Socially Parasitic Ants Evolve a Mosaic of Host-Matching and Parasitic Morphological Traits

Abstract

A basic expectation of evolution by natural selection is that species morphologies will adapt to their ecological niche. In social organisms, this may include selective pressure from the social environment. Many non-ant parasites of ant colonies are known to mimic the morphology of their host species, often in striking fashion [1, 2], indicating there is selection on parasite morphology to match the host (Batesian and/or Wasmannian mimicry [3]). However, ants that parasitize other ant societies are usually closely related to their hosts (Emery's rule) [4-8] and expected to be similar due to common ancestry, making any kind of mimicry difficult to detect [9]. Here, we investigate the diversification of the hyperdiverse ant genus Pheidole in Madagascar, including the evolution of 13 putative social parasite species within a broader radiation of over 100 ant species on the island. We find that the parasitic species are monophyletic and that their associated hosts are spread across the Malagasy Pheidole radiation. This provides an opportunity to test for selection on morphological similarity and divergence between parasites and hosts. Using X-ray microtomography and both linear measurements and three-dimensional (3D) geometric morphometrics, we show that ant social parasite worker morphologies feature a mix of "host-matching" and "parasitic" traits, where the former converge on the host phenotype and the latter diverge from typical Pheidole phenotypes to match a common parasitic syndrome. This finding highlights the role of social context in shaping the evolution of phenotypes and raises questions about the role of morphological sensing in nestmate recognition.