Ecological uncertainty favours the diversification of host use in avian brood parasites.
ABSTRACT: Adaptive responses to ecological uncertainty may affect the dynamics of interspecific interactions and shape the course of evolution within symbioses. Obligate avian brood parasites provide a particularly tractable system for understanding how uncertainty, driven by environmental variability and symbiont phenology, influences the evolution of species interactions. Here, we use phylogenetically-informed analyses and a comprehensive dataset on the behaviour and geographic distribution of obligate avian brood parasites and their hosts to demonstrate that increasing uncertainty in thermoregulation and parental investment of parasitic young are positively associated with host richness and diversity. Our findings are consistent with the theoretical expectation that ecological risks and environmental unpredictability should favour the evolution of bet-hedging. Additionally, these highly consistent patterns highlight the important role that ecological uncertainty is likely to play in shaping the evolution of specialisation and generalism in complex interspecific relationships.
Project description:Parental care is critical for offspring survival in many species. However, parental behaviors have been lost in roughly 1% of avian species known as the obligate brood parasites. To shed light on molecular and neurobiological mechanisms mediating brood parasitic behavior, we compared brain gene expression patterns between two brood parasitic species and one closely related non-parasitic Icterid (blackbird) species. Our analyses focused on gene expression changes specifically in the preoptic area (POA), a brain region known to play a critical role in parental behavior across vertebrates. Using comparative transcriptomic approaches, we identified gene expression patterns associated with brood parasitism. We evaluated three non-mutually exclusive alternatives for the evolution of brood parasitism: (1) retention of juvenile-like (neotenic) gene expression, (2) reduced expression of maternal care-related genes in the POA, and/or (3) increased expression of genes inhibiting maternal care. We find evidence for neotenic expression patterns in both species of parasitic cowbirds as compared to maternal, non-parasites. In addition, we observed differential expression in a number of genes with previously established roles in mediating maternal care. Together, these results provide the first insight into transcriptomic and genetic mechanisms underlying the loss of maternal behavior in avian brood parasites.
Project description:Interspecific brood parasitism is common in many animal systems. Brood parasites enter the nests of other species and divert host resources for producing their own offspring, which can lead to strong antagonistic parasite-host coevolution. Here, we look at commonalities among social insect species that are victims of brood parasites, and use phylogenetic data and information on geographical range size to predict which species are most probably to fall victims to brood parasites in the future. In our analyses, we focus on three eusocial hymenopteran groups and their brood parasites: (i) bumblebees, (ii) Myrmica ants, and (iii) vespine and polistine wasps. In these groups, some, but not all, species are parasitized by obligate workerless inquilines that only produce reproductive-caste descendants. We find phylogenetic signals for geographical range size and the presence of parasites in bumblebees, but not in ants and wasps. Phylogenetic logistic regressions indicate that the probability of being attacked by one or more brood parasite species increases with the size of the geographical range in bumblebees, but the effect is statistically only marginally significant in ants. However, non-phylogenetic logistic regressions suggest that bumblebee species with the largest geographical range sizes may have a lower likelihood of harbouring social parasites than do hosts with medium-sized ranges. Our results provide new insights into the ecology and evolution of host-social parasite systems, and indicate that host phylogeny and geographical range size can be used to predict threats posed by social parasites, as well to design efficient conservation measures for both hosts and their parasites. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.
Project description:Cuckoos (family Cuculidae) show the highest diversity of breeding strategies within one bird family (parental care, facultative and obligate brood parasites). We used independent contrasts from two phylogenies to examine how this variation was related to 13 ecological and life-history variables. The ancestral state was probably tropical, resident, forest cuckoos with parental care. The evolution of brood parasitism was correlated with a shift to more open habitats, a change in diet, increases in species breeding-range size and migration, and a decrease in egg size. Once parasitism had evolved, more elaborate parasitic strategies (more harmful to host fitness) were correlated with decreased egg size, a change in diet, increased breeding-range size and migration, a shortened breeding season and a decrease in local abundance. Establishing the most probable evolutionary pathways, using the method of Pagel, shows that changes in ecological variables (such as migration, range size and diet type) preceded the evolution of brood parasitism, which is likely to be a later adaptation to reduce the cost of reproduction. By contrast, brood parasitism evolved before changes in egg size occurred, indicating that egg size is an adaptive trait in host--parasite coevolution. Our results suggest that the evolution of cuckoo brood parasitism reflects selection from both ecological pressures and host defences.
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:Interspecific brood parasitism occurs in several independent lineages of birds and social insects, putatively evolving from intraspecific brood parasitism. The cuckoo catfish, Synodontis multipunctatus, the only known obligatory non-avian brood parasite, exploits mouthbrooding cichlid fishes in Lake Tanganyika, despite the absence of parental care in its evolutionary lineage (family Mochokidae). Cuckoo catfish participate in host spawning events, with their eggs subsequently collected and brooded by parental cichlids, though they can later be selectively rejected by the host. One scenario for the origin of brood parasitism in cuckoo catfish is through predation of cichlid eggs during spawning, eventually resulting in a spatial and temporal match in oviposition by host and parasite. Here we demonstrate experimentally that, uniquely among all known brood parasites, cuckoo catfish have the capacity to re-infect their hosts at a late developmental stage following egg rejection. We show that cuckoo catfish offspring can survive outside the host buccal cavity and re-infect parental hosts at a later incubation phase by exploiting the strong parental instinct of hosts to collect stray offspring. This finding implies an alternative evolutionary origin for cuckoo catfish brood parasitism, with the parental response of host cichlids facilitating its evolution. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.
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'.
Project description:Before complex nests evolved, birds laid eggs on the ground, and egg retrieval evolved as an adaptation against accidental displacement of eggs outside the nest. Therefore, egg retrieval is an ancient, and likely ancestral, widespread behaviour in birds. However, it has received little attention in studies of avian brood parasitism, perhaps because most parasitism occurs in species with complex nests, a context in which egg retrieval seems irrelevant. However, for cavity-nesting hosts of avian brood parasites, egg retrieval may still play an important role in the coevolutionary interactions between obligate brood parasites and hosts, because egg retrieval can be considered to be antagonistic to egg rejection behaviour in hosts, yet both may involve cognition to recognize eggs. We hypothesized that (1) cavity-nesting hosts should retrieve misplaced eggs from outside the nest cup, (2) brood parasitism has modulated egg retrieval behaviour in cavity-nesting hosts and (3) hosts use the same visual cues for decision-making during egg recognition in both egg retrieval and egg rejection actions. To test these hypotheses, we performed a series of experiments in a cavity-nesting host, the green-backed tit ( Parus monticolus). Foreign eggs with different levels of mimicry were placed within or outside nest cups of hosts to test their responses. We found that host decisions about whether to retrieve or reject an egg both depended on the degree of mimicry. However, hosts sometimes first retrieved poorly mimetic foreign eggs and then rejected them. Alternatively, hosts sometimes failed to retrieve highly mimetic conspecific eggs. We suggest that egg retrieval in hosts is likely to be a result of the interaction between ancient retrieval behaviour and subsequent adaptation against brood parasitism. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.
Project description:Obligate brood-parasitic cheats have fascinated natural historians since ancient times. Passing on the costs of parental care to others occurs widely in birds, insects and fish, and often exerts selection pressure on hosts that in turn evolve defences. Brood parasites have therefore provided an illuminating system for researching coevolution. Nevertheless, much remains unknown about how ecology and evolutionary history constrain or facilitate brood parasitism, or the mechanisms that shape or respond to selection. In this special issue, we bring together examples from across the animal kingdom to illustrate the diverse ways in which recent research is addressing these gaps. This special issue also considers how research on brood parasitism may benefit from, and in turn inform, related fields such as social evolution and immunity. Here, we argue that progress in our understanding of coevolution would benefit from the increased integration of ideas across taxonomic boundaries and across Tinbergen's Four Questions: mechanism, ontogeny, function and phylogeny of brood parasitism. We also encourage renewed vigour in uncovering the natural history of the majority of the world's brood parasites that remain little-known. Indeed, it seems very likely that some of nature's brood parasites remain entirely unknown, because otherwise we are left with a puzzle: if parental care is so costly, why is brood parasitism not more common? This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.
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: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.