Immune priming and pathogen resistance in ant queens

Abstract

Growing empirical evidence indicates that invertebrates become more resistant to a pathogen following initial exposure to a nonlethal dose; yet the generality, mechanisms, and adaptive value of such immune priming are still under debate. Because life-history theory predicts that immune priming and large investment in immunity should be more frequent in long-lived species, we here tested for immune priming and pathogen resistance in ant queens, which have extraordinarily long life span. We exposed virgin and mated queens of Lasius niger and Formica selysi to a low dose of the entomopathogenic fungus Beauveria bassiana, before challenging them with a high dose of the same pathogen. We found evidence for immune priming in naturally mated queens of L. niger. In contrast, we found no sign of priming in virgin queens of L. niger, nor in virgin or experimentally mated queens of F. selysi, which indicates that immune priming in ant queens varies according to mating status and mating conditions or species. In both ant species, mated queens showed higher pathogen resistance than virgin queens, which suggests that mating triggers an up-regulation of the immune system. Overall, mated ant queens combine high reproductive output, very long life span, and elevated investment in immune defense. Hence, ant queens are able to invest heavily in both reproduction and maintenance, which can be explained by the fact that mature queens will be protected and nourished by their worker offspring.

Keywords: formicine ants; immune priming; immunity; life span; life-history; mating.

Figure 1

A queen of Formica selysi. Photo: Joël Meunier.

Figure 2

Test of immune priming in queens of Lasius niger (upper panels, A and B) and Formica selysi (lower panels, C and D). The figure shows Kaplan-Meier survival curves for mated queens (left panels, A and C) and virgin queens (right panels, B and D), respectively. In controls, the queens were exposed to control solvent and challenged with control solvent (Control–Control, black thin dashed line) or exposed to a low dose of the entomopathogenic fungus B. bassiana and challenged with control solvent (Beauveria–Control, black thin continuous line). In the test of priming, queens were exposed to control solvent and challenged with a high dose of B. bassiana (Control–Beauveria, light green bold dashed line) or exposed to a low dose of B. bassiana and challenged with a high dose of B. bassiana (Beauveria–Beauveria, dark green bold continuous line). Sample sizes (number of queens) for each treatment are indicated in brackets. Different lower case letters indicate treatments that differed significantly from one another.

Figure 3

Test of the effect of mating on immune resistance in L. niger queens. The figure shows Kaplan–Meier survival curves for virgin queens (dashed lines) and mated queens (continuous lines) that were either exposed to control solvent (Control, black thin lines) or to a high dose of the entomopathogenic fungus B. bassiana (Beauveria, light green bold lines). No prior exposure (priming) was performed in this experiment. Sample sizes (number of queens) for each treatment are indicated in brackets. Different lower case letters indicate treatments that differed significantly from one another.