Pleiotropic effects of juvenile hormone in ant queens and the escape from the reproduction-immunocompetence trade-off

Abstract

The ubiquitous trade-off between survival and costly reproduction is one of the most fundamental constraints governing life-history evolution. In numerous animals, gonadotropic hormones antagonistically suppressing immunocompetence cause this trade-off. The queens of many social insects defy the reproduction-survival trade-off, achieving both an extraordinarily long life and high reproductive output, but how they achieve this is unknown. Here we show experimentally, by integrating quantification of gene expression, physiology and behaviour, that the long-lived queens of the ant Lasius niger have escaped the reproduction-immunocompetence trade-off by decoupling the effects of a key endocrine regulator of fertility and immunocompetence in solitary insects, juvenile hormone (JH). This modification of the regulatory architecture enables queens to sustain a high reproductive output without elevated JH titres and suppressed immunocompetence, providing an escape from the reproduction-immunocompetence trade-off that may contribute to the extraordinary lifespan of many social insect queens.

Keywords: Lasius niger; immunology; juvenile hormone; life history; social insects; trade-off.

Figure 1.

The mean ± s.e. effects of juvenile hormone on behavioural and reproductive traits of Lasius niger ant queens. (a) The number of eggs laid by queens in the different treatment groups during the two weeks of the experiment. (b) The proportion of eggs containing yolk (vitellogenic) versus eggs not containing yolk (non-vitellogenic) present in the ovaries of queens in the different treatment groups. (c) The time in seconds the queens spent being active during a 2 min observation. (d) The amount of time the queens spent performing maternal behaviour. (e) The amount of total protein present in larvae after three weeks of treatment (wet weight). (f) The proportion of pupae which had pupated at the end of the experiment (as a proxy for developmental speed). (e) The difference in relative Vg expression between different treatment groups in comparison to two reference genes (18S and Elong1). In all figures, CoA = acetone control, CoH = handling control (only present in figure 1a) and JHa = juvenile hormone analogue methoprene-treated queens. Significant differences between treatments are indicated by asterisks; ‘n.s.’ indicates they did not differ (error bars indicate ± s.e.). (Online version in colour.)

Figure 2.

The regulatory effects of JH on the innate immune system of Lasius niger ant queens. (a,b) The effect of JH on the mean ± s.e. maximum activity of the phenoloxidase (PO) and pro-phenoloxidase (PPO) immune enzymes. Enzyme activity was measured during the linear phase of the reaction (V_max). (c,d) The mean ± s.e. relative expression of the cathepsinl and defensin immune genes, normalized against two reference genes (18S and Elong1). (e) The effect of JH on the resistance of queens to the fungal parasite Metarhizium pingshaense (black, JHa and parasite; yellow, JHa and control; orange, control and parasite; red, control and control). CoA, acetone control and JHa, juvenile hormone analogue methoprene-treated queens. Significant differences between treatments at p < 0.05 are indicated by asterisks in (a–d), and by different letters beside lines in (e). (Online version in colour.)

Figure 3.

Summary of the effects of JHa on maternal behaviour, reproductive physiology and immunocompetence. A black arrow indicates a significant increase of the trait in question in response to JHa treatment, whereas a red arrow indicates a significant decrease of the trait in response to JHa. ‘n.s.’ indicates that JHa treatment did not have a significant effect. (Online version in colour.)