Abstract

In coevolutionary arms-races, reciprocal ecological interactions and their fitness impacts shape the course of phenotypic evolution. The classic example of avian host–brood parasite interactions selects for host recognition and rejection of increasingly mimetic foreign eggs. An essential component of perceptual mimicry is that parasitic eggs escape detection by host sensory systems, yet there is no direct evidence that the avian visual system covaries with parasitic egg recognition or mimicry. Here, we used eye size measurements collected from preserved museum specimens as a metric of the avian visual system for species involved in host–brood parasite interactions. We discovered that (i) hosts had smaller eyes compared with non-hosts, (ii) parasites had larger eyes compared with hosts before but not after phylogenetic corrections, perhaps owing to the limited number of independent evolutionary origins of obligate brood parasitism, (iii) egg rejection in hosts with non-mimetic parasitic eggs positively correlated with eye size, and (iv) eye size was positively associated with increased avian-perceived host–parasite eggshell similarity. These results imply that both host-use by parasites and anti-parasitic responses by hosts covary with a metric of the visual system across relevant bird species, providing comparative evidence for coevolutionary patterns of host and brood parasite sensory systems.

Highlights

  • In coevolutionary interactions, reciprocally interacting lineages shape each other’s ecological and physiological milieus and generate selective forces to impact the direction and pace of evolution [1]

  • This is surprising because visible cues at a distance and, greater visual acuity through relatively larger eyes [7] are both critical for parasites to locate host nests [8] and for hosts to recognize and prevent, dampen or eliminate parasitism

  • Obligate avian brood parasites had larger eyes compared with hosts for the non-phylogenetic model royalsocietypublishing.org/journal/rsbl Biol

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Summary

Introduction

Reciprocally interacting lineages shape each other’s ecological and physiological milieus and generate selective forces to impact the direction and pace of evolution [1]. Frequently hypothesized in the context of avian host–parasite coevolution [5,6], direct morphological and physiological evidence is still lacking for the evolutionary impact of brood parasitism upon the sensory systems of hosts and their parasites. This is surprising because visible cues at a distance and, greater visual acuity through relatively larger eyes [7] are both critical for parasites to locate host nests [8] and for hosts to recognize and prevent, dampen or eliminate parasitism (e.g. the detection of approaching adults, parasitic eggs and/or hatched chicks [9]). No study has yet examined the role of eye morphology per se in mediating avian host–brood parasite interactions and coevolutionary paths [8]

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