Abstract
Arms races between avian brood parasites and their hosts often result in parasitic mimicry of host eggs, to evade rejection. Once egg mimicry has evolved, host defences could escalate in two ways: (i) hosts could improve their level of egg discrimination; and (ii) negative frequency-dependent selection could generate increased variation in egg appearance (polymorphism) among individuals. Proficiency in one defence might reduce selection on the other, while a combination of the two should enable successful rejection of parasitic eggs. We compared three highly variable host species of the Afrotropical cuckoo finch Anomalospiza imberbis, using egg rejection experiments and modelling of avian colour and pattern vision. We show that each differed in their level of polymorphism, in the visual cues they used to reject foreign eggs, and in their degree of discrimination. The most polymorphic host had the crudest discrimination, whereas the least polymorphic was most discriminating. The third species, not currently parasitized, was intermediate for both defences. A model simulating parasitic laying and host rejection behaviour based on the field experiments showed that the two host strategies result in approximately the same fitness advantage to hosts. Thus, neither strategy is superior, but rather they reflect alternative potential evolutionary trajectories.
Highlights
Coevolutionary arms races between parasites and their hosts can be a significant driving force in evolution, and in avian brood parasites have led to substantial changes in phenotypic diversity and behaviour [1]
For tawny-flanked prinias, we found that parasitic eggs were significantly different from host eggs with respect to: (i) one axis of colour (CC2: the level of UV stimulation compared with the other three cone types was higher in parasitic eggs than hosts’), (ii) dispersion, (iii) proportion energy, and (iv) filter size
For red-faced cisticolas, we found that parasitic eggs differed from host eggs with respect to: (i) the other axis of colour (CC1: the level of LW cone stimulation compared with the other three cones was higher in parasitic eggs than hosts’), (ii) luminance, (iii) dispersion, (iv) filter size, and (v) total energy
Summary
Coevolutionary arms races between parasites and their hosts can be a significant driving force in evolution, and in avian brood parasites have led to substantial changes in phenotypic diversity and behaviour [1]. We investigate different evolutionary trajectories involving three cooccurring species: two currently exploited hosts and a third that shows strong egg discrimination behaviour, but is not currently parasitized at our study site This system is appropriate for this investigation owing to its evolutionary age (the cuckoo finch diverged from its closest relatives, the brood parasitic Vidua finches, ca 20 Ma [19]), and owing to the extreme levels of egg colour and pattern polymorphism shown by hosts and, correspondingly, by parasites (figure 1). Simultaneously quantifying multiple different aspects of pattern and colour allows us to identify precisely which visual cues are involved in egg discrimination and polymorphism, and their relative importance These may differ among host species: we have previously found that one host species, the tawnyflanked prinia Prinia subflava, uses cues that reveal the most reliable information about egg identity [18].
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