The effects of juvenile hormone on Lasius niger reproduction.
Reproduction has been shown to be costly for survival in a wide diversity of taxa. The resulting trade-off, termed the reproduction-survival trade-off, is thought to be one of the most fundamental forces of life-history evolution. In insects the pleiotropic effect of juvenile hormone (JH), antagonistically regulating reproduction and pathogen resistance, is suggested to underlie this phenomenon. In contrast to the majority of insects, reproductive individuals in many eusocial insects defy this trade-off and live both long and prosper. By remodelling the gonadotropic effects of JH in reproductive regulation, the queens of the long-lived black garden ant Lasius niger (living up to 27 years), have circumvented the reproduction-survival trade off enabling them to maximize both reproduction and pathogen resistance simultaneously. In this study we measure fertility, vitellogenin gene expression and protein levels after experimental manipulation of hormone levels. We use these measurements to investigate the mechanistic basis of endocrinological role remodelling in reproduction and determine how JH suppresses reproduction in this species, rather then stimulating it, like in the majority of insects. We find that JH likely inhibits three key aspects of reproduction both during vitellogenesis and oogenesis, including two previously unknown mechanisms. In addition, we document that juvenile hormone, as in the majority of insects, has retained some stimulatory function in regulating vitellogenin expression. We discuss the evolutionary consequences of this complex regulatory architecture of reproduction in L. niger, which might enable the evolution of similar reproductive phenotypes by alternate regulatory pathways, and the surprising flexibility regulatory role of juvenile hormone in this process.
School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK. Electronic address: t.pamminger@sussex.ac.uk.
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Pamminger
Institut Für Biologie, Molekulare Ökologie, Martin-Luther-Universität Halle-Wittenberg, Halle 06099, Germany.
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Buttstedt
School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK.
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Norman
Institut Für Biochemie, Martin-Luther-Universität Halle Wittenberg, Halle 06099, Germany.
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Schierhorn
School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK.
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Botías
School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK.
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Jones
School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK.
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Basley
School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK.
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Hughes
D000818:Animals; D001000:Ants / Q000235:genetics / Q000502:physiology*; D004305:Dose-Response Relationship, Drug; D005260:Female; D015870:Gene Expression; D007605:Juvenile Hormones / Q000378:metabolism*; D009866:Oogenesis; D010058:Oviposition; D012098:Reproduction; D014818:Vitellogenesis; D014819:Vitellogenins / Q000235:genetics* / Q000378:metabolism
D007605:Juvenile Hormones; D014819:Vitellogenins
Ants; Endocrinology; Gonadotropin; Regulatory architecture; Social insects