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.].

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.

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

The development of high-throughput behavioral assays, where numerous individual animals can be analyzed in various experimental conditions, has facilitated the study of animal personality. Previous research showed that isogenic Drosophila melanogaster flies exhibit striking individual non-heritable locomotor handedness. The variability of this trait, i.e., the predictability of left-right turn biases, varies across genotypes and under the influence of neural activity in specific circuits. This suggests that the brain can dynamically regulate the extent of animal personality. It has been recently shown that predators can induce changes in prey phenotypes via lethal or non-lethal effects affecting the serotonergic signaling system. In this study, we tested whether fruit flies grown with predators exhibit higher variability/lower predictability in their turning behavior and higher survival than those grown with no predators in their environment. We confirmed these predictions and found that both effects were blocked when flies were fed an inhibitor (αMW) of serotonin synthesis. The results of this study demonstrate a negative association between the unpredictability of turning behavior of fruit flies and the hunting success of their predators. We also show that the neurotransmitter serotonin controls predator-induced changes in the turning variability of fruit flies, regulating the dynamic control of behavioral predictability.

Selective selfishness in alarm calling behaviour by some members of wintering mixed-species groups of crested tits and willow tits.

Animals adjust their use of alarm calls depending on social environments. We tested whether dominant (adult) and subordinate (juvenile non-kin) male crested tits (Lophophanes cristatus) warn each other and heterospecific willow tits (Poecile montanus) across the wintering season. Birds rarely alarm called when feeding alone. Both adult and juvenile crested tits warned each other in early winter, and adults did so in the middle of wintering season. However, juvenile males rarely warned conspecific adult males in the middle of the winter. Both adult and juvenile males stopped giving alarm calls when feeding together at the end of wintering season. The results suggest that the mid-winter reduction of juvenile alarms could increase the likelihood of successful predator attacks on adults, increasing the chances for juveniles to replace adults and acquire their territories. By contrast, both adult and juvenile males produced alarm calls throughout the season when foraging together with willow tits. Whether juvenile male crested tits could be selectively altering alarm call propensity to endanger adult males, thereby selfishly enhancing their own succession to territory ownership, is discussed. The results add to the understanding of the origin of mixed-species groups and explain the dynamics of social communication. This article is part of the theme issue 'Mixed-species groups and aggregations: shaping ecological and behavioural patterns and processes'.

Physiological stress and higher reproductive success in bumblebees are both associated with intensive agriculture.

Free-living organisms face multiple stressors in their habitats, and habitat quality often affects development and life history traits. Increasing pressures of agricultural intensification have been shown to influence diversity and abundance of insect pollinators, and it may affect their elemental composition as well. We compared reproductive success, body concentration of carbon (C) and nitrogen (N), and C/N ratio, each considered as indicators of stress, in the buff-tailed bumblebee (Bombus terrestris). Bumblebee hives were placed in oilseed rape fields and semi-natural old apple orchards. Flowering season in oilseed rape fields was longer than that in apple orchards. Reproductive output was significantly higher in oilseed rape fields than in apple orchards, while the C/N ratio of queens and workers, an indicator of physiological stress, was lower in apple orchards, where bumblebees had significantly higher body N concentration. We concluded that a more productive habitat, oilseed rape fields, offers bumblebees more opportunities to increase their fitness than a more natural habitat, old apple orchards, which was achieved at the expense of physiological stress, evidenced as a significantly higher C/N ratio observed in bumblebees inhabiting oilseed rape fields.

Dominance of Fructose-Associated Fructobacillus in the Gut Microbiome of Bumblebees (Bombus terrestris) Inhabiting Natural Forest Meadows.

Bumblebees are key pollinators in agricultural landscapes. However, little is known about how gut microbial communities respond to anthropogenic changes. We used commercially produced colonies of buff-tailed bumblebees (Bombus terrestris) placed in three habitats. Whole guts (midgut, hindgut, and rectum) of B. terrestris specimens were dissected from the body and analyzed using 16S phylogenetic community analysis. We observed significantly different bacterial community composition between the agricultural landscapes (apple orchards and oilseed rape (Brassica napus) fields) and forest meadows, whereas differences in gut communities between the orchards and oilseed rape fields were nonsignificant. Bee-specific bacterial genera such as Lactobacillus, Snodgrassella, and Gilliamella dominated gut communities of B. terrestris specimens. In contrast, the guts of B. terrestris from forest meadows were dominated by fructose-associated Fructobacillus spp. Bacterial communities of workers were the most diverse. At the same time, those of males and young queens were less diverse, possibly reflecting greater exposure to the colony's inner environment compared to the environment outside the colony, as well as bumblebee age. Our results suggest that habitat quality, exposure to environmental microbes, nectar quality and accessibility, and land use significantly affect gut bacterial composition in B. terrestris.

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.

Ecological Stoichiometry of Bumblebee Castes, Sexes, and Age Groups.

Ecological stoichiometry is important for revealing how the composition of chemical elements of organisms is influenced by their physiological functions and ecology. In this study, we investigated the elemental body composition of queens, workers, and males of the bumblebee Bombus terrestris, an important pollinator throughout Eurasia, North America, and northern Africa. Our results showed that body elemental content differs among B. terrestris castes. Young queens and workers had higher body nitrogen concentration than ovipositing queens and males, while castes did not differ significantly in their body carbon concentration. Furthermore, the carbon-to-nitrogen ratio was higher in ovipositing queens and males. We suggest that high body nitrogen concentration and low carbon-to-nitrogen ratio in young queens and workers may be related to their greater amount of flight muscles and flight activities than to their lower stress levels. To disentangle possible effects of stress in the agricultural landscape, further studies are needed to compare the elemental content of bumblebee bodies between natural habitats and areas of high-intensity agriculture.

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.

Serotoninergic Modulation of Phototactic Variability Underpins a Bet-Hedging Strategy in Drosophila melanogaster.

When organisms' environmental conditions vary unpredictably in time, it can be advantageous for individuals to hedge their phenotypic bets. It has been shown that a bet-hedging strategy possibly underlies the high inter-individual diversity of phototactic choice in Drosophila melanogaster. This study shows that fruit flies from a population living in a boreal and relatively unpredictable climate have more variable variable phototactic biases than fruit flies from a more stable tropical climate, consistent with bet-hedging theory. We experimentally show that phototactic variability of D. melanogaster is regulated by the neurotransmitter serotonin (5-HT), which acts as a suppressor of the variability of phototactic choices. When fed 5-HT precursor, boreal flies exhibited lower variability, and they were insensitive to 5-HT inhibitor. The opposite pattern was seen in the tropical flies. Thus, the reduction of 5-HT in fruit flies' brains may be the mechanistic basis of an adaptive bet-hedging strategy in a less predictable boreal climate.

MHC Class II Heterozygosity Associated With Attractiveness of Men and Women.

The genes of the Major Histocompatibility Complex (MHC), which plays a fundamental role in the immune system, are some of the most diverse genes in vertebrates and have been connected to mate choice in several species, including humans. While studies suggest a positive relationship between MHC diversity and male facial attractiveness, the connection of MHC diversity to other visual traits and female attractiveness is still unclear. The purpose of this study was to investigate further whether MHC heterozygosity, indicating genetic quality, is associated with visual traits affecting mate preferences in humans. In total 74 Latvian men and 49 women were genotyped for several MHC loci and rated for facial and, in men, also body attractiveness. The results indicate a preference for MHC heterozygous female and male faces. However, the initially positive relationship between MHC heterozygosity and facial attractiveness becomes non-significant in females, when controlling for multiple testing, and in males, when age and fat content is taken into account, referring to the importance of adiposity in immune function and thus also attractiveness. Thus overall the effect of MHC heterozygosity on attractiveness seems weak. When considering separate loci, we show that the main gene related to facial attractiveness is the MHC class II DQB1; a gene important also in viral infections and autoimmune diseases. Indeed, in our study, heterozygous individuals are rated significantly more attractive than their homozygous counterparts, only in relation to gene DQB1. This study is the first to indicate a link between DQB1 and attractiveness in humans.

Socioeconomic position, immune function, and its physiological markers.

The development of costly traits such as immune function and secondary sexual traits is constrained by resource availability. The quality of developmental conditions and the availability of resources in ontogeny may therefore influence immune system functions and other biological traits. We analyzed causal pathways between family socioeconomic position, strength of immune response, and five physiological biomarkers in young Latvian men (n = 93) using structural equation modeling. Men from wealthier families had higher testosterone levels (rs = 0.280), stronger immune response (rs = 0.551), and higher facial attractiveness (rs = 0.300). There were weak, non-significant correlations between family income, body fat percentage (rs = -0.147), and fluctuating asymmetry (rs = -0.159). Testosterone partially (33.8%) mediated the effect of family income on facial masculinity. Testosterone (positively) and adiposity (negatively) partially (4%) mediated the relationship between family income and immune function. Higher facial masculinity, higher facial symmetry, and lower adiposity were reliable and independent cues of better immune function (R2 = 0.238) in a larger sample of young Latvian men (N = 146). Resource availability in ontogeny has an important role for the development of immune function and physical appearance, and it is a key parameter to be included in human eco-immunological research.

The Obesity Paradox Predicts the Second Wave of COVID-19 to Be Severe in Western Countries.

While COVID-19 infection and mortality rates are soaring in Western countries, Southeast Asian countries have successfully avoided the second wave of the SARS-CoV-2 pandemic despite high population density. We provide a biochemical hypothesis for the connection between low COVID-19 incidence, mortality rates, and high visceral adiposity in Southeast Asian populations. The SARS-CoV-2 virus uses angiotensin-converting enzyme 2 (ACE2) as a gateway into the human body. Although the highest expression levels of ACE2 are found in people's visceral adipose tissue in Southeast Asia, this does not necessarily make them vulnerable to COVID-19. Hypothetically, high levels of visceral adiposity cause systemic inflammation, thus decreasing the ACE2 amount on the surface of both visceral adipocytes and alveolar epithelial type 2 cells in the lungs. Extra weight gained during the pandemic is expected to increase visceral adipose tissue in Southeast Asians, further decreasing the ACE2 pool. In contrast, weight gain can increase local inflammation in fat depots in Western people, leading to worse COVID-related outcomes. Because of the biological mechanisms associated with fat accumulation, inflammation, and their differential expression in Southeast Asian and Western populations, the second wave of the pandemic may be more severe in Western countries, while Southeast Asians may benefit from their higher visceral fat depots.

Effect of Juvenile Hormone on Resistance against Entomopathogenic Fungus Metarhizium robertsii Differs between Sexes.

Juvenile hormone has been suggested to be a potential mediator in the trade-off between mating and insects' immunity. Studies on various insect taxons have found that juvenile hormone interferes with humoral and cellular immunity. Although this was shown experimentally, studies using highly virulent parasites or pathogens are lacking so far. In this study, we tested if juvenile hormone administration affected resistance against entomopathogenic fungi, Metarhizium robertsii, in the mealworm beetle, Tenebrio molitor. In previous studies with T. molitor, juvenile hormone has been found to reduce a major humoral immune effector-system (phenoloxidase) in both sexes and decrease the encapsulation response in males. Here, we found that juvenile hormone administration prolonged survival time after infection with M. robertsii in males but reduced survival time in females. This study indicates that the effects of juvenile hormone on insect immunity might be more complicated than previously considered. We also suggest that there might be a trade-off between specific and non-specific immunity since, in males, juvenile hormone enhances specific immunity but corrupts non-specific immunity. Our study highlights the importance of using real parasites and pathogens in immuno-ecological studies.

Covid-19: Fat, Obesity, Inflammation, Ethnicity, and Sex Differences.

Although obesity is known to be a risk factor for COVID-19 severity, there is an urgent need to distinguish between different kinds of fat-visceral and subcutaneous fat-and their inflammation status in COVID-19. These different fat types have partially diverging biochemical roles in the human body, and they are differentially associated with SARS-CoV-2, which targets the angiotensin-converting enzyme 2 (ACE2) for cell entry. ACE2 is highly expressed in adipose tissue, especially in visceral fat, suggesting an important role for this tissue in determining COVID-19 disease severity. In this perspective article, we discuss group differences in the amount of visceral fat levels and the extent of inflammation in adipocytes of visceral fat tissue, which may, in part, drive population, cross-national, ethnic, and sex differences in COVID-19 disease. It is vital to steer the scientific community's attention to the effects of visceral fat in creating individual and population differences in COVID-19 severity. This can help researchers unravel the reasons for the reported population, ethnic, and sex differences in COVID-19 severity and mortality.

Women's socioeconomic position in ontogeny is associated with improved immune function and lower stress, but not with height.

Immune function, height and resource accumulation comprise important life history traits in humans. Resource availability models arising from life history theory suggest that socioeconomic conditions influence immune function, growth and health status. In this study, we tested whether there are associations between family income during ontogeny, adult height, cortisol level and immune response in women. A hepatitis B vaccine was administered to 66 young Latvian women from different socioeconomic backgrounds, and blood samples were then collected to measure the level of antibodies that the women produced in response to the vaccination. Cortisol levels were measured from plasma samples pre- and post-vaccination. Women from wealthier families had lower cortisol levels, and women from the highest family income group had the highest levels of antibody titers against hepatitis B vaccine. No significant relationships were observed between cortisol level and immune function, nor between family income and height. The results show that income level during ontogeny is associated with the strength of immune response and with psychoneuroendocrine pathways underlying stress perception in early adulthood. The findings indicate that the quality of the developmental niche is associated with the condition-dependent expression of immune function and stress response.

Egalitarian mixed-species bird groups enhance winter survival of subordinate group members but only in high-quality forests.

Only dominant individuals have unrestricted access to contested resources in group-living animals. In birds, subordinates with restricted access to resources may respond to intragroup contests by acquiring extra body reserves to avoid periods of food shortage. In turn, higher body mass reduces agility and increases predation and mortality risk to subordinates. Birds often live in hierarchically organized mixed-species groups, in which heterospecific individuals are considered to substitute for conspecifics as protection against predators at a significantly reduced competition cost. Crested tits (Lophophanes cristatus) and willow tits (Poecile montanus) form mixed-species groups during the non-reproductive season that typically exhibit a nearly linear dominance hierarchy ('despotic' social structure) in which the highest ranking male willow tit is fourth in the overall hierarchy after the dominant male, female and subordinate juvenile crested tit, respectively. Much less frequently, 'egalitarian' dominance structures occur in which the adult willow tits rank second and the hierarchy is less steep, or linear. We present a rare long-term data set in which egalitarian flocks are common enough to assess the consequences of this simple change in hierarchy structure as well as a potential driver of the pattern. A comparison of individuals in the despotic mixed-species groups revealed a strong negative correlation between subcutaneous fat stores and dominance rank in the interspecific dominance hierarchy, whereas in egalitarian groups, subordinate willow tits had significantly lower fat reserves and they foraged in safer parts of the canopy than willow tits in despotic groups. Moreover, egalitarian groups exhibited markedly less within-group aggression, higher group cohesion and improved winter survival in both tit species. However, winter survival of birds in egalitarian groups was impaired relative to despotic groups in forests recently affected by industrial forestry. This suggests that the more egalitarian bird societies may best be adapted to less-disturbed environments.

Eating Disorders: An Evolutionary Psychoneuroimmunological Approach.

Eating disorders are evolutionarily novel conditions. They lead to some of the highest mortality rates of all psychiatric disorders. Several evolutionary hypotheses have been proposed for eating disorders, but only the intrasexual competition hypothesis is extensively supported by evidence. We present the mismatch hypothesis as a necessary extension to the current theoretical framework of eating disorders. This hypothesis explains the evolutionarily novel adaptive metaproblem that has arisen when mating motives conflict with the large-scale and easy availability of hyper-rewarding but obesogenic foods. This situation is exacerbated particularly in those contemporary environments that are characterized by sedentary lifestyles, ever-present junk foods, caloric surplus and the ubiquity of social comparisons that take place via social media. Our psychoneuroimmunological model connects ultimate-level causation with proximate mechanisms by showing how the adaptive metaproblem between mating motives and food rewards leads to chronic stress and, further, to disordered eating. Chronic stress causes neuroinflammation, which increases susceptibility to OCD-like behaviors that typically co-occur with eating disorders. Chronic stress upregulates the serotonergic system and causes dysphoric mood in anorexia nervosa patients. Dieting, however, reduces serotonin levels and dysphoric mood, leading to a vicious serotonergic-homeostatic stress/starvation cycle whereby cortisol and neuroinflammation increase through stringent dieting. Our psychoneuroimmunological model indicates that between-individual and within-individual variation in eating disorders partially arises from (co)variation in gut microbiota and stress responsivity, which influence neuroinflammation and the serotonergic system. We review the advances that have been made in recent years in understanding how to best treat eating disorders, outlining directions for future clinical research. Current evidence indicates that eating disorder treatments should aim to reduce the chronic stress, neuroinflammation, stress responsivity and gut dysbiosis that fuel the disorders. Connecting ultimate causes with proximate mechanisms and treating biopsychosocial causes rather than manifest symptoms is expected to bring more effective and sophisticated long-term interventions for the millions of people who suffer from eating disorders.