Evidence for adaptive brain tissue reduction in obligate social parasites (Polyergus mexicanus) relative to their hosts (Formica fusca)

Abstract

Brain investment is evolutionarily constrained by high costs of neural tissue. Several ecological factors favour the evolution of increased brain investment; we predict reduced brain region investment will accompany the evolution of organismal or social parasitism when parasites rely on host behaviour and cognition to solve ecological problems. To test this idea we investigated whether brain region investments differed between obligate slave-making Polyergus mexicanus ant workers and their Formica fusca slave workers. Polyergus workers perform little labour for their colonies; enslaved workers of Formica host species forage, excavate nests and tend the brood. We focused on the calyces of the mushroom bodies, central processing brain regions that are larger in social insect workers that perform complex tasks. As predicted we found lower relative investment in mushroom body calyx in P. mexicanus workers than in F. fusca workers; by contrast, enslaved and free F. fusca workers did not differ in mushroom body calyx volume. We then tested whether slave-makers and hosts differed in brain investment among sensory modalities. Polyergus slave-makers employ several unique classes of pheromones during raids, and eye size relative to head size was smaller in P. mexicanus workers than in F. fusca workers. The size of antennal brain tissues relative to visual tissues was greater in Polyergus, both in the peripheral sensory lobes and in the mushroom body calyx, suggesting greater relative investment in antennal processing by slave-makers. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 415–422.