Social learning of a brood parasite by its host

Arms races between brood parasites and their hosts provide model systems for studying the evolutionary repercussions of species interactions. However, how naive hosts identify brood parasites as enemies remains poorly understood, despite its ecological and evolutionary significance. Here, we investigate whether young, cuckoo-naive superb fairy-wrens, Malurus cyaneus, can learn to recognize cuckoos as a threat through social transmission of information. Naive individuals were initially unresponsive to a cuckoo specimen, but after observing conspecifics mob a cuckoo, they made more whining and mobbing alarm calls, and spent more time physically mobbing the cuckoo. This is the first direct evidence that naive hosts can learn to identify brood parasites as enemies via social learning.     

A quantitative trait locus for recognition of foreign eggs in the host of a brood parasite

Avian brood parasites reduce the reproductive output of their hosts and thereby select for defence mechanisms such as ejection of parasitic eggs. Such defence mechanisms simultaneously select for counter-defences in brood parasites, causing a coevolutionary arms race. Although coevolutionary models assume that defences and counter-defences are genetically influenced, this has never been demonstrated for brood parasites. Here, we give strong evidence for genetic differences between ejector and nonejectors, which could allow the study of such host defence at the genetic level, as well as studies of maintenance of genetic variation in defences. Briefly, we found that magpies, that are the main host of the great spotted cuckoo in Europe, have alleles of one microsatellite locus (Ase64) that segregate between accepters and rejecters of experimental parasitic eggs. Furthermore, differences in ejection rate among host populations exploited by the brood parasite covaried significantly with the genetic distance for this locus.     

Persistence of host defence behaviour in the absence of avian brood parasitism

The fate of host defensive behaviour in the absence of selection from brood parasitism is critical to long-term host-parasite coevolution. We investigated whether New World Bohemian waxwings Bombycilla garrulus that are allopatric from brown-headed cowbird Molothrus ater and common cuckoo Cuculus canorus parasitism have retained egg rejection behaviour. We found that egg rejection was expressed by 100 per cent of Bohemian waxwings. Our phylogeny revealed that Bohemian and Japanese waxwings Bombycilla japonica were sister taxa, and this clade was sister to the cedar waxwing Bombycilla cedrorum. In addition, there was support for a split between Old and New World Bohemian waxwings. Our molecular clock estimates suggest that egg rejection may have been retained for 2.8-3.0 Myr since New World Bohemian waxwings inherited it from their common ancestor with the rejecter cedar waxwings. These results support the 'single trajectory' model of host-brood parasite coevolution that once hosts evolve defences, they are retained, forcing parasites to become more specialized over time.     

The evolution of egg size in the brood parasitic cuckoos

We compared genera of nonparasitic cuckoos and two groups ofparasitic cuckoos: those raised together with host young ("nonejectors")and those in which the newly hatched cuckoo either ejects thehost eggs or chicks, or kills the host young ("ejectors"). Nonejectorsare similar to their hosts in body size and parasitize largerhosts than do ejectors, which parasitize hosts much smallerthan themselves. In both types of parasite, the cuckoo's eggtends to match the host eggs in size. To achieve this, nonejectorshave evolved a smaller egg for their body size than have nonparasiticcuckoos, and ejectors have evolved an even smaller egg. Amongejector cuckoo genera, larger cuckoos have larger eggs relativeto the eggs of their hosts, and the relationship between cuckooegg volume (mass of the newly-hatched cuckoo) and host egg volume(mass to be ejected) did not differ from that predicted by weight-liftingallometry. However, comparing among Cuculus cuckoo species,the allometric slope differed from the predicted, so it is notclear that egg size is related to the need to give the cuckoochick sufficient strength for ejection. Comparing the two mostspeciose ejector genera, Chrysococcyx cuckoos (smaller and parasitizedome-nesting hosts) lay eggs more similar in size to their host'seggs than do Cuculus cuckoos (larger and parasitize open cup–nestinghosts). Closer size-matching of host eggs in Chrysococcyx mayreflect the following: (1) selection to reduce adult body massto facilitate entry through small domed nest holes to lay, and(2) less need for a large egg, because longer incubation periodsin dome-nesting hosts allow the young cuckoo more time to growbefore it need eject host eggs.     

Hosts of avian brood parasites have evolved egg signatures with elevated information content

Hosts of brood-parasitic birds must distinguish their own eggs from parasitic mimics, or pay the cost of mistakenly raising a foreign chick. Egg discrimination is easier when different host females of the same species each lay visually distinctive eggs (egg ‘signatures’), which helps to foil mimicry by parasites. Here, we ask whether brood parasitism is associated with lower levels of correlation between different egg traits in hosts, making individual host signatures more distinctive and informative. We used entropy as an index of the potential information content encoded by nine aspects of colour, pattern and luminance of eggs of different species in two African bird families (Cisticolidae parasitized by cuckoo finches Anomalospiza imberbis, and Ploceidae by diederik cuckoos Chrysococcyx caprius). Parasitized species showed consistently higher entropy in egg traits than did related, unparasitized species. Decomposing entropy into two variation components revealed that this was mainly driven by parasitized species having lower levels of correlation between different egg traits, rather than higher overall levels of variation in each individual egg trait. This suggests that irrespective of the constraints that might operate on individual egg traits, hosts can further improve their defensive ‘signatures'' by arranging suites of egg traits into unpredictable combinations.     

A comparative analysis of the evolution of variation in appearance of eggs of European passerines in relation to brood parasitism

Host of brood parasites increase the ability of rejecting cuckooeggs by production of (1) a clutch with little variation amongeggs and (2) a clutch that differs the most from the modal phenotypeof the population. These hypotheses have been tested by Øienet at. (1995), although they did not control for common phylogeneticancestry. We analyze the evolution of egg color and markingpatterns in European passerines, which are potential hosts ofdie European cuckoo (Cuculus canorus), using Felsenstein's (1985)independent comparative method to control for the effect ofcommon phylogenetic descent We found a significant positiverelationship between interclutch variation in appearance ofhost eggs and parasitism rate, but this relationship disappearedwhen hole-nesting species were excluded from the analysis; andwe found a highly significant multiple regression between rejectionrate and intra- and interclutch variation in egg appearance,even when hole nesters were excluded from the analysis. Thepartial correlation coefficients were negative for intraclutchvariation and positive with interclutch variation in agreementwidi the hypotheses. Therefore, the use of the independent comparativemethod strengthens the hypothesis that the evolution of eggpatterns in hosts is associated with different stages of coevolutionwith the brood parasite.     

鸟类巢寄生伤害理论的进化

鸟类巢寄生的寄主无论是成乌还是雏鸟,对宿主都是极具伤害性的,因为它们降低了宿主的生育力,然而,无论是在寄主种内还是种间,其伤害性的差异变化很大。综述了以往对这种伤害性差异的各种解释,以往的解释在很大程度上集中在伤害性所带来的利益。认为寄主的伤害性行为可以像病原体的伤害性一样进行分类,伤害性在为寄主带来利益的同时,也伴随着代价,所以,由病原体伤害性进化研究衍生而来的平衡假说,适用于解释鸟类巢寄生伤害理论的进化。     

A stab in the dark: chick killing by brood parasitic honeyguides

The most virulent avian brood parasites obligately kill host young soon after hatching, thus ensuring their monopoly of host parental care. While the host eviction behaviour of cuckoos (Cuculidae) is well documented, the host killing behaviour of honeyguide (Indicatoridae) chicks has been witnessed only once, 60 years ago, and never in situ in host nests. Here, we report from the Afrotropical greater honeyguide the first detailed observations of honeyguides killing host chicks with their specially adapted bill hooks, based on repeated video recordings (available in the electronic supplementary material). Adult greater honeyguides puncture host eggs when they lay their own, but in about half of host nests at least one host egg survived, precipitating chick killing by the honeyguide hatchling. Hosts always hatched after honeyguide chicks, and were killed within hours. Despite being blind and in total darkness, honeyguides attacked host young with sustained biting, grasping and shaking motions. Attack time of 1-5 min was sufficient to cause host death, which took from 9 min to over 7 h from first attack. Honeyguides also bit unhatched eggs and human hands, but only rarely bit the host parents feeding them.     

On the origin of brood parasitism in altricial birds

The probability that obligate interspecific brood parasitism(OP), among altricial birds evolved directly from the normalbreeding (no parasitism, NP) mode or indirectly through intraspecificnest parasitism (INP) was examined by using maximum-likelihoodand parsimony approaches. We examined the probability of ancestralstates at 24 key nodes in order to test our hypotheses. Thestate of the most basal node in a tree of 565 genera of altricialbirds is equivocal; however, the state probability of NP atthis node is about 5.5-fold more likely than the state of obligateparasite. A similar trend was observed for basal nodes of mostfamilies examined. The INP state was supported only in the Hirundinidae.The high incidence of INP among martins and swallows explainsthis finding. Contrary to our predictions, even in other groupswhere there is a high incidence of INP and OP, such as in thetribe Icteri and the Old World finches, the probability of NPbeing ancestral was very high. We conclude that in all casesbut one (Hirundinidae) obligate, and probably facultative, broodparasitism evolved directly from normal breeding mode ratherthan indirectly through some other form of parasitism.