Person:

Haig, David

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.

When a measure becomes a target, it often ceases to be a good measure – an effect familiar from the declining usefulness of standardized testing in schools. This economic principle also applies to mate choice and, perhaps surprisingly, pregnancy. Just as females screen potential mates under many metrics, human mothers unconsciously screen embryos for quality. ‘Examinees’ are under intense selection to improve test performance by exaggerating formerly ‘honest’ signals of quality. Examiners must change their screening criteria to maintain useful information (but cannot abandon old criteria unilaterally). By the resulting ‘proxy treadmill’, new honest indicators arise while old degraded indicators linger, resulting in trait elaboration and exaggeration. Hormone signals during pregnancy show extreme evolutionary escalation (akin to elaborate mating displays).

Red, orange, and yellow carotenoid-colored plumages have been considered honest signals of condition. We comprehensively quantified carotenoid signals in the social, sexually-dimorphic tanager genus Ramphocelus using scanning electron microscopy (SEM), finite-difference time-domain (FDTD) optical modeling, liquid chromatography–mass spectrometry (LC-MS), and spectrophotometry. Despite males having significantly more saturated color patches, males and females within a species have equivalent amounts and types of carotenoids. Male, but not female, feathers have elaborate microstructures which amplify color appearance. Expanded barbs enhance color saturation (for the same amount of pigment) by increasing the transmission of optical power through the feather. Dihedral barbules (vertically-angled, strap-shaped barbules) reduce total reflectance to generate “super black” plumage, an optical illusion to enhance nearby color. Dihedral barbules paired with red carotenoid pigment produce “velvet red” plumage. Together, our results suggest that a widely cited index of honesty—carotenoid pigments—cannot fully explain male appearance. We propose that males are selected to evolve amplifiers of honest signals—in this case, microstructures that enhance appearance —that are not necessarily themselves linked to quality.