Prolactin mediates behavioural rejection responses to avian brood parasitism

Adaptations resulting from co-evolutionary interactions between avian brood parasites and their hosts have been extensively studied, yet the physiological mechanisms underlying antiparasitic host defences remain little known. Prolactin, one of the main hormones involved in the regulation of avian parental behaviour, might play a key role in the orchestration of the host responses to avian brood parasitism. Given the positive association between prolactin and parental behaviour during incubation, decreasing prolactin levels are expected to facilitate egg-rejection decisions. We tested this prediction by implanting Eurasian blackbird (Turdus merula) females with an inhibitor of prolactin secretion, bromocriptine mesylate, to experimentally decrease their plasma prolactin levels. Bromocriptine-implanted individuals ejected mimetic model eggs at higher rates, and showed shorter latency to egg ejection, than placebo-treated birds. To our knowledge, this is the first experimental evidence that behavioural host defences against avian brood parasitism are mediated by prolactin.

The neuroethology of avian brood parasitism

ABSTRACT Obligate brood-parasitic birds never build nests, incubate eggs or supply nestlings with food or protection. Instead, they leave their eggs in nests of other species and rely on host parents to raise their offspring, which allows the parasite to continue reproducing throughout the breeding season. Although this may be a clever fitness strategy, it is loaded with a set of dynamic challenges for brood parasites, including recognizing individuals from their own species while growing up constantly surrounded by unrelated individuals, remembering the location of potential host nests for successful reproduction and learning the song of their species while spending time being entirely surrounded by another species during a critical developmental period, a predicament that has been likened to being ‘raised by wolves’. Here, I will describe what we currently know about the neurobiology associated with the challenges of being a brood parasite and what is known about the proximate mechanisms of brood parasite evolution. The neuroethology of five behaviors (mostly social) in brood parasites is discussed, including: (1) parental care (or the lack thereof), (2) species recognition, (3) song learning, (4) spatial memory and (5) pair-bonding and mate choice. This Review highlights how studies of brood parasites can lend a unique perspective to enduring neuroethological questions and describes the ways in which studying brood-parasitic species enhances our understanding of ecologically relevant behaviors.

A Meta-Analysis of Avian Egg Traits Cueing Egg-Rejection Defenses Against Brood Parasitism

The capability of hosts to reject the odd egg from their nest is one of the key defenses against avian brood parasitism. Considerable research effort has been devoted to exploring which phenotypic traits of eggshells facilitate to cue the recognition of the parasitic egg. Here we have reviewed studies addressing salient egg traits involved in the rejection of foreign eggs and used a formal meta-analysis to quantify their relative importance. Hosts appear to rely to a large extent on eggshell color traits, followed by maculation patterns. Hosts respond with similar rates of egg rejection to natural vs. model eggs and when breeding in both closed and open nests. Analyses of experiments on hosts of Cuculus and Molothrus parasites, the two best studied brood parasitic lineages with different co-evolutionary histories, yield similar conclusions. We also identify several poorly studied potential egg recognition cues, such as odor or weight, and recommend exploring even the visual traits in more detail, including chromatic and achromatic contrasts or experimentally manipulated egg maculation characteristics. Recent technological and sensory ecological advances open many new research avenues to experimentally examine the role of diverse egg characteristics in antiparasite defenses.

Variations of Hawk Mimicry Traits in the Four Sympatric Cuculus Cuckoos

A well-known visual signal, hawk-like features such as yellow eyes and feet, and barred underparts have been recognized as coevolutionary traits obtained against host defense in Cuculus cuckoos. However, the variation of these traits within and among species remains poorly understood because empirical studies quantifying these traits are limited in terms of the number of studies and the number of species concerned, and mostly depend on museum collections. In this study, we quantified and compared these traits as well as other new features (e.g., inner wing spot and underpart background color) in the four sympatric Cuculus cuckoos (Cuculus poliocephalus, Cuculus micropterus, Cuculus optatus, and Cuculus canorus) that were wild-captured in South Korea. We found that the yellow color of the eye ring and feet was fairly consistent across the four species. However, the iris color appeared to vary within a species (e.g., between sexes) and varied more substantially among species from nearly black in C. micropterus to bright yellow in C. canorus. In addition, there were significant differences among species with respect to the thickness of the underpart bars, from the thinnest in C. canorus to the thickest in C. micropterus. We also found that the underpart color (pure white versus yellowish brown) and the number of inner wing spots varied within and among species. These results indicate that although hawk-like traits are widely present in Cuculus cuckoos, detailed quantitative features of these traits vary across species. We discuss the potential reasons that generate such variations and suggest future directions to increase our understanding of visual signals in avian brood parasitism.

Impact of nest sanitation behavior on hosts’ egg rejection: An empirical study and meta-analyses

Egg rejection in birds is a specific adaptation toward avian brood parasitism, while nest sanitation is a general behavior for cleaning the nest and avoiding predation. However, both behaviors refer to the action of ejecting objects out of the nest, and nest sanitation has been proposed as a pre-adaptation for egg rejection. Here we tested the eliciting effect of nest sanitation on egg rejection in the red-whiskered bulbul Pycnonotus jocosus, a potential host species that is sympatric with parasitic cuckoos. We conducted meta-analyses of previous studies on both nest sanitation and egg rejection, in order to evaluate the consistency of our conclusions. Our results showed that nest sanitation did not elicit egg rejection in P. jocosus. The conclusions concerning such an eliciting effect from previous studies were mixed, while the methodologies were inconsistent, making the studies unsuitable for comparisons. However, the ejection frequency of nest sanitation was consistently higher than the frequency of egg rejection across different host species or populations. These results suggest that nest sanitation, which is an ancient behavior, is more fundamental than egg rejection, but the effect of the former on the latter is complex and needs further study. Standardized methodologies and the integration of behavior, physiology, and modeling may provide better opportunities to explore the relationship between nest sanitation and egg rejection.

An Experimental Test of Defenses Against Avian Brood Parasitism in a Recent Host

Theoretical studies predict that hosts of avian brood parasites should evolve defenses against parasitism in a matter of decades. However, opportunities to test these predictions are limited because brood parasites rarely switch to naïve hosts. Here, we capitalize on a recent host switch by the brood-parasitic Pacific Koel (Eudynamys orientalis) in eastern Australia, to investigate how quickly the Red Wattlebird (Anthochaera carunculata), a recent host that has been annexed by the koel within the last 90 years, can learn to recognize and mob adult cuckoos and evolve the ability to eject parasite eggs. Pacific Koel nestlings kill all host young, so there should be strong selection for hosts to evolve defenses. However, low parasitism rates and high egg recognition costs might slow the spread of egg ejection in our study populations, while adult parasite recognition should be able to spread more rapidly, as this defense has been shown to be a learned trait rather than a genetically inherited defense. We tested Red Wattlebirds at two sites where parasitism rate differed. As predicted, we found that the Red Wattlebird showed little or no ability to eject foreign model eggs at either site, whereas two historical hosts showed high levels of egg ejection at both sites. However, Red Wattlebirds responded significantly more aggressively to a koel mount than to mounts of a harmless control and nest predator at the site with the higher parasitism rate and gave significantly more alarm calls overall toward the koel mount. Our results support previous evidence that recognition and mobbing of a brood parasite are learned traits and may be especially beneficial to naïve hosts that have not had enough time or a high enough selection pressure to evolve egg rejection.

Coevolution of acoustical communication between obligate avian brood parasites and their hosts

The mutually antagonistic processes producing adaptations and counter-adaptations in avian brood parasites and their hosts provide a model system for the study of coevolution; this topic has long been an area of focus in ornithology and evolutionary biology. Although there is an extensive body of literature dealing with avian brood parasitism, few empirical studies have considered the effects of the coevolutionary processes associated with brood parasitism on the acoustic characteristics of parent–offspring communication. Under the strong selection pressures associated with brood parasitism, parasitic birds may, for instance, produce deceptive songs. The host may in turn evolve the ability to recognize these sounds as deceptive. At present, the mechanisms underlying the different competitive strategies employed by hosts and parasitic birds remain unclear. Here, we reviewed previous studies that investigated acoustic traits in scenarios of brood parasitism, highlighting possible adaptive functions. Using a meta-analysis, we identified no heterogeneity among studies of begging call adaptations in parasitic nestlings. However, our results may have been affected by the small number of applicable papers available for analysis. Our meta-analysis also suggested that studies of acoustic communication and transmission in adult hosts were highly heterogenous, suggesting that research methods were inconsistent among studies. Finally, we identified knowledge gaps and proposed several lines of future research.