Canchao Yang

Are cuckoos maximizing egg mimicry by selecting host individuals with better matching egg phenotypes

Background Avian brood parasites and their hosts are involved in complex offence-defense coevolutionary arms races. The most common pair of reciprocal adaptations in these systems is egg discrimination by hosts and egg mimicry by parasites. As mimicry improves, more advanced host adaptations evolve such as decreased intra- and increased interclutch variation in egg appearance to facilitate detection of parasitic eggs. As interclutch variation increases, parasites able to choose hosts matching best their own egg phenotype should be selected, but this requires that parasites know their own egg phenotype and select host nests correspondingly. Methodology/Principal Findings We compared egg mimicry of common cuckoo Cuculus canorus eggs in naturally parasitized marsh warbler Acrocephalus palustris nests and their nearest unparasitized conspecific neighbors having similar laying dates and nest-site characteristics. Modeling of avian vision and image analyses revealed no evidence that cuckoos parasitize nests where their eggs better match the host eggs. Cuckoo eggs were as good mimics, in terms of background and spot color, background luminance, spotting pattern and egg size, of host eggs in the nests actually exploited as those in the neighboring unparasitized nests. Conclusions/Significance We reviewed the evidence for brood parasites selecting better-matching host egg phenotypes from several relevant studies and argue that such selection probably cannot exist in host-parasite systems where host interclutch variation is continuous and overall low or moderate. To date there is also no evidence that parasites prefer certain egg phenotypes in systems where it should be most advantageous, i.e., when both hosts and parasites lay polymorphic eggs. Hence, the existence of an ability to select host nests to maximize mimicry by brood parasites appears unlikely, but this possibility should be further explored in cuckoo-host systems where the host has evolved discrete egg phenotypes.

Nest defenses and egg recognition of yellow-bellied prinia against cuckoo parasitism

Parasites may, in multi-parasite systems, block the defenses of their hosts and thus thwart host recognition of parasites by frequency-dependent selection. Nest defenses as frontline may block or promote the subsequent stage of defenses such as egg recognition. We conducted comparative studies of the defensive strategies of a host of the Oriental cuckoo Cuculus optatus, the yellow-bellied prinia Prinia flaviventris, in mainland China with multiple species of cuckoos and in Taiwan with a single cuckoo species. Cuckoo hosts did not exhibit aggression toward cuckoos in the presence of multiple cuckoo species but showed strong aggressive defenses of hosts directed toward cuckoos in Taiwan. Furthermore, the cuckoo host in populations with a single cuckoo species was able to distinguish adults of its brood parasite, the Oriental cuckoo, from adult common cuckoos (Cuculus canorus). This represents the first case in which a cuckoo host has been shown to specifically distinguish Oriental cuckoo, from other Cuculus species. Hosts ejected eggs at a higher rate in a single cuckoo species system than in a multi-species cuckoo system, which supports the strategy facilitation hypothesis. Granularity analysis of variation in egg phenotype based on avian vision modeling supported the egg signature hypothesis in hosts because Taiwanese prinias increased consistency in the appearance of their eggs within individual hosts thus favoring efficient discrimination against cuckoo eggs. This study significantly improves our knowledge of intraspecific variation in antiparasitism behavior of hosts between single- and multi-cuckoo systems.

Avoiding parasitism by breeding indoors: cuckoo parasitism of hirundines and rejection of eggs

Brood parasitism is costly to hosts, and, therefore, a number of anti-parasite defenses have evolved. Surprisingly, several high-quality hosts such as martins and swallows are rarely parasitized, raising the question why that is the case. We hypothesize that martins and swallows may avoid parasitism by breeding in close association with humans, and by building nests that are inaccessible for common cuckoos Cuculus canorus and other brood parasites. Here we show using egg rejection experiments that red-rumped swallows Hirundo daurica, house martins Delichon urbica, and barn swallows Hirundo rustica in Europe do not reject foreign eggs placed in their nests, while barn swallows in China often reject foreign eggs. The frequency of parasitism of barn swallows in Europe was significantly higher than in house martins relative to the expectation based on the abundance of the two species. Barn swallows in Europe that were parasitized by cuckoos more often placed their nests outdoors than expected by chance, suggesting that avoidance of cuckoo parasitism can be achieved by breeding indoors. These findings suggest that barn swallows in China have gained egg rejection behavior because they cannot avoid parasitism when breeding outdoors.

Egg color variation, but not egg rejection behavior, changes in a cuckoo host breeding in the absence of brood parasitism

Interactions between parasitic cuckoos and their songbird hosts form a classical reciprocal “arms race,” and are an excellent model for understanding the process of coevolution. Changes in host egg coloration via the evolution of interclutch variation in egg color or intraclutch consistency in egg color are hypothesized counter adaptations that facilitate egg recognition and thus limit brood parasitism. Whether these antiparasitism strategies are maintained when the selective pressure of parasitism is relaxed remains debated. However, introduced species provide unique opportunities for testing the direction and extent of natural selection on phenotypic trait maintenance and variation. Here, we investigated egg rejection behavior and egg color polymorphism in the red-billed leiothrix (Leiothrix lutea), a common cuckoo (Cuculus canorus) host, in a population introduced to Hawaii 100 years ago (breeding without cuckoos) and a native population in China (breeding with cuckoos). We found that egg rejection ability was equally strong in both the native and the introduced populations, but levels of interclutch variation and intraclutch consistency in egg color in the native population were higher than in the introduced population. This suggests that egg rejection behavior in hosts can be maintained in the absence of brood parasitism and that egg appearance is maintained by natural selection as a counter adaptation to brood parasitism. This study provides rare evidence that host antiparasitism strategies can change under parasite-relaxed conditions and reduced selection pressure.

Extreme levels of hunting of birds in a remote village of Hainan Island, China.

In China, many bird species are generally thought to be threatened mainly, or at least partly, by hunting. However, there have been few studies of bird hunting at a local scale. Bird hunting and trade in Nanmao, a remote mountainous village of Hainan Island, China, was investigated during March–July 2003 and September–October 2005. In total, 86 households were visited, of which 43% reported that they engaged in hunting of birds while 91% of households were seen to have hunted birds or hunting tools. This indicated that hunting by village people was widespread. Most hunters were male, and were between 12 and 68 years old. A total of 78 bird species were hunted, including 2 First Class and 19 Second Class national protected species. This extreme level of hunting has changed from a more moderate subsistence hunting tradition since about 1980, when local urban markets for wild meat started to develop. We outline a strategic plan designed to conserve birds, other wildlife and their forest habitats, whilst improving the livelihoods and preserving the minority tribal traditions of the people of Nanmao forest.

Nest sanitation behavior in hirundines as a pre-adaptation to egg rejection to counter brood parasitism

Previous studies suggested that nest sanitation behavior may have been a pre-adaptation from which egg rejection of brood parasite eggs evolved. We tested this hypothesis in two swallow species, the red-rumped swallow (Cecropis daurica) and the barn swallow (Hirundo rustica). Our results indicated that the red-rumped swallow, which is an accepter of foreign eggs, rejected a low percentage of non-egg-shaped objects and did so less often than the barn swallow, which is an intermediate rejecter of foreign eggs. Furthermore, the egg rejection rates of the barn swallow increased with the increase in rejection rates of non-egg-shaped objects among different populations. These results showed that nest cleaning behavior could have evolved into a means of reducing the costs of brood parasitism, suggesting that egg recognition ability has evolved from recognition of non-egg-shaped objects. This finding advances our understanding of the evolution of egg recognition behavior in birds.

Modelling the maintenance of egg polymorphism in avian brood parasites and their hosts

In avian brood parasitism, egg phenotype plays a key role for both host and parasite reproduction. Several parrotbill species of the genus Paradoxornis are parasitized by the common cuckoo Cuculus canorus, and clear polymorphism in egg phenotype is observed. In this article, we develop a population genetics model in order to identify the key parameters that control the maintenance of egg polymorphism. The model analyses show that egg polymorphism can be maintained either statically as an equilibrium or dynamically with frequency oscillations depending on the sensitivity of the host against unlike eggs and how the parasite targets host nests with specific egg phenotypes. On the basis of the model, we discuss egg polymorphism observed in parrotbills and other host species parasitized by the cuckoo. We suggest the possibility that frequencies of egg phenotypes oscillate and we appeal for monitoring of cuckoo–host interactions over a large spatiotemporal scale.

Nestling recognition in red-rumped and barn swallows

Nestling recognition and rejection is a rare defense strategy against avian brood parasitism that was previously thought to be too costly to evolve. Recently, several examples of nestling recognition and rejection by fosterers have been reported. Here, we tested for chick recognition ability in red-rumped swallows (Hirundo daurica), which build closed nests and do not discriminate against foreign eggs, by using cross-fostering experiments while controlling for responses to intraspecific and interspecific parasitism in closely related swallow species. We show that red-rumped swallows do not discriminate against conspecific or barn swallow (H. rustica) nestlings, but eject or reject cuckoo nestlings cross-fostered in red-rumped swallow nests by starving the introduced chicks to death. Assuming that the behavior of red-rumped swallows evolved in response to cuckoo parasitism, this study represents novel empirical evidence showing that chick discrimination evolved when brood parasites have completely evaded host defenses at the egg stage. The evolution of such recognition ability may be explained as a defense against avian brood parasitism by small-sized cuckoos or a pre-adaptation to specific communication between host parents and offspring. Our results are consistent with the “rarer enemy” hypothesis predicting that nestling discrimination should evolve only in hosts that accept all naturally laid parasite eggs and thus do not decrease effective parasitism rate at the nestling stage. In contrast, the findings were inconsistent with a number of alternative hypotheses.

Variation in Russet Sparrow (Passer cinnamomeus) Breeding Biology in Relation to Small-Scale Altitudinal Differences in China

Evolution of avian life histories is typically strongly influenced by both altitude and latitude. To date, most studies have investigated the effects of extreme differences in altitude and latitude on variation in reproductive traits. Studies based on small altitude and latitude spans are needed to better understand the resolution of selective pressures. We compared several aspects of russet sparrow (Passer cinnamomeus) breeding biology between a low-altitude (200 m) and a high-altitude (1,500 m) population in China, representing a relatively small altitudinal gradient (1,300 m). High-altitude birds initiated breeding significantly later compared to their low-altitude counterparts. Interestingly, breeding season was significantly longer in the high-altitude site (57 vs. 84 d). Lowland sparrows laid larger clutches (4.92 vs. 4.09 eggs) and showed greater fledging success (4.20 vs. 3.46 fledgings) than did upland birds. Variation in life history traits thus appears to occur even along a smallscale altitudinal gradient. We suggest that the longer breeding season and smaller clutch size in the highland population may be an adaptation or acclimation to compensate for the reduced annual productivity resulting from unfavourable or sub-optimal habitats for these sparrows.

Egg recognition as antiparasitism defence in hosts does not select for laying of matching eggs in parasitic cuckoos

Recent studies have suggested that parasitic cuckoos have evolved laying behaviour resulting in matching of host and cuckoo eggs by choosing to lay eggs in host nests with host eggs that match the cuckoo eggs as an adaptation against egg recognition by the hosts. However, previous studies provided weak and indirect evidence with mixed results, leaving this question unresolved. Here, for the first time, we developed a robust methodology to provide unambiguous evidence that egg recognition in the host does not select for optimal egg matching during laying by the cuckoo. By using experiments that attracted parasitism, we showed that cuckoos, Cuculus canorus, indiscriminately laid eggs in oriental reed warbler, Acrocephalus orientalis, host nests containing real host eggs, egg-shaped models, stick models or coin models without any preference. Furthermore, cuckoos only selected to lay their eggs in nests with active hosts. These experiments provide evidence of cuckoos being indiscriminate in their choice of host nests, implying that coevolution of the egg phenotype of host and cuckoo eggs must have arisen from mechanisms other than matching of host eggs and those of the parasite.