Colour, vision and coevolution in avian brood parasitism

Abstract

The coevolutionary interactions between avian brood parasites and their hosts provide a powerful system for investigating the diversity of animal coloration. Specifically, reciprocal selection pressure applied by hosts and brood parasites can give rise to novel forms and functions of animal coloration, which largely differ from those that arise when selection is imposed by predators or mates. In the study of animal colours, avian brood parasite-host dynamics therefore invite special consideration. Rapid advances across disciplines have paved the way for an integrative study of colour and vision in brood parasite-host systems. We now know that visually driven host defences and host life history have selected for a suite of phenotypic adaptations in parasites, including mimicry, crypsis and supernormal stimuli. This sometimes leads to vision-based host counter-adaptations and increased parasite trickery. Here, we review vision-based adaptations that arise in parasite-host interactions, emphasizing that these adaptations can be visual/sensory, cognitive or phenotypic in nature. We highlight recent breakthroughs in chemistry, genomics, neuroscience and computer vision, and we conclude by identifying important future directions. Moving forward, it will be essential to identify the genetic and neural bases of adaptation and to compare vision-based adaptations to those arising in other sensory modalities.This article is part of the themed issue 'Animal coloration: production, perception, function and application'.

Keywords: animal coloration; avian vision; brood parasitism; coevolution; mimicry; sensory ecology.

Figure 1.

Adaptations involving colour at the frontline, egg, chick and fledgling stages. (a) The rufous-morph female common cuckoo mimics the appearance of a (b) sparrowhawk, which can reduce mobbing behaviour by hosts. The rufous-morph cuckoo has an added advantage if hosts recognize it less readily than the more common grey-morph. (c) The parasitic cuckoo finch has evolved polymorphic eggs to match the range of polymorphic egg colours exhibited by their hosts, the tawny-flanked prinia. The inner circle shows eggs laid by different cuckoo finch females, while the outer circle shows eggs laid by prinia females. (d) Genetically distinct host-races of the common cuckoo lay a range of eggs (top row) to match those of their preferred European hosts (bottom row). The degree of egg colour and pattern mimicry varies. (e) Various Chalcites cuckoo chicks (left) mimic the skin coloration—and even the natal down—of host chicks (right). (f) The parasitic pin-tailed whydah (left) mimics the gape markings of its host, the common waxbill (right). (g) The horsfield's hawk-cuckoo elicits increased feeding from its foster parent by displaying a wing patch that mimics an extra gape. (h) Parasitic fledgling screaming cowbirds (centre) mimic the plumage patterns of host fledgling greyish baywings (left), and receive prolonged parental care, unlike non-mimetic fledgling shiny cowbirds (right). (i) An adult parasitic female cuckoo finch (left) looks almost identical to a harmless adult female red bishop (right), which confuses host tawny-flanked prinias. Image credits: (a) C. Fleming, (b) D. Kjaer, (c) C. Spottiswoode, (d) M. C. Stoddard (copyright Natural History Museum, UK), (e) N. E. Langmore [25], (f) J. Schuetz [48], (g) K. Tanaka, (h) C. De Marsico and J. Reboreda [49], and (i) C. Spottiswoode [50].

Figure 2.

The coevolutionary dynamics of vision-based adaptations. Host vision (a) and parasite vision (b) are implicated in the evolution of visual and cognitive adaptations, which can influence reciprocal selection for phenotypic adaptations. In turn, phenotypic adaptations can lead to further refinements of vision and cognition. In some cases, phenotypic adaptations in the parasite can evolve to ‘tune’ into aspects of the host's life history (A, light grey arrow), such as visual behaviours involved in incubation and provisioning.