Mating triggers dynamic immune regulations in wood ant queens

Abstract

Mating can affect female immunity in multiple ways. On the one hand, the immune system may be activated by pathogens transmitted during mating, sperm and seminal proteins, or wounds inflicted by males. On the other hand, immune defences may also be down‐regulated to reallocate resources to reproduction. Ants are interesting models to study post‐mating immune regulation because queens mate early in life, store sperm for many years, and use it until their death many years later, while males typically die after mating. This long‐term commitment between queens and their mates limits the opportunity for sexual conflict but raises the new constraint of long‐term sperm survival. In this study, we examine experimentally the effect of mating on immunity in wood ant queens. Specifically, we compared the phenoloxidase and antibacterial activities of mated and virgin Formica paralugubris queens. Queens had reduced levels of active phenoloxidase after mating, but elevated antibacterial activity 7 days after mating. These results indicate that the process of mating, dealation and ovary activation triggers dynamic patterns of immune regulation in ant queens that probably reflect functional responses to mating and pathogen exposure that are independent of sexual conflict.

Ant sperm storage organs do not have phenoloxidase constitutive immune activity

“…These results are consistent with those previously reported in two other ant species where queen immune activity was shown to vary around the mating period. Virgin queens of Formica paralugubris had higher proPO levels than freshly mated queens (Castella et al, 2009) and A. colombica queens up-regulated their melanization immune response a few days after mating (Baer et al, 2006). Our limited sample availability did not allow us to corroborate this variation in proPO/PO activity over time in A. colombica and A. echinatior, but it seems likely that the activation of the proPO system within a few days after mating is an adaptive response to pathogen exposure during colony founding.…”

“…Such damages can be prevented thanks to the activity of antioxidative enzymes, such as catalase, superoxyde dismutase or glutathione-S-transferase (Weirich et al, 2002;Collins et al, 2004;DeJong et al, 2007). To date, several studies of insect immune capacity have shown an increase in the hemolymph PO-level associated with the presence of 'non-self' elements such as lipopolysaccharides injections or nylon inserts (Castella et al, 2009;Baer et al, 2006;McNamara et al, 2013;Schwarzenbach and Ward, 2006).…”

Reproduction–Immunity Trade-Offs in Insects

“…Fedorka et al (44) showed that female ground crickets ( Allonemobius socius ) sustained progressively fewer circulating hemocytes with increasing copulation frequency. Mealworm beetles ( Tenebrio molitor ) and wood ants ( Formica paralugubris ) show a reduction in phenoloxidase activity after mating (24, 112), although Fedorka et al (44) saw the opposite pattern with A. socius . Nevertheless, hemolymph samples from mated A. socius females were less bacteriolytic than hemolymph samples from virgin females (44), demonstrating reduced constitutive immunological effectiveness.…”

Recognition of caste and mating status maintains monogyny in the ant Aphaenogaster senilis

“…According to the "honest signalling" theory, the queen pheromone is predicted to reliably signal both her mating status and reproductive potential, and the brood and/or worker behavioural and physiological responses are expected to be proportional to the queen's quality (Hannonen et al 2002;Kocher et al 2009). The importance of signalling mating status in the competition between virgin and newly-mated queens is corroborated by several studies showing that important changes in pheromone composition accompany the post-mating physiological modifications (Hora et al 2008;Kocher et al 2008;Castella et al 2009). In the present study, we investigated whether, in A. senilis, signalling of the mating status resolves or at least mitigates the conflicts over which queen will head the colony.…”