Host defences against avian brood parasitism: an endocrine perspective.
ABSTRACT: Host defences against avian brood parasites are the outcome of well-documented coevolutionary arms races, yet important questions about variation in hosts' antiparasitic response traits remain poorly understood. Why are certain defences employed by some species or individuals and not by others? Here, we propose that understanding variability in and the evolution of host defences can be facilitated by the study of the underlying physiological mechanisms. Specifically, because antiparasitic strategies involve behaviours that have been shown to be hormonally regulated in other contexts, we hypothesize that host responses to brood parasites are likely to be mediated by related endocrine mechanisms. We outline the hallmarks of the endocrine bases of parasite defence-related avian behaviours, review the current understanding of antiparasitic host tactics and propose testable hypotheses about the hormonal mechanisms that may mediate host defences. We consider these mechanisms in a life-history framework and discuss how endocrine factors may shape variation in host defences. By providing a hypothesis-driven mechanistic framework for defences against parasitism, this perspective should stimulate the study of their endocrine bases to enhance our understanding of the intricate arms races in avian host-parasite systems.
Project description:Virulent brood parasites refrain from arduous parental care, often kill host progeny and inflict rearing costs upon their hosts. Quantifying the magnitude of such costs across the whole period of care (from incubation through to parasite fledgling independence) is essential for understanding the selection pressures on hosts to evolve antiparasitic defences. Despite the central importance of such costs for our understanding of coevolutionary dynamics, they have not yet been comprehensively quantified in any host of any avian brood parasite. We quantified parasite-rearing costs in common redstarts Phoenicurus phoenicurus raising either parasitic common cuckoo Cuculus canorus or their own chicks throughout the complete breeding cycle, and used multiple cost parameters for each breeding stage: incubation, brooding and feeding effort; length of parental/host care; parent/host body condition; and heterophil/lymphocyte ratio (stress-level indicator). Contrary to traditional assumptions, rearing the parasite per se was not associated with overall higher physiological or physical costs to hosts above the natural levels imposed by efforts to rear their own progeny. The low parasite-rearing costs imposed on hosts may, in part, explain the low levels of known host counter-defences in this unusually frequently parasitized cuckoo host.
Project description:Maternal inheritance via the female-specific W chromosome was long ago proposed as a potential solution to the evolutionary enigma of co-existing host-specific races (or 'gentes') in avian brood parasites. Here we report the first unambiguous evidence for maternal inheritance of egg colouration in the brood-parasitic common cuckoo Cuculus canorus. Females laying blue eggs belong to an ancient (?2.6 Myr) maternal lineage, as evidenced by both mitochondrial and W-linked DNA, but are indistinguishable at nuclear DNA from other common cuckoos. Hence, cuckoo host races with blue eggs are distinguished only by maternally inherited components of the genome, which maintain host-specific adaptation despite interbreeding among males and females reared by different hosts. A mitochondrial phylogeny suggests that blue eggs originated in Asia and then expanded westwards as female cuckoos laying blue eggs interbred with the existing European population, introducing an adaptive trait that expanded the range of potential hosts.
Project description:Coevolution is often invoked as an engine of biological diversity. Avian brood parasites and their hosts provide one of the best-known examples of coevolution. Brood parasites lay their eggs in the nests of other species, selecting for host defences and reciprocal counteradaptations in parasites. In theory, this arms race should promote increased rates of speciation and phenotypic evolution. Here, we use recently developed methods to test whether the three largest avian brood parasitic lineages show changes in rates of phenotypic diversity and speciation relative to non-parasitic lineages. Our results challenge the accepted paradigm, and show that there is little consistent evidence that lineages of brood parasites have higher speciation or extinction rates than non-parasitic species. However, we provide the first evidence that the evolution of brood parasitic behaviour may affect rates of evolution in morphological traits associated with parasitism. Specifically, egg size and the colour and pattern of plumage have evolved up to nine times faster in parasitic than in non-parasitic cuckoos. Moreover, cuckoo clades of parasitic species that are sympatric (and share similar host genera) exhibit higher rates of phenotypic evolution. This supports the idea that competition for hosts may be linked to the high phenotypic diversity found in parasitic cuckoos.
Project description:Host defences become increasingly costly as parasites breach successive lines of defence. Because selection favours hosts that successfully resist parasitism at the lowest possible cost, escalating coevolutionary arms races are likely to drive host defence portfolios towards ever more expensive strategies. We investigated the interplay between host defence portfolios and social parasite pressure by comparing 17 populations of two Temnothorax ant species. When successful, collective aggression not only prevents parasitation but also spares host colonies the cost of searching for and moving to a new nest site. However, once parasites breach the host's nest defence, host colonies should resort to flight as the more beneficial resistance strategy. We show that under low parasite pressure, host colonies more likely responded to an intruding Protomognathus americanus slavemaker with collective aggression, which prevented the slavemaker from escaping and potentially recruiting nest-mates. However, as parasite pressure increased, ant colonies of both host species became more likely to flee rather than to fight. We conclude that host defence portfolios shift consistently with social parasite pressure, which is in accordance with the degeneration of frontline defences and the evolution of subsequent anti-parasite strategies often invoked in hosts of brood parasites.
Project description: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.
Project description:The spatial distribution of hosts can be a determining factor in the reproductive success of parasites. Highly aggregated hosts may offer more opportunities for reproduction but can have better defences than isolated hosts. Here we connect macro- and micro-evolutionary processes to understand the link between host density and parasitism, using avian brood parasites as a model system. We analyse data across more than 200 host species using phylogenetic comparative analyses and quantify parasitism rate and host reproductive success in relation to spatial distribution using field data collected on one host species over 6 years. Our comparative analysis reveals that hosts occurring at intermediate densities are more likely to be parasitized than colonial or widely dispersed hosts. Correspondingly, our intraspecific field data show that individuals living at moderate densities experience higher parasitism rates than individuals at either low or high densities. Moreover, we show for the first time that the effect of host density on host reproductive success varies according to the intensity of parasitism; hosts have greater reproductive success when living at high densities if parasitism rates are high, but fare better at low densities when parasitism rates are low. We provide the first evidence of the trade-off between host density and parasitism at both macro- and micro-evolutionary scales in brood parasites. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.
Project description:Parasites that exploit multiple hosts often experience diversifying selection for host-specific adaptations. This can result in multiple strains of host specialists coexisting within a single parasitic species. A long-standing conundrum is how such sympatric host races can be maintained within a single parasitic species in the face of interbreeding among conspecifics specializing on different hosts. Striking examples are seen in certain avian brood parasites such as cuckoos, many of which show host-specific differentiation in traits such as host egg mimicry. Exploiting a Zambian egg collection amassed over several decades and supplemented by recent fieldwork, we show that the brood parasitic Greater Honeyguide Indicator indicator exhibits host-specific differentiation in both egg size and egg shape. Genetic analysis of honeyguide eggs and chicks show that two highly divergent mitochondrial DNA lineages are associated with ground- and tree-nesting hosts, respectively, indicating perfect fidelity to two mutually exclusive sets of host species for millions of years. Despite their age and apparent adaptive diversification, however, these ancient lineages are not cryptic species; a complete lack of differentiation in nuclear genes shows that mating between individuals reared by different hosts is sufficiently frequent to prevent speciation. These results indicate that host specificity is maternally inherited, that host-specific adaptation among conspecifics can be maintained without reproductive isolation, and that host specificity can be remarkably ancient in evolutionary terms.
Project description:Mimicry of a harmless model (aggressive mimicry) is used by egg, chick and fledgling brood parasites that resemble the host's own eggs, chicks and fledglings. However, aggressive mimicry may also evolve in adult brood parasites, to avoid attack from hosts and/or manipulate their perception of parasitism risk. We tested the hypothesis that female cuckoo finches (Anomalospiza imberbis) are aggressive mimics of female Euplectes weavers, such as the harmless, abundant and sympatric southern red bishop (Euplectes orix). We show that female cuckoo finch plumage colour and pattern more closely resembled those of Euplectes weavers (putative models) than Vidua finches (closest relatives); that their tawny-flanked prinia (Prinia subflava) hosts were equally aggressive towards female cuckoo finches and southern red bishops, and more aggressive to both than to their male counterparts; and that prinias were equally likely to reject an egg after seeing a female cuckoo finch or bishop, and more likely to do so than after seeing a male bishop near their nest. This is, to our knowledge, the first quantitative evidence for aggressive mimicry in an adult bird, and suggests that host-parasite coevolution can select for aggressive mimicry by avian brood parasites, and counter-defences by hosts, at all stages of the reproductive cycle.
Project description:Obligate brood parasites manipulate other species into raising their offspring. Avian and insect brood parasitic systems demonstrate how interacting species engage in reciprocal coevolutionary arms races through behavioral and morphological adaptations and counteradaptations. Mouthbrooding cichlid fishes are renowned for their remarkable evolutionary radiations and complex behaviors. In Lake Tanganyika, mouthbrooding cichlids are exploited by the only obligate nonavian vertebrate brood parasite, the cuckoo catfish Synodontis multipunctatus. We show that coevolutionary history and individual learning both have a major impact on the success of cuckoo catfish parasitism between coevolved sympatric and evolutionarily naïve allopatric cichlid species. The rate of cuckoo catfish parasitism in coevolved Tanganyikan hosts was 3 to 11 times lower than in evolutionarily naïve cichlids. Moreover, using experimental infections, we demonstrate that parasite egg rejection in sympatric hosts was much higher, leading to seven times greater parasite survival in evolutionarily naïve than sympatric hosts. However, a high rejection frequency of parasitic catfish eggs by coevolved sympatric hosts came at a cost of increased rejection of their own eggs. A significant cost of catfish parasitism was universal, except for coevolved sympatric cichlid species with previous experience of catfish parasitism, demonstrating that learning and individual experience both contribute to a successful host response.
Project description:Classic evolutionary theory predicts that monogamy should be intimately linked with parental care. It has long been assumed, therefore, that avian brood parasites-which lay their eggs in the nests of 'host' species and provide little, if any, parental care-should be overwhelmingly promiscuous. However, recent studies have revealed that the social mating systems of brood parasites are surprisingly diverse, encompassing lek polygyny, monogamy, polygamy and promiscuity. What ecological or phylogenetic factors explain this variation, and why are some brood parasites apparently monogamous? Here we review the social and genetic mating systems of all 75 brood parasitic species for which data are available and evaluate several hypotheses that may help explain these patterns. We find that social monogamy is widespread, often co-occurring with territoriality and cooperative behaviour by the mated pair. Comparative studies, though preliminary, suggest that in some species, monogamy is associated with low host density and polygamy with higher host density. Interestingly, molecular data show that genetic and social mating systems can be entirely decoupled: genetic monogamy can occur in parasitic species that lack behavioural pair-bonds, possibly as a by-product of territoriality; conversely, social monogamy has been reported in parasites that are genetically polygamous. This synthesis suggests that social and genetic monogamy may result from very different selective pressures, and that male-female cooperative behaviours, population density and territoriality may all interact to favour the evolution of monogamous mating in brood parasites. Given that detailed descriptive data of social, and especially genetic, mating systems are still lacking for the majority of brood parasitic species, definitive tests of these hypotheses await future work. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.