Evolutionary loss of threat display in more social species: phylogenetic comparisons, natural interactions in the wild, and experiments with models

Fitness can be increased dramatically by communication. So why, given the benefits of communication, would displays ever be completely lost evolutionarily? Threat displays, in particular, are relatively cheap to produce and are precursors of attack, so should be especially hard for both senders and receivers to lose completely. Here we explore an evolutionary transition in sociality, testing whether complete evolutionary loss of threat display has occurred in ‘more social’ hermit crab species, which interact more frequently with conspecifics. First, we synthesised literature and observations on the presence versus absence of threat display across hermit crab species, mapping this information onto a phylogenetic tree. We found that all ‘less social’ species — marine and terrestrial — produce threat displays, consistent with threat display being the ancestral state. But ‘more social’ terrestrial species, which are highly derived, do not produce a threat display, suggesting an evolutionary loss. Next, we contrasted natural interactions in the wild within a less social species (Pagurus bernhardus) versus within a more social species (Coenobita compressus), finding that the less social species, despite a lower rate of social encounter, had a higher rate of display per encounter (24%). In contrast, the more social species’ rate of display per encounter was negligible (<1%), effectively indicating a loss in production. Finally, we experimentally reanimated threat display in the more social species, using postured models to test whether receivers retained any responsiveness to threat display. Starkly, receivers were not deterred by threat display, showing equal responsiveness across both threat and non-threat models, regardless of whether the models were stationary or dynamically moving. Our results thus reveal a case of complete collapse of communication involving threat display, implicating the social environment in this loss. In more social species, an extreme dependence on conspecific-derived shells likely drove a ‘desperado effect’, with threat displays being lost because they could not stop others from pursuing these valuable resources.

The fear gasping face as a threat display in a Melanesian society

Theory and research show that humans attribute both emotions and intentions to others on the basis of facial behavior: A gasping face can be seen as showing “fear” and intent to submit. The assumption that such interpretations are pancultural derives largely from Western societies. Here, we report two studies conducted in an indigenous, small-scale Melanesian society with considerable cultural and visual isolation from the West: the Trobrianders of Papua New Guinea. Our multidisciplinary research team spoke the vernacular and had extensive prior fieldwork experience. In study 1, Trobriand adolescents were asked to attribute emotions, social motives, or both to a set of facial displays. Trobrianders showed a mixed and variable attribution pattern, although with much lower agreement than studies of Western samples. Remarkably, the gasping face (traditionally considered a display of fear and submission in the West) was consistently matched to two unpredicted categories: anger and threat. In study 2, adolescents were asked to select the face that was threatening; Trobrianders chose the “fear” gasping face whereas Spaniards chose an “angry” scowling face. Our findings, consistent with functional approaches to animal communication and observations made on threat displays in small-scale societies, challenge the Western assumption that “fear” gasping faces uniformly express fear or signal submission across cultures.

Multimodal signals: ultraviolet reflectance and chemical cues in stomatopod agonistic encounters

Complex signals are commonly used during intraspecific contests over resources to assess an opponent's fighting ability and/or aggressive state. Stomatopod crustaceans may use complex signals when competing aggressively for refuges. Before physical attacks, stomatopods assess their opponents using chemical cues and perform threat displays showing a coloured patch, the meral spot. In some species, this spot reflects UV. However, despite their complex visual system with up to 20 photoreceptor classes, we do not know if stomatopods use chromatic or achromatic signals in contests. In a field study, we found that Neogonodactylus oerstedii meral spot luminance varies with sex, habitat and, more weakly, body length. Next, we conducted an experimental manipulation which demonstrated that both chemical cues and chromatic signals are used during contests. In the absence of chemical cues, stomatopods approached an occupied refuge more quickly and performed offensive behaviours at a lower rate. When UV reflectance was absent, stomatopods performed offensive behaviours more frequently and contest duration trended towards shorter fights. These results provide new evidence that UV reflectance and/or visible spectrum luminance is used to amplify threat displays. Our results are the first to demonstrate that chemical and chromatic cues comprise a multimodal signal in stomatopod contests.

Does sexual selection explain human sex differences in aggression?

I argue that the magnitude and nature of sex differences in aggression, their development, causation, and variability, can be better explained by sexual selection than by the alternative biosocial version of social role theory. Thus, sex differences in physical aggression increase with the degree of risk, occur early in life, peak in young adulthood, and are likely to be mediated by greater male impulsiveness, and greater female fear of physical danger. Male variability in physical aggression is consistent with an alternative life history perspective, and context-dependent variability with responses to reproductive competition, although some variability follows the internal and external influences of social roles. Other sex differences, in variance in reproductive output, threat displays, size and strength, maturation rates, and mortality and conception rates, all indicate that male aggression is part of a sexually selected adaptive complex. Physical aggression between partners can be explained using different evolutionary principles, arising from the conflicts of interest between males and females entering a reproductive alliance, combined with variability following differences in societal gender roles. In this case, social roles are particularly important since they enable both the relatively equality in physical aggression between partners from Western nations, and the considerable cross-national variability, to be explained.

Dual gratings interspersed on a single butterfly scale

Iridescent butterfly wing colours result from the interaction of light with sub-micrometre structures in the scales. Typically, one scale contains one such photonic structure that produces a single iridescent signal. Here, however, we show how the dorsal wings of male Lamprolenis nitida emit two independent signals from two separate photonic structures in the same scale. Multiple independent signals from separate photonic structures within the same sub-micrometre device are currently unknown in animals. However, they would serve to increase the complexity and specificity of the optical signature, enhancing the information conveyed. This could be important during intrasexual encounters, in which iridescent male wing colours are employed as threat displays. Blazed diffraction gratings, like those found in L. nitida , are asymmetric photonic structures and drive most of the incident light into one diffraction order. Similar gratings are used in spectrometers, limiting the spectral range over which the spectrometer functions. By incorporating two interchangeable gratings onto a single structure, as they are in L. nitida , the functional range of spectrometers could be extended.