Extra-pair paternity explains cooperation in a bird species.

In many social animals, females mate with multiple males, but the adaptive value of female extra-pair mating is not fully understood. Here, we tested whether male pied flycatchers (Ficedula hypoleuca) engaging in extra-pair copulations with neighboring females were more likely to assist their neighbors in antipredator defense. We found that extra-pair sires joined predator-mobbing more often, approached predators more closely, and attacked predators more aggressively than males without extra-pair offspring in the neighboring nest. Extra-pair mating may incentivize males to assist in nest defense because of the benefits that this cooperative behavior has on their total offspring production. For females, this mating strategy may help recruit more males to join in antipredator defense, offering better protection and ultimately improving reproductive success. Our results suggest a simple mechanism by which extra-pair mating can improve reproductive success in breeding birds. In summary, males siring extra-pair offspring in neighboring nests assist neighbors in antipredator defense more often than males without extra-pair offspring.

A diabetes-like biochemical and behavioural phenotype of Drosophila induced by predator stress.

Predation can have both lethal and non-lethal effects on prey. The non-lethal effects of predation can instil changes in prey life history, behaviour, morphology and physiology, causing adaptive evolution. The chronic stress caused by sustained predation on prey is comparable to chronic stress conditions in humans. Conditions like anxiety, depression, and post-traumatic stress syndrome have also been implicated in the development of metabolic disorders such as obesity and diabetes. In this study, we found that predator stress induced during larval development in fruit flies Drosophila melanogaster impairs carbohydrate metabolism by systemic inhibition of Akt protein kinase, which is a central regulator of glucose uptake. However, Drosophila grown with predators survived better under direct spider predation in the adult phase. Administration of metformin and 5-hydroxytryptophan (5-HTP), a precursor of the neurotransmitter serotonin, reversed these effects. Our results demonstrate a direct link between predator stress and metabolic impairment, suggesting that a diabetes-like biochemical phenotype may be adaptive in terms of survival and reproductive success. We provide a novel animal model to explore the mechanisms responsible for the onset of these metabolic disorders, which are highly prevalent in human populations.

Manipulating mtDNA in vivo reprograms metabolism via novel response mechanisms.

Mitochondria have been increasingly recognized as a central regulatory nexus for multiple metabolic pathways, in addition to ATP production via oxidative phosphorylation (OXPHOS). Here we show that inducing mitochondrial DNA (mtDNA) stress in Drosophila using a mitochondrially-targeted Type I restriction endonuclease (mtEcoBI) results in unexpected metabolic reprogramming in adult flies, distinct from effects on OXPHOS. Carbohydrate utilization was repressed, with catabolism shifted towards lipid oxidation, accompanied by elevated serine synthesis. Cleavage and translocation, the two modes of mtEcoBI action, repressed carbohydrate rmetabolism via two different mechanisms. DNA cleavage activity induced a type II diabetes-like phenotype involving deactivation of Akt kinase and inhibition of pyruvate dehydrogenase, whilst translocation decreased post-translational protein acetylation by cytonuclear depletion of acetyl-CoA (AcCoA). The associated decrease in the concentrations of ketogenic amino acids also produced downstream effects on physiology and behavior, attributable to decreased neurotransmitter levels. We thus provide evidence for novel signaling pathways connecting mtDNA to metabolism, distinct from its role in supporting OXPHOS.

Ecological traps: evidence of a fitness cost in a cavity-nesting bird.

Habitat quality has direct effects on the evolutionary fitness of breeding organisms, which is why it is believed that animals tend to have an evolved preference for the best possible habitats. However, some animals may mistakenly choose to reproduce in habitats that decrease their fitness, resulting in 'ecological traps'. In this study, we tested whether great tits (Parus major) attracted to areas affected by outbreaks of the great web-spinning sawfly (Acantholyda posticalis) had fitness detriments characteristic of ecological traps. Sawfly larvae consume pine needles, which decreases resource availability for birds co-habiting the forest. Using artificial nesting sites, we found that great tits inhabiting areas of sawfly outbreaks had similar clutch sizes as tits breeding in healthy forest patches; however, the fledgling number was significantly lower, and fledgling condition was worse in the damaged forests. While moth larvae are the most important food for bird nestlings, the forest patches damaged by sawflies had lower larval biomass. Although most ecological traps occur in environments altered by humans, this study shows that pest insects can lower habitat quality, forming ecological traps. Our results indicate that attracting cavity-nesting birds should be done with caution because it may negatively impact birds' nutritional status and reproductive fitness.

A head start for life history development? Family income mediates associations between height and immune response in men.

OBJECTIVES: Male height and health affect a diverse range of social and economic outcomes such as competition for resources and mates. Life history theory predicts that limited availability of bioenergetic resources curbs the development of central life history functions such as somatic growth, immunity, and investment in offspring. Although genetic factors are important determinants of height, other factors such as income level may affect the incidence of infections during ontogeny, thus having indirect effects on somatic growth. We tested whether growing up in families with a higher income positively affects height and immune function. MATERIALS AND METHODS: Seventy-three young Latvian men from various socioeconomic backgrounds were given a hepatitis B vaccine. Blood samples were subsequently collected to measure the antibodies produced in response to the vaccination. Tweedie compound Poisson generalized linear models were used to examine relationships between height, family income, and antibody titers. RESULTS: Both height and family income positively correlated with the strength of men's immune response. However, when testing for the simultaneous effects of height and income on antibody titers, the statistical models showed that height affected antibody levels indirectly because income level mediated variance in height. DISCUSSION: The results of this study show that the relationships between height and immune function in young men are more complex than previously thought. Associations between taller stature of men and the robustness of their immune response are indirect because resource availability affects both somatic growth and the development of the immune system.

Independent and interactive effects of immune activation and larval diet on adult immune function, growth and development in the greater wax moth (Galleria mellonella).

Organisms in the wild are likely to face multiple immune challenges as well as additional ecological stressors, yet their interactive effects on immune function are poorly understood. Insects are found to respond to cues of increased infection risk by enhancing their immune capacity. However, such adaptive plasticity in immune function may be limited by physiological and environmental constraints. Here, we investigated the effects of two environmental stressors - poor larval diet and an artificial parasite-like immune challenge at the pupal stage - on adult immune function, growth and development in the greater wax moth (Galleria mellonella). Males whose immune system was activated with an artificial parasite-like immune challenge had weaker immune response - measured as strength of encapsulation response - as adults compared to the control groups, but only when reared on high-nutrition larval diet. Immune activation did not negatively affect adult immune response in males reared on low-nutrition larval diet, indicating that poor larval diet improved the capacity of the insects to respond to repeated immune challenges. Low-nutrition larval diet also had a positive independent effect on immune capacity in females, yet it negatively affected development time and adult body mass in both sexes. As in the nature immune challenges are rarely isolated, and adverse nutritional environment may indicate an elevated risk of infection, resilience to repeated immune challenges as a response to poor nutritional conditions could provide a significant fitness advantage. This study highlights the importance of considering environmental context when investigating the effects of immune activation in insects.

Metabolic rate associates with, but does not generate covariation between, behaviours in western stutter-trilling crickets, Gryllus integer.

The causes and consequences of among-individual variation and covariation in behaviours are of substantial interest to behavioural ecology, but the proximate mechanisms underpinning this (co)variation are still unclear. Previous research suggests metabolic rate as a potential proximate mechanism to explain behavioural covariation. We measured the resting metabolic rate (RMR), boldness and exploration in western stutter-trilling crickets, Gryllus integer, selected differentially for short and fast development over two generations. After applying mixed-effects models to reveal the sign of the covariation, we applied structural equation models to an individual-level covariance matrix to examine whether the RMR generates covariation between the measured behaviours. All traits showed among-individual variation and covariation: RMR and boldness were positively correlated, RMR and exploration were negatively correlated, and boldness and exploration were negatively correlated. However, the RMR was not a causal factor generating covariation between boldness and exploration. Instead, the covariation between all three traits was explained by another, unmeasured mechanism. The selection lines differed from each other in all measured traits and significantly affected the covariance matrix structure between the traits, suggesting that there is a genetic component in the trait integration. Our results emphasize that interpretations made solely from the correlation matrix might be misleading.

Microbiome symbionts and diet diversity incur costs on the immune system of insect larvae.

Communities of symbiotic microorganisms that colonize the gastrointestinal tract play an important role in food digestion and protection against opportunistic microbes. Diet diversity increases the number of symbionts in the intestines, a benefit that is considered to impose no cost for the host organism. However, less is known about the possible immunological investments that hosts have to make in order to control the infections caused by symbiont populations that increase because of diet diversity. Using taxonomical composition analysis of the 16S rRNA V3 region, we show that enterococci are the dominating group of bacteria in the midgut of the larvae of the greater wax moth (Galleria mellonella). We found that the number of colony-forming units of enterococci and expressions of certain immunity-related antimicrobial peptide (AMP) genes such as Gallerimycin, Gloverin, 6-tox, Cecropin-D and Galiomicin increased in response to a more diverse diet, which in turn decreased the encapsulation response of the larvae. Treatment with antibiotics significantly lowered the expression of all AMP genes. Diet and antibiotic treatment interaction did not affect the expression of Gloverin and Galiomicin AMP genes, but significantly influenced the expression of Gallerimycin, 6-tox and Cecropin-D Taken together, our results suggest that diet diversity influences microbiome diversity and AMP gene expression, ultimately affecting an organism's capacity to mount an immune response. Elevated basal levels of immunity-related genes (Gloverin and Galiomicin) might act as a prophylactic against opportunistic infections and as a mechanism that controls the gut symbionts. This would indicate that a diverse diet imposes higher immunity costs on organisms.

Habitat quality affects stress responses and survival in a bird wintering under extremely low ambient temperatures.

Animals normally respond to stressful environmental stimuli by releasing glucocorticoid hormones. We investigated whether baseline corticosterone (CORT), handling-induced corticosterone concentration(s), and body condition indices of members of willow tit (Poecile montanus) groups differed while wintering in old growth forests and managed young forests in mild weather conditions and during cold spells. Willow tits spend the winter season in non-kin groups in which dominant individuals typically claim their priority to access resources, while subordinate individuals may experience greater levels of stress and higher mortality, especially during cold spells. We captured birds to measure baseline CORT and levels of handling-induced CORT secretion after 20 min of capture. Willow tits in the young forests had higher baseline CORT and a smaller increase in CORT in response to capture than individuals in the old forests. Baseline CORT was higher in females and juvenile birds compared to adult males, whereas handling-induced CORT secretion did not differ between birds of different ages. During cold spells, baseline CORT of willow tits increased and handling-induced CORT secretion decreased, especially in birds in young forests. Willow tits' survival was higher in the old forests, with dominant individuals surviving better than subordinates. Our results show that changes in CORT secretion reflect responses to habitat quality and climate harshness, indicating young managed coniferous forests as a suboptimal habitat for the willow tit.

A dark cuticle allows higher investment in immunity, longevity and fecundity in a beetle upon a simulated parasite attack.

Cuticle melanism in insects is linked to a number of life history traits: a positive relationship is hypothesized between melanism, immune function, fecundity and lifespan. However, it is not clear how activation of the immune system affects trade-offs between life history traits in female mealworm beetles (Tenebrio molitor) differing in cuticle melanization. The females with tan, brown and black cuticles examined in the present study did not differ in the intensity of encapsulation response, fecundity and longevity when their immune system was not activated. However, we found that immune activation and cuticle melanization have a significant effect on life history traits. Offspring number and lifespan decreased in females with tan and brown cuticles, while the fecundity and lifespan of black females were not affected. Importantly, we inserted the implants again and found a significant decrease in the strength of encapsulation response in females with tan and brown cuticles. In contrast, black females increased melanotic reactions against the nylon implant, suggesting immunological priming. The results show that cuticle melanization plays an important adaptive role under the risk of being infected, while the lack of these benefits before the insertion of nylon monofilaments suggests that there are costs associated with an activated immunity system.

Resource availability as a proxy for terminal investment in a beetle.

Terminal investment hypothesis is a longstanding theoretical idea that organisms should increase their reproductive effort as their prospects for survival and reproduction decline. However, numerous attempts to test the terminal investment in reproduction have yielded contradictory results. This study reports an experimental confirmation of the terminal investment hypothesis. It was predicted that immune-challenged yellow mealworm beetles (Tenebrio molitor) are more likely to follow terminal investment strategy when their food resources are limited. Our results suggest the key role of food resources while making decisions to follow a terminal investment strategy. We found that male individuals invested in their sexual attractiveness at the expense of immune response and survival when food was not available. In contrast, the beetles did not decrease their lifespan and did not invest in the attractiveness of their sex odours under conditions of food ad libitum. Our results show the importance of food availability and quality in understanding the evolution of reproductive strategies.

Tufted titmouse (Baeolophus bicolor) calling and risk-sensitive foraging in the face of threat.

Individuals often produce alarm or mobbing calls when they detect a threat such as a predator. Little is known about whether such calling is affected by the facial orientation of a potential threat, however. We tested for an effect of facial orientation of a potential threat on tufted titmice, Baeolophus bicolor, a songbird that uses chick-a-dee calls in a variety of social contexts. In two studies, a human observer wore an animal mask that either faced or faced away from the focal bird(s). In Study 1, focal birds were individual titmice captured in a walk-in trap, and the observer stood near the trapped bird. In Study 2, focal birds were titmouse flocks utilizing a feeding station and the observer stood near the station. In both studies, calling behavior was affected by mask orientation. In Study 2, foraging and agonistic behavior were also affected. Titmice can therefore perceive the facial orientation of a potential threat, and this perception affects different behavioral systems, including calling. Our results indicate sensitivity of titmice to the facial orientation of a potential predator in two quite different motivational contexts. This work suggests the possibility of strategic signaling by prey species depending upon the perceptual space of a detected predator.

Body height, immunity, facial and vocal attractiveness in young men.

Health, facial and vocal attributes and body height of men may affect a diverse range of social outcomes such as attractiveness to potential mates and competition for resources. Despite evidence that each parameter plays a role in mate choice, the relative role of each and inter-relationships between them, is still poorly understood. In this study, we tested relationships both between these parameters and with testosterone and immune function. We report positive relationships between testosterone with facial masculinity and attractiveness, and we found that facial masculinity predicted facial attractiveness and antibody response to a vaccine. Moreover, the relationship between antibody response to a hepatitis B vaccine and body height was found to be non-linear, with a positive relationship up to a height of 188 cm, but an inverse relationship in taller men. We found that vocal attractiveness was dependent upon vocal masculinity. The relationship between vocal attractiveness and body height was also non-linear, with a positive relationship of up to 178 cm, which then decreased in taller men. We did not find a significant relationship between body height and the fundamental frequency of vowel sounds provided by young men, while body height negatively correlated with the frequency of second formant. However, formant frequency was not associated with the strength of immune response. Our results demonstrate the potential of vaccination research to reveal costly traits that govern evolution of mate choice in humans and the importance of trade-offs among these traits.

Corrigendum: Development under predation risk increases serotonin-signaling, variability of turning behavior and survival in adult fruit flies Drosophila melanogaster.

[This corrects the article DOI: 10.3389/fnbeh.2023.1189301.].

The excuse principle can maintain cooperation through forgivable defection in the Prisoner's Dilemma game.

Reciprocal altruism describes a situation in which an organism acts in a manner that temporarily reduces its fitness while increasing another organism's fitness, but there is an ultimate fitness benefit based on an expectation that the other organism will act in a similar manner at a later time. It creates the obvious dilemma in which there is always a short-term benefit to cheating, therefore cooperating individuals must avoid being exploited by non-cooperating cheaters. This is achieved by following various decision rules, usually variants of the tit-for-tat (TFT) strategy. The strength of TFT, however, is also its weakness-mistakes in implementation or interpretation of moves, or the inability to cooperate, lead to a permanent breakdown in cooperation. We show that pied flycatchers (Ficedula hypoleuca) use a TFT with an embedded 'excuse principle' to forgive the neighbours that were perceived as unable to cooperate during mobbing of predators. The excuse principle dramatically increases the stability of TFT-like behavioural strategies within the Prisoner's Dilemma game.

Adiposity, compared with masculinity, serves as a more valid cue to immunocompetence in human mate choice.

According to the 'good genes' hypothesis, females choose males based on traits that indicate the male's genetic quality in terms of disease resistance. The 'immunocompetence handicap hypothesis' proposed that secondary sexual traits serve as indicators of male genetic quality, because they indicate that males can contend with the immunosuppressive effects of testosterone. Masculinity is commonly assumed to serve as such a secondary sexual trait. Yet, women do not consistently prefer masculine looking men, nor is masculinity consistently related to health across studies. Here, we show that adiposity, but not masculinity, significantly mediates the relationship between a direct measure of immune response (hepatitis B antibody response) and attractiveness for both body and facial measurements. In addition, we show that circulating testosterone is more closely associated with adiposity than masculinity. These findings indicate that adiposity, compared with masculinity, serves as a more important cue to immunocompetence in female mate choice.

Facial attractiveness is related to women's cortisol and body fat, but not with immune responsiveness.

Recent studies suggest that facial attractiveness indicates immune responsiveness in men and that this relationship is moderated by stress hormones which interact with testosterone levels. However, studies testing whether facial attractiveness in women signals their immune responsiveness are lacking. Here, we photographed young Latvian women, vaccinated them against hepatitis B and measured the amount of specific antibodies produced, cortisol levels and percentage body fat. Latvian men rated the attractiveness of the women's faces. Interestingly, in women, immune responsiveness (amount of antibodies produced) did not predict facial attractiveness. Instead, plasma cortisol level was negatively associated with attractiveness, indicating that stressed women look less attractive. Fat percentage was curvilinearly associated with facial attractiveness, indicating that being too thin or too fat reduces attractiveness. Our study suggests that in contrast to men, facial attractiveness in women does not indicate immune responsiveness against hepatitis B, but is associated with two other aspects of long-term health and fertility: circulating levels of the stress hormone cortisol and percentage body fat.

Nocturnal loss of body reserves reveals high survival risk for subordinate great tits wintering at extremely low ambient temperatures.

Winter acclimatization in birds is a complex of several strategies based on metabolic adjustment accompanied by long-term management of resources such as fattening. However, wintering birds often maintain fat reserves below their physiological capacity, suggesting a cost involved with excessive levels of reserves. We studied body reserves of roosting great tits in relation to their dominance status under two contrasting temperature regimes to see whether individuals are capable of optimizing their survival strategies under extreme environmental conditions. We predicted less pronounced loss of body mass and body condition and lower rates of overnight mortality in dominant great tits at both mild and extremely low ambient temperatures, when ambient temperature dropped down to -43 °C. The results showed that dominant great tits consistently maintained lower reserve levels than subordinates regardless of ambient temperature. However, dominants responded to the rising risk of starvation under low temperatures by increasing their body reserves, whereas subdominant birds decreased reserve levels in harsh conditions. Yet, their losses of body mass and body reserves were always lower than in subordinate birds. None of the dominant great tits were found dead, while five young females and one adult female were found dead in nest boxes during cold spells when ambient temperatures dropped down to -43 °C. The dead great tits lost up to 23.83 % of their evening body mass during cold nights while surviving individuals lost on average 12.78 % of their evening body mass. Our results show that fattening strategies of great tits reflect an adaptive role of winter fattening which is sensitive to changes in ambient temperatures and differs among individuals of different social ranks.