Understanding the Loss of Maternal Care in Avian Brood Parasites Using Preoptic Area Transcriptome Comparisons in Brood Parasitic and Non-parasitic Blackbirds.
ABSTRACT: 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:The original life-history strategy of brood-parasitic birds has been the focus of a large number of studies in ecology and evolution. Whether species adopting such a strategy differ in their response to global changes remains, however, unknown. Both the absence of investment in parental care and the capacity to spread nesting failure by laying eggs in several nests might help brood parasites in dealing with environmental changes. Alternatively, brood parasites might cumulate the negative effects of environmental changes on their own environment and on their hosts' environment. Here, I tested whether brood parasites' extinction risk and population trend differed from those of species with parental care. Focusing on the five bird families containing brood parasite species, I show that brood parasites are less at risk of extinction, and have a more stable population trend than species with parental care. In addition, I found that brood parasites with a higher host diversity were more likely to be increasing than those with fewer hosts. The bet-hedging strategy of brood parasites, by allowing them to spread nesting failure risks associated with environmental changes, is likely to help them resist current global changes.
Project description:The fitness and virulence of parasites is often determined by how many resources they can wrangle out of their hosts. Host defenses that help to keep resources from the parasites will then reduce virulence and parasite fitness. Here, we study whether host brood care and brood size regulation can protect host fitness and harm a parasite. We use the biparental brood-caring burying beetle Nicrophorus vespilloides and its phoretic Poecilochirus carabi mites as a model. Since paternal brood care does not seem to benefit the offspring in a clean laboratory setting, the male presence has been suggested to strengthen the defense against parasites. We manipulated male presence and found no effect on the fitness of the parasitic mites or the beetle offspring. We further manipulated beetle brood size and found larger broods to reduce parasite fitness. The specific pattern we observed suggests that beetle larvae are strong competitors and consume the carrion resource before all parasites develop. They thus starve the parasites. These results shed new light on the observation that the parasites appear to reduce host brood size early on-potentially to avert later competition their offspring might have to face.
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: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: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:Offspring ornamentation typically occurs in taxa with parental care, suggesting that selection arising from social interactions between parents and offspring may underlie signal evolution. American coot babies are among the most ornamented offspring found in nature, sporting vividly orange-red natal plumage, a bright red beak, and other red parts around the face and pate. Previous plumage manipulation experiments showed that ornamented plumage is favored by strong parental choice for chicks with more extreme ornamentation but left unresolved the question as to why parents show the preference. Here we explore natural patterns of variation in coot chick plumage color, both within and between families, to understand the context of parental preference and to determine whose fitness interests are served by the ornamentation. Conspecific brood parasitism is common in coots and brood parasitic chicks could manipulate hosts by tapping into parental choice for ornamented chicks. However, counter to expectation, parasitic chicks were duller (less red) than nonparasitic chicks. This pattern is explained by color variation within families: Chick coloration increases with position in the egg-laying order, but parasitic eggs are usually the first eggs a female lays. Maternal effects influence chick coloration, but coot females do not use this mechanism to benefit the chicks they lay as parasites. However, within families, chick coloration predicts whether chicks become "favorites" when parents begin control over food distribution, implicating a role for the chick ornamentation in the parental life-history strategy, perhaps as a reliable signal of a chick's size or age.
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: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:Avian brood parasitism is an exceptional reproductive strategy whereby parasites reduce their own costs associated with parental care and impose them on the host parents. Consequently, host species have evolved multiple defensive mechanisms to combat parasitism. The vast majority of research attention to date has examined host defenses to recognize and reject parasitic eggs. The recently proposed "egg arrangement hypothesis" suggests that hosts may not focus solely on individual eggs' features, but instead the overall arrangement of the clutch may also provide a cue that parasitism has occurred. Correlative data revealed that host females maintaining a consistent egg arrangement across the incubation period were more likely to reject foreign egg models than females that did not keep a consistent egg arrangement. Here, we provide the first experimental test of this hypothesis in the European blackbird (Turdus merula). We experimentally parasitized nests such that the egg arrangement was either disrupted or not disrupted. We found no evidence that altered egg arrangement was used as a cue for egg rejection by host females. Therefore, we suggest that females that keep consistent egg arrangement are more likely to eject foreign eggs for other correlated reasons. Thus, egg arrangement does not serve as an independent cue to trigger egg rejection responses to parasitism in this host species.
Project description:Avian brood parasites lay their eggs in the nests of other birds, and impose the costs associated with rearing parasitic young onto these hosts. Many hosts of brood parasites defend against parasitism by removing foreign eggs from the nest. In systems where parasitic eggs mimic host eggs in coloration and patterning, extensive intraclutch variation in egg appearances may impair the host's ability to recognize and reject parasitic eggs, but experimental investigation of this effect has produced conflicting results. The cognitive mechanism by which hosts recognize parasitic eggs may vary across brood parasite hosts, and this may explain variation in experimental outcome across studies investigating egg rejection in hosts of egg-mimicking brood parasites. In contrast, for hosts of non-egg-mimetic parasites, intraclutch egg color variation is not predicted to co-vary with foreign egg rejection, irrespective of cognitive mechanism. Here we tested for effects of intraclutch egg color variation in a host of nonmimetic brood parasite by manipulating egg color in American robins (Turdus migratorius), hosts of brown-headed cowbirds (Molothrus ater). We recorded robins' behavioral responses to simulated cowbird parasitism in nests where color variation was artificially enhanced or reduced. We also quantified egg color variation within and between unmanipulated robin clutches as perceived by robins themselves using spectrophotometric measures and avian visual modeling. In unmanipulated nests, egg color varied more between than within robin clutches. As predicted, however, manipulation of color variation did not affect rejection rates. Overall, our results best support the scenario wherein egg rejection is the outcome of selective pressure by a nonmimetic brood parasite, because robins are efficient rejecters of foreign eggs, irrespective of the color variation within their own clutch.