J Integr Plant Biol ›› 2017, Vol. 59 ›› Issue (1): 44-59.DOI: 10.1111/jipb.12507

Special Issue: Plant Signal Transduction

• Molecular Ecology and Evolution • Previous Articles     Next Articles

Sex ratio of mirid populations shifts in response to hostplant co-infestation or altered cytokinin signaling

Nora Adam1,2, Theresa Erler1, Mario Kallenbach1†, Martin Kaltenpoth3‡, Grit Kunert4, Ian T. Baldwin1 and Meredith C. Schuman1,2*   

  1. 1Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany
    2German Centre for Integrative Biodiversity Research (iDiv), 04103 Leipzig, Germany
    3Max Planck Research Group Insect Symbiosis, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany
    4Department of Biochemistry, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany
  • Received:2016-08-13 Accepted:2016-11-08 Published:2016-11-14
  • About author:Current address: Shimadzu Germany Ltd., Technical Office Jena, Tatzendpromenade 2, 07745 Jena, Germany
    Current address: Department for Evolutionary Ecology, Johannes Gutenberg-University Mainz, Johann-Joachim-Becher-Weg 13, 55128 Mainz, Germany
    *Correspondence: E-mail: Meredith C. Schuman (mschuman@ice.mpg.de)

Abstract:

Herbivore species sharing a host plant often compete. In this study, we show that host plant-mediated interaction between two insect herbivores − a generalist and a specialist − results in a sex ratio shift of the specialist's offspring. We studied demographic parameters of the specialist Tupiocoris notatus (Hemiptera: Miridae) when co-infesting the host plant Nicotiana attenuata (Solanaceae) with the generalist leafhopper Empoasca sp. (Hemiptera: Cicadellidae). We show that the usually female-biased sex ratio of T. notatus shifts toward a higher male proportion in the offspring on plants co-infested by Empoasca sp. This sex ratio change did not occur after oviposition, nor is it due differential mortality of female and male nymphs. Based on pyrosequencing and PCR of bacterial 16S rRNA amplicons, we concluded that sex ratio shifts were unlikely to be due to infection with Wolbachia or other known sex ratio-distorting endosymbionts. Finally, we used transgenic lines of N. attenuata to evaluate if the sex ratio shift could be mediated by changes in general or specialized host plant metabolites. We found that the sex ratio shift occurred on plants deficient in two cytokinin receptors (irCHK2/3). Thus, cytokinin-regulated traits can alter the offspring sex ratio of the specialist T. notatus.

The specialist herbivore T. notatus usually has a female-biased sex ratio on N. attenuata plants. When plants are co-infested with the generalist Empoasca sp., the sex ratio of T. notatus progeny becomes more male-biased. Similar affects were observed without Empoasca sp. co-infestation on plants deficient in two cytokinin receptors.

Key words: cytokinin, Empoasca sp. , 17-hydroxygeranyllinalool diterpene glycosides (HGL-DTGs), interspecific competition, jasmonic acid, Nicotiana attenuata, RuBPCase activase

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