The question of how reproductives and sterile workers differentiate within eusocial groups has long been a core issue in sociobiology because it requires the loss of individual direct fitness in favor of indirect or group-level fitness gains. The evolution of social behavior requires that differentiation between workers and female reproductives be environmentally determined, because genetically determined sterility would be quickly eliminated. Nevertheless, we report clear evidence of genetic caste determination in populations of two seed harvester ant species common to the southwestern USA, Pogonomyrmex rugosus and Pogonomyrmex barbatus. The genetic differentiation between workers and queens is found only in areas of sympatry of the two species, and thus appears to arisen from hybridization. Our data suggest that this hybridization has had a profound historical effect on the caste determination systems and mating patterns of each of these species.
The behavior of reproductive female ants distinctly changes during the transition from virgin to mature, egg-laying queen. A winged female ant flies only once during her lifetime when she engages in the nuptial flight. Once she is mated she sheds her wings, excavates a nest and starts laying eggs, the basis for her future colony. We show for two species of harvester ants that this transition is accompanied by changes in the performance of behavioral tests: flying virgins are positively phototactic and prefer open areas, whereas young queens prefer the dark, avoid open areas and, given the opportunity, dig into the soil. These behavioral changes coincide with morphological changes in the brain. The brains of mature queens are significantly smaller than those of virgin females at the time of their mating flight. A disproportionately large shrinkage occurs in the medulla and other parts of the visual system during the early adult life of the queen. The brain reduction appears to be adaptive as mature queens show reduced behavioral repertoires and live in the dark. In contrast to virgin females, they do not rely on vision and might increase their fitness by reducing metabolically costly neural tissue.
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