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Phenotypic plasticity enables animals to adjust their behavior flexibly to their social environment—sometimes through the expression of adaptive traits that have not been exhibited for several generations. We investigated how long social adaptations can usefully persist when they are not routinely expressed, by using experimental evolution to document the loss of social traits associated with the supply and demand of parental care. We allowed populations of burying beetles Nicrophorus vespilloides to evolve in two different social environments for 48 generations in the lab. In “Full Care” populations, traits associated with the supply and demand of parental care were expressed at every generation, whereas in “No Care” populations we prevented expression of these traits experimentally. We then revived trait expression in the No Care populations at generations 24, 43, and 48 by allowing parents to supply post-hatching care and compared these social traits with those expressed by the Full Care populations. We found that offspring demands for care and male provision of care in the No Care populations were lost sooner than female provision of care. We suggest that this reflects differences in the strength of selection for the expression of alternative traits in offspring, males and females, which can enhance fitness when post-hatching care is disrupted.

Benevolent social behaviours, such as parental care, are thought to enable mildly deleterious mutations to persist. We tested this prediction experimentally using the burying beetle Nicrophorus vespilloides , an insect with biparental care. For 20 generations, we allowed replicate experimental burying beetle populations to evolve either with post-hatching care (‘Full Care’ populations) or without it (‘No Care’ populations). We then established new lineages, seeded from these experimental populations, which we inbred to assess their mutation load. Outbred lineages served as controls. We also tested whether the deleterious effects of a greater mutation load could be concealed by parental care by allowing half the lineages to receive post-hatching care, while half did not. We found that inbred lineages from the Full Care populations went extinct more quickly than inbred lineages from the No Care populations—but only when offspring received no post-hatching care. We infer that Full Care lineages carried a greater mutation load, but that the associated deleterious effects on fitness could be overcome if larvae received parental care. We suggest that the increased mutation load caused by parental care increases a population's dependence upon care. This could explain why care is seldom lost once it has evolved.

When biological material is transferred from one individual’s body to another, as in ejaculate, eggs, and milk, secondary donor-produced molecules are often transferred along with the main cargo, and influence the physiology and fitness of the receiver. Both social and solitary animals exhibit such social transfers at certain life stages. The secondary, bioactive, and transfer-supporting components in socially transferred materials have evolved convergently to the point where they are used in applications across taxa and type of transfer. The composition of these materials is typically highly dynamic and context dependent, and their components drive the physiological and behavioral evolution of many taxa. Our establishment of the concept of socially transferred materials unifies this multidisciplinary topic and will benefit both theory and applications., Trends in Ecology & Evolution, 38 (5), ISSN:0169-5347, ISSN:1872-8383

Insects can adjust their behaviour in relation to experience in a wide range of contexts including foraging, mate selection, and choice of oviposition site. Here we investigate whether burying beetles modulate their choice of carrion in relation to the outcome of their past breeding experience. Burying beetles require small vertebrate carrion to reproduce. Beetle parents convert carrion into an edible nursery for their larvae, whom they typically care for throughout larval development. We tested whether a beetle’s past breeding experience influenced its subsequent choice of carrion, when presented simultaneously with either a dead mouse or a dead chick. We found that both male and female beetles favoured the same carrion as used in their first breeding attempt – but only if they had produced many larvae and only if they had previously bred on a mouse. Beetles that had produced fewer larvae on a dead mouse switched to favouring dead chicks in their second breeding attempt. Those that had bred on a dead chick chose carrion at random subsequently, regardless of their previous breeding success. Our general conclusion is that burying beetles can integrate different sources of information about their past breeding experience with current cues when selecting carrion for reproduction.

Generalist brood parasites that share nests with host nestlings can optimize resource acquisition from host parents by balancing the benefits that host nest-mates provide, including attracting increased provisions to the nest, against the costs of competing with the same host young over foster parental resources. However, it is unclear how parasitic chicks cope when faced with more nest-mates than are optimal for their survival upon hatching. We suggest that, in the obligate brood parasitic brown-headed cowbird ( Molothrus ater ), chicks use a niche construction strategy and reduce larger, more competitive host broods to maximize the parasites' survival to fledging. We experimentally altered brood sizes to test for Goldilocks principle patterns (i.e. a ‘just right’ intermediate brood size) of cowbird survival in nests of prothonotary warbler ( Protonotaria citrea ) hosts. We found that intermediate brood sizes of two host nestlings maximized cowbird fledging success relative to 0 or 4 host nest-mates at hatching. Specifically, cowbird nestlings lowered host brood sizes towards this optimum when placed in broods with more host nestlings. The results suggest that cowbirds reduce, but do not eliminate, host broods as a niche construction mechanism to improve their own probability of survival.

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.

The joint actions of animals in partnerships or social groups evolve under both natural selection, from the wider environment, and social selection, imposed by other members of the pair or group. We used experimental evolution to investigate how jointly expressed actions evolve upon exposure to a new environmental challenge. Our work focused on the evolution of carrion nest preparation by pairs of burying beetlesNicrophorus vespilloides, a joint activity undertaken by the pair but typically led by the male. In previous work, we found that carrion nest preparation evolved to be faster in experimental populations without post-hatching care (No Care lines) than with post-hatching care (Full Care lines). Here we investigate how this joint activity evolved. After 15 generations of experimental evolution, we created heterotypic pairs (No Care females with Full Care males, and No Care males with Full Care females) and compared their carrion nest making with homotypic No Care and Full Care pairs. We found that pairs with No Care males prepared the nest more rapidly than pairs with Full Care males, regardless of the female’s line of origin. This suggests that males led the way by adapting their nest preparation behaviour to the No Care environment first, with females secondarily co-adapting their behaviour to the male’s behaviour by reducing their nest preparation behaviour. We discuss how social coadaptations within pairs or groups could act as a post-mating barrier to gene flow.

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.

Models of “plasticity-first” evolution are attractive because they explain the rapid evolution of new complex adaptations. Nevertheless, it is unclear whether plasticity can facilitate rapid microevolutionary change between diverging populations. Here, we show how plasticity may have generated adaptive differences in fecundity between neighboring wild populations of burying beetles Nicrophorus vespilloides. These populations occupy distinct Cambridgeshire woodlands that are just 2.5 km apart and that probably originated from a common ancestral population about 1000-4000 years ago. We find that populations are divergently adapted to breed on differently sized carrion. Adaptive differences in clutch size and egg size are associated with divergence at loci connected with oogenesis. The populations differ specifically in the elevation of the reaction norm linking clutch size to carrion size (i.e., genetic accommodation), and in the likelihood that surplus offspring will be lost after hatching. We suggest that these two processes may have facilitated rapid local adaptation on a fine-grained spatial scale.

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.

Phenotypic plasticity enables animals to adjust their behaviour flexibly to their social environment – sometimes through the expression of adaptive traits that have not been exhibited for several generations. We investigated how long social adaptations can usefully persist when they are not routinely expressed, by using experimental evolution to document the loss of social traits associated with the supply and demand of parental care. We allowed populations of burying beetles Nicrophorus vespilloides to evolve in two social environments for 48 generations in the lab. In ‘Full Care’ populations, traits associated with the supply and demand of parental care were expressed at every generation, whereas in ‘No Care’ populations we prevented expression of these traits experimentally. We then revived trait expression in the No Care populations at generations 24, 43 and 48 by allowing parents to supply post-hatching care, and compared these social traits with those expressed by the Full Care populations. We found that offspring demands for care decayed in the No Care populations more rapidly than a parent’s capacity to supply care. Furthermore, male care decayed before female care. We suggest that this reflects differences in the strength of selection for the expression of alternative traits in offspring, males and females, which can enhance fitness when post-hatching care is disrupted.Impact SummarySocial interactions between animals are suggested to be increasingly vulnerable to breakdown in our changing world. Our experiments offer a rare insight into what happens next, by assessing in real time the durability of social behaviours that are no longer routinely expressed. Our results also have implications for conservation captive breeding programmes where compensatory husbandry techniques prevent trait expression and so could inadvertently induce rapid, irreversible trait loss.We investigated how long it took populations to lose the ability to express appropriate social behaviour when they had been prevented from doing so for many generations. We did this by evolving replicate populations of burying beetles Nicrophorus vespilloides in the laboratory for 48 generations. The burying beetle is a common insect that is well-known for caring for its larvae, although larvae can survive in the lab without any care at all. In two populations (“Full Care”), we allowed parents and offspring to interact during the supply of post-hatching care, as usual. In two other populations (“No Care”), parents were removed before offspring hatched and so could not interact socially with their young.Over the course of 48 generations of experimental evolution, we periodically revived social interactions between parents and offspring in the No Care populations. We assessed the extent to which larval begging behaviours, and parental care behaviours, had decayed by comparing their expression with those in the Full Care populations. We found that larval begging behaviour eroded rapidly in No Care populations, and more rapidly than the supply of care by parents. Furthermore, paternal care decayed to a greater extent than maternal care (which was largely unchanged relative to its expression in the Full Care populations). We suggest that these differences could be due to differences in the strength of selection on each family member for alternative traits to enhance fitness.

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.

Recent studies have shown that intraspecific patterns of phenotypic plasticity can mirror patterns of evolutionary diversification among species. This appears to be the case in Nicrophorus beetles. Within species, body size is positively correlated with the size of carrion used to provision larvae and parental performance. Likewise, among species, variation in body size influences whether species exploit smaller or larger carrion and the extent to which larvae depend on parental care. However, it is unclear whether developmental plasticity in response to carcass size, parental care, or both underlie transitions to new carcass niches. We examined this by testing whether variation in the conditions experienced by Nicrophorus vespilloides larvae influenced their ability to breed efficiently upon differently sized carcasses as adults. We found that the conditions experienced by larvae during development played a critical role in determining their ability to use large carcasses effectively as adults. Specifically, individuals that developed with parental care and on large carcasses were best able to convert the resources on a large carcass into offspring when breeding themselves. Our results suggest that parentally induced plasticity can be important in the initial stages of niche expansion.

Levels of parental care critically influence the developmental environment with the capacity to impact the growth, survival, physiology, and behaviour of offspring. Plastic changes in DNA methylation have been hypothesised to modulate gene expression responses to parental environments. Moreover, these effects can be inherited and so may affect the process of adaptive evolution. In this study, using experimental evolution, we investigated how plastic changes in DNA methylation induced by the loss of parental care have evolved in a biparental insect (Nicrophorus vespilloides) using experimental evolution. We show that removal of care in a single generation is associated with changes in gene expression in stress-related pathways in 1st instar larvae. However, in larvae that have adapted to the loss of parental care after being deprived of care for 30 generations, gene expression is shifted from stress-related gene expression towards growth and brain development pathways. We found that changes in gene body methylation arose both as a direct response to the loss of parental care and stochastically as populations diverged. Overall, our results suggest that a complex interplay between transcription and DNA methylation shapes the molecular adaptation to environmental change.

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.

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.

Sexual conflict arises when the optimal reproductive strategy differs for males and females. It is associated with every reproductive stage, yet few studies have considered how the outcome may be changed by interactions with other species. Here, we show that phoretic mites Poecilochirus carabi change the outcome of sexual conflict over the supply of prehatching parental investment in the burying beetle Nicrophorus vespilloides. Burying beetles require a small dead vertebrate for reproduction, which they prepare by shaving it, rolling up the flesh, and burying it. When pairs were given a medium‐sized mouse to prepare (13–16 g), mites changed how the costs of reproduction were divided between the sexes, with males then sustaining greater costs than females. We found no equivalent difference when pairs prepared larger or smaller carcasses. Thus, our experiment shows that the outcome of sexual conflict over prehatching parental investment is changed by interactions with other species during reproduction.

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.

When animals potentially occupy diverse microhabitats, how can camouflage be achieved? Here we combine descriptive and experimental methods to uncover a novel form of phenotypic plasticity in the camouflage of bird eggs that may be present in other avian taxa. Soil from the bare substrate adheres to the blue-footed booby’s (Sula nebouxii’s) pale eggs, which parents manipulate both under and on top of their webs. Analysis of digital images confirmed that dirtiness increases progressively during the first 16 days of the incubation period, making eggs more similar to the nest substrate. Observations of 3,668 single-egg clutches showed that the probability of egg loss declines progressively over the same time frame and then remains low for the rest of the 41-day incubation period. An experiment showed that when chicken eggs are soiled and exposed in artificial booby nests, they are less likely to be taken by Heermann’s gulls (Larus heermanni) than clean eggs.

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.

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.

Lay Summary Birds that color their feathers with dietary carotenoid pigments are expected to seek out these pigments when they are molting. We show that molting male hihi, who express carotenoid-based plumage, seek out naturally occurring foods that are rich in carotenoid pigments. Female hihi, who do not express carotenoid-based plumage, do not seek out carotenoid-rich foods. This lends strength to the idea that carotenoid-based plumage reveals an individual’s foraging ability., Dietary access to carotenoids is expected to determine the strength of carotenoid-based signal expression and potentially to maintain signal honesty. Species that display carotenoid-based yellow, orange, or red plumage are therefore expected to forage selectively for carotenoid-rich foods when they are depositing these pigments during molt, but whether they actually do so is unknown. We set out to address this in the hihi (Notiomystis cincta), a New Zealand passerine where males, but not females, display yellow carotenoid-based plumage. We measured circulating carotenoid concentrations in male and female hihi during breeding and molt, determined the nutritional content of common foods in the hihi diet, and conducted feeding observations of male and female hihi during molt. We found that although male and female hihi do not differ significantly in plasma carotenoid concentration, male hihi have a greater proportion of carotenoid-rich foods in their diet than do females. This is a consequence of a greater fruit and lower invertebrate intake than females and an avoidance of low-carotenoid content fruit. By combining behavioral observations with quantification of circulating carotenoids, we present evidence that colorful birds forage to maximize carotenoid intake, a conclusion we would not have drawn had we examined plasma carotenoids alone.

Our data suggest that, unlike many cuckoos, the Horsfield's bronze-cuckoo may have evolved an "average" egg morph that equally resembles that of many host species. In combination with previous work, these results suggest that this cuckoo has evolved to be a "jack-of-all-trades" mimic to facilitate brood parasitism.Parasitism of multiple host species by a generalist poses the difficulty of overcoming a potentially diverse array of host defenses. In some generalist avian obligate brood parasites, selection for egg mimicry by hosts has given rise to host-specific races (gentes), each of which lays an egg that mimics that of its favored host. However, it is unknown how generalist parasites lacking races are able to circumvent egg rejection by hosts. The Horsfield's bronze-cuckoo, Chalcites basalis, is a generalist brood parasite that exploits a diversity of hosts yet is reported to lay monomorphic eggs. Using reflectance spectrometry and visual modeling, we tested for egg polymorphisms in Horsfield's bronze-cuckoo eggs laid in the nests of 17 host species. We found that the host species possess broadly similar egg phenotypes that differ subtly but significantly from one another in their color and luminance. However, the Horsfield's bronze-cuckoo does not mimic this diversity, thus ruling out the existence of host-specific egg color and luminance phenotypes that are visible to birds but hidden from humans. Instead, our analyses support the idea that the Horsfield's bronze-cuckoo egg is a jack-of-all-trades mimic, lying in an intermediate position in avian visual space between the eggs of its various hosts. We suggest that jack-of-all-trades mimicry may be favored among brood parasites that parasitize hosts with a narrow range of egg phenotypes and where individual female brood parasites exploit multiple host species.

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.

Providing supplementary food to endangered bird species is a common management action. Research has tended to focus on whether or not supplementary food should be provided, and relatively less attention has been paid to the form that food should take. Supplementation is also commonly made directly to adult individuals. However, the potentially long-lasting consequences of developmental diet make it relevant to consider what type of supplementary food is most appropriate for nestling birds. We sought to explore these issues in a wild population of hihi (Notiomystis cincta), an endangered New Zealand passerine in which adults in four out of five extant populations receive supplementary food. We directly provisioned nestling hihi with four alternative dietary treatments (protein- or carbohydrate-based diet with or without carotenoids) and assessed the effect of supplementation on (1) nestling growth parameters; (2) survival from hatching to fledging; (3) survival from fledging to recruitment (breeding age). Firstly, we found a sex-specific effect of protein supplementation on growth inflection point: inflection point was later for females that received a high-protein diet compared with controls, and earlier for males. Secondly, we found an interacting effect of sex and diet on survival from hatching to fledging, such that females benefitted from a high-protein diet while males suffered. We also found an interacting effect of protein treatment and carotenoid treatment on survival to fledging, such that the positive effects of carotenoid supplementation were negated if carotenoids were provided in combination with the protein supplement. Finally, we were unable to detect an effect of nestling dietary treatment on survival from fledging to recruitment. Our results suggest that the short-term consequences of nestling supplementary feeding are more pronounced than any long-term effects. We also found evidence that dietary supplementation had opposing effects on male and female nestlings, which may be an important, previously overlooked, consideration when evaluating the conservation value of feeding regimes.