Alison Bell

University of Illinois, Urbana-Champaign | UIUC · School of Integrative Biology

There is growing evidence that the environment experienced by one generation can influence phenotypes in the next generation via transgenerational plasticity (TGP). One of the best-studied examples of TGP in animals is predator-induced transgenerational plasticity, whereby exposing parents to predation risk triggers changes in offspring phenotypes....

Parental care has attracted attention from both proximate and ultimate perspectives. While understanding the adaptive significance of care has been the focus of work in diverse organisms in behavioral ecology, most of what we know about the proximate mechanisms underlying parental care behavior comes from studies in mammals. Although studies on mam...

There is growing evidence that offspring receive information about their environment vertically, i.e. from their parents (environmental parental effects or transgenerational plasticity). For example, parents exposed to predation risk may produce offspring with heightened antipredator defences. At the same time, organisms can gain information about...

For a species to expand its range, it needs to be good at dispersing and also capable of exploiting resources and adapting to different environments. Therefore, behavioral and cognitive traits could play key roles in facilitating invasion success. Marine threespined sticklebacks (Gasterosteus aculeatus) have repeatedly colonized freshwater environm...

The environment experienced by one generation can influence the phenotypes of future generations. Because parental cues can be conveyed to offspring at multiple points in time, ranging from fertilization to posthatching/parturition, offspring can potentially receive multiple cues from their parents via different mechanisms. We have relatively littl...

Fuelled by the ongoing genomic revolution, broadscale RNA expression surveys are fast replacing studies targeting one or a few genes to understand the molecular basis of behaviour. Yet, the timescale of RNA-sequencing experiments and the dynamics of neural gene activation are insufficient to drive real-time switches between behavioural states. More...

Appendices for Stamps&Bell 21

Experiences of parents and/or offspring are often assumed to affect the development of trait values in offspring because they provide information about the external environment. However, it is currently unclear how information from parental and offspring experiences might jointly affect the information-states that provide the foundation for the off...

Behavioral genetics in non-model organisms is currently gated by technological limitations. However, with the growing availability of genome editing and functional genomic tools, complex behavioral traits such as social behavior can now be explored in diverse organisms. Here we present a minimally invasive neurosurgical procedure for a classic beha...

Experiences of parents and/or offspring are often assumed to affect the development of trait values in offspring because they provide information about the external environment, but it is currently unclear how information from different sources and times might combine to affect the information-states that provide the foundation for the patterns obs...

Parental effects may help offspring respond to challenging environments, but whether parental exposure to different environmental challenges induces similar responses in offspring is largely unknown. We compared the offspring of threespine stickleback (Gasterosteus aculeatus) fathers who had been exposed to a potentially threatening stimulus (net),...

What makes individuals unique? The answer to this question lies in understanding why and how individuals respond to numerous internal and external factors that they experience over their lifetimes. This fundamental question lies at the heart of the study of human and animal behavior and is best addressed by integrating both proximate and ultimate p...

For a species to expand its range, it needs to be good at dispersing and also capable of exploiting resources and adapting to different environments. Therefore, behavioral and cognitive traits could play key roles in facilitating invasion success. Here, we show that dispersing sticklebacks are bold, while sticklebacks that have recently established...

Empirical studies of phenotypic plasticity often use an experimental design in which the subjects in experimental treatments are exposed to cues, while the subjects in control treatments are maintained in the absence of those cues. However, researchers have virtually ignored the question of what, if any, information might be provided to subjects by...

Transgenerational plasticity (TGP) occurs when the environment encountered by one generation (F0) alters the phenotypes of one or more future generations (e.g. F1 and F2). Sex selective TGP, via specific lineages or to only male or female descendants, has been underexplored in natural systems, and may be adaptive if it allows past generations to fi...

Intergenerational plasticity or parental effects—when parental environments alter the phenotype of future generations—can influence how organisms cope with environmental change. An intriguing, underexplored possibility is that sex—of both the parent and the offspring—plays an important role in driving the evolution of intergenerational plasticity i...

Behavioral flexibility is a type of phenotypic plasticity that can influence how animals cope with environmental change and is often measured with a reversal learning paradigm. The goal of this study was to understand why individuals differ in behavioral flexibility, and whether individual differences in behavioral flexibility fit the predictions o...

Parental effects can help offspring cope with challenging environments, but whether these effects are unique to specific environmental conditions is largely unknown. Parental effects may evolve via a core pathway that generally prepares offspring for risky environments or could be stimuli-specific, with offspring developing phenotypes that are tail...

Behavioral genetics in non-model organisms is currently gated by technological limitations. However, with the growing availability of genome editing and functional genomic tools, complex behavioral traits such as social behavior can now be explored in diverse organisms. Here we present a minimally invasive neurosurgical procedure for a classic beha...

There is growing evidence that personality traits can change throughout the life course in humans and nonhuman animals. However, the proximate and ultimate causes of personality trait change are largely unknown, especially in adults. In a controlled, longitudinal experiment, we tested whether a key life event for adults––mating––can cause personali...

Predation often has consistent effects on prey behavior and morphology, but whether the physiological mechanisms underlying these effects show similarly consistent patterns across different populations remains an open question. In vertebrates, predation risk activates the hypothalamic-pituitary-adrenal (HPA) axis, and there is growing evidence that...

There is growing evidence that personality traits can change throughout the life course in humans and nonhuman animals. However, the proximate and ultimate causes of personality trait change are largely unknown, especially in adults. In a controlled, longitudinal experiment, we tested whether a key life event for adults - mating - can cause persona...

Our ability to predict how species will respond to human-induced rapid environmental change (HIREC) may depend upon our understanding of transgenerational plasticity (TGP), which occurs when environments experienced by previous generations influence phenotypes of subsequent generations. TGP evolved to help organisms cope with environmental stressor...

Transgenerational plasticity (TGP) occurs when the environment encountered by one generation (F0) alters the phenotypes of one or more future generations (e.g. F1 and F2). Sex selective TGP, via specific lineages or to only male or female descendants, has been underexplored in natural systems, and may be adaptive if it allows past generations to fi...

Motherhood is characterized by dramatic changes in brain and behavior, but less is known about fatherhood. Here we report that male sticklebacks—a small fish in which fathers provide care—experience dramatic changes in neurogenomic state as they become fathers. Some genes are unique to different stages of paternal care, some genes are shared across...

Transgenerational plasticity (TGP) or parental effects – when parental environments alter the phenotype of future generations – can influence how organisms cope with environmental change. An intriguing, underexplored possibility is that sex –of both the parent and the offspring – plays an important role in driving the evolution of transgenerational...

[This corrects the article DOI: 10.1098/rsos.171029.].

Populations of animals are composed of individuals that differ in ecologically relevant behaviors. Building evidence also suggests that individuals occupy different social niches. Here, in a mark–recapture experiment, we show evidence of an interacting effect of behavior and social niche on survival in the wild: Bold individuals had higher survival...

Establishing a causal relationship between genes and social behavior is challenging. We developed a viral-mediated transgenesis protocol to test the effects of increased expression of candidate genes in the brain on behavior in sticklebacks. This method is fast and flexible, allowing us to compare individual behavior before and after transgenesis....

In this paper I discuss how the challenge hypothesis (Wingfield et al., 1990) influenced the development of ideas about animal personality, and describe particularly promising areas for future study at the intersection of these two topics. I argue that the challenge hypothesis influenced the study of animal personality in at least three specific wa...

Transgenerational plasticity (TGP) occurs when the environment experienced by a parent influences the development of their offspring. In this article, we develop a framework for understanding the mechanisms and multigenerational consequences of TGP. First, we conceptualize the mechanisms of TGP in the context of communication between parents (sende...

Viral-mediated transgenesis of MAOA and AVP increases territorial aggression in stickleback

Phenotypic plasticity might influence evolutionary processes such as adaptive radiations. Plasticity in parental care might be especially effective in facilitating adaptive radiations if it allows populations to persist in novel environments. Here, we test the hypothesis that behavioral plasticity by parents in response to predation risk facilitate...

Establishing a causal relationship between genes and social behavior is challenging since gene expression is dynamic. One gene may have drastically different effects when expressed in different parts of the social behavior network (areas in the fore- and mid-brain) or at different times. Thus, to determine the causal relationship between a gene of...

Differential allocation occurs when individuals alter their reproductive investment based on their mate's traits. A previous study showed that male threespine sticklebacks, Gasterosteus aculeatus, reduced courtship towards females that had previously been exposed to predation risk compared to unexposed females. This suggests that males can detect a...

Organisms can gain information about their environment from their ancestors, their parents or their own personal experience. 'Cue integration' models often start with the simplifying assumption that information from different sources is additive. Here, we test key assumptions and predictions of cue integration theory at both the phenotypic and mole...

Social challenges like territorial intrusions evoke behavioral responses in widely diverging species. Recent work has revealed that evolutionary “toolkits” – genes and modules with lineage‐specific variations but deep conservation of function – participate in the behavioral response to social challenge. Here, we develop a multi‐species computationa...

Genotype‐by‐environment interaction (G × E), that is, genetic variation in phenotypic plasticity, is a central concept in ecology and evolutionary biology. G×E has wide‐ranging implications for trait development and for understanding how organisms will respond to environmental change. Although G × E has been extensively documented, its presence and...

Social challenges like territorial intrusions evoke behavioral responses in widely diverging species. Recent work has revealed that evolutionary “toolkits” – genes and modules with lineage-specific variations but deep conservation of function – participate in the behavioral response to social challenge. Here, we develop a multi-species computationa...

Animals must identify reliable cues amidst environmental noise during learning, and the cues that are most reliable often depend on the local ecology. Comparing the performance of populations of the same species across multiple versions of a cognitive task can reveal whether some populations learn to use certain cues faster than others. Here, using...

Establishing a causal relationship between genes and social behavior is challenging due to dynamic spatial and temporal gene expression. One gene can have drastically different consequences on behavior when expressed in different parts of the social behavior network (a combination of areas in the fore- and mid-brain). Thus, to determine the causal...

Behaviour is a key interface between an animal's genome and its environment. Repeatable individual differences in behaviour have been extensively documented in animals, but the molecular underpinnings of behavioural variation among individuals within natural populations remain largely unknown. Here, we offer a critical review of when molecular tech...

Parental care is critical for fitness, yet little is known about its genetic basis. Here, we estimate the heritability of parenting behaviour in a species famous for its diversity and its behavioural repertoire: three-spined stickleback (Gasterosteus aculeatus). Male three-spined stickleback are the sole providers of parental care that is necessary...

Motherhood is a period of intense behavioral and brain activity. However, we know less about the neural and molecular mechanisms associated with the demands of fatherhood. Here, we report the results of two experiments designed to track changes in behavior and brain activation associated with fatherhood in male threespined stickleback fish (Gastero...

Listen to the news and you are bound to hear that researchers are increasingly interested in the biological manifestations of trauma that reverberate through the generations. Research in this area can be controversial in the public realm, provoking societal issues about personal responsibility (are we really born free or are we born with the burden...

Maternal stress can prenatally influence offspring phenotypes and there are an increasing number of ecological studies that are bringing to bear biomedical findings to natural systems. This is resulting in a shift from the perspective that maternal stress is unanimously costly, to one in which maternal stress may be beneficial to offspring. However...

Animals exhibit dramatic immediate behavioral plasticity in response to social interactions, and brief social interactions can shape the future social landscape. However, the molecular mechanisms contributing to behavioral plasticity are unclear. Here, we show that the genome dynamically responds to social interactions with multiple waves of transc...

TRN highlighting top hubs in the network and region-specific DEGs. The TRN contains 352 TFs, which regulate 1155 genes through a total of 3683 interactions. The top 20 TFs (“hubs”) with the highest number of targets (over 30 each) are highlighted in pink. Target genes that are differentially expressed in Diencephalon or Telencephalon (CFDR < 0.1) a...

Baseline accessibility of diencephalon DEGx at 30 and 120 minutes. (DOCX)

Functional gene ontology enrichment of genes in S1 Table, with separate tabs for biological processes and molecular functions. GO terms were further summarized according to their biological significance in the ‘comments’ column. (XLSX)

Chromatin accessibility–Baseline and DAPs. There are separate tabs for each individual replicate compared to corresponding input, DAPs at 30 and 120 minutes, and for baseline peaks at 30 and 120 minutes. (XLSX)

H3K27Ac ChIP-Seq samples read mapping and quality control information. (XLSX)

Shared genes across brain regions, with separate tabs for each time point. Discordant genes at 120 min are in red. (XLSX)

Functional enrichment of DAPs with separate columns for DAPDEGx and genes near peaks that were not accessible at baseline but became accessible in response to a territorial challenge (!AccDAPDEGx). There are separate tabs for biological processes and molecular function. (XLSX)

Transcription factors and their targets as predicted by ASTRIX generated TRN. (XLSX)

RNA-Seq quality control. This directory contains six subdirectories. The subdirectory “correlation” contains correlation heatmaps among all samples in diencephalon and telencephalon respectively. The subdirectory “mapping_stat” contains read mapping information on genomic features for each sample. The subdirectory “MDS” shows three dimensional MDS...

Differentially expressed genes whose expression profile changed over time in response to a territorial challenge (DEGx), and their associated cluster with separate tabs for each brain region. (XLSX)

Differentially expressed genes between control and experimental identified using pairwise contrasts at each time point within each brain region with separate tabs for each time point (30, 60, 120) within a brain region (D, T). (XLSX)

Functional enrichment of DEGx (biological processes) with separate tabs for each brain region. GO terms were further summarized according to their biological significance in the ‘comments’ column. (XLSX)

TRN TFs enrichments in clusters. Numbers indicate p-values. (XLSX)

H3K27Ac peaks–Separate tabs include HOMER assigned peaks for each replicate compared to its corresponding input sample. (XLSX)

Integrating TFs with DEGx and chromatin accessibility. These TFs are in the TRN and are enriched in the DAPDEGx with accessibility indicated. Some of the TFs (in bold) were differentially expressed and in a cluster. The general expression pattern of their cluster is indicated. A subset of this table is in Table 1. (DOCX)

21st Annual Meeting

Social learning is an important process in the spread of information, especially in changing environments where inherited behaviors may not remain relevant. In many species, the decision of whom to trust to have reliable information depends on the relationship between individuals. Many fish species, including three-spined sticklebacks, preferential...

Coping styles theory provides a framework for understanding individual variation in how animals respond to environmental change, and predicts how individual differences in stress responsiveness and behavior might relate to cognitive differences. According to coping styles theory, proactive individuals are bolder, less reactive to stressors, and mor...

[ Proc. R. Soc. B 279 , 4929–4938. (12 November 2012; Published online 24 October 2012) ([doi:10.1098/rspb.2012.2087][2])][2] It has come to our attention that the direction of regulation reported in Sanogo et al. [[1][2]] is incorrect. Genes that were upregulated in experimental males were, in

A method for quantifying consistent individual differences in schooling behaviour is presented. This method, which utilizes a school of models, improves on previous methods by removing the unwanted variation that is introduced by live stimulus fish while still providing the physiological experience of schooling to the focal fish. Three-spined stick...

Within many species, some individuals are consistently more aggressive than others. We examine whether there are differences in brain gene expression between aggressive versus nonaggressive behavioural types of individuals within a natural population of male three-spined sticklebacks (Gasterosteus aculeatus). We compared gene expression profiles of...

Background: Threespine stickleback are an important model for behaviour and evolutionary studies. A growing number of quantitative trait loci (QTL) and gene expression studies are identifying genes related to ecologically important traits in sticklebacks. In order to visualize the expression of candidate genes, we developed a fluorescence in situ...

In nature, animals often face conflicting demands. For example, breeding males must attract a mate but at the same time be ready to defend against rivals. The molecular mechanisms by which the brain resolves behavioral tradeoffs are largely unknown. In this study, we compared the brain transcriptional responses of territorial male threespined stick...

Offspring from females that experience stressful conditions during reproduction often exhibit altered phenotypes and many of these effects are thought to arise owing to increased exposure to maternal glucocorticoids. While embryos of placental vertebrates are known to regulate exposure to maternal glucocorticoids via placental steroid metabolism, m...

Although one of the hallmarks of personality traits is their consistency over time, we might expect personality traits to change during life history shifts. Becoming a parent is a major life history event, when individuals undergo dramatic behavioural and physiological changes. Here we employ a longitudinal experiment to ask whether personality cha...

Differential allocation occurs when individuals adjust their reproductive investment based on their partner's traits. However, it remains unknown whether animals differentially allocate based on their partner's past experiences with predation risk. If animals can detect a potential mate's experience with predators, this might inform them about the...

Maternal stress can have long-term negative consequences for offspring learning performance. However, it is unknown whether these maternal effects extend to the ability of offspring to apply previously learned information to new situations. In this study, we first demonstrate that juvenile threespine sticklebacks, Gasterosteus aculeatus, are indeed...

We present a protocol for FISH on fresh or flash-frozen dissected tissue, using either cryo- or paraffin embedding. The protocol covers probe design guidelines and synthesis, sample embedding, sectioning, and the hybridization process. The protocol is optimized for brain tissue. Key steps for modifying the protocol for other tissues were noted. Re...

Embryonic exposure to steroids often leads to long-term phenotypic effects. It has been hypothesized that mothers may be able to create a steroid environment that adjusts the phenotypes of offspring to current environmental conditions. Complicating this hypothesis is the potential for developing embryos to modulate their early endocrine environment...

Species abundances and distributions are inherently tied to individuals' decisions about movement within their habitat. Therefore, integrating individual phenotypic variation within a larger ecological framework may provide better insight into how populations structure themselves. Recent evidence for consistent individual differences in behaviour p...

Significance In some cases similar molecular programs (i.e., conserved genes and gene networks) underlie the expression of phenotypic traits that evolve repeatedly across diverse species. We investigated this possibility in the context of social behavioral response, using a comparative genomics approach for three distantly related species: house mo...

In many animals, including humans, interactions with caring parents can have long-lasting effects on offspring sensitivity to stressors. However, whether these parental effects impact offspring fitness in nature is often unclear. In addition, despite evidence that maternal care can influence offspring behaviour via epigenetic alterations to the gen...

Consistent individual differences in parenting are widespread; however, we know little about why there is variation in parenting behavior among individuals within species. One possible explanation for consistent individual differences in parenting is that individuals invest in different aspects of parental care, such as provisioning or defense. In...