Testosterone amplifies the negative valence of an agonistic gestural display by exploiting receiver perceptual bias

Many animals communicate by performing elaborate displays that are incredibly extravagant and wildly bizarre. So, how do these displays evolve? One idea is that innate sensory biases arbitrarily favour the emergence of certain display traits over others, leading to the design of an unusual display. Here, we study how physiological factors associated with signal production influence this process, a topic that has received almost no attention. We focus on a tropical frog, whose males compete for access to females by performing an elaborate waving display. Our results show that sex hormones like testosterone regulate specific display gestures that exploit a highly conserved perceptual system, evolved originally to detect ‘dangerous' stimuli in the environment. Accordingly, testosterone makes certain gestures likely to appear more perilous to rivals during combat. This suggests that hormone action can interact with effects of sensory bias to create an evolutionary optimum that guides how display exaggeration unfolds.

Male Barn Swallows Tolerate Nestling-Like Courtship Calls of Rival Males

Animals often exhibit conspicuous, and sometimes curious, courtship traits, such as nestling-like courtship display in birds, though modern studies of nestling-like courtship display (and calls) are virtually lacking. An exception is previous experiments on the barn swallow Hirundo rustica, demonstrating that females are equally attracted to playback of two structurally similar calls, nestling-like male courtship calls and nestling food-begging calls. The experiments support the sensory trap hypothesis, i.e., that male signals mimic nestling stimuli to exploit female parental care for nestlings. However, female attraction might not be the sole function of nestling-like traits, and males might also have a sensory bias toward nestling-like traits, in which males would be less aggressive toward characteristics typical of immature individuals. Here, I conducted playback experiments to study the function of nestling-like male courtship calls in the context of male–male interactions. Playback of male courtship songs induced frequent approaches by neighbouring males, while nestling-like male courtship calls or nestling food-begging calls induced fewer approaches, though male responses to the latter two vocalisations increased when approaching the nestling period. The observed pattern indicates that, by mimicking immature individuals, males attract intended signal receivers (i.e., females) while avoiding interference from eavesdroppers (i.e., neighbouring males). This unique function can explain why species with parental care exhibit immature-like behaviour.

A sensory bias overrides learned preferences of bumblebees for honest signals in Mimulus guttatus

Insect pollinators readily learn olfactory cues, and this is expected to select for ‘honest signals' that provide reliable information about floral rewards. However, plants might alternatively produce signals that exploit pollinators' sensory biases, thereby relaxing selection for signal honesty. We examined the innate and learned preferences of Bombus impatiens for Mimulus guttatus floral scent phenotypes corresponding to different levels of pollen rewards in the presence and absence of the innately attractive floral volatile compound β-trans-bergamotene. Bees learned to prefer honest signals after foraging on live M. guttatus flowers, but only exhibited this preference when presented floral scent phenotypes that did not include β-trans-bergamotene. Our results suggest that a sensory bias for β-trans-bergamotene overrides the ability of B. impatiens to use honest signals when foraging on M. guttatus . This may represent a deceptive pollination strategy that allows plants to minimize investment in costly rewards without incurring reduced rates of pollinator visitation.

Responses of intended and unintended receivers to a novel sexual signal suggest clandestine communication

Inadvertent cues can be refined into signals through coevolution between signalers and receivers, yet the earliest steps in this process remain elusive. In Hawaiian populations of the Pacific field cricket, a new morph producing a novel and incredibly variable song (purring) has spread across islands. Here we characterize the current sexual and natural selection landscape acting on the novel signal by (1) determining fitness advantages of purring through attraction to mates and protection from a prominent deadly natural enemy, and (2) testing alternative hypotheses about the strength and form of selection acting on the novel signal. In field studies, female crickets respond positively to purrs, but eavesdropping parasitoid flies do not, suggesting purring may allow private communication among crickets. Contrary to the sensory bias and preference for novelty hypotheses, preference functions (selective pressure) are nearly flat, driven by extreme inter-individual variation in function shape. Our study offers a rare empirical test of the roles of natural and sexual selection in the earliest stages of signal evolution.

Interspecific introgression reveals a role of male genital morphology during the evolution of reproductive isolation in Drosophila

Rapid divergence in genital structures among nascent species has been posited to be an early-evolving cause of reproductive isolation, although evidence supporting this idea as a widespread phenomenon remains mixed. Using a collection of interspecific introgression lines between two Drosophila species that diverged ∼240,000 years ago, we tested the hypothesis that even modest divergence in genital morphology can result in substantial fitness losses. We studied the reproductive consequences of variation in the male epandrial posterior lobes between Drosophila mauritiana and D. sechellia and found that divergence in posterior lobe morphology has significant fitness costs on several pre-fertilization and post-copulatory reproductive measures. Males with divergent posterior lobe morphology also significantly reduced the life span of their mates. Interestingly, one of the consequences of genital divergence was decreased oviposition and fertilization, which suggests that a sensory bias for posterior lobe morphology could exist in females, and thus posterior lobe morphology may be the target of cryptic female choice in these species. Our results provide evidence that divergence in genitalia can in fact give rise to substantial reproductive isolation early during species divergence, and they also reveal novel reproductive functions of the external male genitalia in Drosophila.

Spider lures exploit insect preferences for floral colour and symmetry

Sensory systems can capture only a fraction of available information, which creates opportunities for deceptive signalling. The sensory traps and sensory bias models have proven valuable for explaining how visual systems and environments shape the design of sexual signals, but their application to deceptive signals is largely untapped. Here we use the ‘jewelled’ orb-web spiderGasteracantha fornicatato experimentally test two longstanding hypotheses for the function of deceptive visual lures. Namely, that they: (1) exploit generalised preferences for conspicuous colouration (sensory bias), or (2) co-opt the otherwise-adaptive foraging response of prey toward flowers (sensory traps). In a field-based study we manipulated the conspicuous dorsal signal of female spiders along two axes —– colour pattern and symmetry — to generate a gradient of floral resemblance, and monitored the per-individual consequences for prey interception. As predicted by the traps model, the most attractive phenotypes were those with flower-like radial symmetry and solid colour patterns, and their attractiveness equaled that of wild-type models. These results demonstrate that deceptive orb-web spider lures function, in part, as inter-kingdom sensory traps via floral mimicry, and support the broader extension of sensory-based models to deceptive signalling contexts.

Structurally assisted super black in colourful peacock spiders

Male peacock spiders ( Maratus , Salticidae) compete to attract female mates using elaborate, sexually selected displays. They evolved both brilliant colour and velvety black. Here, we use scanning electron microscopy, hyperspectral imaging and finite-difference time-domain optical modelling to investigate the deep black surfaces of peacock spiders. We found that super black regions reflect less than 0.5% of light (for a 30° collection angle) in Maratus speciosus (0.44%) and Maratus karrie (0.35%) owing to microscale structures. Both species evolved unusually high, tightly packed cuticular bumps (microlens arrays), and M. karrie has an additional dense covering of black brush-like scales atop the cuticle. Our optical models show that the radius and height of spider microlenses achieve a balance between (i) decreased surface reflectance and (ii) enhanced melanin absorption (through multiple scattering, diffraction out of the acceptance cone of female eyes and increased path length of light through absorbing melanin pigments). The birds of paradise (Paradiseidae), ecological analogues of peacock spiders, also evolved super black near bright colour patches. Super black locally eliminates white specular highlights, reference points used to calibrate colour perception, making nearby colours appear brighter, even luminous, to vertebrates. We propose that this pre-existing, qualitative sensory experience—‘sensory bias’—is also found in spiders, leading to the convergent evolution of super black for mating displays in jumping spiders.