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.

Color is necessary for specialized face learning in the Northern paper wasp, Polistes fuscatus

“…This study adds to a growing body of literature examining what constitutes a 'face' for P. fuscatus wasps. Thus far we know that the correct positions of internal features are required [12] and antennae or antennae and body are needed to be present [12,23]. This study adds that facial color patterning alone can confer identity as we controlled all other aspects of body position within the images.…”

“…In fact, P. fuscatus female wasps are specialized for learning face stimuli, and their ability to discriminate among images is dramatically reduced when images are digitally altered, either by removal of the antenna or rearrangement of the internal features of the face [12]. This finding and others suggests that like primates, faces in P. fuscatus are holistically processed [23] and seem to be special perceptual objects [12]. P. fuscatus facial patterns typically consist of only 3 pigments: a reddish-brown pigmentation, a yellow pigmentation, and a melanized black pigmentation [24,25].…”

“…Most importantly, this study demonstrates that chromatic information is required facial learning in P. fuscatus. As in primates, faces in the P. fuscatus system appear to be special, holistically processed perceptual objects [23,35,36]. While the neural mechanisms of face recognition remain elusive in Polistes fuscatus, the anterior optic tubercle and its downstream targets remain prime candidates due to the fact that it is socially plastic [27] and knowledge from other insects of its role in chromatic information processing [37], figureground detection [38] and female-female aggression [39].…”

“…A major strength of the presented behavioral assay is the confirmation that unreinforced trials show robust learning performance. Unlike in prior studies of learning in P. fuscatus [12,23,32] in this study we added unreinforced testing trials every 3 trials during training, in which animals received no shock. These un-reinforced trials allow animals to display choices that are potentially unbiased by shock-escape responses.…”

Identity signaling, identity reception and the evolution of social recognition in a Neotropical frog

“…Across animals, recognized social categories vary along a continuum of specificity, ranging from species recognition at the most general end of the continuum to the recognition of particular individuals at the most specific [4]. Social recognition often involves learning the features of another individual's communication signals, such as their visual markings (e.g., [5]) or voices (e.g., [6]). Two non-mutually exclusive hypotheses explain how signalers and receivers in a communication system can be targets of selection for social recognition.…”