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Paternal inheritance in mealybugs (Hemiptera: Coccoidea: Pseudococcidae)

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Abstract

Mealybugs have a haplodiploid reproduction system, with paternal genome elimination (PGE); the males are diploid soon after fertilization, but during embryogenesis, the male paternal set of chromosomes becomes heterochromatic (HC) and therefore inactive. Previous studies have suggested that paternal genes can be passed on from mealybug males to their sons, but not necessarily by any son, to the next generation. We employed crosses between two mealybug species—Planococcus ficus (Signoret) and Planococcus citri (Risso)—and between two populations of P. ficus, which differ in their mode of pheromone attraction, in order to demonstrate paternal inheritance from males to F2 through F1 male hybrids. Two traits were monitored through three generations: mode of male pheromone attraction (pherotype) and sequences of the internal transcribed spacer 2 (ITS2) gene segment (genotype). Our results demonstrate that paternal inheritance in mealybugs can occur from males to their F2 offspring, through F1 males (paternal line). F2 backcrossed hybrid males expressed paternal pherotypes and ITS2 genotypes although their mother originated through a maternal population. Further results revealed other, hitherto unknown, aspects of inheritance in mealybugs, such as that hybridization between the two species caused absence of paternal traits in F2 hybrid females produced by F1 hybrid females. Furthermore, hybridization between the two species raised the question of whether unattracted males have any role in the interactions between P. ficus and P. citri.

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Acknowledgments

The authors wish to thank Dr. Alex Protasov and Miriam Eliyahu for invaluable technical support; Dr. Anat Levi-Zada for her advice and supply of the pheromone solutions; Prof. Uri Lavi-Gefel, Prof. Eva Jablonka, and Dr. Laura Ross, for their guidance concerning inheritance and epigenetic issues; and Dr. Adi Faigenboim for the bioinformatics support. Finally, we wish to greatly thank and acknowledge Prof. Benjamin Normark as he brought to our attention and suggested the hypotheses of the intersexual arm race, which were discussed in the manuscript.

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Authors and Affiliations

  1. Department of Entomology, The Volcani Center, ARO, 50250, Bet Dagan, Israel

    Hofit Kol-Maimon, Zvi Mendel & Murad Ghanim

  2. Department of Entomology, Robert H. Smith Faculty of Agriculture, Food and Environment, Hebrew University of Jerusalem, POB 12, 76100, Rehovot, Israel

    Hofit Kol-Maimon, Zvi Mendel & Murad Ghanim

  3. Departamento de Ciências e Engenharia de Biossistemas/Centro de Estudos Florestais, Instituto Superior de Agronomia, Universidade de Lisboa, 1349-017, Lisboa, Portugal

    José Carlos Franco

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  1. Hofit Kol-Maimon
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  2. Zvi Mendel
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  3. José Carlos Franco
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  4. Murad Ghanim
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Correspondence to Murad Ghanim.

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Communicated by: Sven Thatje

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Kol-Maimon, H., Mendel, Z., Franco, J.C. et al. Paternal inheritance in mealybugs (Hemiptera: Coccoidea: Pseudococcidae). Naturwissenschaften 101, 791–802 (2014). https://doi.org/10.1007/s00114-014-1218-7

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  • DOI: https://doi.org/10.1007/s00114-014-1218-7

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