Mating with an allopatric male triggers immune response and decreases longevity of ant queens

Abstract

In species with lifelong pair bonding, the reproductive interests of the mating partners are aligned, and males and females are expected to jointly maximize their reproductive success. Mating increases both longevity and fecundity of female reproductives (queens) of the ant Cardiocondyla obscurior, indicating a tight co-evolution of mating partners. Here, we show that mating with a male from their own population increases lifespan and reproductive success of queens more than mating with a male from a different population, with whom they could not co-evolve. A comparison of transcriptomes revealed an increased expression of genes involved in immunity processes in queens, which mated with males from a different population. Increased immune response might be proximately associated with decreased lifespan. Our study suggests a synergistic co-evolution between the sexes and sheds light on the proximate mechanisms underlying the decreased fitness of allopatrically mated queens.

Interruption points in the wing gene regulatory network underlying wing polyphenism evolved independently in male and female morphs in Cardiocondyla ants

“…In this species, colony fragmentation stimulates the development of the winged male morph (Cremer & Heinze, ; Du, Schrempf, & Heinze, ; Schrader, Simola, Heinze, & Oettler, ; Schrempf & Heinze, ), but the precise environmental cues that induce winged or wingless males are not yet fully understood. Wingless males have been shown to play a prominent role in all aspects of the colony life cycle—not only are they at the core of competition over sex allocation under local mate competition (Cremer & Heinze, ) or reproductive dominance (Suefuji, Cremer, Oettler, & Heinze, ), they also have direct effects on queen fitness (Schrempf et al, ; Von Wyschetzki, Rueppell, Oettler & Heinze, ).…”

When invasive ants meet: effects of outbreeding on queen performance in the tramp ant Cardiocondyla itsukii

“…), queens that had mated with an allopatric male had a shorter lifespan than queens that had mated with a male from their parental colony. Proximately, outbreeding appeared to be associated with an increased immune response, probably triggered by the seminal fluid of the alien male (Schrempf et al ., ). Shorter lifespan was also observed in C. itsukii queens, indicating a similar cost of mating with an alien male for the queen.…”

“…Schrempf et al . () studied the consequence of interpopulation crosses in the tramp ant Cardiocondyla obscurior . While only few of the staged crosses were unsuccessful (A. Schrempf, pers.…”

“…In introduced populations, adoption and outbreeding might involve individuals with different invasion history and geographical origin. In C. obscurior , mating between sexuals from different introduced populations negatively affected the longevity and the reproductive success of the queen, apparently because sperm and seminal fluid from alien males elicited an increased immune response in their mates (Schrempf et al ., ).…”

Life-history evolution in ants: the case ofCardiocondyla

“…This-and genetic estimates of fixation coefficientsindicate that a certain fraction of sexuals disperse and outbreed. Nevertheless, forced outbreeding between sexuals from different populations resulted in an elevated immune response in C. obscurior queens, accompanied by decreased queen fecundity and lifespan relative to queens that mated with a related male [61].…”