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.].

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.

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.

Lunar Phases and Wildlife-Vehicle Collisions: Application of the Lunar Disk Percentage Method.

We investigated the relationship between lunar illumination based on the percentage of the visible lunar disk (LDP) and the frequency of wildlife-vehicle collisions (WVCs) in Lithuania. We analyzed WVC frequency during ten 10% LDP intervals to more precisely reflect the relationship between LDP and WVC. The 10% LDP interval approach showed a significant trend of increasing WVC frequencies with an increasing LDP at night. We also examined the correlation between the daily numbers of WVCs and LDP for different months and seasons. The relationship seemed to be stronger at night and during the late autumn-winter months, particularly in December, suggesting the importance of lunar illumination on WVCs. There was a weak positive correlation between LDP and overall daily number of WVCs (rs = 0.091; p < 0.001) and between LDP and night WVCs (rs = 0.104; p < 0.001). We found significant positive correlations for winter (December-February) (rs = 0.118; p = 0.012) and autumn (August-November) (rs = 0.127; p = 0.007). Our study suggests that the LDP interval approach may provide more possibilities for the evaluation and quantification of WVCs and lunar light relationships than the traditional lunar phase approach.

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.

BCG epidemiology supports its protection against COVID-19? A word of caution.

The COVID-19 pandemic, caused by type 2 Severe Acute Respiratory Syndrome Coronavirus (SARS-CoV-2), puts all of us to the test. Epidemiologic observations could critically aid the development of protective measures to combat this devastating viral outbreak. Recent observations, linked nation based universal Bacillus Calmette-Guerin (BCG) vaccination to potential protection against morbidity and mortality from SARS-CoV-2, and received much attention in public media. We wished to validate the findings by examining the country based association between COVID-19 mortality per million population, or daily rates of COVID-19 case fatality (i.e. Death Per Case/Days of the endemic [dpc/d]) and the presence of universal BCG vaccination before 1980, or the year of the establishment of universal BCG vaccination. These associations were examined in multiple regression modeling based on publicly available databases on both April 3rd and May 15th of 2020. COVID-19 deaths per million negatively associated with universal BCG vaccination in a country before 1980 based on May 15th data, but this was not true for COVID-19 dpc/d on either of days of inquiry. We also demonstrate possible arbitrary selection bias in such analyses. Consequently, caution should be exercised amidst the publication surge on COVID-19, due to political/economical-, arbitrary selection-, and fear/anxiety related biases, which may obscure scientific rigor. We argue that global COVID-19 epidemiologic data is unreliable and therefore should be critically scrutinized before using it as a nidus for subsequent hypothesis driven scientific discovery.

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.

Ecological Stoichiometry: A Link Between Developmental Speed and Physiological Stress in an Omnivorous Insect.

The elemental composition of organisms belongs to a suite of functional traits that may adaptively respond to fluctuating selection pressures. Life history theory predicts that predation risk and resource limitations impose selection pressures on organisms' developmental time and are further associated with variability in energetic and behavioral traits. Individual differences in developmental speed, behaviors and physiology have been explained using the pace-of-life syndrome (POLS) hypothesis. However, how an organism's developmental speed is linked with elemental body composition, metabolism and behavior is not well understood. We compared elemental body composition, latency to resume activity and resting metabolic rate (RMR) of western stutter-trilling crickets (Gryllus integer) in three selection lines that differ in developmental speed. We found that slowly developing crickets had significantly higher body carbon, lower body nitrogen and higher carbon-to-nitrogen ratio than rapidly developing crickets. Slowly developing crickets had significantly higher RMR than rapidly developing crickets. Male crickets had higher RMR than females. Slowly developing crickets resumed activity faster in an unfamiliar relative to a familiar environment. The rapidly developing crickets did the opposite. The results highlight the tight association between life history, physiology and behavior. This study indicates that traditional methods used in POLS research should be complemented by those used in ecological stoichiometry, resulting in a synthetic approach that potentially advances the whole field of behavioral and physiological ecology.

Linking organismal growth, coping styles, stress reactivity, and metabolism via responses against a selective serotonin reuptake inhibitor in an insect.

Evidence suggests that brain serotonin (5-HT) is one of the central mediators of different types of animal personality. We tested this assumption in field crickets Gryllus integer using a selective serotonin reuptake inhibitor (SSRI). Crickets were selected for slow and rapid development and tested for their coping styles under non-stressful conditions (time spent exploring a novel object). Resting metabolic rate, maximum metabolic rate and latency to resume activity were measured under stressful conditions (stress reactivity). Measurements were taken (i) before and (ii) during the SSRI treatment. Before the SSRI treatment, a strong negative correlation was observed between coping style and stress reactivity, which suggests the existence of a behavioral syndrome. After the SSRI treatment, the syndrome was no longer evident. The results of this study show that 5-HT may be involved in regulating behavior not only along a stress reactivity gradient but also along a coping styles axis. The relationship between personality and the strength and direction of 5-HT treatment on observed behaviors indicates trait-like individual differences in 5-HT signaling. Overall, these findings do not support recent ideas arising from the pace-of-life syndrome (POLS) hypothesis, which predict higher exploration and metabolic rates in rapidly developing bold animals.

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.

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.

Short-term exposure to predation affects body elemental composition, climbing speed and survival ability in Drosophila melanogaster.

Factors such as temperature, habitat, larval density, food availability and food quality substantially affect organismal development. In addition, risk of predation has a complex impact on the behavioural and morphological life history responses of prey. Responses to predation risk seem to be mediated by physiological stress, which is an adaptation for maintaining homeostasis and improving survivorship during life-threatening situations. We tested whether predator exposure during the larval phase of development has any influence on body elemental composition, energy reserves, body size, climbing speed and survival ability of adult Drosophila melanogaster. Fruit fly larvae were exposed to predation by jumping spiders (Phidippus apacheanus), and the percentage of carbon (C) and nitrogen (N) content, extracted lipids, escape response and survival were measured from predator-exposed and control adult flies. The results revealed predation as an important determinant of adult phenotype formation and survival ability. D. melanogaster reared together with spiders had a higher concentration of body N (but equal body C), a lower body mass and lipid reserves, a higher climbing speed and improved adult survival ability. The results suggest that the potential of predators to affect the development and the adult phenotype of D. melanogaster is high enough to use predators as a more natural stimulus in laboratory experiments when testing, for example, fruit fly memory and learning ability, or when comparing natural populations living under different predation pressures.

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.

The impact of Great Cormorants on biogenic pollution of land ecosystems: Stable isotope signatures in small mammals.

Studying the isotopic composition of the hair of two rodent species trapped in the territories of Great Cormorant colonies, we aimed to show that Great Cormorants transfer biogens from aquatic ecosystems to terrestrial ecosystems, and that these substances reach small mammals through the trophic cascade, thus influencing the nutrient balance in the terrestrial ecosystem. Analysis of δ(13)C and δ(15)N was performed on two dominant species of small mammals, Apodemus flavicollis and Myodes glareolus, inhabiting the territories of the colonies. For both species, the values of δ(13)C and δ(15)N were higher in the animals trapped in the territories of the colonies than those in control territories. In the hair of A. flavicollis and M. glareolus, the highest values of δ(15)N (16.31±3.01‰ and 17.86±2.76‰, respectively) were determined in those animals trapped in the biggest Great Cormorant colony. δ(15)N values were age dependent, highest in adult A. flavicollis and M. glareolus and lowest in juvenile animals. For δ(13)C values, age-dependent differences were not registered. δ(15)N values in both small mammal species from the biggest Great Cormorant colony show direct dependence on the intensity of influence. Biogenic pollution is at its strongest in the territories of the colonies with nests, significantly diminishing in the ecotones of the colonies and further in the control zones, where the influence of birds is negligible. Thus, Great Cormorant colonies alter ecosystem functioning by enrichment with biogens, with stable isotope values in small mammals significantly higher in the affected territories.