Maternal stress and the maternal microbiome have sex-specific effects on offspring development and aggressive behavior in Siberian hamsters (Phodopus sungorus).

The gut microbiome, a community of commensal, symbiotic and pathogenic bacteria, fungi, and viruses, interacts with many physiological systems to affect behavior. Prenatal experiences, including exposure to maternal stress and different maternal microbiomes, are important sources of organismal variation that can affect offspring development. These physiological systems do not act in isolation and can have long-term effects on offspring development and behavior. Here we investigated the interactive effects of maternal stress and manipulations of the maternal microbiome on offspring development and social behavior using Siberian hamsters, Phodopus sungorus. We exposed pregnant females to either a social stressor, antibiotics, both the social stressor and antibiotics, or no treatment (i.e., control) over the duration of their pregnancy and quantified male and female offspring growth, gut microbiome composition and diversity, stress-induced cortisol concentrations, and social behavior. Maternal antibiotic exposure altered the gut microbial communities of male and female offspring. Maternal treatment also had sex-specific effects on aspects of offspring development and aggressive behavior. Female offspring produced by stressed mothers were more aggressive than other female offspring. Female, but not male, offspring produced by mothers exposed to the combined treatment displayed low levels of aggression, suggesting that alteration of the maternal microbiome attenuated the effects of prenatal stress in a sex-specific manner. Maternal treatment did not affect non-aggressive behavior in offspring. Collectively, our study offers insight into how maternal systems can interact to affect offspring in sex-specific ways and highlights the important role of the maternal microbiome in mediating offspring development and behavior.

Breeder aggression does not predict current or future cooperative group formation in a cooperatively breeding bird.

In cooperatively breeding species, subordinates forgo reproduction to assist breeders in raising offspring. When cooperative breeding is facultative, breeders from the same population may differ in whether they are assisted by non-breeding helpers. Predation risk is a major source of nest failure and assistance during nest defense is often an overlooked, yet important, way helpers assist breeders. A breeder's aggressive response to a nest predator could have important implications for whether they form cooperatively breeding groups. We investigated the hypothesis that breeder aggression towards a nest predator is related to current and future helper recruitment. We tested the prediction that less aggressive breeders were more likely to form cooperative groups, which could occur if these breeders benefit from helper assistance during nest defense. We also considered the possibility that more aggressive breeders were more likely to form cooperative groups. We assessed the effects of partnerships and tested whether aggression exhibited by breeding partners was correlated. We conducted this work in the facultative, cooperatively breeding brown-headed nuthatch (Sitta pusilla). We measured breeder aggression in response to a taxidermy model of a nest predator to determine whether breeders' aggression correlated with their current or future helper recruitment. We found no evidence of a sex difference in aggression among breeders and aggression scores of breeding partners were not significantly correlated. Aggression scores for both breeding males and breeding females were unrelated to whether they formed cooperative groups in the current year. We followed most of the breeding males, though not breeding females, across years and found that breeding males' aggression scores were unrelated to helper recruitment the following year. Our results suggest that breeders' responses to nest predators are not related to cooperative group formation in this species and that males and females showed comparable levels of aggression towards a nest predator.

The ontogeny of personality: Repeatability of social and escape behaviors across developmental stages in Siberian hamsters (Phodopus sungorus).

Animal personality is defined as behavioral tendencies that are consistent across time and contexts within an individual, but differ across individuals. Studies investigating personality typically examine individuals across short time periods or within a single life stage. Growing evidence suggests that personality may be less stable across life stages, highlighting the need to consider the effects of ontogeny on the expression of consistent behavioral traits. We investigated individual consistency in social and escape behaviors across developmental stages using Siberian hamsters (Phodopus sungorus). To determine whether individuals were consistent in these behaviors as juveniles and across developmental stages, we measured male and female social and escape behaviors twice as juveniles and once as adults. Individuals' social scores were significantly repeatable within the juvenile stage, but not across developmental stages. In contrast, escape scores were highly repeatable across developmental stages, with males' scores being more repeatable than females' scores. Our results support previous findings that personality traits, especially those associated with social behavior, are less stable across development, whereas behaviors associated with stress or coping may represent a more permanent feature of an individual's phenotype. Our results also indicate potential sex differences in long-term repeatability of personality. Considering how ontogeny affects animal personality for males and females can provide insight into the evolution and mechanisms that maintain animal personality.

The call of the wild: using non-model systems to investigate microbiome-behaviour relationships.

On and within most sites across an animal's body live complex communities of microorganisms. These microorganisms perform a variety of important functions for their hosts, including communicating with the brain, immune system and endocrine axes to mediate physiological processes and affect individual behaviour. Microbiome research has primarily focused on the functions of the microbiome within the gastrointestinal tract (gut microbiome) using biomedically relevant laboratory species (i.e. model organisms). These studies have identified important connections between the gut microbiome and host immune, neuroendocrine and nervous systems, as well as how these connections, in turn, influence host behaviour and health. Recently, the field has expanded beyond traditional model systems as it has become apparent that the microbiome can drive differences in behaviour and diet, play a fundamental role in host fitness and influence community-scale dynamics in wild populations. In this Review, we highlight the value of conducting hypothesis-driven research in non-model organisms and the benefits of a comparative approach that assesses patterns across different species or taxa. Using social behaviour as an intellectual framework, we review the bidirectional relationship between the gut microbiome and host behaviour, and identify understudied mechanisms by which these effects may be mediated.

Mercury offloading in gametes and potential adverse effects of high mercury concentrations in blood and tissues of Atlantic Goliath Grouper Epinephelus itajara in the southeastern United States.

Mercury (Hg) is a ubiquitous and non-essential heavy metal that is highly toxic to aquatic organisms. Few studies examine Hg and its effects on wild fish populations. Here, we investigated the potential effects of Hg exposure on a large and long-lived marine species of conservation concern, the vulnerable Atlantic Goliath Grouper Epinephelus itajara. Our objectives were (1) to measure Hg (methyl-Hg; and total Hg = combined methyl-Hg and inorganic-Hg) concentrations in whole blood (WB) and gametes (eggs and sperm); (2) to investigate the relationships between Hg concentrations in muscle and liver with WB and gametes; (3) to investigate the relationships between Hg concentrations in liver, muscle, and WB with hematological and plasma biochemical analytes; and (4) to investigate the relationship between liver Hg and pigmented macrophage aggregates in liver tissue sections. We found several lines of evidence for potential adverse effects on Goliath Grouper health and reproduction by high Hg concentrations in liver, muscle, WB, and gametes, including (1) Hg concentrations in all tissues and gametes were well above observable ranges of marine and freshwater fishes from experimental exposure studies; (2) gamete Hg concentrations were among the highest recorded in wild fishes, with seasonal patterns suggesting females offload significant amounts of Hg into their eggs during the spawning season; (3) Methyl-Hg was highest in muscle, followed by sperm, liver, eggs, and WB; (4) there were significant correlations between liver, muscle, and WB Hg concentrations with various blood analytes; (5) vitellogenin positively correlated with female liver methyl-Hg concentrations, and was abnormally high in males, suggesting direct endocrine effects; and (6) liver total Hg positively correlated with pigmented macrophage aggregate count and percent area. This work will help guide future research examining the potential adverse effects of Hg and its role as an additional stressor on wild fish populations.