Areas of Research
Molecular mechanisms of female aggression
What mechanisms encode social experiences in females?
Our understanding of the regulation of aggression has largely been derived from research in males while female competition has remained comparatively less studied. During my postdoctoral work in the Rosvall Lab we addressed this by experimentally manipulating competition in the wild using a fiercely competitive cavity-nesting songbird (tree swallows). We reduced cavity availability to generate social instability in the wild, and quantified the immediate and lasting effects of this instability on behavioral and physiological traits in females. ​Females were collected during peak competition (see video of competition to the right), after it had ended, and as date-matched controls to measure neurogenomic changes via RNA-seq. We found that natural bouts of competition can lead to neurogenomic changes that persist even after the competition has ended and are currently using Methylcap-seq to explore the mechanisms that encoded this social experience. Behavioral responses to competition can lead to genomic changes within adults that “prime” them for future fights; yet, these changes can become pathological if social instability persists. Thus, this work has a strong potential to provide novel information about how social competition causes transcriptional profiles to switch from adaptive priming to lasting pathologies. Continuing work will examine how social experiences create genomic, epigenomic, and physiological changes across time and in other tissues (e.g., sensory organs and gonads).
Environmental & evolutionary determinants of transgenerational plasticity
A female’s response to her social environment can have lasting consequences for her offspring. Females engaging in social competition tend to transfer more testosterone to their egg yolks, resulting in offspring with numerous phenotypic changes (e.g., enhanced growth and more aggressive behaviors).
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In what contexts are the effects of maternally derived hormones adaptive?
While it certainly seems beneficial to create more aggressive offspring in more competitive environment, the adaptive value of this hormone-mediated maternal effect has long been assumed but not shown. Past work had either manipulated the female environment and measured egg hormones or artificially enhanced yolk hormones and measured offspring traits. Our work provided an environmental context for this maternal effect and demonstrated that maternally derived testosterone can create potentially adaptive phenotypes for competitive environments. We increased social competition for tree swallows by manipulating their breeding density and measured the amount of natural testosterone transferred to egg yolks, along with the effects on offspring phenotype using a partial cross-foster design. We found that high-density environments elicited more social aggression and yolk testosterone, the nestlings from which grew more quickly and had a greater competitive ability regardless of their postnatal environment. Future work will address the adaptive implications of this maternal effect by combining environmental and pharmacological manipulations with long-term monitoring of offspring outcomes ​in wild-caught songbirds. ​
What evolutionary factors influence whether a female transfers hormones?
Creating more aggressive offspring in more competitive environments seems beneficial; yet, not all species show a positive relationship between competition and yolk testosterone. This variation has yet to be explained, which limits our ability to predict how species will respond to social environments. Taking a meta-analysis approach, we identified life-history traits that influence yolk testosterone allocation. We found that species coloniality was the strongest predictor of whether a female would allocate yolk testosterone in response to social competition. Solitary, but not colonial species, will allocate more yolk testosterone when in more competitive environments. We then experimentally tested this finding in a colonial species (zebra finches) by exposing females to conspecific intruders and measuring yolk testosterone. Despite showing aggressive behaviors toward the intruder, these colonial females did not allocate more yolk testosterone, support the findings in the meta-analysis. Our work will continue to explore how selection shaped behavioral and hormonal responses across life-history traits. The next steps will use phylogenetic comparative methods to uncover the molecular mechanisms that differentiate these responses.
Bentz et al. 2016 R. Soc. Open Sci.
Molecular mechanisms of transgenerational behavioral plasticity
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How do prenatal hormones generate lasting changes?
Prenatal exposure to testosterone can generate long-lasting behavioral changes in offspring, but the underlying mechanisms are unknown. We have addressed this issue using genomic and epigenomic techniques in the field and lab. Working with captive songbirds, we injected eggs with testosterone, generating offspring with more aggressive phenotypes well into adulthood. Then, using RNA-seq and MethylC-Seq, we were able to detect genome-wide changes in gene expression and methylation in adults. Males exposed to prenatal testosterone had hundreds of differentially expressed genes in the hypothalamus, including genes enriched in processes with established links to aggression. Furthermore, several of these genes also showed differential methylation. We also showed that this likely occurs in the wild. We manipulated the social environment of wild Eastern bluebirds, causing natural variation in yolk testosterone allocation, and found differential methylation of a behaviorally relevant gene (i.e., estrogen receptor) in the resulting juveniles.This work provides promising candidate genes and processes for explaining how maternal hormones generate transgenerational phenotypic plasticity. The key next questions to address are the role the candidate pathways we previously identified play and further exploring how prenatal hormones alter epigenetic patterns (i.e., the mechanisms used and the sensitive developmental windows).