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.

Flock size increases with the diversity and abundance of local predators in an avian family.

Group living has long been viewed as an adaptation to reduce predation risk. Earlier comparative analyses provided support for the hypothesis but typically ignored variation in group size at the local scale and included proxies of predation risk rather than more direct estimates. Here, we related variation in group size at the scale of a study site in various species with the diversity and abundance of local predators. If larger groups provide protection against predators, we expected larger groups to evolve in species facing locally more diverse and abundant predators. We examined this hypothesis in one avian family, the Paridae, which are small arboreal birds that include some of the better studied species in ecology. From the literature, we gathered 275 flock size estimates from 34 species. In a phylogenetic framework and controlling for the potential confounding effect of latitude, we found that flock size increased with predation risk but only in flocks that included more than one species. We suggest that competition sets an upper limit to the size of flocks including conspecifics only. Joining flocks with other species, thus, allows individuals to increase flock size in response to higher predation risk without a substantial increase in competition. Overall, our results based on more direct estimates of predation risk provide further comparative evidence for an association between predation and the evolution of flocking in birds.

The son-killer microbe Arsenophonus nasoniae is a widespread associate of the parasitic wasp Nasonia vitripennis in Europe.

Heritable microbes that exhibit reproductive parasitism are common in insects. One class of these are the male-killing bacteria, which are found in a broad range of insect hosts. Commonly, our knowledge of the incidence of these microbes is based on one or a few sampling sites, and the degree and causes of spatial variation are unclear. In this paper, we examine the incidence of the son-killer microbe Arsenophonus nasoniae across European populations of its wasp host, Nasonia vitripennis. In preliminary work, we noticed two female N. vitripennis producing highly female biased sex ratios in a field study from the Netherlands and Germany. When tested, the brood from Germany was revealed to be infected with A. nasoniae. We then completed a broad survey in 2012, in which fly pupal hosts of N. vitripennis were collected from vacated birds' nests from four European populations, N. vitripennis wasps allowed to emerge and then tested for A. nasoniae presence through PCR assay. We then developed a new screening methodology based on direct PCR assays of fly pupae and applied this to ethanol-preserved material collected from great tit (Parus major) nests in Portugal. These data show A. nasoniae is found widely in European N. vitripennis, being present in Germany, the UK, Finland, Switzerland and Portugal. Samples varied in the frequency with which they carry A. nasoniae, from being rare to being present in 50% of the pupae parasitised by N. vitripennis. Direct screening of ethanol-preserved fly pupae was an effective method for revealing both wasp and A. nasoniae infection, and will facilitate sample transport across national boundaries. Future research should examine the causes of variation in frequency, in particular testing the hypothesis that N. vitripennis superparasitism rates drive the variation in A. nasoniae frequency through providing opportunities for infectious transmission.

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.

The costs of the immune memory within generations.

Immune response is evolutionary costly, but it is not clear whether these costs affect energetic expenditure (short-term cost), growth (medium-term cost), or reproduction (long-term cost). We tested the costs of immune memory in Tenebrio molitor against Metarhizium brunneum. To do this, we used two groups of T. molitor larvae: (a) the control group, which was injected first with Tween solution and 10 days later with M. brunneum and (b) the memory group, which was first injected with M. brunneum and 10 days later with M. brunneum. Compared to controls, larvae of the memory group were more likely to survive, but they also had an increased metabolic rate (CO2 production), spent a long time before becoming pupae, and had a shorter time from pupae to adulthood. In the adult stage, control females preferred control males, but there was no significant difference in the preference of memory females. Finally, control and memory males preferred control females. These results confirm that immune memory has costs in terms of energetic expenditure, growth, and reproduction. To the best of our knowledge, this is the first experimental demonstration that immune memory in larvae is traded-off with adult sexual selection involving mate choice.

A Life History Approach to the Female Sexual Orientation Spectrum: Evolution, Development, Causal Mechanisms, and Health.

Women's capacity for sexual fluidity is at least as interesting a phenomenon from the point of view of evolutionary biology and behavioral endocrinology as exclusively homosexual orientation. Evolutionary hypotheses for female nonheterosexuality have failed to fully account for the existence of these different categories of nonheterosexual women, while also overlooking broader data on the causal mechanisms, physiology, ontogeny, and phylogeny of female nonheterosexuality. We review the evolutionary-developmental origins of various phenotypes in the female sexual orientation spectrum using the synergistic approach of Tinbergen's four questions. We also present femme-specific and butch-specific hypotheses at proximate and ultimate levels of analysis. This review article indicates that various nonheterosexual female phenotypes emerge from and contribute to hormonally mediated fast life history strategies. Life history theory provides a biobehavioral explanatory framework for nonheterosexual women's masculinized body morphology, psychological dispositions, and their elevated likelihood of experiencing violence, substance use, obesity, teenage pregnancy, and lower general health. This pattern of life outcomes can create a feedback loop of environmental unpredictability and harshness which destabilizes intrauterine hormonal conditions in mothers, leading to a greater likelihood of fast life history strategies, global health problems, and nonheterosexual preferences in female offspring. We further explore the potential of female nonheterosexuality to function as an alloparental buffer that enables masculinizing alleles to execute their characteristic fast life history strategies as they appear in the female and the male phenotype. Synthesizing life history theory with the female sexual orientation spectrum enriches existing scientific knowledge on the evolutionary-developmental mechanisms of human sex differences.

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.

England first, America second: The ecological predictors of life history and innovation.

We present data from 122 nations showing that Baumard's argument on the ecological predictors of life history strategies and innovation is incomplete. Our analyses indicate that wealth, parasite stress, and cold climate impose orthogonal effects on life histories, innovation, and industrialization. Baumard also overlooks the historical exploitation of other nations which significantly enlarged the "pooled energy budget" available to England.

Phenological sensitivity to climate change is higher in resident than in migrant bird populations among European cavity breeders.

Many organisms adjust their reproductive phenology in response to climate change, but phenological sensitivity to temperature may vary between species. For example, resident and migratory birds have vastly different annual cycles, which can cause differential temperature sensitivity at the breeding grounds, and may affect competitive dynamics. Currently, however, adjustment to climate change in resident and migratory birds have been studied separately or at relatively small geographical scales with varying time series durations and methodologies. Here, we studied differential effects of temperature on resident and migratory birds using the mean egg laying initiation dates from 10 European nest box schemes between 1991 and 2015 that had data on at least one resident tit species and at least one migratory flycatcher species. We found that both tits and flycatchers advanced laying in response to spring warming, but resident tit populations advanced more strongly in relation to temperature increases than migratory flycatchers. These different temperature responses have already led to a divergence in laying dates between tits and flycatchers of on average 0.94 days per decade over the current study period. Interestingly, this divergence was stronger at lower latitudes where the interval between tit and flycatcher phenology is smaller and winter conditions can be considered more favorable for resident birds. This could indicate that phenological adjustment to climate change by flycatchers is increasingly hampered by competition with resident species. Indeed, we found that tit laying date had an additional effect on flycatcher laying date after controlling for temperature, and this effect was strongest in areas with the shortest interval between both species groups. Combined, our results suggest that the differential effect of climate change on species groups with overlapping breeding ecology affects the phenological interval between them, potentially affecting interspecific interactions.

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.

Depression subtyping based on evolutionary psychiatry: Proximate mechanisms and ultimate functions.

Major depressive disorder constitutes one of the leading causes of disability worldwide. However, it is not a unitary disease-it is a heterogeneous syndrome, with patients differing remarkably in symptom profile, pathophysiology and treatment responsiveness. Previous attempts to subtype major depressive disorder have showed limited clinical applicability. We present a classification of major depressive disorder episodes based on the proximate mechanisms that led to the original mood change that caused the depressive episode. We identify discrete depression subtypes that are induced by: 1) infection, 2) long-term stress, 3) loneliness, 4) traumatic experience, 5) hierarchy conflict, 6) grief, 7) romantic rejection, 8) postpartum events, 9) the season, 10) chemicals, 11) somatic diseases and 12) starvation. We further examine the ultimate functions of these subtypes and show that not all types of mood changes that trigger depression are adaptive. Instead, some are clearly maladaptive and some are byproducts of other adaptations. In modern societies, low mood after adverse life events may turn into a pathological depressive state. Modern lifestyle increases susceptibility to inflammatory dysregulation and chronic stress, both of which increase the amount of proinflammatory cytokines in peripheral blood, leading to low mood and sickness behaviour. Proinflammatory cytokines may aggravate the previously adaptive short-term mood changes to a chronic maladaptive depressive state by preventing the normalization of mood after adverse life events. Subtyping depression enables an effective and intelligent long-term treatment of patients in each subtype by treating the underlying causes of depression.

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.

Alkylresorcinol metabolites in urine and plasma as potential biomarkers of rye and wheat fiber consumption in prostate cancer patients and controls.

Alkylresorcinols (ARs) are phytochemicals mainly associated with rye/wheat bran. Plasma ARs and their plasma and urine metabolites are considered as biomarkers for whole-grain rye/wheat intake. However ARs metabolite day and night variations have not been studied in prostate cancer patients yet. We investigated ARs metabolites 3, 5-dihydroxy-benzoic acid (DHBA), and 3-(3, 5-dihydroxyphenyl)-1-propanoic acid (DHPPA) in urine and plasma in prostate cancer patients and in control group. DHPPA in 12-h overnight urine correlated with the intake of rye bread and bread fiber across short time periods (3 days). Plasma DHPPA concentration was significantly greater in the prostate cancer group than in the control group. DHPPA and DHBA excretion was significantly higher in the overnight urine than in day urine in the prostate cancer group but not in the control group. DHPPA concentration in plasma in the prostate cancer group did not depend on the intake of rye bread in the previous day, suggesting an impaired metabolism of ARs metabolites in the prostate cancer group. The results of this study suggest DHPPA in 12-h overnight urine as a biomarker to estimate the intake of rye bread and bread fiber.

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.