Metabolic control of BRISC-SHMT2 assembly regulates immune signalling.

Serine hydroxymethyltransferase 2 (SHMT2) regulates one-carbon transfer reactions that are essential for amino acid and nucleotide metabolism, and uses pyridoxal-5'-phosphate (PLP) as a cofactor. Apo SHMT2 exists as a dimer with unknown functions, whereas PLP binding stabilizes the active tetrameric state. SHMT2 also promotes inflammatory cytokine signalling by interacting with the deubiquitylating BRCC36 isopeptidase complex (BRISC), although it is unclear whether this function relates to metabolism. Here we present the cryo-electron microscopy structure of the human BRISC-SHMT2 complex at a resolution of 3.8 Å. BRISC is a U-shaped dimer of four subunits, and SHMT2 sterically blocks the BRCC36 active site and inhibits deubiquitylase activity. Only the inactive SHMT2 dimer-and not the active PLP-bound tetramer-binds and inhibits BRISC. Mutations in BRISC that disrupt SHMT2 binding impair type I interferon signalling in response to inflammatory stimuli. Intracellular levels of PLP regulate the interaction between BRISC and SHMT2, as well as inflammatory cytokine responses. These data reveal a mechanism in which metabolites regulate deubiquitylase activity and inflammatory signalling.

Guppies in large groups cooperate more frequently in an experimental test of the group size paradox.

The volunteer's dilemma, in which a single individual is required to produce a public good, predicts that individuals in larger groups will cooperate less frequently. Mechanistically, this could result from trade-offs between costs associated with volunteering and costs incurred if the public good is not produced (nobody volunteers). During predator inspection, one major contributor to the cost of volunteering is likely increased probability of predation; however, a predator also poses a risk to all individuals if nobody inspects. We tested the prediction that guppies in larger groups will inspect a predator less than those in smaller groups. We also predicted that individuals in larger groups would perceive less threat from the predator stimulus because of the protective benefits of larger groups (e.g. dilution). Contrary to prediction, we found that individuals in large groups inspected more frequently than those in smaller groups, but (as predicted) spent less time in refuges. There was evidence that individuals in intermediate-sized groups made fewest inspections and spent most time in refuges, suggesting that any link between group size, risk and cooperation is not driven by simple dilution. Extensions of theoretical models that capture these dynamics will likely be broadly applicable to risky cooperative behaviour.

Intraspecific variation in inhibitory motor control in guppies, Poecilia reticulata.

Inhibitory control (IC) is the ability to overcome impulsive or prepotent but ineffective responses in favour of more appropriate behaviours. The ability to inhibit internal predispositions or external temptations is vital in coping with a complex and variable world. Traditionally viewed as cognitively demanding and a main component of executive functioning and self-control, IC was historically examined in only a few species of birds and mammals but recently a number of studies has shown that a much wider range of taxa rely on IC. Furthermore, there is growing evidence that inhibitory abilities may vary within species at the population and individual levels owing to genetic and environmental factors. Here we use a detour-reaching task, a standard paradigm to measure motor inhibition in nonhuman animals, to quantify patterns of interindividual variation in IC in wild-descendant female guppies, Poecilia reticulata. We found that female guppies displayed inhibitory performances that were, on average, half as successful as the performances reported previously for other strains of guppies tested in similar experimental conditions. Moreover, we showed consistent individual variation in the ability to inhibit inappropriate behaviours. Our results contribute to the understanding of the evolution of fish cognition and suggest that IC may show considerable variation among populations within a species. Such variation in IC abilities might contribute to individual differences in other cognitive functions such as spatial learning, quantity discrimination or reversal learning.

Trinidadian guppies use a social heuristic that can support cooperation among non-kin.

Cooperation among non-kin is well documented in humans and widespread in non-human animals, but explaining the occurrence of cooperation in the absence of inclusive fitness benefits has proven a significant challenge. Current theoretical explanations converge on a single point: cooperators can prevail when they cluster in social space. However, we know very little about the real-world mechanisms that drive such clustering, particularly in systems where cognitive limitations make it unlikely that mechanisms such as score keeping and reputation are at play. Here, we show that Trinidadian guppies (Poecilia reticulata) use a 'walk away' strategy, a simple social heuristic by which assortment by cooperativeness can come about among mobile agents. Guppies cooperate during predator inspection and we found that when experiencing defection in this context, individuals prefer to move to a new social environment, despite having no prior information about this new social group. Our results provide evidence in non-human animals that individuals use a simple social partner updating strategy in response to defection, supporting theoretical work applying heuristics to understanding the proximate mechanisms underpinning the evolution of cooperation among non-kin.

Dynamics of the energy seascape can explain intra-specific variations in sea-crossing behaviour of soaring birds.

Thermal soaring birds extract energy from the atmosphere to achieve energetically low-cost movement. When encountering regions that are energetically costly to fly over, such as open seas, they should attempt to adjust the spatio-temporal pattern of their passage to maximize energy extraction from the atmosphere over these ecological barriers. We applied the concept of energy landscapes to investigate the spatio-temporal dynamics of energy availability over the open sea for soaring flight. We specifically investigated how the 'energy seascape' may shape age-specific sea-crossing behaviour of European honey buzzards, Pernis apivorus, over the Mediterranean Sea in autumn. We found uplift potential over the sea to be the main determinant of sea-crossing distance, rather than wind conditions. Considering this variable as a proxy for available energy over the sea, we constructed the energy seascape for the autumn migration season using 40 years of temperature data. Our results indicate that early-migrating adult buzzards are likely to encounter adverse energy subsidence over the Mediterranean, whereas late-migrating juveniles face less adverse flight conditions, and even conditions conducive to soaring flight. Our study provides evidence that the dynamics of the energy landscape can explain intra-specific variation in migratory behaviour also at sea.

The Evolution of Cooperation: Interacting Phenotypes among Social Partners.

Models of cooperation among nonkin suggest that social assortment is important for the evolution of cooperation. Theory predicts that interacting phenotypes, whereby an individual's behavior depends on the behavior of its social partners, can drive such social assortment. We measured repeated indirect genetic effects (IGEs) during cooperative predator inspection in eight populations of Trinidadian guppies (Poecilia reticulata) that vary in their evolutionary history of predation. Four broad patterns emerged that were dependent on river, predation history, and sex: (i) current partner behavior had the largest effect on focal behavior, with fish from low-predation habitats responding more to their social partners than fish from high-predation habitats; (ii) different focal/partner behavior combinations can generate cooperation; (iii) some high-predation fish exhibited carryover effects across social partners; and (iv) high-predation fish were more risk averse. These results provide the first large-scale comparison of interacting phenotypes during cooperation across wild animal populations, highlighting the potential importance of IGEs in maintaining cooperation. Intriguingly, while focal fish responded strongly to current social partners, carryover effects between social partners suggest generalized reciprocity (in which one helps anyone if helped by someone) may contribute to the evolution of cooperation in some, but not all, populations of guppies.

Determinants of spring migration departure decision in a bat.

Migratory decisions in birds are closely tied to environmental cues and fat stores, but it remains unknown if the same variables trigger bat migration. To learn more about the rare phenomenon of bat migration, we studied departure decisions of female common noctules (Nyctalus noctula) in southern Germany. We did not find the fattening period that modulates departure decisions in birds. Female noctules departed after a regular evening foraging session, uniformly heading northeast. As the day of year increased, migratory decisions were based on the interactions among wind speed, wind direction and air pressure. As the migration season progressed, bats were likely to migrate on nights with higher air pressure and faster tail winds in the direction of travel, and also show high probability of migration on low-pressure nights with slow head winds. Common noctules thus monitor complex environmental conditions to find the optimal migration night.

Global aerial flyways allow efficient travelling.

Birds migrate over vast distances at substantial costs. The highly dynamic nature of the air makes the selection of the best travel route difficult. We investigated to what extent migratory birds may optimise migratory route choice with respect to wind, and if route choice can be subject to natural selection. Following the optimal route, calculated using 21 years of empirical global wind data, reduced median travel time by 26.5% compared to the spatially shortest route. When we used a time-dependent survival model to quantify the adaptive benefit of choosing a fixed wind-optimised route, 84.8% of pairs of locations yielded a route with a higher survival than the shortest route. This suggests that birds, even if incapable of predicting wind individually, could adjust their migratory routes at a population level. As a consequence, this may result in the emergence of low-cost flyways representing a global network of aerial migratory pathways.

Social preferences based on sexual attractiveness: a female strategy to reduce male sexual attention.

Male sexual harassment of females is common across sexually reproducing species and can result in fitness costs to females. We hypothesized that females can reduce unwanted male attention by constructing a social niche where their female associates are more sexually attractive than themselves, thus influencing the decision-making of males to their advantage. We tested this hypothesis in the Trinidadian guppy (Poecilia reticulata), a species with high levels of male sexual harassment. First, we confirmed that non-receptive females were harassed less when they were paired with a more sexually attractive (receptive) female than with another non-receptive female. We then found that, indeed, females exploit this as a strategy to reduce sexual harassment; non-receptive females actively preferred to associate with receptive over non-receptive females. Importantly, when given access only to chemosensory cues, non-receptive females still showed this preference, suggesting that they use information from chemical cues to assess the sexual attractiveness of potential female partners. Receptive females in contrast showed no such preferences. Our results demonstrate that females can decrease male harassment by associating with females that are more sexually attractive than themselves and that they perform active partner choices based on this relative attractiveness. We propose that this strategy is likely to represent an important pathway by which females can construct social niches that influence the decision-making of others to their advantage; in this case, to reduce the sexual harassment they experience.

Male sexual harassment alters female social behaviour towards other females.

Male harassment of females to gain mating opportunities is a consequence of an evolutionary conflict of interest between the sexes over reproduction and is common among sexually reproducing species. Male Trinidadian guppies Poecilia reticulata spend a large proportion of their time harassing females for copulations and their presence in female social groups has been shown to disrupt female-female social networks and the propensity for females to develop social recognition based on familiarity. In this study, we investigate the behavioural mechanisms that may lead to this disruption of female sociality. Using two experiments, we test the hypothesis that male presence will directly affect social behaviours expressed by females towards other females in the population. In experiment one, we tested for an effect of male presence on female shoaling behaviour and found that, in the presence of a free-swimming male guppy, females spent shorter amounts of time with other females than when in the presence of a free-swimming female guppy. In experiment two, we tested for an effect of male presence on the incidence of aggressive behaviour among female guppies. When males were present in a shoal, females exhibited increased levels of overall aggression towards other females compared with female only shoals. Our work provides direct evidence that the presence of sexually harassing males alters female-female social behaviour, an effect that we expect will be recurrent across taxonomic groups.

Social partner cooperativeness influences brain oxytocin transcription in Trinidadian guppies (Poecilia reticulata).

For non-kin cooperation to be maintained, individuals need to respond adaptively to the cooperative behaviour of their social partners. Currently, however, little is known about the biological responses of individuals to experiencing cooperation. Here, we quantify the neuroregulatory response of Trinidadian guppies (Poecilia reticulata) experiencing cooperation or defection by examining the transcriptional response of the oxytocin gene (oxt; also known as isotocin), which has been implicated in cooperative decision-making. We exposed wild-caught females to social environments where partners either cooperated or defected during predator inspection, or to a control (non-predator inspection) context, and quantified the relative transcription of the oxt gene. We tested an experimental group, originating from a site where individuals are under high predation threat and have previous experience of large aquatic predators (HP), and a control group, where individuals are under low predation threat and naïve to large aquatic predators (LP). LP, but not HP, fish showed different behavioural responses to the behaviour of their social environment, cooperating with cooperative partners and defecting when paired with defecting ones. In HP, but not LP, fish brain mid-section oxt relative transcription varied depending on social partner behaviour. HP fish experiencing cooperation during predator inspection had lower oxt transcription than those experiencing defection. This effect was not present in the control population or in the control context, where the behaviour of social partners did not affect oxt transcription. Our findings provide insight into the neuromodulation underpinning behavioural responses to social experiences, and ultimately to the proximate mechanisms underlying social decision-making.

The evolution of mammalian brain size.

Relative brain size has long been considered a reflection of cognitive capacities and has played a fundamental role in developing core theories in the life sciences. Yet, the notion that relative brain size validly represents selection on brain size relies on the untested assumptions that brain-body allometry is restrained to a stable scaling relationship across species and that any deviation from this slope is due to selection on brain size. Using the largest fossil and extant dataset yet assembled, we find that shifts in allometric slope underpin major transitions in mammalian evolution and are often primarily characterized by marked changes in body size. Our results reveal that the largest-brained mammals achieved large relative brain sizes by highly divergent paths. These findings prompt a reevaluation of the traditional paradigm of relative brain size and open new opportunities to improve our understanding of the genetic and developmental mechanisms that influence brain size.

A Matador-like Predator Diversion Strategy Driven by Conspicuous Coloration in Guppies.

Understanding the adaptive function of conspicuous coloration has been a major focus of evolutionary biology for much of the last century. Although considerable progress has been made in explaining how conspicuous coloration can be used in functions as diverse as sexual and social signaling, startling predators, and advertising toxicity [1], there remain a multitude of species that display conspicuous coloration that cannot be explained by existing theory. Here we detail a new "matador-like" divertive antipredator strategy based on conspicuous coloration in Trinidadian guppies (Poecilia reticulata). Guppies encountering predatory fish rapidly enhance the conspicuousness of their eyes by blackening their irises. By pitting biomimetic robotic guppies against real predatory fish, we show this conspicuous eye coloration diverts attacks away from the guppies' center of mass to their head. To determine the function of this seemingly counterintuitive behavior, we developed a method for simulating escape probabilities when live prey interact with ballistic attacking predators, and find this diversion effect significantly benefits black-eyed guppies because they evade capture by rapidly pivoting away from the predator once it has committed to its attack. Remarkably, this antipredator strategy reverses the commonly observed negative scaling relationship between prey size and evasive ability, with larger fish benefiting most from diverting predators. Taken together, our results introduce a new antipredator divertive strategy that may be widely used by conspicuously colored prey that rely on agility to escape their predators.

Social implications of the battle of the sexes: sexual harassment disrupts female sociality and social recognition.

Across sexually reproducing species, males and females are in conflict over the control of reproduction. At the heart of this conflict in a number of taxa is male harassment of females for mating opportunities and female strategies to avoid this harassment. One neglected consequence that may result from sexual harassment is the disruption of important social associations. Here, we experimentally manipulate the degree of sexual harassment that wild female guppies (Poecilia reticulata) experience by establishing replicated, semi-natural pools with different population sex ratios. We quantify the effects of sexual harassment on female social structure and the development of social recognition among females. When exposed to sexual harassment, we found that females had more disparate social networks with limited repeated interactions when compared to females that did not experience male harassment. Furthermore, females that did not experience harassment developed social recognition with familiar individuals over an 8-day period, whereas females that experienced harassment did not, an effect we suggest is due to disruption of association patterns. These results show that social network structure and social recognition can be affected by sexual harassment, an effect that will be relevant across taxonomic groups and that we predict will have fitness consequences for females.

Evolution of non-kin cooperation: social assortment by cooperative phenotype in guppies.

Cooperation among non-kin constitutes a conundrum for evolutionary biology. Theory suggests that non-kin cooperation can evolve if individuals differ consistently in their cooperative phenotypes and assort socially by these, such that cooperative individuals interact predominantly with one another. However, our knowledge of the role of cooperative phenotypes in the social structuring of real-world animal populations is minimal. In this study, we investigated cooperative phenotypes and their link to social structure in wild Trinidadian guppies (Poecilia reticulata). We first investigated whether wild guppies are repeatable in their individual levels of cooperativeness (i.e. have cooperative phenotypes) and found evidence for this in seven out of eight populations, a result which was mostly driven by females. We then examined the social network structure of one of these populations where the expected fitness impact of cooperative contexts is relatively high, and found assortment by cooperativeness, but not by genetic relatedness. By contrast, and in accordance with our expectations, we did not find assortment by cooperativeness in a population where the expected fitness impact of cooperative contexts is lower. Our results provide empirical support for current theory and suggest that assortment by cooperativeness is important for the evolution and persistence of non-kin cooperation in real-world populations.

Sound transmission at ground level in a short-grass prairie habitat and its implications for long-range communication in the swift fox Vulpes velox.

The acoustic environment of swift foxes Vulpes velox vocalizing close to the ground and the effect of propagation on individual identity information in vocalizations were quantified in a transmission experiment in prairie habitat. Sounds were propagated (0.45 m above the ground) at distances up to 400 m. Effects of transmission were measured on three sound types: synthesized sweeps with 1.3 kHz bandwidths spanning in the range of 0.3-8.0 kHz; single elements of swift fox barking sequences (frequency range of 0.3-4.0 kHz) and complete barking sequences. Synthesized sweeps spanning 0.3-1.6 and 1.2-2.5 kHz propagated the furthest and the latter sweeps exhibited the best transmission properties for long-range propagation. Swift fox barking sequence elements are centered toward the lower end of this frequency range. Nevertheless, measurable individual spectral characteristics of the barking sequence seem to persist to at least 400 m. Individual temporal features were very consistent to at least 400 m. The communication range of the barking sequences is likely to be farther than 400 m and it should be considered a long-ranging vocalization. However, relative to the large home ranges of swift foxes (up to 16 km(2) in the experimental area) the barking sequence probably functions at intermediate distances.

Dynamic eye colour as an honest signal of aggression.

Animal eyes are some of the most widely recognisable structures in nature. Due to their salience to predators and prey, most research has focused on how animals hide or camouflage their eyes [1]. However, across all vertebrate Classes, many species actually express brightly coloured or conspicuous eyes, suggesting they may have also evolved a signalling function. Nevertheless, perhaps due to the difficulty with experimentally manipulating eye appearance, very few species beyond humans [2] have been experimentally shown to use eyes as signals [3]. Using staged behavioural trials we show that Trinidadian guppies (Poecilia reticulata), which can rapidly change their iris colour, predominantly express conspicuous eye colouration when performing aggressive behaviours towards smaller conspecifics. Furthermore, using a novel, visually realistic robotic system to create a mismatch between signal and relative competitive ability, we show that eye colour is used to honestly signal aggressive motivation. Specifically, robotic 'cheats' (that is, smaller, less-competitive robotic fish that display aggressive eye colouration when defending a food patch) attracted greater food competition from larger real fish. Our study suggests that eye colour may be an under-appreciated aspect of signalling in animals, shows the utility of our biomimetic robotic system for investigating animal behaviour, and provides experimental evidence that socially mediated costs towards low-quality individuals may maintain the honesty of dynamic colour signals.

Fear of predation drives stable and differentiated social relationships in guppies.

Social relationships can have important consequences for fitness in animals. Whilst numerous studies have shown that individuals often join larger groups in response to perceived predation risk (i.e. fear of predation), the importance of predation risk in driving the formation and stability of social relationships within groups has been relatively ignored. We experimentally tested how predation threat influenced fine-scale social network structure using Trinidadian guppies (Poecilia reticulata). When perceived predation risk was high, individuals developed stable and more differentiated social ties compared to when perceived risk was low. Intriguingly, social differentiation coincided with shoals being somewhat smaller under high-perceived risk, suggesting a possible conflict between forming stable social relationships and larger social groups. Individuals most at risk of predation (large and bold individuals) showed the most exaggerated responses in several social measures. Taken together, we provide the first experimental evidence that proximate risk of predation can increase the intensity of social relationships and fine-scale social structure in animal populations.

Male sexually coercive behaviour drives increased swimming efficiency in female guppies.

Sexual coercion of females by males is widespread across sexually reproducing species. It stems from a conflict of interest over reproduction and exerts selective pressure on both sexes. For females, there is often a significant energetic cost of exposure to male sexually coercive behaviours.Our understanding of the efficiency of female resistance to male sexually coercive behaviour is key to understanding how sexual conflict contributes to population level dynamics and ultimately to the evolution of sexually antagonistic traits.Overlooked within this context are plastic physiological responses of traits within the lifetime of females that could moderate the energetic cost imposed by coercive males. Here, we examined whether conflict over the frequency and timing of mating between male and female guppies Poecilia reticulata can induce changes in swimming performance and aerobic capacity in females as they work to escape harassment by males.Females exposed to higher levels of harassment over a 5-month period used less oxygen to swim at a given speed, but displayed no difference in resting metabolic rate, maximal metabolic rate, maximal sustained swimming speed or aerobic scope compared to females receiving lower levels of harassment.The observed increase in swimming efficiency is at least partially related to differences in swimming mechanics, likely brought on by a training effect of increased activity, as highly harassed females spent less time performing pectoral fin-assisted swimming.Sexual conflict results in sexually antagonistic traits that impose a variety of costs, but our results show that females can reduce costs through phenotypic plasticity. It is also possible that phenotypic plasticity in swimming physiology or mechanics in response to sexual coercion can potentially give females more control over matings and affect which male traits are under selection.

Adaptive prolonged postreproductive life span in killer whales.

Prolonged life after reproduction is difficult to explain evolutionarily unless it arises as a physiological side effect of increased longevity or it benefits related individuals (i.e., increases inclusive fitness). There is little evidence that postreproductive life spans are adaptive in nonhuman animals. By using multigenerational records for two killer whale (Orcinus orca) populations in which females can live for decades after their final parturition, we show that postreproductive mothers increase the survival of offspring, particularly their older male offspring. This finding may explain why female killer whales have evolved the longest postreproductive life span of all nonhuman animals.