Maternal social environment shapes yolk testosterone allocation and embryonic neural gene expression in tree swallows
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ABSTRACT: A female's behavioral and physiological response to her environment can have lasting effects on the development of her offspring. This type of non-genetic inheritance (or maternal effect) occurs across taxa but is particularly well-studied in birds due to the relative ease of measuring maternal hormones in externally developing eggs. For example, females breeding in areas of high social competition allocate more of the hormone testosterone (T) to their egg yolks. These high-T offspring exhibit numerous phenotypic changes, including faster juvenile growth and enhanced aggression well into adulthood, which are potentially beneficial traits in high-competition areas. Thus, females may be able to communicate the current social environment to their offspring and prepare them for adverse conditions. Yet, the proximate mechanisms underlying how maternal hormones affect offspring are largely ignored, impairing our understanding of an ecologically important source of phenotypic plasticity. Here, we explored the effects of the maternal social environment on yolk T allocation and genome-wide patterns of neural gene expression in male and female tree swallow (Tachycineta bicolor) embryos. We observed a population of free-living tree swallows breeding at sites with variable breeding densities. We performed behavioral observations to record the rate of physical aggression at these sites, which was significantly higher at high density sites. We collected eggs at two developmental timepoints: the day laid to measure maternally derived T concentrations and embryonic day 11 (ED11) to measure gene expression patterns in whole brains using RNA-seq. We took a genome-wide approach to help clarify the potentially diverse mechanisms regulated by early T exposure across variable social environments. We additionally molecularly sexed the embryos to explore sex-specific effects.
Project description:The ovary plays an important role in mediating both a female’s response to her own social environment and communicating it to her developing offspring. However, we know little about the underlying genomic mechanisms that facilitate social responsiveness in the ovary. This issue is further complicated by mixed support linking female competition to ovarian production of testosterone, the often-evoked mechanism mediating both social aggression and maternal effects. Here, we experimentally generated social competition among wild, cavity-nesting female birds (tree swallows, Tachycineta bicolor). After territorial settlement, we reduced the availability of key breeding resources (i.e., nest boxes), generating heightened competition; within 24hr we reversed the manipulation, causing aggressive interactions to subside. We measured transcriptomic responses in the ovary during the peak of competition and 48hr after it ended, along with date-matched controls. Network analyses indicated that competing females experienced an immediate and temporary decrease in the expression of genes involved in the early stages of steroidogenesis; however, two days after competition had ended, there was a marked increase in the expression of genes involved in the final stages of sex steroid biosynthesis, including HSD17B1. In addition, ovaries that had been socially primed also displayed altered activity in gene networks related to the cell cycle, muscle performance, and extracellular matrix organization, which collectively point to social effects on future reproduction. Altogether, these findings show how the social environment shapes ovarian processes associated with both social behavior and adaptive transgenerational plasticity.
Project description:Periods of social instability can elicit adaptive phenotypic plasticity to promote success in future competition. However, the underlying molecular mechanisms have primarily been studied in captive and lab-reared animals, leaving uncertainty as to how natural competition among free-living animals affects gene activity. Here, we experimentally generated social competition among wild, cavity-nesting female birds (tree swallows, Tachycineta bicolor). After territorial settlement, we reduced the availability of key breeding resources (i.e., nest boxes), generating heightened competition; within 24 hr we reversed the manipulation, causing aggressive interactions to subside. We sampled females during the peak of competition and 48hr after it ended, along with date-matched controls. We measured transcriptomic and epigenomic responses to competition in two socially relevant brain regions (hypothalamus and ventromedial telencephalon). Gene network analyses suggest that processes related to energy mobilization and social aggression (e.g., dopamine synthesis) were upregulated during competition, the latter of which persisted 2 days after competition had ended. Cellular maintenance processes were also downregulated after competition. Competition additionally altered methylation patterns, particularly in pathways related to hormonal signaling, which appeared transcriptionally poised to respond to future competition . Thus, experimental competition among free-living animals shifts gene expression in ways that may facilitate the demands of competition at the expense of self-maintenance. Further, some of these effects persisted after competition ended, demonstrating the potential for epigenetic biological embedding of the social environment in ways that could “prime” individuals for success in future social instability.
Project description:Aggressive behavior is ubiquitous across many contexts, including defense of territories, mates, and offspring. For decades, researchers have detailed the effect of aggressive behavior on physiology, but our understanding of these mechanisms in females lags behind that of males, despite the fact that female aggression is widespread, particularly in the context of maternal defense (i.e., maternal aggression). Here, we measured effects of a social challenge on brain gene expression in free-living incubating females. We hypothesized that the social challenge would generate at least one of three transcriptomic effects: (1) sensitizing the brain to otherwise low levels of sex steroids, (2) changing other neuroendocrine signaling pathways associated with social behavior (e.g., dopamine), or (3) broad shifts related to metabolism or immune function. We tested these hypotheses in incubating female tree swallows (Tachycineta bicolor), exposing 10 females to a 30-minute simulated territorial intrusion, which elicited maternal aggression. After this challenge, we measured neural gene expression via RNA-seq and compared gene expression to 10 unchallenged controls. We saw no global treatment effect on gene expression. However, within the experimental group, more maternal aggression was correlated with upregulation of genes associated with immune activation and downregulation of genes associated with synaptic plasticity. Though more research is needed to understand the downstream effects of these transcriptional differences, our findings generate key questions about how the brain responds to social challenges across different contexts.
Project description:The brain plays a critical role in upstream regulation of processes central to mating effort, parental effort, and self-maintenance. For seasonally breeding animals, the brain is likely mediating trade-offs among these processes within a short breeding season, yet research thus far has only explored neurogenomic changes from non-breeding to breeding states or select pathways (e.g., steroids) in male and/or lab-reared animals. Here, we use RNA-seq to explore neural plasticity in three behaviorally relevant neural tissues (ventromedial telencephalon [VmT], hypothalamus [HYPO], and hindbrain), comparing free-living female tree swallows (Tachycineta bicolor) as they shift from territory establishment to incubation. We additionally highlight changes in candidate aggression-related genes to explore the potential for a neurogenomic shift in the mechanisms regulating aggression, a critical behavior both in establishing and maintaining a territory and in defense of offspring. We found hundreds of differentially expressed genes in the VmT and HYPO. Enrichment analyses for the VmT revealed higher expression of genes related to neuroplasticity and processes beneficial for competition during territory establishment, but down-regulated immune processes. The HYPO showed signs of high neuroplasticity during incubation, and a decreased potential for glucocorticoid signaling. Furthermore, expression of aggression-related genes shifted from steroidal to non-steroidal pathways across the breeding season. Altogether, we found genomic signatures suggestive of trade-offs between enhanced activity and immunity in the VmT and between stress responsiveness and parental care in the HYPO, along with a potential shift in the mechanisms regulating aggression. These data highlight important gene regulatory pathways that may underlie behavioral plasticity in females.
Project description:We explored the molecular mechanisms that mediate changes in neural gene expression (i.e., hypothalamus and nucleus taenia of the amygdala) and aggression in male and female zebra finches (Taeniopygia guttata) exposed to prenatal testosterone. We used egg injections of testosterone or the vehicle to mimic maternal hormones, which are transferred to offspring during prenatal development. Many researchers have postulated that prenatal maternal hormones can generate adaptive phenotypic plasticity; however, no study has determined the mechanism facilitating these long-term changes. Thus, we analyzed neural tissues from behaviorally relevant brain regions for changes in gene expression via RNA-Seq and methylation via Methyl-Seq resulting from the prenatal hormone treatment.
Project description:Mothers contribute cytoplasmic components to their progeny in a process called maternal provisioning. Provisioning is influenced by the parental environment, but the molecular pathways that transmit environmental cues between generations are not well understood. Here we show that in C. elegans, social cues modulate maternal provisioning to regulate gene silencing in offspring. Intergenerational signal transmission depends on a pheromone-sensing neuron and neuronal FMRFamide (Phe-Met-Arg-Phe)-like peptides. Parental FMRFamide-like peptide signaling dampens oxidative stress resistance and promotes the deposition of mRNAs for translational components in progeny, which in turn reduces gene silencing. This study identifies a new pathway for intergenerational communication that links neuronal responses to maternal provisioning. We suggest that loss of social cues in the parental environment represents an adverse environment that stimulates stress responses across generations.
Project description:Environmental changes may affect paternal condition and following generations but the underlying mechanisms are poorly understood. Male-male competition induces a physiological stress response and affects male hormone levels, ejaculate traits and development in their offspring. Here we investigated the role of sperm-mediated small RNAs in the transmission of male condition to the next generation. We exposed male zebrafish Danio rerio to high and low male-male competition environments for two weeks and collected sperm samples at the end. We also performed IVFs using a split-clutch design to distinguish between paternal and maternal effects and collected embryos at 24 hours to test for differentially expressed genes and transposable elements (TE)s at this key developmental stage. We sequenced micro- (mi) and Piwi-interacting (pi)RNAs in sperm and the full transcriptome in the embryos and ran differential expression analyses. We identified differentially expressed sperm mi- and piRNAs, with the strongest effects observed in sperm of males switching from high to low competition environments. We identified 612 differentially expressed genes in the embryos. These results confirm that the social environment does not only affect males but also the molecular ecology of their sperm and the gene expression in their offspring suggesting a putative role of sRNAs.
Project description:Maternal investment directly shapes early developmental conditions and therefore has long-term fitness consequences for the offspring. In oviparous species prenatal maternal investment is fixed at the time of laying. To ensure the best survival chances for most of their offspring, females must equip their eggs with the resources required to perform well under various circumstances, yet the actual mechanisms remain unknown. Here we describe the blue tit egg albumen and yolk proteome and evaluate its potential to mediate maternal effects. We show that variation in egg composition (proteins, lipids, carotenoids) primarily depends on laying order, female age and paternity (within- versus extra-pair) and that the investment in the egg proteome is functionally biased among eggs. Our results suggest that maternal effects on egg composition result from both passive and active (partly compensatory) mechanisms, and that the between- and within-clutch variation in egg composition creates diverse biochemical environments for embryonic development.
Project description:Maternal exposure to social stress during pregnancy is associated with an increased risk of psychiatric disorders in the offspring in later life. How the effects of maternal social stress are transmitted to the developing foetus is unclear. Using a rat model of maternal social stress during pregnancy, we explored the mechanisms by which maternal stress is conveyed to the foetus and the potential for targeted treatment to prevent disease in the offspring. Maternal stress induced oxidative stress in the placenta, but not in the foetal brain, which was prevented by a single administration of nanoparticle-bound antioxidant prior to the stress exposure. Moreover, this antioxidant treatment prevented prenatal stress-induced anxiety-like behaviour in juvenile male offspring, along with neurological and gene expression changes in the offspring brain. In vitro, placental conditioned medium or foetal plasma from stressed pregnancies caused changes to cultured cortical neurons, similar to those observed in the brains of juvenile offspring exposed to prenatal stress, and were found to contain altered levels of extracellular microRNAs but not corticosterone. The present study highlights the crucial role of the placenta, and molecules secreted from the placenta, in foetal brain development and provides evidence of the potential for treatment that can prevent maternal stress-induced foetal programming of neurological disease.