Trade-offs between immunity and competitive ability in fighting ant males

Background: Fighting disease while fighting rivals exposes males to
constraints and trade-offs during male-male competition. We here tested
how both the stage and intensity of infection with the fungal pathogen
Metarhizium robertsii interfered with fighting success in Cardiocondyla
obscurior ant males. Males of this species have evolved long lifespans
during which they can gain many matings with the young queens of the
colony, if successful in male-male competition. Since male fights occur
inside the colony, the outcome of male-male competition can further be
biased by interference of the colony’s worker force. Results: We found
that severe, but not yet mild, infection strongly impaired male fighting
success. In late-stage infection, this could be attributed to worker
aggression directed towards the infected rather than the healthy male and
an already very high male morbidity even in the absence of fighting.
Shortly after pathogen exposure, however, male mortality was particularly
increased during combat. Since these males mounted a strong immune
response, their reduced fighting success suggests a trade-off between
immune investment and competitive ability already early in the infection.
Even if the males themselves showed no difference in the number of attacks
they raised against their healthy rivals across infection stages and
levels, severely infected males were thus losing in male-male competition
from an early stage of infection on. Conclusions: Males of the ant C.
obscurior have evolved high immune investment, triggering an effective
immune response very fast after fungal exposure. This allows them to cope
with mild pathogen exposures without cost to their success in male-male
competition, and hence to gain multiple mating opportunities with the
emerging virgin queens of the colony. Under severe infection, however,
they are weak fighters and rarely survive combat already at early
infection when raising an immune response, as well as at progressed
infection, when they are morbid and preferentially targeted by worker
aggression. Workers thereby remove males that pose a future disease threat
by biasing male-male competition. Our study thus revealed a novel social
immunity mechanism for how social insect workers protect the colony
against disease risk.