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Parasite lineages vary widely in species richness. In some clades, speciation is linked to the colonization of new hosts. This is the case in the indigobirds and whydahs (Vidua), brood-parasitic finches whose nestlings mimic the phenotypes of their specific hosts. To understand the factors limiting host colonization and, therefore, speciation, we simulated the colonization of a host using cross-fostering experiments in the field. Despite DNA barcoding suggesting that host species feed their chicks similar diets, nestling Vidua had low survival in their new host environment. Nestling Vidua did not alter their begging calls plastically to match those of the new hosts and were fed less compared to both host chicks and to Vidua chicks in their natural host nests. This suggests that a key hurdle in colonizing new hosts is obtaining the right amount rather than the right type of food from host parents. This highlights the importance of mimetic nestling phenotypes in soliciting feeding from foster parents and may explain why successful colonizations tend to be of hosts closely related to the ancestral one. That nonmimetic chicks are fed less but not actively rejected by host parents suggests how selection from hosts can be sufficiently intense to cause parasite adaptation, yet sufficiently relaxed that parasitic chicks can sometimes survive in and colonize new host environments even if they lack accurate mimetic phenotypes. The difficulties of soliciting sufficient food from novel foster parents, together with habitat filters, likely limit the colonization of new hosts and, therefore, speciation in this parasite radiation.

Early-life conditions have been shown to have a profound effect on an animal's body size and fecundity across diverse taxa. However, less is known about how early-life effects on fecundity within each sex interact to determine reproductive success. We used experiments with burying beetles Nicrophorus vespilloides to analyse this problem. The nutritional conditions experienced by burying beetles in early life are a key determinant of adult body size in both sexes, and adult body size in turn influences male reproductive tactics. In previous work, we showed that smaller males are more effective than larger males at stimulating virgin female fecundity. In this study, we manipulated male and female body size by restricting access to food in early development. We then conducted breeding assays, in which small and large females were mated sequentially with small and large males, and then allowed to raise offspring without paternal care. We tested whether large females, which are potentially more fecund, laid even more eggs when mated with small males. We found no evidence to support this prediction. Instead, we detected only a weak non-significant trend in the predicted direction and no equivalent trend in the number of larvae produced. However, we did find that larvae attained a greater mass by the end of development when their mother was large and mated with a small male first. We suggest that large females might have evolved counter-measures that prevent exploitation by small fecundity-stimulating males, including partial filial cannibalism. By eating surplus larvae during reproduction, larger females would leave more of the carrion for their offspring to consume. This could explain why their surviving larvae are able to attain a greater mass by the time they complete their development.

Brood parasites use the parental care of others to raise their young and sometimes employ mimicry to dupe their hosts. The brood-parasitic finches of the genus Vidua are a textbook example of the role of imprinting in sympatric speciation. Sympatric speciation is thought to occur in Vidua because their mating traits and host preferences are strongly influenced by their early host environment. However, this alone may not be sufficient to isolate parasite lineages, and divergent ecological adaptations may also be required to prevent hybridization collapsing incipient species. Using pattern recognition software and classification models, we provide quantitative evidence that Vidua exhibit specialist mimicry of their grassfinch hosts, matching the patterns, colors and sounds of their respective host's nestlings. We also provide qualitative evidence of mimicry in postural components of Vidua begging. Quantitative comparisons reveal small discrepancies between parasite and host phenotypes, with parasites sometimes exaggerating their host's traits. Our results support the hypothesis that behavioral imprinting on hosts has not only enabled the origin of new Vidua species, but also set the stage for the evolution of host-specific, ecological adaptations.

A fundamental question in biology is how diversity evolves and why some clades are more diverse than others. Phenotypic diversity has often been shown to result from morphological adaptation to different habitats. The role of behavioral interactions as a driver of broadscale phenotypic diversity has received comparatively less attention. Behavioral interactions, however, are a key agent of natural selection. Antagonistic behavioral interactions with predators or with parasites can have significant fitness consequences, and hence act as strong evolutionary forces on the phenotype of species, ultimately generating diversity between species of both victims and exploiters. Avian obligate brood parasites lay their eggs in the nests of other species, their hosts, and this behavioral interaction between hosts and parasites is often considered one of the best examples of coevolution in the natural world. In this review, we use the coevolution between brood parasites and their hosts to illustrate the potential of behavioral interactions to drive evolution of phenotypic diversity at different taxonomic scales. We provide a bridge between behavioral ecology and macroevolution by describing how this interaction has increased avian phenotypic diversity not only in the brood parasitic clades but also in their hosts.

Funder: EC | FP7 | FP7 Ideas: European Research Council (FP7 Ideas); Id: 100011199; Grant(s): 310785, Parental care can be partitioned into traits that involve direct engagement with offspring and traits that are expressed as an extended phenotype and influence the developmental environment, such as constructing a nursery. Here, we use experimental evolution to test whether parents can evolve modifications in nursery construction when they are experimentally prevented from supplying care directly to offspring. We exposed replicate experimental populations of burying beetles (Nicrophorus vespilloides) to different regimes of posthatching care by allowing larvae to develop in the presence (Full Care) or absence of parents (No Care). After only 13 generations of experimental evolution, we found an adaptive evolutionary increase in the pace at which parents in the No Care populations converted a dead body into a carrion nest for larvae. Cross-fostering experiments further revealed that No Care larvae performed better on a carrion nest prepared by No Care parents than did Full Care larvae. We conclude that parents construct the nursery environment in relation to their effectiveness at supplying care directly, after offspring are born. When direct care is prevented entirely, they evolve to make compensatory adjustments to the nursery in which their young will develop. The rapid evolutionary change observed in our experiments suggests there is considerable standing genetic variation for parental care traits in natural burying beetle populations-for reasons that remain unclear.

Mutually beneficial interactions between species play a key role in maintaining biodiversity and ecosystem function. Nevertheless, such mutualisms can erode into antagonistic interactions. One explanation is that the fitness costs and benefits of interacting with a partner species vary among individuals. However, it is unclear why such variation exists. Here, we demonstrate that social behavior within species plays an important, though hitherto overlooked, role in determining the relative fitness to be gained from interacting with a second species. By combining laboratory experiments with field observations, we report that conflict within burying beetles Nicrophorus vespilloides influences the fitness that can be gained from interacting with the mite Poecilochirus carabi. Beetles transport these mites to carrion, upon which both species breed. We show that mites help beetles win intraspecific contests for this scarce resource: mites raise beetle body temperature, which enhances beetle competitive prowess. However, mites confer this benefit only upon smaller beetles, which are otherwise condemned by their size to lose contests for carrion. Larger beetles need no assistance to win a carcass and then lose reproductive success when breeding alongside mites. Thus, the extent of mutualism is dependent on an individual's inability to compete successfully and singlehandedly with conspecifics. Mutualisms degrade into antagonism when interactions with a partner species start to yield a net fitness loss, rather than a net fitness gain. This study suggests that interactions with conspecifics determine where this tipping point lies.

Ecological conditions are known to change the expression of mutualisms though the causal agents driving such changes remain poorly understood. Here we show that temperature stress modulates the harm threatened by a common enemy, and thereby induces a phoretic mite to become a protective mutualist. Our experiments focus on the interactions between the burying beetle Nicrophorus vespilloides, an associated mite species Poecilochirus carabi and their common enemy, blowflies, when all three species reproduce on the same small vertebrate carrion. We show that mites compete with beetle larvae for food in the absence of blowflies, and reduce beetle reproductive success. However, when blowflies breed on the carrion too, mites enhance beetle reproductive success by eating blowfly eggs. High densities of mites are especially effective at promoting beetle reproductive success at higher and lower natural ranges in temperature, when blowfly larvae are more potent rivals for the limited resources on the carcass.

Significance The evolution of sibling rivalry is a classic problem in behavioral ecology. Our approach of observing the experimental evolution of sibling interactions in real time reveals three key insights. First, when parents provide parental care, siblings evolve to compete. Parental care compensates for the costs of sibling rivalry. Second, when parents do not supply care, siblings evolve to cooperate. Sibling cooperation compensates for the loss of parental care. Third, rapid evolutionary switching between sibling rivalry and sibling cooperation is possible because siblings induce greater levels of rivalry (or cooperation) in each other. This generates positive evolutionary feedback, rapidly locking larvae into evolving greater levels of competition (or cooperation) in the presence (or absence) of parental care., Sibling rivalry is commonplace within animal families, yet offspring can also work together to promote each other’s fitness. Here we show that the extent of parental care can determine whether siblings evolve to compete or to cooperate. Our experiments focus on the burying beetle Nicrophorus vespilloides, which naturally provides variable levels of care to its larvae. We evolved replicate populations of burying beetles under two different regimes of parental care: Some populations were allowed to supply posthatching care to their young (Full Care), while others were not (No Care). After 22 generations of experimental evolution, we found that No Care larvae had evolved to be more cooperative, whereas Full Care larvae were more competitive. Greater levels of cooperation among larvae compensated for the fitness costs caused by parental absence, whereas parental care fully compensated for the fitness costs of sibling rivalry. We dissected the evolutionary mechanisms underlying these responses by measuring indirect genetic effects (IGEs) that occur when different sibling social environments induce the expression of more cooperative (or more competitive) behavior in focal larvae. We found that indirect genetic effects create a tipping point in the evolution of larval social behavior. Once the majority of offspring in a brood start to express cooperative (or competitive) behavior, they induce greater levels of cooperation (or competition) in their siblings. The resulting positive feedback loops rapidly lock larvae into evolving greater levels of cooperation in the absence of parental care and greater levels of rivalry when parents provide care.

Several recent hypotheses suggest that parental care can influence the extent of phenotypic variation within populations; however, there have been few tests of these ideas. We exploited the facultative nature of posthatching parental care in the burying beetle, Nicrophorus vespilloides, to test whether parental care influences the expression of phenotypic variation in an important fitness trait (body size). We found that parental care and brood size (which influences sibling competition) had positive and independent effects on variation in body size. First, the mean coefficient of variation (CV) of body size was significantly greater in broods that received care than in those that did not. Second, CV body size increased with brood size in both parental care treatments. These results are not consistent with predictions from recent hypotheses that predict parental care will reduce phenotypic variation among siblings. The positive effects of parental care and brood size on phenotypic variation that we observed are likely due to sibling competition for access to provisioning parents and competition for limiting resources contained in the breeding carcass. Our results suggest that future theory linking parental care to the generation and maintenance of phenotypic variation must integrate the nature of interactions among family members.

It is often assumed that there is a positive relationship between egg size and offspring fitness. However, recent studies have suggested that egg size has a greater effect on offspring fitness in low‐quality environments than in high‐quality environments. Such observations suggest that mothers may compensate for poor posthatching environments by increasing egg size. In this paper we test whether there is a limit on the extent to which increased egg size can compensate for the removal of posthatching parental care in the burying beetle, Nicrophorus vespilloides. Previous experiments with N. vespilloides suggest that an increased egg size can compensate for a relatively poor environment after hatching. Here, we phenotypically engineered female N. vespilloides to produce large or small eggs by varying the amount of time they were allowed to feed on the carcass as larvae. We then tested whether differences between these groups in egg size translated into differences in larval performance in a harsh postnatal environment that excluded parental care. We found that females engineered to produce large eggs did not have higher breeding success, and nor did they produce larger larvae than females engineered to produce small eggs. These results suggest that there is a limit on the extent to which increased maternal investment in egg size can compensate for a poor posthatching environment. We discuss the implication of our results for a recent study showing that experimental N. vespilloides populations can adapt rapidly to the absence of posthatching parental care.

Social interactions within species can modulate the response to selection and determine the extent of evolutionary change. Yet relatively little work has determined whether the social environment can influence the evolution of traits that are selected by interactions with other species - a major source of natural selection. Here we show that the amount of parental care received as an offspring can influence the expression, and potential evolution, of warning displays deployed against predators in adulthood. In theory, warning displays by prey are selected by predators for uniformity and to reliably advertise the extent to which individuals are chemically defended. However, the correlated evolution of intensity of the visual display and strength of the chemical defense is only possible if there is a genetic correlation between them. Adult burying beetlesNicrophorus vespilloidesbear bright orange elytral markings which advertise their chemical defenses. We experimentally manipulated the level of maternal care that individuals received when they were larvae and then measured the strength of the correlation between the component parts of the warning display when they reached adulthood. We found that under limited care individuals were smaller and produced less conspicuous warning displays. The underlying family (genetic) correlation between the visual display and the chemical defense was weaker in individuals that received little care as larvae. We conclude that parenting by burying beetles modulates the evolvability of aposematic defense, making correlated evolutionary change in signal intensity and chemical defense less likely when they restrict care to their young.Significance StatementParental care can improve early offspring survival against predators. However, we have little knowledge of how its effects shape the evolution of predator-prey interactions later in the offspring’s life. We tested this with carrion beetles who provide care for offspring and who carry warning coloration to advertise to predators that they are chemically defended. We show that more parental care resulted in larger, more brightly coloured and chemically defended adult beetles. Furthermore, when parents had provided little care for their young we found weaker genetic correlations between warning signal salience and chemical defense. Over time, this could result in untrustworthy warning signals, which could render them ineffective against predators.

Symbiotic organisms adapt to one another but the extent of co-adaptation commonly varies among pairs of the same symbiotic species drawn from different populations. Here we identify some ecological causes of such differences between populations. We analysed the extent of local co-adaptation between burying beetles Nicrophorus vespilloides and their phoretic mites Poecilochirus carabi in Gamlingay and Waresley Woods, in Cambridgeshire, UK. Burying beetles transport mites to small vertebrate carrion upon which they both reproduce. We conducted reciprocal transplant experiments to test for evidence of local co-adaptation during reproduction. We found variation in the extent of local co-adaptation that was explained by cryptic host specialisation within P. carabi mites. P. carabi is a species complex, within which races of mites are specialised to associate with different species of burying beetle. We found that N. vespilloides from Gamlingay Wood carries a mixture of mite races, from each of the four Nicrophorus species that inhabits this wood. This mixture of races makes P.carabi harmful to Gamlingay N. vespilloides: together, they reduce beetle reproductive success. Experimentally purifying mites, so that Gamlingay N. vespilloides is associated only with the vespilloides mite race, improves beetle reproductive success. Waresley N. vespilloides, by contrast, carry a near pure race of vespilloides mites, which cause negligible damage to Waresley N. vespilloides reproductive success. This is probably because Waresley Wood harbours only two burying beetle species, which differ markedly in their reproductive biology. Cryptic host specialisation with P. carabi mites, combined with differences in the Nicrophorus guild between Gamlingay and Waresley Woods, therefore explain population differences in the extent of local adaptation between N. vespilloides and P. carabi.

Models of ‘plasticity-first’ evolution are attractive because they explain the rapid evolution of new complex adaptations. Nevertheless, it is unclear whether plasticity can still facilitate rapid evolution when diverging populations are connected by gene flow. Here we show how plasticity has generated adaptive divergence in fecundity in wild populations of burying beetlesNicrophorus vespilloides, which are still connected by gene flow, which occupy distinct Cambridgeshire woodlands that are just 2.5km apart and which diverged from a common ancestral population c. 1000-4000 years ago. We show that adaptive divergence is duetothe coupling of an evolved increase in the elevation of the reaction norm linking clutch size to carrion size (i.e. genetic accommodation) with plastic secondary elimination of surplus offspring. Working in combination, these two processes have facilitated rapid adaptation to fine-scale environmental differences, despite ongoing gene flow.

Mutualisms are so ubiquitous, and play such a key role in major biological processes, that it is important to understand how they will function in a changing world. Here we test whether mutualisms can help populations to persist in challenging new environments, by focusing on the protective mutualism between burying beetles Nicrophorus vespilloides and their phoretic mites (Poecilochirus carabi). Our experiments identify the burying beetle’s fundamental thermal niche and show that it is restricted by competition with blowfly larvae at higher and lower temperatures (within the natural range). We further demonstrate that mites expand the burying beetle’s realised thermal niche, by reducing competition with blowflies at lower and higher temperatures, thereby enabling beetles to produce more offspring across a wider thermal range. We conclude that mutualisms can play an important role in promoting survival under novel and adverse conditions, particularly when these conditions enhance the performance of a common enemy.

We tested whether the early‐life environment can influence the extent of individual plasticity in a life‐history trait. We asked: can the early‐life environment explain why, in response to the same adult environmental cue, some individuals invest more than others in current reproduction? Moreover, can it additionally explain why investment in current reproduction trades off against survival in some individuals, but is positively correlated with survival in others? We addressed these questions using the burying beetle, which breeds on small carcasses and sometimes carries phoretic mites. These mites breed alongside the beetle, on the same resource, and are a key component of the beetle's early‐life environment. We exposed female beetles to mites twice during their lives: during their development as larvae and again as adults during their first reproductive event. We measured investment in current reproduction by quantifying average larval mass and recorded the female's life span after breeding to quantify survival. We found no effect of either developing or breeding alongside mites on female reproductive investment, nor on her life span, nor did developing alongside mites influence her size. In post hoc analyses, where we considered the effect of mite number (rather than their mere presence/absence) during the female's adult breeding event, we found that females invested more in current reproduction when exposed to greater mite densities during reproduction, but only if they had been exposed to mites during development as well. Otherwise, they invested less in larvae at greater mite densities. Furthermore, females that had developed with mites exhibited a trade‐off between investment in current reproduction and future survival, whereas these traits were positively correlated in females that had developed without mites. The early‐life environment thus generates individual variation in life‐history plasticity. We discuss whether this is because mites influence the resources available to developing young or serve as important environmental cues.

Although cooperative social interactions within species are considered an important driver of evolutionary change, few studies have experimentally demonstrated that they cause adaptive evolution. Here we address this problem by studying the burying beetle Nicrophorus vespilloides. In this species, parents and larvae work together to obtain nourishment for larvae from the carrion breeding resource: parents feed larvae and larvae also self-feed. We established experimentally evolving populations in which we varied the assistance that parents provided for their offspring and investigated how offspring evolved in response. We show that in populations where parents predictably supplied more care, larval mandibles evolved to be smaller in relation to larval mass, and larvae were correspondingly less self-sufficient. Previous work has shown that antagonistic social interactions can generate escalating evolutionary arms races. Our study shows that cooperative interactions can yield the opposite evolutionary outcome: when one party invests more, the other evolves to invest less., The amount and predictability of parental care may influence the evolution of offspring traits. Here, the authors experimentally evolve burying beetles at different levels of parental care and find smaller mandibles and lower self-sufficiency in populations with more care.

Social interactions within species, and mutualisms between species are both well characterised, but their influence on each other is poorly understood. We determined how interactions among burying beetlesNicrophorus vespilloidesinfluence the value of their interactions with the mitePoecilochirus carabi.Beetles transport these mites to carrion, upon which both species breed. We show that mites help beetles win intraspecific contests for this scarce resource: mites raise beetle body temperature, which enhances beetle competitive prowess. However, mites confer this benefit only upon smaller beetles, which are otherwise doomed by their size to lose contests for carrion. Larger beetles need no assistance to win a carcass and lose reproductive success when breeding alongside mites. We conclude that social interactions within species explain whether interactions with another species are mutualistic or parasitic.One Sentence SummarySocial interactions within species can explain whether interactions with a second species are mutualistic or parasitic.

Animals are now known to be intimately associated with microbial communities, some of which enhance animal fitness. Yet relatively little is known about how these beneficial associations initially arose. We investigated this problem with an experiment on burying beetles, Nicrophorus vespilloides, which breed on the body of a small dead vertebrate. We found that burying beetles breeding on germ-free mice produced smaller larvae, with lower fitness, than those breeding on conventional germ-laden mice. Thus, burying beetles gain benefits from the microbial community associated with their carrion breeding resource, because they lose fitness when this community is removed experimentally. Our experiment suggests that a symbiosis between an animal and a microbial community might begin as an adaptation to the microbial ecosystem in which the animal lives, even when these microbes exist outside the animal, are transiently associated with it at each generation and are not directly transmitted from parents to offspring.

Interactions among siblings are finely balanced between rivalry and cooperation, but the factors that tip the balance towards cooperation are incompletely understood. Previous observations of insect species suggest that (i) sibling cooperation is more likely when siblings hatch at the same time, and (ii) this is more common when parents provide little to no care. In this paper, we tested these ideas experimentally with the burying beetle, Nicrophorus vespilloides . Burying beetles convert the body of a small dead vertebrate into an edible nest for their larvae, and provision and guard their young after hatching. In our first experiment, we simulated synchronous or asynchronous hatching by adding larvae at different intervals to the carrion-breeding resource. We found that ‘synchronously’ hatched broods survived better than ‘asynchronously’ hatched broods, probably because ‘synchronous hatching’ generated larger teams of larvae, that together worked more effectively to penetrate the carrion nest and feed upon it. In our second experiment, we measured the synchronicity of hatching in experimental populations that had evolved for 22 generations without any post-hatching care, and control populations that had evolved in parallel with post-hatching care. We found that larvae were more likely to hatch earlier, and at the same time as their broodmates, in the experimental populations that evolved without post-hatching care. We suggest that synchronous hatching enables offspring to help each other when parents are not present to provide care. However, we also suggest that greater levels of cooperation among siblings cannot compensate fully for the loss of parental care.

SummaryWhen females mate promiscuously, sperm compete within females to fertilise the ova. In theory, a male can increase his success at siring offspring by inducing the female to lay more eggs, as well as by producing more competitive sperm. Here we report that the evolutionary consequences of fecundity stimulation extend beyond rival males, by experimentally uncovering effects on offspring. With experiments on the burying beetle Nicrophorus vespilloides, we show that smaller subordinate males are better able to stimulate female fecundity than larger, dominant males. Furthermore dominant males also benefit from the greater fecundity induced by smaller males, and so gain from the female’s earlier promiscuity just as predicted by theory. By inducing females to produce more offspring on a limited resource, smaller males cause each larva to be smaller, even those they do not sire themselves. Fecundity stimulation thus promotes the non-genetic inheritance of offspring body size, and provides a mechanism for telegony.

Why is there so much variation within species in the extent to which males contribute to offspring care? Answers to this question commonly focus on intraspecific sources of variation in the relative costs and benefits of supplying paternal investment. With experiments in the laboratory on the burying beetle, Nicrophorus vespilloides, and its phoretic mite Poecilochirus carabi, we investigated whether interactions with a second species might also account for intraspecific variation in the extent of paternal care, and whether this variation is due to adaptation or constraint. In our first experiment we bred beetles in the presence or absence of phoretic mites, using a breeding box that mimicked natural conditions by allowing parents to leave the breeding attempt at a time of their choosing. We found that males abandoned their brood sooner when breeding alongside mites than when breeding in their absence. Female patterns of care were unchanged by the mites. Nevertheless, in this experiment, no correlates of beetle fitness were affected by the presence of the mites during reproduction (neither paternal life span after reproduction nor brood size or average larval mass). In a second experiment, we again bred beetles with or without mites but this time we prevented parents from abandoning the brood. This time we found that both parents and the brood suffered fitness costs when breeding alongside mites, compared with families breeding in the absence of mites. We conclude that males adaptively reduce their contributions to care when mites are present, so as to defend their offspring's fitness and their own residual fitness. Interspecific interactions thus account for intraspecific variation in the duration of paternal care., Highlights • The extent of paternal care varies greatly within species. • Some of this variation might be due to interspecific interactions. • We investigated how mites influence paternal care in the burying beetle. • We found that males leave their brood earlier when mites are present. • We show that this is adaptive because it enhances offspring fitness.

Parents play a key role in determining the phenotype of their offspring. However, relatively few studies have investigated whether parents can change their offspring's behaviour in a sustained way that persists into adulthood. With experiments on the burying beetle, Nicrophorus vespilloides, we investigated how the developmental environment created by parents affects their offspring's wing morphology in adulthood, and the correlated effects on adult flight behaviour. Burying beetles exhibit complex biparental care, but offspring can survive without parental provisioning. By removing parents just prior to hatching, while holding the nutritional environment constant, we investigated the downstream consequences for offspring morphology and behaviour. Larvae that developed in the absence of their parents had relatively long and more slender wings than those that developed in their parents' presence. Flight mill tests revealed that flight performance was dependent on the presence of parents during development but not on wing shape. Our results demonstrate that parents have long-lasting effects on the behaviour of their offspring, by influencing the morphology and flight behaviour of their young even after they have matured into adults., Highlights • We investigated parental influence on offspring's morphology and flight behaviour. • Parental care quality affects wing shape allometries and flight performance. • Wing shape and body size do not affect flight performances in a flight mill. • Parental care quality affects offspring's morphology and behaviour into adulthood.

Burying beetles (Nicrophorus vespilloides) bear distinctive and variable orange-black patterning on their elytra and produce an anal exudate from their abdomen when threatened. During breeding, the anal exudates contribute to the antimicrobial defence of the breeding resource. We investigated whether the anal exudates also provide a responsive chemical defence, which is advertised to potential avian predators by the beetle’s orange and black elytral markings. We found that that the orange-black elytral markings of the burying beetle are highly conspicuous for avian predators against range of backgrounds, by using computer simulations. Using bioassays with wood ants, we also showed that the burying beetle’s anal exudates are aversive to potential predators. From these results, and other evidence in the literature, we conclude that the evidence for aposematism in the burying beetle is as strong as the evidence for many other classically aposematic species, such as defended Hymenopterans, ladybirds or poisonous frogs. Nevertheless, we also report unexpectedly high levels of individual variation in coloration and chemical defences, as well as sex differences. We suggest that this variation might be due partly to conflicting selection pressures, particularly on the dual function of the exudates, and partly to nutritional differences in the developmental environment. The ecology of the burying beetles (Nicrophorus spp.) differs markedly from better-studied aposematic insects. This genus thus offers new potential for understanding the evolution of aposematism in general.

Burying beetles (Nicrophorus vespilloides) breed on small vertebrate carcasses, which they shave and smear with antimicrobial exudates. Producing antimicrobials imposes a fitness cost on burying beetles, which rises with the potency of the antimicrobial defence. Burying beetles also carry phoretic mites (Poecilochirus carabi complex), which breed alongside them on the carcass. Here we test the novel hypothesis that P. carabi mites assist burying beetles in clearing the carcass of bacteria as a side-effect of grazing on the carrion. We manipulated the bacterial environment on carcasses and measured the effect on the beetle in the presence and absence of mites. With next-generation sequencing, we investigated how mites influence the bacterial communities on the carcass. We show that mites: 1) cause beetles to reduce the antibacterial activity of their exudates but 2) there are no consistent fitness benefits of breeding alongside mites. We also find that mites increase bacterial diversity and richness on the carcass, but do not reduce bacterial abundance. The current evidence does not support a cleaning mutualism between burying beetles and P. carabi mites, but more work is needed to understand the functional significance and fitness consequences for the beetle of mite-associated changes to the bacterial community on the carcass.

1.The role of bacteria in animal development, ecology and evolution is increasingly well-understood, yet little is known of how animal behaviour affects bacterial communities. Animals that benefit from defending a key resource from microbial competitors are likely to evolve behaviours to control or manipulate the animal's associated external microbiota. 2.We describe four possible mechanisms by which animals could gain a competitive edge by disrupting a rival bacterial community: ‘weeding’, ‘seeding’, ‘replanting’ and ‘preserving’. By combining detailed behavioural observations with molecular and bioinformatic analyses, we then test which of these mechanisms best explains how burying beetles, Nicrophorus vespilloides, manipulate the bacterial communities on their carcass breeding resource. 3.Burying beetles are a suitable species to study how animals manage external microbiota because reproduction revolves around a small vertebrate carcass. Parents shave a carcass and apply antimicrobial exudates on its surface, shaping it into an edible nest for their offspring. We compared bacterial communities in mice carcasses that were either fresh, prepared by beetles or unprepared but buried underground for the same length of time. We also analysed bacterial communities in the burying beetle's gut, during and after breeding, to understand whether beetles could be ‘seeding’ the carcass with particular microbes. 4.We show that burying beetles do not ‘preserve’ the carcass by reducing bacterial load, as is commonly supposed. Instead, our results suggest they ‘seed’ the carcass with bacterial groups which are part of the Nicrophorus core microbiome. They may also ‘replant’ other bacteria from the carcass gut onto the surface of their carrion nest. Both these processes may lead to the observed increase in bacterial load on the carcass surface in the presence of beetles. Beetles may also ‘weed’ the bacterial community by eliminating some groups of bacteria on the carcass, perhaps through the production of antimicrobials themselves. 5.Whether these alterations to the bacterial community are adaptive from the beetle's perspective, or are simply a by-product of the way in which the beetles prepare the carcass for reproduction, remains to be determined in future work. In general, our work suggests that animals might use more sophisticated techniques for attacking and disrupting rival microbial communities than is currently appreciated. This article is protected by copyright. All rights reserved.

Classical models of evolution seldom predict the rate at which populations evolve in the wild. One explanation is that the social environment affects how traits change in response to natural selection. Here, we determine how social interactions between parents and offspring, and among larvae, influence the response to experimental selection on adult size. Our experiments focus on burying beetles (Nicrophorus vespilloides), whose larvae develop within a carrion nest. Some broods exclusively self-feed on the carrion while others are also fed by their parents. We found populations responded to selection for larger adults but only when parents cared for their offspring. We also found populations responded to selection for smaller adults too, but only by removing parents and causing larval interactions to exert more influence on eventual adult size. Comparative analyses revealed a similar pattern: evolutionary increases in species size within the genus Nicrophorus are associated with the obligate provision of care. Synthesising our results with previous studies, we suggest that cooperative social environments enhance the response to selection whereas excessive conflict can prevent further directional selection.

Burying beetles (genusNicrophorus) are relatively rare among insects in providing sophisticated parental care. Consequently, they have become model species in research analysing social evolution, the evolution of parental care and mating systems. We used the recently publishedN. vespilloidesgenome and transcriptome to develop microsatellite markers. Specifically, we developed 14 polymorphic markers with five to 13 alleles per locus and used them to investigate levels of genetic differentiation in four south Cambridgeshire (UK) populations ofN. vespilloides, separated by 21 km at most. The markers revealed significant genetic structuring among populations (globalFST= 0.023) with all but one of the pairwise comparisons among populations being significant. The single exception was the comparison between the two closest populations, which are approximately 2.5 km apart. In general, the microsatellite markers showed lower observed heterozygosity than expected. We infer that there is limited dispersal between populations and potentially also some inbreeding within them and suggest that this may be due to habitat fragmentation. We discuss these results in the context of recent laboratory experiments on inbreeding and beetle flight.

Classical models of evolution seldom predict evolution in the wild. One explanation is that the social environment has important, yet overlooked, effects on how traits change in response to natural selection. We tested this idea with selection experiments on burying beetles (Nicrophorus vespilloides), sub-social insects that exhibit biparental care. Populations responded to selection for larger adults only when parents cared for their offspring, and responded to selection for smaller adults only when we prevented parents from providing care. Comparative analyses revealed a similar pattern: evolutionary increases in species size within the genusNicrophorusare associated with the obligate provision of care. Synthesising our results with previous studies, we suggest that cooperative social environments enhance the response to selection whereas conflict can prevent further directional selection.

Sexually selected weapons are assumed to trade off with traits related to ejaculates, such as testes. However, remarkably little is known about what governs resource allocation and why trade-offs are found in some cases and not others. Often-used models depict competitive allocation occurring within the functional grouping of traits (e.g. reproduction); however, other factors including tissue expense and developmental timing may influence allocation. Experimental comparisons of investment across the sexes have the potential to illuminate allocation rules, because the sexes do not always use traits for the same functions. Here, we capitalize upon a species where females have weapons–testes homologues. We report that a documented trade-off in investment between hind-limb weapons and testes in leaf-footed cactus bugs, Narnia femorata , is even more pronounced in female hind limbs and ovaries. Female hind limbs in this species do not share the clear reproductive function of male hind limbs; therefore, this trade-off spans trait functional groups. Such patterns of investment suggest that future studies of reproductive trade-offs should consider factors such as tissue expense and developmental timing.

Begging calls provide nestling brood parasites with a powerful and flexible tool for avoiding rejection, altering parental provisioning and competing with host nestmates. Despite much research into the topic, no synthesis of parasite vocal strategies for host manipulation has yet been made. In this chapter, we begin by reviewing the literature on reported similarity between the begging calls of avian brood parasites and their hosts. We show that such similarity is a more widespread phenomenon than previously appreciated. Secondly, we examine the selection pressures that drive the evolution of begging call mimicry by avian brood parasites, assess their importance and illustrate them with empirical examples. Finally, we propose a theoretical framework to explain variation in the ways that brood parasite begging calls develop. We suggest that the mode of development can be predicted from a consideration of the accuracy of genetic cues (as mediated by parasite specialisation levels) and the benefits to the young parasite of using environmental cues to modulate their begging call (as influenced by levels of discrimination shown by host parents). Perhaps the main contribution of this chapter is to highlight how little we know about brood parasitic begging calls. This points the way for future work on this topic.

It is well-known that features of animal nest architecture can be explained by fitness benefits gained by the offspring housed within. Here we focus on the little-tested suggestion that the fitness costs associated with building and maintaining a nest should additionally account for aspects of its architecture. Burying beetles prepare an edible nest for their young from a small vertebrate carcass, by ripping off any fur or feathers and rolling the flesh into a rounded ball. We found evidence that only larger beetles are able to construct rounder carcass nests, and that rounder carcass nests are associated with lower maintenance costs. Offspring success, however, was not explained by nest roundness. Our experiment thus provides rare support for the suggestion that construction and maintenance costs are key to understanding animal architecture.

Brood parasitism by cuckoos imposes high reproductive costs on hosts, selecting for the evolution of host defences. Cuckoos retaliate by evolving counter-adaptations to host defences, giving rise to a coevolutionary arms race betweencuckoosandtheirhosts.Herewereviewtheobservationalandexperimentalevidenceforacoevolutionaryarmsrace betweenHorsfield'sBronze-Cuckoos(Chalcitesbasalis)andSuperbFairy-wrens(Maluruscyaneus).Wepresentevidence that the arms race has reached a uniquely advanced stage in this cuckoo-host pair; mimicry of host chicks by cuckoos has evolvedinresponsetorejectionofcuckoochicksbyhosts.Wediscusstheescalationofthearmsracebetweenthesespeciesin relationtotheevolutionofdefenceportfolios.Defencesevolvedbyhostsarenotonlydependentonattributesofthecuckoo, but arealso dependenton thesuccess ofother behavioursinhost-defenceportfolios. Thus,SuperbFairy-wrensrely heavily on rejection of cuckoo chicks, even though it is the costliest possible line of defence, because Horsfield's Bronze-Cuckoos can usually breach the cheaper defences against parasitism mounted earlier in the breeding attempt.

Social immunity refers to any immune defence that benefits others, besides the individual that mounts the response. Since contributions to social immunity are known to be personally costly, they are contributions to a public good. However, individuals vary in their contributions to this public good and it is unclear why. Here we investigate whether they are responding to contributions made by others with experiments on burying beetle (Nicrophorus vespilloides) families. In this species, females, males and larvae each contribute to social immunity through the application of antimicrobial exudates upon the carrion breeding resource. We show experimentally that mothers reduce their contributions to social immunity when raising large broods, and test two contrasting hypotheses to explain why. Either mothers are treating social immunity as a public good, investing less in social immunity when their offspring collectively contribute more, or mothers are trading off investment in social immunity with investment in parental care. Overall, our experiments yield no evidence to support the existence of a trade-off between social immunity and other parental care traits: we found no evidence of a trade-off in terms of time allocated to each activity, nor did the relationship between social immunity and brood size change with female condition. Instead, and consistent with predictions from models of public goods games, we found that higher quality mothers contributed more to social immunity. Therefore our results suggest that mothers are playing a public goods game with their offspring to determine their personal contribution to the defence of the carrion breeding resource. Electronic supplementary material The online version of this article (doi:10.1007/s10682-015-9806-3) contains supplementary material, which is available to authorized users.

Parents have a limited amount of resources to invest in reproduction and commonly trade-off how much they invest in offspring size (or quality) versus brood size. A negative relationship between offspring size and number has been shown in numerous taxa and it underpins evolutionary conflicts of interest between parents and their young. For example, previous work on vertebrates shows that selection favours mothers that produce more offspring, at the expense of individual offspring size, yet favours offspring that have relatively few siblings and therefore attain a greater size at independence. Here we analyse how this trade-off is temporarily affected by stochastic variation in the intensity of interspecific interactions. We examined the effect of the mite Poecilochirus carabi on the relationship between offspring size and number in the burying beetle, Nicrophorus vespilloides. We manipulated the initial number of mites in the reproductive event (by introducing either no mites, 4 mites, 10 mites, or 16 mites), and assessed the effect on the brood. We found a similar trade-off between offspring size and number in all treatments, except in the '16 mite' treatment where the correlation between offspring number and size flattened considerably. This effect arose because larvae in small broods failed to attain a high mass by dispersal. Our results show that variation in the intensity of interspecific interactions can temporarily change the strength of the trade-off between offspring size and number. In this study, high densities of mites prevented individual offspring from attaining their optimal weight, thus potentially temporarily biasing the outcome of parent-offspring conflict in favour of parents.

Some group-living species exhibit social immunity, where the immune system of one individual can protect others in the group from infection. In burying beetles this is part of parental care. Larvae feed on vertebrate carcasses which their parents smear with exudates that inhibit microbial growth. We have sequenced the transcriptome of the burying beetle Nicrophorus vespilloides and identified six genes that encode lysozymes – a type of antimicrobial enzyme that has previously been implicated in social immunity in burying beetles. When females start breeding and producing antimicrobial anal exudates, we found that the expression of one of these genes was increased by ~1000 times to become one of the most abundant transcripts in the transcriptome. We conclude that we have likely identified a gene for social immunity, and that it was recruited during evolution from a previous function in personal immunity.

Cryptic evolution occurs when evolutionary change is masked by concurrent environmental change. In most cases, evolutionary changes in the phenotype are masked by changing abiotic factors. However, evolutionary change in one trait might also be masked by evolutionary change in another trait, a phenomenon referred to as evolutionary environmental deterioration. Nevertheless, detecting this second type of cryptic evolution is challenging and there are few compelling examples. Here, we describe a likely case of evolutionary environmental deterioration occurring in experimental burying beetle ( Nicrophorus vespilloides ) populations that are adapting to a novel social environment that lacks post-hatching parental care. We found that populations rapidly adapted to the removal of post-hatching parental care. This adaptation involved clear increases in breeding success and larval density (number of dispersing larvae produced per gram of breeding carcass), which in turn masked a concurrent increase in the mean larval mass across generations. This cryptic increase in larval mass was accomplished through a change in the reaction norm that relates mean larval mass to larval density. Our results suggest that cryptic evolution might be commonplace in animal families, because evolving trophic and social interactions can potentially mask evolutionary change in other traits, like body size.

Indole is a key environmental cue that is used by many organisms. Based on its biochemistry, we suggest indole is used so universally, and by such different organisms, because it derives from the metabolism of tryptophan, a resource essential for many species yet rare in nature. These properties make it a valuable, environmental cue for resources almost universally important for promoting fitness. We then describe how indole is used to coordinate actions within organisms, to influence the behavior of conspecifics and can even be used to change the behavior of species that belong to other kingdoms. Drawing on the evolutionary framework that has been developed for understanding animal communication, we show how this is diversely achieved by indole acting as a cue, a manipulative signal, and an honest signal, as well as how indole can be used synergistically to amplify information conveyed by other molecules. Clarifying these distinct functions of indole identifies patterns that transcend different kingdoms of organisms.

Natural populations might exhibit resilience to changing climatic conditions if they already show adaptive flexibility in their reproductive strategies. In cooperative breeders, theory predicts that mothers with helpers should provide less care when environmental conditions are favourable, but maintain high investment when conditions are challenging. Here, we test for evidence of climate-mediated flexibility in maternal investment in the cooperatively breeding superb fairy-wren Malurus cyaneus . We focus on egg size because in this species egg size influences offspring size, and females reduce egg investment when there are helpers at the nest. We report that females lay larger eggs during dry, hot conditions. However, the effect of temperature is modulated by the presence of helpers: the average egg size of females with helpers is reduced during cooler conditions but increased during hot conditions relative to females without helpers. This appears to reflect plasticity in egg investment rather than among female differences. Analysis of maternal survival suggests that helped females are better able to withstand the costs of breeding in hot conditions than females without helpers. Our study suggests that females can use multiple, independent cues to modulate egg investment flexibly in a variable environment.

Many passerine birds lay white eggs with reddish brown speckles produced by protoporphyrin pigment. However, the function of these spots is contested. Recently, the sexually selected eggshell coloration (SSEC) hypothesis proposed that eggshell color is a sexually selected signal through which a female advertises her quality (and hence the potential quality of her future young) to her male partner, thereby encouraging him to contribute more to breeding attempts. We performed a test of the SSEC hypothesis in a common passerine, the great tit Parus major. We used a double cross-fostering design to determine whether males change their provisioning behavior based on eggshell patterns they observe at the nest. We also tested the assumption that egg patterning reflects female and/or offspring quality. Because birds differ from humans in their color and pattern perception, we used digital photography and models of bird vision to quantify egg patterns objectively. Neither male provisioning nor chick growth was related to the pattern of eggs males observed during incubation. Although heavy females laid paler, less speckled eggs, these eggs did not produce chicks that grew faster. Therefore, we conclude that the SSEC hypothesis is an unlikely explanation for the evolution of egg speckling in great tits.

Sexual conflict drives the coevolution of sexually antagonistic traits, such that an adaptation in one sex selects an opposing coevolutionary response from the other. Although many adaptations and counteradaptations have been identified in sexual conflict over mating interactions, few are known for sexual conflict over parental investment. Here we investigate a possible coevolutionary sequence triggered by mate desertion in the burying beetle Nicrophorus vespilloides, where males commonly leave before their offspring reach independence. Rather than suffer fitness costs as a consequence, our data suggest that females rely on the male's absence to recoup some of the costs of larval care, presumably because they are then free to feed themselves on the carcass employed for breeding. Consequently, forcing males to stay until the larvae disperse reduces components of female fitness to a greater extent than caring for young singlehandedly. Therefore we suggest that females may have co-evolved to anticipate desertion by their partners so that they now benefit from the male's absence.