Brown‐headed cowbirds (
Egg rejection is an effective and widespread antiparasitic defense to eliminate foreign eggs from the nests of hosts of brood parasitic birds. Several lines of observational and critical experimental evidence support a role for learning by hosts in the recognition of parasitic versus own eggs; specifically, individual hosts that have had prior or current experience with brood parasitism are more likely to reject foreign eggs. Here we confirm experimentally the role of prior experience in altering subsequent egg-rejection decisions in the American robin Turdus migratorius, a free-living host species of an obligate brood parasite, the brown-headed cowbird Molothrus ater. We then model the coevolutionary trajectory of both the extent of mimicry of host eggs by parasitic eggs and the host’s egg rejection thresholds in response to an increasing role of learning in egg recognition. Critically, with more learning, we see the evolution of both narrower (more discriminating) rejection thresholds in hosts and greater egg mimicry in parasites. Increasing host clutch size (number of eggs/nest) and increasing parasite load (parasitism rate) also have narrowing effects on the egg-rejection threshold. Together, these results suggest that learning from prior experience with egg rejection may play an important role in the coevolution of egg-mimetic lineages of brood parasites and the refined egg rejection defenses of hosts.more » « less
- NSF-PAR ID:
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Evolution Letters
- Medium: X Size: p. 413-421
- ["p. 413-421"]
- Sponsoring Org:
- National Science Foundation
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Brown‐headed cowbirds (
Molothrus ater) are generalist obligate brood parasites, laying in the nest of nearly 300 avian species, and successfully parasitizing well over 100 host species. Cowbird eggs are generally considered non‐mimetic, although some have suggested that cowbird eggs resemble several of their host species’ eggs. To date, no investigation has examined the level of avian‐perceived similarity between cowbird and diverse host eggs in the contexts of light characteristics at the nest and the visual system of the relevant viewer. Because the cowbird exploits a wide range of species that lay in a variety of nest types, hosts view these eggs under an array of light conditions which could facilitate or hinder egg discrimination. When considering the visual system of the relevant viewers and the light conditions at their nest, we found that the coloration of cowbird eggs was more similar to host than non‐host species’ eggs. Host responses (whether they accept or reject cowbird eggs) were not statistically different when hosts perceived a large chromatic difference between their own eggs and the cowbird's eggs. Instead, we found that host responses were predicted by the degree to which nesting light conditions facilitated color similarity between host and cowbird eggs, such that hosts typically nesting under light conditions where this color discrimination task was more challenging were more likely to reject cowbird eggs. This suggests that the nesting light environment may have selected for increased coevolved egg recognition abilities in a suite of cowbird host species, even in the absence of parasitic egg color mimicry.
To avoid mobbing attacks by their hosts during egg laying, some avian brood parasites have evolved traits to visually and/or acoustically resemble predator(s) of their hosts. Prior work established that reed warblers (
Acrocephalus scirpaceus), a small host species of the brood parasitic common cuckoo ( Cuculus canorus), delayed returning to the nest when confronted by either the calls of the female cuckoo or that of the predatory sparrowhawk ( Accipiter nisus). It remains less clear, however, whether female cuckoo calls also suppress the nest defences of larger and more aggressive hosts. Such hosts typically attack vigorously, and can even hurt the brood parasitic intruders, instead of fleeing in the face of danger. Here, we tested whether the female cuckoo calls dampen mobbing intensity in a much larger Acrocephalushost of the common cuckoo, the great reed warbler ( A. arundinaceus). We presented great reed warbler pairs with female common cuckoo models at their nests without and then with playing back the female‐specific bubbling calls of the cuckoo. As controls, we tested the hosts’ responses to harmless collared dove ( Streptopelia decaocto) models, also without and then with the playbacks of dove calls. We found that the playback of female brood parasite calls reduced the aggression of hosts towards the cuckoo models as compared to model presentations without female calls, but we detected no such effect of the control calls with dove models. Our results revealed that female cuckoo calls effectively suppress the antiparasitic responses of great reed warbler hosts, which could aid parasites to approach the nest undiscovered and to evade the costly attacks of this large host. Therefore, the female call can be regarded as a general part of the cuckoo's trickery repertoire for successful parasitism.
Many avian species are negatively impacted by obligate avian brood parasites, which lay their eggs in the nests of host species. The yellow warbler (Setophaga petechia), which is host to the brood-parasitic brown-headed cowbird (Molothrus ater), represents one of the best-replicated study systems assessing antiparasitic host defenses. Over 15 prior studies on yellow warblers have used model-presentation experiments, whereby breeding hosts are exposed to models of brown-headed cowbirds or other nest threats, to test for anti-parasitic defenses unique to this species. Here we present results from our own quasi-replication study of the yellow warbler/brown-headed cowbird system, which used a novel design compared to previous experiments by pivoting to conduct acoustic playback treatments only, rather than presenting visual models with or without calls. We exposed active yellow warbler nests to playbacks of brown-headed cowbird chatters (brood parasite), blue jay (Cyanocitta cristata; nest predator) calls, conspecific “seet” calls (a referential alarm call for brood parasitism risk), conspecific “chip” calls (a generic alarm call), or control wood thrush (Hylocichla mustelina; harmless heterospecific) songs during the incubation stage. Similar to previous studies, we found that female yellow warblers seet called more frequently in response to playbacks of both brood parasitic chatter calls and conspecific seet calls whereas they produced more chip calls in response to the playback of nest predator calls. In contrast, female yellow warblers approached all playbacks to similar distances, which was different from the proximity patterns seen in previous studies. Our study demonstrates the importance of both replicating, and also pivoting, experimental studies on nest defense behaviors, as differences in experimental design can elicit novel behavioral response patterns in the same species.more » « less
Social parasites exploit the brood care behavior of their hosts to raise their own offspring. Social parasites are common among eusocial Hymenoptera and exhibit a wide range of distinct life history traits in ants, bees, and wasps. In ants, obligate inquiline social parasites are workerless (or nearly-so) species that engage in lifelong interactions with their hosts, taking advantage of the existing host worker forces to reproduce and exploit host colonies’ resources. Inquiline social parasites are phylogenetically diverse with approximately 100 known species that evolved at least 40 times independently in ants. Importantly, ant inquilines tend to be closely related to their hosts, an observation referred to as ‘Emery’s Rule’. Polygyny, the presence of multiple egg-laying queens, was repeatedly suggested to be associated with the origin of inquiline social parasitism, either by providing the opportunity for reproductive cheating, thereby facilitating the origin of social parasite species, and/or by making polygynous species more vulnerable to social parasitism via the acceptance of additional egg-laying queens in their colonies. Although the association between host polygyny and the evolution of social parasitism has been repeatedly discussed in the literature, it has not been statistically tested in a phylogenetic framework across the ants. Here, we conduct a meta-analysis of ant social structure and social parasitism, testing for an association between polygyny and inquiline social parasitism with a phylogenetic correction for independent evolutionary events. We find an imperfect but significant over-representation of polygynous species among hosts of inquiline social parasites, suggesting that while polygyny is not required for the maintenance of inquiline social parasitism, it (or factors associated with it) may favor the origin of socially parasitic behavior. Our results are consistent with an intra-specific origin model for the evolution of inquiline social parasites by sympatric speciation but cannot exclude the alternative, inter-specific allopatric speciation model. The diversity of social parasite behaviors and host colony structures further supports the notion that inquiline social parasites evolved in parallel across unrelated ant genera in the formicoid clade via independent evolutionary pathways.
ABSTRACT Some host species of avian obligate brood parasites reject parasitic eggs from their nest whereas others accept them, even though they recognize them as foreign. One hypothesis to explain this seemingly maladaptive behavior is that acceptors are unable to pierce and remove the parasitic eggshell. Previous studies reporting on the force and energy required to break brood parasites' eggshells were typically static tests performed against hard substrate surfaces. Here, we considered host nest as a substrate to simulate this potentially critical aspect of the natural context for egg puncture while testing the energy required to break avian eggshells. Specifically, as a proof of concept, we punctured domestic chicken eggs under a series of conditions: varying tool shape (sharp versus blunt), tool dynamics (static versus dynamic) and the presence of natural bird nests (of three host species). The results show a complex set of statistically significant interactions between tool shapes, puncture dynamics and nest substrates. Specifically, the energy required to break eggs was greater for the static tests than for the dynamic tests, but only when using a nest substrate and a blunt tool. In turn, in the static tests, the addition of a nest significantly increased energy requirements for both tool types, whereas during dynamic tests, the increase in energy associated with the nest presence was significant only when using the sharp tool. Characterizing the process of eggshell puncture in increasingly naturalistic contexts will help in understanding whether and how hosts of brood parasites evolve to reject foreign eggs.more » « less