common honeybee to rare bees that feed on the pollen of a single type of plant. With many new facts, reclassifications, and revisions, the second edition of The Bees of the World provides the most comprehensive treatment of the 1,200 genera and subgenera of the Apiformes. Included are hundreds of updated citations to work published since the appearance of the first edition and a new set of plates of fossil bees. The book begins with extensive introductory sections that include bee evolution, classification of the various bee families, the coevolution of bees and flowering plants, nesting behavior, differences between solitary and social bees, and the anatomy of these amazing insects. Drawing on modern studies and evidence from the fossil record, Michener reveals what the ancestral bee—the protobee—might have looked like. He also cites the major literature on bee biology and describes the need for further research on the systematics and natural history of bees, including their importance as pollinators of crops and natural vegetation. The greater part of the work consists of an unprecedented treatment of bee systematics, with keys for identification to the subgenus level. For each genus and subgenus, Michener includes a brief natural history describing geographical range, number of species, and noteworthy information pertaining to nesting or floral biology. The book is beautifully illustrated with more than 500 drawings and photographs that depict behavior, detailed morphology, and ecology. Accented with color plates of select bees, The Bees of the World will continue to be the world's best reference on these diverse insects.
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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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              Vive la différence: males vs females in flies vs worms.

              For 600 million years, the two best-understood metazoan species, the nematode Caenorhabditis elegans and fruit fly Drosophila melanogaster, have developed independent strategies for solving a biological problem faced by essentially all metazoans: how to generate two sexes in the proper proportions. The genetic program for sexual dimorphism has been a major focus of research in these two organisms almost from the moment they were chosen for study, and it may now be the best-understood general aspect of their development. In this review, we compare and contrast the strategies used for sex determination (including dosage compensation) between "the fly" and "the worm" and the way this understanding has come about. Although no overlap has been found among the molecules used by flies and worms to achieve sex determination, striking similarities have been found in the genetic strategies used by these two species to differentiate their sexes.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                Insects
                Insects
                insects
                Insects
                MDPI
                2075-4450
                12 May 2021
                May 2021
                : 12
                : 5
                : 437
                Affiliations
                [1 ]Dipartimento di Scienze e Tecnologie Agro-Alimentari (DISTAL), Alma Mater Studiorum-Università di Bologna, Viale G. Fanin 42, 40127 Bologna, BO, Italy; daniele.sommaggio@ 123456unipd.it
                [2 ]Department of Biology, University of Padova, Via U. Bassi 58/B, 35131 Padova, PD, Italy; alessandro.minelli@ 123456unipd.it
                [3 ]Via Cavaizza 16/B, 35020 Codevigo, PD, Italy; marco.uliana.1@ 123456gmail.com
                Author notes
                Author information
                https://orcid.org/0000-0002-4690-6049
                https://orcid.org/0000-0001-7180-6659
                https://orcid.org/0000-0003-3387-1489
                Article
                insects-12-00437
                10.3390/insects12050437
                8151954
                34066094
                098be634-c763-44b2-a41e-bac98b32141f
                © 2021 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( https://creativecommons.org/licenses/by/4.0/).

                History
                : 08 April 2021
                : 08 May 2021
                Categories
                Article

                hymenoptera,sex determination,sex differentiation,genetic mosaic,epigenetic sex mosaic,alternative splicing,developmental stability,modularity

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