Cooperation by harvester ant queens brings direct energetic benefits during colony founding

Cooperative behavior by nonrelatives is an evolutionary puzzle, because costs of cooperation are often strong while selective factors favoring cooperative groups remain unclear. In some populations of the seed harvester ant P ogonomyrmex californicus , unrelated queens form groups at colony founding (pleometrosis), whereas in other populations, colonies are initiated by single queens (haplometrosis). We tested the hypothesis that energetic savings of grouping contribute a benefit that may enhance queen success during colony founding and early growth for pleometrotic colonies. We measured metabolic rates and locomotor activity of individuals or pairs of freshly collected, newly mated P. californicus queens from pleometrotic and haplometrotic populations. Population source did not significantly affect metabolic rates, but paired queens from both populations had mass-specific metabolic rates only 86% of those of individual queens. The metabolic effect of grouping was not explained by differences in locomotion. To test whether this degree of energetic saving could be biologically significant, we assessed metabolic rate, body mass, and egg production for pleometrotic pairs at four time points of colony founding and compared the energetic content of stored lipid to energy use up to the point of worker emergence. Metabolic rates dropped over time for queens, as did body mass, and gas exchange switched from continuous to discontinuous, suggestive of metabolic suppression. Total joules required for queens to reach the worker emergence stage were 1.5 times the energy content of stored lipids, consistent with the need for foraging for these queens, and supporting the hypothesis that energetic savings of grouping can be beneficial by extending energetic stores and reducing the need for risky foraging. Significance statement Animal cooperation has fascinated people since well before Darwin, but the factors impacting whether cooperation occurs remain controversial. We investigated the energetic cost of nest initiation in ant queens that naturally vary in their propensity to cooperate. We determined that the energy costs of nest initiation prior to worker emergence exceed the energy in the queen’s lipid stores, partly explaining why these queens forage and experience high mortality. Queen pairing significantly lowered metabolic rates, demonstrating that energetic savings from grouping can be an important advantage of cooperation in this system.