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.

Differential investment in visual and olfactory brain regions mirrors the sensory needs of a paper wasp social parasite and its host

“…Established parasitic queens, in contrast, will not forage and instead remain on the host nest (Cervo, 2006). This pattern is consistent with the observed higher calyx investment for the host ant Formica fusta compared to workers of its obligate social parasite P. mexicanus, which rarely forage (Sulger et al, 2014). These two hypotheses may not be mutually exclusive, and further experiments that include molecular, cellular and circuitry approaches (Godfrey & Gronenberg, 2019) would elucidate the effect of these two selective pressures towards sensory investment.…”

“…nimpha, as the parasite's large size can hinder effective usurpation in the latter two social species (Cervo, 2006;Cini, Bruschini, Signorotti, et al, 2011). The high investment in vision and low investment in sensory processing (e.g., calyx) also reflects the initial needs of the parasite, which is remarkably similar to neural tissue allocation in the obligate parasitic ant Polyergus mexicanus (Sulger et al, 2014). In addition, the central complex, the navigation center of the brain, is significantly larger in the social parasite compared to the host (Honkanen et al, 2019).…”

“…mexicanus, which rarely forage (Sulger et al, 2014). These two hypotheses may not be mutually exclusive, and further experiments that include molecular, cellular and circuitry approaches (Godfrey & Gronenberg, 2019) would elucidate the effect of these two selective pressures towards sensory investment.…”

Neuroanatomical and Morphological Trait Clusters in the Ant Genus <b><i>Pheidole:</i></b> Evidence for Modularity and Integration in Brain Structure

“…The central complex is involved in visual signal processing and locomotion (and its spatial control) and has additional functions in spatial memory and place learning; its origin is linked to the evolution of compound eyes and walking legs [Pfeiffer and Homberg, 2014]. Variation in these macroscopic and cellular aspects of brain organization is predicted to reflect sociobiological and ecological differences within [Giraldo et al, 2013;Groh et al, 2014;Kelber et al, 2010;Kuebler et al, 2010;Seid and Wehner, 2009;Stieb et al, 2010] and among ant species [Kelber et al, 2009;Muscedere et al, 2014;Stieb et al, 2011;Sulger et al, 2014].…”

Are ants botanists? Ant associative learning of plant chemicals mediates foraging for carbohydrates

“…These ants occupy separate subfamilies that independently evolved to rely on plant‐based sugar‐rich rewards (Hölldobler & Wilson, ). Compared with F. podzolica , T. sessile ants have smaller brains (cross‐sectional widths of approximately 1 and 0.35 mm, respectively) (Muscedere et al ., ; Sulger et al ., ) and live in smaller colonies (Deslippe & Savolainen, ; Buczkowski, ), although they also often recruit more workers to baits (A. S. Nelson & K. A. Mooney, unpublished data). Such differences in brain and colony size, as well as recruitment to resources, could have potentially altered the capacity for both individual and social learning in these ants.…”