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Individual recognition is associated with holistic face processing in Polistes paper wasps in a species-specific way.

ABSTRACT: Most recognition is based on identifying features, but specialization for face recognition in primates relies on a different mechanism, termed 'holistic processing' where facial features are bound together into a gestalt which is more than the sum of its parts. Here, we test whether individual face recognition in paper wasps also involved holistic processing using a modification of the classic part-whole test in two related paper wasp species: Polistes fuscatus, which use facial patterns to individually identify conspecifics, and Polistes dominula, which lacks individual recognition. We show that P. fuscatus use holistic processing to discriminate between P. fuscatus face images but not P. dominula face images. By contrast, P. dominula do not rely on holistic processing to discriminate between conspecific or heterospecific face images. Therefore, P. fuscatus wasps have evolved holistic face processing, but this ability is highly specific and shaped by species-specific and stimulus-specific selective pressures. Convergence towards holistic face processing in distant taxa (primates, wasps) as well as divergence among closely related taxa with different recognition behaviour (P. dominula, P. fuscatus) suggests that holistic processing may be a universal adaptive strategy to facilitate expertise in face recognition.

SUBMITTER: Tibbetts EA

PROVIDER: S-EPMC7893282 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Understanding intraspecific geographic variation in animal signals poses a challenging evolutionary problem. Studies addressing geographic variation typically focus on signals used in mate-choice, however, geographic variation in intrasexual signals involved in competition is also known to occur. In Polistes dominulus paper wasps, females have black facial spots that signal dominance: individuals wasps with more complex 'broken' facial patterns are better fighters and are avoided by rivals. Recent work suggests there is dramatic geographic variation in these visual signals of quality, though this variation has not been explicitly described or quantified. Here, we analyze variation in P. dominulus signals across six populations and explore how environmental conditions may account for this variation. Overall, we found substantial variation in facial pattern brokenness across populations and castes. Workers have less broken facial patterns than gynes and queens, which have similar facial patterns. Strepsipteran parasitism, body size and temperature are all correlated with the facial pattern variation, suggesting that developmental plasticity likely plays a key role in this variation. First, the extent of parasitism varies across populations and parasitized individuals have lower facial pattern brokenness than unparasitized individuals. Second, there is substantial variation in body size across populations and a weak but significant relationship between facial pattern brokenness and body size. Wasps from populations with smaller body size (e.g. Italy) tend to have less broken facial patterns than wasps from populations with larger body size (e.g. New York, USA). Third, there is an apparent association between facial patterns and climate, with wasp from cooler locations tending to have higher facial pattern brokenness than wasps from warmer locations. Additional experimental work testing the causes and consequences of facial pattern variation will be important, as geographic variation in signals has important consequences for the evolution of communication systems and social behavior.

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Individual recognition is associated with holistic face processing in Polistes paper wasps in a species-specific way.

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