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 plasticity of immune memory in invertebrates.

Whether specific immune protection after initial pathogen exposure (immune memory) occurs in invertebrates has long been uncertain. The absence of antibodies, B-cells and T-cells, and the short lifespans of invertebrates led to the hypothesis that immune memory does not occur in these organisms. However, research in the past two decades has supported the existence of immune memory in several invertebrate groups, including Ctenophora, Cnidaria, Nematoda, Mollusca and Arthropoda. Interestingly, some studies have demonstrated immune memory that is specific to the parasite strain. Nonetheless, other work does not provide support for immune memory in invertebrates or offers only partial support. Moreover, the expected biphasic immune response, a characteristic of adaptive immune memory in vertebrates, varies within and between invertebrate species. This variation may be attributed to the influence of biotic or abiotic factors, particularly parasites, on the outcome of immune memory. Despite its critical importance for survival, the role of phenotypic plasticity in immune memory has not been systematically examined in the past two decades. Additionally, the features of immune responses occurring in diverse environments have yet to be fully characterized.

To live free or being a parasite: The optimal foraging behavior may favor the evolution of entomopathogenic nematodes.

Facultative parasites can alternate between a free-living and a parasitic existence to complete their life cycle. Yet, it remains uncertain which lifestyle they prefer. The optimal foraging theory suggests that food preferences align with fitness benefits. To test this hypothesis, we investigated the facultative parasite nematode Rhabditis regina, assessing its host preference and the associated benefits. Two experiments were conducted using wild nematode populations collected from Phyllophaga polyphylla, their natural host. In the first experiment, we used a behavioral arena to assess host preference between the natural host and two experimental hosts: Spodoptera frugiperda which is an alternative host and dead Tenebrio molitor, which simulates a saprophytic environment. In the second experiment, we subjected wild nematodes to "experimental evolution" lasting 50 generations in S. frugiperda and 53 generations in T. molitor carcass. We then compared life history traits (the size, survival, number of larvae, and glycogen and triglycerides as energy reserves) of dauer larvae with those nematodes from P. polyphylla (control group). We found a significant preference for P. polyphylla, which correlated with higher values in the nematode's life history traits. In contrast, the preference for S. frugiperda and the saprophytic environment was lower, resulting in less efficient life history traits. These findings align with the optimal foraging theory, as the nematode's parasitic preferences are in line with maximizing fitness. This also indicates that R. regina exhibits specificity to P. polyphylla and is better adapted to a parasitic lifestyle than a free-living one, suggesting an evolutionary pathway towards parasitism.

The immune response of the whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) when parasitized by Eretmocerus eremicus (Hymenoptera: Aphelinidae).

In insects, the innate immune system is subdivided into cellular and humoral defenses. When parasitoids attack insects, both reactions can be activated and notably, the phenoloxidase (PO) cascade and lytic activity are part of both cellular and humoral defenses. However, to our knowledge, no study has characterized any immune response of the whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) to the attack of Eretmocerus eremicus (Hymenoptera: Aphelinidae). Therefore, the first objective of the present study was to determine whether whitefly nymphs recently parasitized by E. eremicus exhibit any immune response. For this, we estimate the level of prophenoloxidase (proPO), phenoloxidase (PO), and lytic activity by colorimetric assays. A second objective was to assess whether the observed whitefly immune response could be related to a previously reported preference of the predator Geocoris punctipes (Hemiptera: Lygaeidae) for non-parasitized nymphs. We therefore offered non-parasitized and recently parasitized nymphs to the predator. Our results show that parasitism of whitefly nymphs by E. eremicus induced a highly estimated level of proPO and PO, and a lower level of lytic activity. In addition, we found that G. punctipes did not show a preference for non-parasitized over recently parasitized nymphs. The nymphs of T. vaporariorum activated the PO pathway against E. eremicus; however, the increase in proPO and PO levels was traded-off with decreased lytic activity. In addition, the previously reported preference for non-parasitized nymphs was not seen in our experiments, indicating that the induced immune response did not affect predator behavior by G. punctipes.

Incubation in shaded hatcheries biases sex-determination but preserves Lepidochelys olivacea hatchling physiology.

Some studies have associated ex situ conservation with cerebral and gonadal developmental delay, as well as decreased motor performance in Lepidochelys olivacea offspring. Ex situ management is also related to a more mature spleen and a differential leukocyte count in newly emerged Lepidochelys olivacea hatchlings. The physiological relevance of a more mature spleen is unknown in sea turtles, but studies in birds suggest an increased immune response. Because egg relocation to hatcheries is a common conservation practice, it is imperative to know its impact on hatchling physiology. Herein, plasma activity of superoxide dismutase, alkaline phosphatase and the alternative complement pathway, as well as total antioxidant capacity and hydrogen peroxide concentrations were quantified in hatchlings from in situ and ex situ nests under basal conditions at nest emergence. Toll-like receptor 4 (tlr4), heat shock proteins (hsp) 70 and hsp90 expression were quantified in the spleen and liver of the hatchlings. Hepatocyte density and nuclear area were quantified in histological sections of the liver and all turtles were sexed by histological sectioning of the gonads. Total antioxidant capacity and hydrogen peroxide concentrations in plasma were lower in turtles from ex situ nests, while tlr4 and hsp70 mRNA expression was higher in the spleen but not in the liver. Ex situ incubation produced 98% male hatchlings, whereas in situ incubation produced 100% females. There were no other differences in the attributes sampled between hatchlings emerging from ex situ and in situ treatments. The results suggest that ex situ relocated turtles may be less prone to oxidative stress than in situ incubated hatchlings and could have more mature splenic function. Together, the data suggest that ex situ relocation to shaded hatcheries biased sex determination but preserved the general physiological condition of sea turtle hatchlings.

Genomics of the relict species Baronia brevicornis sheds light on its demographic history and genome size evolution across swallowtail butterflies.

Relict species, like coelacanth, gingko, tuatara, are the remnants of formerly more ecologically and taxonomically diverse lineages. It raises the questions of why they are currently species-poor, have restrained ecology, and are often vulnerable to extinction. Estimating heterozygosity level and demographic history can guide our understanding of the evolutionary history and conservation status of relict species. However, few studies have focused on relict invertebrates compared to vertebrates. We sequenced the genome of Baronia brevicornis (Lepidoptera: Papilionidae), which is an endangered species, the sister species of all swallowtail butterflies, and is the oldest lineage of all extant butterflies. From a dried specimen, we were able to generate both long-read and short-read data and assembled a genome of 406 Mb for Baronia. We found a fairly high level of heterozygosity (0.58%) compared to other swallowtail butterflies, which contrasts with its endangered and relict status. Taking into account the high ratio of recombination over mutation, demographic analyses indicated a sharp decline of the effective population size initiated in the last million years. Moreover, the Baronia genome was used to study genome size variation in Papilionidae. Genome sizes are mostly explained by transposable elements activities, suggesting that large genomes appear to be a derived feature in swallowtail butterflies as transposable elements activity is recent and involves different transposable elements classes among species. This first Baronia genome provides a resource for assisting conservation in a flagship and relict insect species as well as for understanding swallowtail genome evolution.

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.

Greater traditionalism predicts COVID-19 precautionary behaviors across 27 societies.

People vary both in their embrace of their society's traditions, and in their perception of hazards as salient and necessitating a response. Over evolutionary time, traditions have offered avenues for addressing hazards, plausibly resulting in linkages between orientations toward tradition and orientations toward danger. Emerging research documents connections between traditionalism and threat responsivity, including pathogen-avoidance motivations. Additionally, because hazard-mitigating behaviors can conflict with competing priorities, associations between traditionalism and pathogen avoidance may hinge on contextually contingent tradeoffs. The COVID-19 pandemic provides a real-world test of the posited relationship between traditionalism and hazard avoidance. Across 27 societies (N = 7844), we find that, in a majority of countries, individuals' endorsement of tradition positively correlates with their adherence to costly COVID-19-avoidance behaviors; accounting for some of the conflicts that arise between public health precautions and other objectives further strengthens this evidence that traditionalism is associated with greater attention to hazards.

Love and affectionate touch toward romantic partners all over the world.

Touch is the primary way people communicate intimacy in romantic relationships, and affectionate touch behaviors such as stroking, hugging and kissing are universally observed in partnerships all over the world. Here, we explored the association of love and affectionate touch behaviors in romantic partnerships in two studies comprising 7880 participants. In the first study, we used a cross-cultural survey conducted in 37 countries to test whether love was universally associated with affectionate touch behaviors. In the second study, using a more fine-tuned touch behavior scale, we tested whether the frequency of affectionate touch behaviors was related to love in romantic partnerships. As hypothesized, love was significantly and positively associated with affectionate touch behaviors in both studies and this result was replicated regardless of the inclusion of potentially relevant factors as controls. Altogether, our data strongly suggest that affectionate touch is a relatively stable characteristic of human romantic relationships that is robustly and reliably related to the degree of reported love between partners.

The Coincidental Evolution of Virulence Partially Explains the Virulence in a Generalist Entomopathogenic.

PURPOSE: The parasites' virulence is labile after jumping to a new host species, and it might derivate in gaining virulence against a new host as a side effect of living in a non-host environment (coincidental evolution of virulence hypothesis). METHODS: To test this hypothesis, we monitored the experimental evolution of the Rhabditis regina nematode for over 290 generations (4 years) in three environments (strains): (1) the natural host, Phyllophaga polyphylla, (2) an alternate host, Tenebrio molitor, and (3) saprophytic medium (beef; the food that may provide evidence for the coincidental evolution of virulence). Each strain was exposed to P. polyphylla, T. molitor, or Galleria mellonella. We compared the host survival and immune response (proPO, PO, and lytic activity) of infected versus uninfected hosts. RESULTS: The saprophytic nematodes gained virulence only against G. mellonella. However, the P. polyphylla strain was more effective in killing P. polyphylla than T. molitor, and the T. molitor strain was more effective against T. molitor than P. polyphylla. Additionally, one dauer larva was sufficient to kill the hosts. Finally, the immune response did not differ between the challenged and control groups. CONCLUSION: The coincidental evolution of virulence partially explains our results, but they might also support the short-sighted hypothesis. Additionally, we found evidence for immunomodulation because nematodes passed unnoticed to the immune response. It is crucial to analyze the virulence of entomopathogens from the point of view of the evolution of virulence to be aware of potential scenarios that might limit biological control.

Effect of juvenile hormone on phenoloxidase and hemocyte number: The role of age, sex, and immune challenge.

Hormones are key factors in determining the response of organisms to their environment. For example, the juvenile hormone (JH) coordinates the insects' development, reproduction, and survival. However, it is still unclear how the impact of juvenile hormone on insect immunity varies depending on the sex and reproductive state of the individual, as well as the type of the immune challenge (i.e., Gram-positive or Gram-negative bacteria). We used Tenebrio molitor and methoprene, a JH analog (JHa) to explore these relationships. We tested the effect of methoprene on phenoloxidase activity (PO), an important component of humoral immunity in insects, and hemocyte number. Lyophilized Gram-positive Staphylococcus aureus or Gram-negative Escherichia coli were injected for the immune challenge. The results suggest that JH did not affect the proPO, PO activity, or hemocyte number of larvae. JH and immune challenge affected the immune response and consequently, affected adult developmental stage and sex. We propose that the influence of JH on the immune response depends on age, sex, the immune response parameter, and the immune challenge, which may explain the contrasting results about the role of JH in the insect immune response.

The honey bees immune memory.

Invertebrates' immune priming or innate immune memory is an analogous response to the vertebrates' adaptive memory. We investigated if honey bees have immune memory. We compared survival and immune response between bees that were: 1) manipulated (Naïve), 2) challenged twice with the same pathogen Escherichia coli (Memory), 3) challenged twice with different pathogens (Staphylococcus aureus versus E. coli, Micrococcus lysodeikticus versus E. coli), or 4) with PBS (the diluent of bacteria) versus E. coli (heterologous challenge; Control). Results indicate better survival in the Memory than the Control group, and the Memory group showed a similar survival than Naïve insects. The Memory group had higher lytic activity but lower prophenoloxidase, phenoloxidase activity, and hemocyte count than the Control and Naïve groups. No differences were found in relative expression of defensin-1. This first demonstration of immune memory opens the questions about its molecular mechanisms and whether, immune memory could be used against natural parasites that affect honey bees, hence, if they could be "vaccinated" against some natural parasites.

Neural mechanisms involved in female mate choice in invertebrates.

Mate choice is a critical decision with direct implications for fitness. Although it has been recognized for over 150 years, our understanding of its underlying mechanisms is still limited. Most studies on mate choice focus on the evolutionary causes of behavior, with less attention given to the physiological and molecular mechanisms involved. This is especially true for invertebrates, where research on mate choice has largely focused on male behavior. This review summarizes the current state of knowledge on the neural, molecular and neurohormonal mechanisms of female choice in invertebrates, including behaviors before, during, and after copulation. We identify areas of research that have not been extensively explored in invertebrates, suggesting potential directions for future investigation. We hope that this review will stimulate further research in this area.

Survival, Body Condition, and Immune System of Apis mellifera liguistica Fed Avocado, Maize, and Polyfloral Pollen Diet.

Nutritional stress is the major factor contributing to decline in the honey bee (Apis mellifera L.) populations given the high degree of dependence on floral resources, and due to the habitat loss. In this sense, monocultures of maize and avocado have great extensions in Mexico, but their impact on the physiology and morphology of A. mellifera is unknown. This research evaluated the effect of total protein content in monofloral (maize or avocado pollen diets) and polyfloral (using five types of pollen: Persea americana Mill., Zea mays L., Melampodium perfoliatum Cav., Drymaria villosa Cham Schltdl., and Lopezia racemosa Cav.) on their survival, body condition (controlled density, head mass, and development of hypopharyngeal glands; protein content in hemolymph), and immune response [lytic activity and activity of prophenoloxidase in the hemolymph (proPO)]. Corbicular pollen of P. americana had the highest protein content, followed by the corbicular pollen of Z. mays, M. perfoliatum, D. villosa, and L. racemosa. Polyfloral diet seems to be better for A. mellifera than the monofloral maize and avocado. Bees fed polyfloral pollen diet showed a high content of protein in the hemolymph in comparison with that fed maize or avocado pollen diets. Bees fed polyfloral and avocado pollen diet had the highest lytic activity but showed a decrease in proPO activity. In conclusion, polyfloral diets seem to be better for A. mellifera than the monofloral maize and avocado.

Are Toxoplasma-infected subjects more attractive, symmetrical, or healthier than non-infected ones? Evidence from subjective and objective measurements.

Background: Parasites are among the main factors that negatively impact the health and reproductive success of organisms. However, if parasites diminish a host's health and attractiveness to such an extent that finding a mate becomes almost impossible, the parasite would decrease its odds of reproducing and passing to the next generation. There is evidence that Toxoplasma gondii (T. gondii) manipulates phenotypic characteristics of its intermediate hosts to increase its spread. However, whether T. gondii manipulates phenotypic characteristics in humans remains poorly studied. Therefore, the present research had two main aims: (1) To compare traits associated with health and parasite resistance in Toxoplasma-infected and non-infected subjects. (2) To investigate whether other people perceive differences in attractiveness and health between Toxoplasma-infected and non-infected subjects of both sexes. Methods: For the first aim, Toxoplasma-infected (n = 35) and non-infected subjects (n = 178) were compared for self-perceived attractiveness, number of sexual partners, number of minor ailments, body mass index, mate value, handgrip strength, facial fluctuating asymmetry, and facial width-to-height ratio. For the second aim, an independent group of 205 raters (59 men and 146 women) evaluated the attractiveness and perceived health of facial pictures of Toxoplasma-infected and non-infected subjects. Results: First, we found that infected men had lower facial fluctuating asymmetry whereas infected women had lower body mass, lower body mass index, a tendency for lower facial fluctuating asymmetry, higher self-perceived attractiveness, and a higher number of sexual partners than non-infected ones. Then, we found that infected men and women were rated as more attractive and healthier than non-infected ones. Conclusions: Our results suggest that some sexually transmitted parasites, such as T. gondii, may produce changes in the appearance and behavior of the human host, either as a by-product of the infection or as the result of the manipulation of the parasite to increase its spread to new hosts. Taken together, these results lay the foundation for future research on the manipulation of the human host by sexually transmitted pathogens and parasites.

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.

Innate immune memory in invertebrates: Concept and potential mechanisms.

Invertebrates are the protagonists of a recent paradigm shift because they now show that vertebrates are not the only group with immune memory. This review discusses the concept of immune priming, its characteristics, and differences with trained immunity and immune enhancement. We include an update of the current status of immune priming within generations in different groups of invertebrates which now include work in 5 Phyla: Ctenophora, Cnidaria, Mollusca, Nematoda, and Arthropoda. Clearly, few Phyla have been studied. We also resume and discuss the effector mechanism related to immune memory, including integrating viral elements into the genome, endoreplication, and epigenetics. The roles of other elements are incorporated, such as hemocytes, immune pathways, and metabolisms. We conclude that taking care of the experimental procedure will discern if results provide or do not support the invertebrates' immune memory and that regarding mechanisms, indeed, there are no studies on the immune memory mechanisms, this is how specificity is reached, and how and where the immune memory is stored and how is recall upon subsequent encounters. Finally, we discuss the possibility of having more than one mechanism working in different groups of invertebrates depending on the environmental conditions.

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.