Sensory limitations and the maintenance of colour polymorphisms: viewing the ‘alba’ female polymorphism through the visual system of male Colias butterflies

Abstract

Summary Although colour polymorphisms are a widespread and conspicuous component of extant biodiversity, the selective pressures that act to maintain multiple morphs within populations remain poorly understood in most cases. In particular, the role that visual system limitations may play in maintaining multiple colour morphs is not well explored. We used a female‐limited colour polymorphism common to the butterfly genus Colias, called the ‘alba’ polymorphism, to investigate the hypotheses that mate‐searching males may struggle to discriminate pale ‘alba’ females from co‐occurring heterospecific white butterflies and/or heterospecific ‘alba’ females, or that ‘alba’ females may be more difficult to detect than non‘alba’ females in natural scenes. Such perceptual limitations may influence the relative mating rates of ‘alba’ versus non‘alba’ females, contributing to the evolutionary persistence of both morphs. Based on receptor‐noise‐limited modelling of the male Colias visual system, we find that ‘alba’ females exhibit chromatic and luminance contrasts against background foliage that are most similar to the ‘alba’ females of other co‐occurring Colias species and females of the co‐occurring white butterfly Pieris rapae. When compared to other co‐flying butterflies including non‘alba’ females, ‘alba’ females are consistently lower in chromatic contrast against background, but higher in luminance contrast. When viewed side‐by‐side, we estimate that male Colias should be able to discriminate ‘alba’ females from other co‐occurring heterospecific butterflies, including heterospecific ‘albas’. However, under field conditions that involve larger distances in space or time, males are likely to face challenges discriminating between conspecific ‘alba’ females and co‐occurring heterospecific white butterflies, particularly heterospecific ‘alba’ females. Our results suggest that constraints arising from male visual function may be involved in the maintenance of this colour polymorphism, particularly in populations that co‐occur with other ‘alba’‐polymorphic Colias species. We argue that such visual system constraints may play a larger role in the maintenance of colour polymorphism than has been empirically appreciated to date.