Publications by authors named "Alison M Bell"

74 Publications

Vertical transmission of horizontally acquired social information in sticklebacks: implications for transgenerational plasticity.

Proc Biol Sci 2022 07 20;289(1979):20220571. Epub 2022 Jul 20.

Department of Evolution, Ecology and Behavior, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA.

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 the environment horizontally, from conspecifics. In this study, we provide some of the first evidence that horizontally acquired social information can be transmitted vertically across generations. Three-spined stickleback () fathers produced larval offspring with altered antipredator behaviour when fathers received visual and olfactory cues from predator-chased neighbours. Although fathers did not personally witness their neighbours being chased (i.e. they never saw the predator), changes in offspring traits were similar to those induced by direct paternal exposure to predation risk. These findings suggest that two different non-genetic pathways (horizontal transfer of social information, vertical transfer via sperm-mediated paternal effects) can combine to affect offspring phenotypes. The implications of simultaneous horizontal and vertical transmission are widely appreciated in the context of disease and culture; our results suggest that they could be equally important for the maintenance of phenotypic variation and could have profound consequences for the rate at which information flows within and across generations.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1098/rspb.2022.0571DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9297010PMC
July 2022

The interplay between sperm-mediated and care-mediated paternal effects in threespine sticklebacks.

Anim Behav 2021 Sep 12;179:267-277. Epub 2021 Aug 12.

Carl R. Woese Institute for Genomic Biology, University of Illinois Urbana-Champaign, Urbana, IL, U.S.A.

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 little information regarding how different mechanisms operate in isolation and in tandem, but it is possible, for example, that offspring phenotypes induced by nongenetic changes to gametes may be amplified by, mitigated by, or depend upon parental care. Here, we manipulated paternal experience with predation risk prior to fertilization in threespine stickleback, , and then examined the potential of paternal care to mitigate and/or amplify sperm-mediated paternal effects. Specifically, we compared (1) offspring of predator-exposed fathers who were reared without paternal care, (2) offspring of predator-exposed fathers who were reared with paternal care, (3) offspring of control (unexposed) fathers who were reared without paternal care and (4) offspring of control fathers who were reared with paternal care. We found that offspring of predator-exposed fathers were less active and had higher cortisol following a simulated predator attack. Although predator-exposed males shifted their paternal care behaviours - reduced fanning early in egg development and increased fanning right before egg hatching compared to control males - this shift in paternal behavior did not appear to affect offspring traits. This suggests that paternal care neither amplifies nor compensates for these phenotypic effects induced by sperm and that nongenetic changes induced by sperm may occur independently of nongenetic changes induced by paternal care. Overall, these results underscore the importance of considering how parents may have multiple nongenetic mechanisms by which they can influence offspring.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.anbehav.2021.07.005DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8513676PMC
September 2021

Back to the basics? Transcriptomics offers integrative insights into the role of space, time and the environment for gene expression and behaviour.

Biol Lett 2021 09 15;17(9):20210293. Epub 2021 Sep 15.

Department of Evolution, Ecology, and Behavior, School of Integrative Biology, University of Illinois, Urbana-Champaign, IL 61801, USA.

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. Moreover, the spatial, functional and transcriptional complexity of the brain (the most commonly targeted tissue in studies of behaviour) further complicates inference. We argue that a Central Dogma-like 'back-to-basics' assumption that gene expression changes cause behaviour leaves some of the most important aspects of gene-behaviour relationships unexplored, including the roles of environmental influences, timing and feedback from behaviour-and the environmental shifts it causes-to neural gene expression. No perfect experimental solutions exist but we advocate that explicit consideration, exploration and discussion of these factors will pave the way toward a richer understanding of the complicated relationships between genes, environments, brain gene expression and behaviour over developmental and evolutionary timescales.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1098/rsbl.2021.0293DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8440035PMC
September 2021

Combining information from parental and personal experiences: Simple processes generate diverse outcomes.

PLoS One 2021 13;16(7):e0250540. Epub 2021 Jul 13.

Department of Evolution, Ecology, and Behavior, University of Illinois, Urbana-Champaign, Urbana, Illinois, United States of America.

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 offspring phenotypes observed in empirical studies of developmental plasticity in response to environmental cues. We analyze Bayesian models designed to mimic fully-factorial experimental studies of trans and within- generational plasticity (TWP), in which parents, offspring, both or neither are exposed to cues from predators, to determine how different durations of cue exposure for parents and offspring, the devaluation of information from parents or the degradation of information from parents would affect offspring estimates of environmental states related to risk of predation at the end of such experiments. We show that the effects of different cue durations, the devaluation of information from parents, and the degradation of information from parents on offspring estimates are all expected to vary as a function of interactions with two other key components of information-based models of TWP: parental priors and the relative cue reliability in the different treatments. Our results suggest empiricists should expect to observe considerable variation in the patterns observed in experimental studies of TWP based on simple principles of information-updating, without needing to invoke additional assumptions about costs, tradeoffs, development constraints, the fitness consequences of different trait values, or other factors.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0250540PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8277055PMC
October 2021

Sex-specific plasticity across generations I: Maternal and paternal effects on sons and daughters.

J Anim Ecol 2020 12 15;89(12):2788-2799. Epub 2020 Nov 15.

Department of Evolution, Ecology and Behavior, School of Integrative Biology, University of Illinois Urbana-Champaign, Urbana, IL, USA.

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 in both adaptive and non-adaptive ways. Here, we evaluate the potential for sex-specific parental effects in a freshwater population of three-spined sticklebacks Gasterosteus aculeatus by independently and jointly manipulating maternal and paternal experiences and separately evaluating their phenotypic effects in sons versus daughters. We tested the adaptive hypothesis that daughters are more responsive to cues from their mother, whereas sons are more responsive to cues from their father. We exposed mothers, fathers or both parents to visual cues of predation risk and measured offspring antipredator traits and brain gene expression. Predator-exposed fathers produced sons that were more risk-prone, whereas predator-exposed mothers produced more anxious sons and daughters. Furthermore, maternal and paternal effects on offspring survival were non-additive: offspring with a predator-exposed father, but not two predator-exposed parents, had lower survival against live predators. There were also strong sex-specific effects on brain gene expression: exposing mothers versus fathers to predation risk activated different transcriptional profiles in their offspring, and sons and daughters strongly differed in the ways in which their brain gene expression profiles were influenced by parental experience. We found little evidence to support the hypothesis that offspring prioritize their same-sex parent's experience. Parental effects varied with both the sex of the parent and the offspring in complicated and non-additive ways. Failing to account for these sex-specific patterns (e.g. by pooling sons and daughters) would have underestimated the magnitude of parental effects. Altogether, these results draw attention to the potential for sex to influence patterns of intergenerational plasticity and raise new questions about the interface between intergenerational plasticity and sex-specific selective pressures, sexual conflict and sexual selection.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1111/1365-2656.13364DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7902357PMC
December 2020

Sex-specific plasticity across generations II: Grandpaternal effects are lineage specific and sex specific.

J Anim Ecol 2020 12 15;89(12):2800-2812. Epub 2020 Nov 15.

Department of Evolution, Ecology and Behavior, School of Integrative Biology, University of Illinois Urbana-Champaign, Urbana, IL, USA.

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 fine-tune the phenotypes of future generations in response to sex-specific life-history strategies. We sought to understand if exposing males to predation risk can influence grandoffspring via sperm in three-spined stickleback Gasterosteus aculeatus. We specifically tested the hypothesis that grandparental effects are transmitted in a sex-specific way down the male lineage, from paternal grandfathers to F2 males. We reared F1 offspring of unexposed and predator-exposed F0 males under 'control' conditions and used them to generate F2s with control grandfathers, a predator-exposed maternal grandfather (i.e. predator-exposed F0 males to F1 daughters to F2s), a predator-exposed paternal grandfather (i.e. predator-exposed F0 males to F1 sons to F2s) or two predator-exposed grandfathers. We then assayed male and female F2s for a variety of traits related to antipredator defence. We found little evidence that transgenerational effects were mediated to only male descendants via the paternal lineage. Instead, grandpaternal effects depended on lineage and were mediated largely across sexes, from F1 males to F2 females and from F1 females to F2 males. When their paternal grandfather was exposed to predation risk, female F2s were heavier and showed a reduced change in behaviour in response to a simulated predator attack relative to grandoffspring of control, unexposed grandparents. In contrast, male F2s showed reduced antipredator behaviour when their maternal grandfather was exposed to predation risk. However, these patterns were only evident when one grandfather, but not both grandfathers, was exposed to predation risk, suggesting the potential for non-additive interactions across lineages. If sex-specific and lineage effects are common, then grandparental effects are likely underestimated in the literature. These results draw attention to the importance of sex-selective inheritance of environmental effects and raise new questions about the proximate and ultimate causes of selective transmission across generations.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1111/1365-2656.13365DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7902365PMC
December 2020

The information provided by the absence of cues: insights from Bayesian models of within and transgenerational plasticity.

Oecologia 2020 Dec 30;194(4):585-596. Epub 2020 Oct 30.

Evolution, Ecology and Behavior, University of Illinois at Urbana-Champaign, Urbana, Il, USA.

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 the absence of the cues in control treatments. We apply basic principles of information-updating to several experimental protocols used to study phenotypic plasticity in response to cues from predators to show why the reliability of the information provided by the absence of those cues in a control treatment might vary as a function of the subjects' experiences in the experimental treatment. We then analyze Bayesian models designed to mimic fully factorial experimental studies of trans and within-generational plasticity, in which parents, offspring, both or neither are exposed to cues from predators, and the information-states of the offspring in the different groups are compared at the end of the experiment. The models predict that the pattern of differences in offspring information-state across the four treatment groups will vary among experiments, depending on the reliability of the information provided by the control treatment, and the parent's initial estimate of the value of the state (the parental Prior). We suggest that variation among experiments in the reliability of the information provided by the absence of particular cues in the control treatment may be a general phenomenon, and that Bayesian approaches can be useful in interpreting the results of such experiments.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1007/s00442-020-04792-9DOI Listing
December 2020

Predictors of individual variation in reversal learning performance in three-spined sticklebacks.

Anim Cogn 2020 Sep 8;23(5):925-938. Epub 2020 Jun 8.

Program in Ecology, Evolution, and Conservation Biology, School of Integrative Biology, University of Illinois, 505 S. Goodwin Ave., Urbana, IL, 61801, USA.

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 of coping styles theory. We tested whether individual variation in flexibility correlates with response to novelty (response to a novel object), boldness (emergence into a novel environment), and behavioral persistence (response to a barrier), and tested for trade-offs between how quickly individuals learn an initial discrimination and flexibility. We compare results when reversal learning performance is measured during an early step of reversal learning (e.g. the number of errors during the first reversal session) to when reversal learning performance is measured by time to criterion. Individuals that made fewer mistakes during an early step of reversal learning spent more time away from the novel object, were less bold, less persistent, and performed worse during initial discrimination learning. In contrast, time to criterion was not correlated with any of the behaviors measured. This result highlights the utility of dissecting the steps of reversal learning to better understand variation in behavioral flexibility. Altogether, this study suggests that individuals differ in flexibility because flexibility is a key ingredient to their overall integrated strategy for coping with environmental challenges.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1007/s10071-020-01399-8DOI Listing
September 2020

Personality traits change after an opportunity to mate.

Proc Biol Sci 2020 05 29;287(1926):20192936. Epub 2020 Apr 29.

Department of Evolution, Ecology and Behavior, Carl R. Woese Institute for Genomic Biology, Program in Neuroscience, University of Illinois, Urbana, IL, USA.

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 personality traits to change in female threespine sticklebacks. We confirmed that there are consistent individual differences in activity, sociability and risk-taking, and then compared these personality traits among three groups of females: (i) control females; (ii) females that had physically mated, and (iii) females that had socially experienced courtship but did not mate. Both the physical experience of mating and the social experience of courtship caused females to become less willing to take risks and less social. To understand the proximate mechanisms underlying these changes, we measured levels of excreted steroids. Both the physical experience of mating and the social experience of courtship caused levels of dihydroxyprogesterone (17α,20β-P) to increase, and females with higher 17α,20β-P were less willing to take risks and less social. These results provide experimental evidence that personality traits and their underlying neuroendocrine correlates are influenced by formative social and life-history experiences well into adulthood.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1098/rspb.2019.2936DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7282925PMC
May 2020

Effects of predation risk on egg steroid profiles across multiple populations of threespine stickleback.

Sci Rep 2020 03 23;10(1):5239. Epub 2020 Mar 23.

School of Integrative Biology, Program in Neuroscience, Program in Ecology, Evolution and Conservation Biology, Carl R. Woese Institute for Genomic Biology, University of Illinois, Urbana Champaign, Urbana, IL, USA.

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 activation of the maternal HPA axis can have intergenerational consequences via, for example, maternally-derived steroids in eggs. Here, we investigated how predation risk affects a suite of maternally-derived steroids in threespine stickleback eggs across nine Alaskan lakes that vary in whether predatory trout are absent, native, or have been stocked within the last 25 years. Using liquid chromatography coupled with mass spectroscopy (LC-MS/MS), we detected 20 steroids within unfertilized eggs. Factor analysis suggests that steroids covary within and across steroid classes (i.e. glucocorticoids, progestogens, sex steroids), emphasizing the modularity and interconnectedness of the endocrine response. Surprisingly, egg steroid profiles were not significantly associated with predator regime, although they were more variable when predators were absent compared to when predators were present, with either native or stocked trout. Despite being the most abundant steroid, cortisol was not consistently associated with predation regime. Thus, while predators can affect steroids in adults, including mothers, the link between maternal stress and embryonic development is more complex than a simple one-to-one relationship between the population-level predation risk experienced by mothers and the steroids mothers transfer to their eggs.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1038/s41598-020-61412-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7090078PMC
March 2020

Transgenerational Plasticity in Human-Altered Environments.

Trends Ecol Evol 2020 02 6;35(2):115-124. Epub 2019 Nov 6.

Department of Environmental Science and Policy, University of California, One Shields Avenue, Davis, CA 95616, USA.

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 stressors when parental environments are highly predictive of offspring environments. HIREC can alter conditions that favored TGP in historical environments by reducing parents' ability to detect environmental conditions, disrupting previous correlations between parental and offspring environments, and interfering with the transmission of parental cues to offspring. Because of the propensity to produce errors in these processes, TGP will likely generate negative fitness outcomes in response to HIREC, though beneficial fitness outcomes may occur in some cases.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.tree.2019.09.003DOI Listing
February 2020

Do male sticklebacks use visual and/or olfactory cues to assess a potential mate's history with predation risk?

Anim Behav 2018 Nov 26;145:151-159. Epub 2018 Oct 26.

Department of Animal Biology, School of Integrative Biology, University of Illinois at Urbana-Champaign.

Differential allocation occurs when individuals alter their reproductive investment based on their mate's traits. A previous study showed that male threespine sticklebacks, , reduced courtship towards females that had previously been exposed to predation risk compared to unexposed females. This suggests that males can detect a female's previous history with predation risk, but the mechanisms by which males assess a female's history are unknown. To determine whether males use chemical and/or visual cues to detect a female's previous history with predation risk, we compared rates of courtship behaviour in the presence of visual and/or olfactory cues of predator-exposed females versus unexposed females in a 2×2 factorial design. We found that males differentiate between unexposed and predator-exposed females using visual cues: regardless of the olfactory cues present, males performed fewer zigzags (a conspicuous courtship behaviour) when they were exposed to visual cues from predator-exposed females compared to unexposed females. However, males' response to olfactory cues changed over the course of the experiment: initially, males performed fewer courtship displays when they received olfactory cues of predator-exposed females compared to unexposed females, but they did not discriminate between cues from predator-exposed and unexposed females later in the experiment. A follow-up experiment found that levels of cortisol released by both predator-exposed and unexposed females decreased over the course of the experiment. If cortisol is linked to or correlated with olfactory cues of predation risk that are released by females, then this suggests that the olfactory cues became less potent over the course of the experiment. Altogether, these results suggest that males use both visual and olfactory cues to differentiate between unexposed and predator-exposed females, which may help ensure reliable communication in a noisy environment.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.anbehav.2018.09.015DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6820985PMC
November 2018

Neurogenomic insights into paternal care and its relation to territorial aggression.

Nat Commun 2019 09 30;10(1):4437. Epub 2019 Sep 30.

Carl R. Woese Institute for Genomic Biology, University of Illinois, Urbana Champaign, 1206 Gregory Drive, Urbana, IL, 61801, USA.

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 stages, and some genes are added to the previously acquired neurogenomic state. Comparative genomic analysis suggests that some of these neurogenomic dynamics resemble changes associated with pregnancy and reproduction in mammalian mothers. Moreover, gene regulatory analysis identifies transcription factors that are regulated in opposite directions in response to a territorial challenge versus during paternal care. Altogether these results show that some of the molecular mechanisms of parental care might be deeply conserved and might not be sex-specific, and suggest that tradeoffs between opposing social behaviors are managed at the gene regulatory level.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1038/s41467-019-12212-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6768867PMC
September 2019

Correction to 'Parenting behaviour is highly heritable in male stickleback'.

R Soc Open Sci 2019 Aug 21;6(8):191372. Epub 2019 Aug 21.

[This corrects the article DOI: 10.1098/rsos.171029.].
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1098/rsos.191372DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6731727PMC
August 2019

Individual variation and the challenge hypothesis.

Authors:
Alison M Bell

Horm Behav 2020 07 20;123:104549. Epub 2019 Jul 20.

Department of Evolution, Ecology and Behavior, School of Integrative Biology, Carl R. Woese Institute for Genomic Biology, Program in Ecology, Evolution and Conservation, Neuroscience Program, University of Illinois, Urbana Champaign, United States of America. Electronic address:

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 ways. First, the challenge hypothesis drew attention to the ways in which the environment experienced by an organism - including the social environment - can influence biological processes internal to the organism, e.g. changes to physiology, gene expression, neuroendocrine state and epigenetic modifications. That is, the challenge hypothesis illustrated the bidirectional, dynamic relationship between hormones and (social) environments, thereby helping us to understand how behavioral variation among individuals can emerge over time. Because the paper was inspired by data collected on free living animals in natural populations, it drew behavioral ecologists' attention to this phenomenon. Second, the challenge hypothesis highlighted what became a paradigmatic example of a hormonal mechanism for a behavioral spillover, i.e. testosterone's pleiotropic effects on both territorial aggression and parental care causes aggression to "spillover" to influence parenting behavior, thereby limiting behavioral plasticity. Third, the challenge hypothesis contributed to what is now a cottage industry examining individual differences in hormone titres and their relationship with behavioral variation. I argue that one particularly promising future research direction in this area is to consider the active role of behavior and behavioral types in eliciting social interactions, including territorial challenges.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.yhbeh.2019.06.013DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6980443PMC
July 2020

The role of variation and plasticity in parental care during the adaptive radiation of three-spine sticklebacks.

Evolution 2019 05 25;73(5):1037-1044. Epub 2019 Mar 25.

Department of Animal Biology, University of Illinois Urbana-Champaign, Urbana, Illinois, 61801.

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 facilitated the adaptive radiation of three-spine sticklebacks. We compared the behavior of fathers across multiple ancestral (marine) and derived (freshwater) stickleback populations that differ in time since establishment. We measured behavioral plasticity in fathers in response to a predator found only in freshwater environments, simulating conditions marine males experience when colonizing freshwater. The antipredator behavior of males from newly established freshwater populations was intermediate between marine populations and well-established freshwater populations. In contrast to our predictions, on average, there was greater behavioral plasticity in derived freshwater populations than in ancestral marine populations. However, we found greater individual variation in behavioral reaction norms in marine populations compared to well-established freshwater populations, with newly established freshwater populations intermediate. This suggests that standing variation in behavioral reaction norms within ancestral populations might provide different evolutionary trajectories, and illustrates how plasticity can contribute to adaptive radiations.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1111/evo.13711DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6542286PMC
May 2019

Intraspecific variation in cue-specific learning in sticklebacks.

Anim Behav 2018 Mar 19;137:161-168. Epub 2018 Feb 19.

Program in Ecology, Evolution, and Conservation Biology, School of Integrative Biology, University of Illinois, Urbana, IL, U.S.A.

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 a criterion-based protocol, we assessed whether two natural populations of sticklebacks differed in how quickly they learned to associate two different discrimination cues with the location of food. One version of the discrimination task required animals to use visual (colour) cues while the other required animals to use egocentric (side) cues. There were significant behavioural differences between the two populations, but no evidence that one population was generally better at learning, or that one version of the task was generally harder than the other. However, the two populations excelled on different tasks: fish from one population performed significantly better on the side version than they did on the colour version, while the opposite was observed in the other population. These results suggest that the two populations are equally capable of discrimination learning, but are primed to form associations with different cues. Ecological differences between the populations in environmental stability might account for the observed variation in learning. These findings highlight the value of comparing cognitive performance on different variations of the same task in order to understand variation in cognitive mechanisms.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.anbehav.2018.01.003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6239167PMC
March 2018

Omadacycline Enters the Ring: A New Antimicrobial Contender.

Pharmacotherapy 2018 12 15;38(12):1194-1204. Epub 2018 Nov 15.

Department of Pharmacy Practice, University of Mississippi School of Pharmacy, Jackson, Mississippi.

Omadacycline is a novel aminomethylcycline approved for the treatment of community-acquired bacterial pneumonia and acute bacterial skin and skin structure infections. This article reviews existing data pertaining to the biochemistry, mechanism of action, pharmacokinetics/pharmacodynamics, in vitro activity, and current progress with omadacycline in clinical trials. Omadacycline inhibits protein synthesis by binding to the 30S subunit of the bacterial ribosome at the tetracycline-binding site with an affinity similar to glycylcyclines. It is able to bypass older tetracycline resistance mechanisms and demonstrates activity against bacterial strains that are tetracycline resistant. In addition, omadacycline displays broad-spectrum activity against gram-positive organisms (including methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci), gram-negative organisms, atypical organisms, and anaerobes. It has been evaluated against infections in adults both intravenously and orally. Dosage adjustments are not required for patients with renal impairment. Omadacycline displays a comparable efficacy and safety profile to standard-of-care agents, with the most common side effects observed being gastrointestinal. Currently available data for omadacycline suggest that this is a promising agent added to our antimicrobial armamentarium.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1002/phar.2185DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6587716PMC
December 2018

Why does the magnitude of genotype-by-environment interaction vary?

Ecol Evol 2018 Jun 8;8(12):6342-6353. Epub 2018 May 8.

University of Illinois at Urbana-Champaign Urbana Illinois.

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 magnitude vary dramatically across populations and traits. Despite this, we still know little about why G × E is so evident in some traits and populations, but minimal or absent in others. To encourage synthetic research in this area, we review diverse hypotheses for the underlying biological causes of variation in G × E. We extract common themes from these hypotheses to develop a more synthetic understanding of variation in G × E and suggest some important next steps.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1002/ece3.4128DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6024136PMC
June 2018

Personal and transgenerational cues are nonadditive at the phenotypic and molecular level.

Nat Ecol Evol 2018 08 9;2(8):1306-1311. Epub 2018 Jul 9.

Department of Animal Biology, University of Illinois, Urbana, IL, USA.

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 molecular level in threespined sticklebacks (Gasterosteus aculeatus). We show that regardless of whether cues about predation risk were provided by their father or acquired through personal experience, sticklebacks produced the same set of predator-adapted phenotypes. Moreover, there were nonadditive effects of personal and paternal experience: animals that received cues from both sources resembled animals that received cues from a single source. A similar pattern was detected at the molecular level: there was a core set of genes that were differentially expressed in the brains of offspring regardless of whether risk was experienced by their father, themselves or both. These results provide strong support for cue integration theory because they show that cues provided by parents and personal experience are comparable at both the phenotypic and molecular level, and draw attention to the importance of nonadditive responses to multiple cues.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1038/s41559-018-0605-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6062471PMC
August 2018

Cross-species systems analysis of evolutionary toolkits of neurogenomic response to social challenge.

Genes Brain Behav 2019 01 16;18(1):e12502. Epub 2018 Jul 16.

Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois.

Social challenges like territorial intrusions evoke behavioral responses in widely diverging species. Recent work has showed 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 multispecies computational-experimental approach to characterize such a toolkit at a systems level. Brain transcriptomic responses to social challenge was probed via RNA-seq profiling in three diverged species-honey bees, mice and three-spined stickleback fish-following a common methodology, allowing fair comparisons across species. Data were collected from multiple brain regions and multiple time points after social challenge exposure, achieving anatomical and temporal resolution substantially greater than previous work. We developed statistically rigorous analyses equipped to find homologous functional groups among these species at the levels of individual genes, functional and coexpressed gene modules, and transcription factor subnetworks. We identified six orthogroups involved in response to social challenge, including groups represented by mouse genes Npas4 and Nr4a1, as well as common modulation of systems such as transcriptional regulators, ion channels, G-protein-coupled receptors and synaptic proteins. We also identified conserved coexpression modules enriched for mitochondrial fatty acid metabolism and heat shock that constitute the shared neurogenomic response. Our analysis suggests a toolkit wherein nuclear receptors, interacting with chaperones, induce transcriptional changes in mitochondrial activity, neural cytoarchitecture and synaptic transmission after social challenge. It shows systems-level mechanisms that have been repeatedly co-opted during evolution of analogous behaviors, thus advancing the genetic toolkit concept beyond individual genes.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1111/gbb.12502DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6314924PMC
January 2019

Genomic tools for behavioural ecologists to understand repeatable individual differences in behaviour.

Nat Ecol Evol 2018 06 12;2(6):944-955. Epub 2018 Feb 12.

Department of Animal Biology, The University of Illinois, Urbana-Champaign, Urbana, IL, USA.

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 techniques may yield new insights, and we provide specific guidance on how and whether the latest tools available are appropriate given different resources, system and organismal constraints, and experimental designs. Integrating molecular genetic techniques with other strategies to study the proximal causes of behaviour provides opportunities to expand rapidly into new avenues of exploration. Such endeavours will enable us to better understand how repeatable individual differences in behaviour have evolved, how they are expressed and how they can be maintained within natural populations of animals.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1038/s41559-017-0411-4DOI Listing
June 2018

Parenting behaviour is highly heritable in male stickleback.

R Soc Open Sci 2018 Jan 10;5(1):171029. Epub 2018 Jan 10.

School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.

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 (). Male three-spined stickleback are the sole providers of parental care that is necessary for offspring survival; therefore, this system offers the opportunity to study the inheritance of parental behaviour when selection is primarily acting on males. Fanning behaviour is a conspicuous parental behaviour that is readily quantified in this species. We show that the heritability of fanning behaviour is ≥0.9 and significantly different from zero within a freshwater population. Moreover, there was abundant genetic variation for fanning behaviour, indicating that it could readily evolve. These results suggest that parenting behaviour is tractable for further genetic dissection in this system.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1098/rsos.171029DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5792893PMC
January 2018

Changes in behavior and brain immediate early gene expression in male threespined sticklebacks as they become fathers.

Horm Behav 2018 01 14;97:102-111. Epub 2017 Nov 14.

School of Integrative Biology, Program in Neuroscience, Program in Ecology, Evolution and Conservation, Institute for Genomic Biology, University of Illinois, Urbana Champaign, United States. Electronic address:

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 (Gasterosteus aculeatus), a species in which fathers are the sole providers of parental care. In experiment 1, we tested whether males' behavioral reactions to different social stimuli depends on parental status, i.e. whether they were providing parental care. Parental males visited their nest more in response to social stimuli compared to nonparental males. Rates of courtship behavior were high in non-parental males but low in parental males. In experiment 2, we used a quantitative in situ hybridization method to compare the expression of an immediate early gene (Egr-1) across the breeding cycle - from establishing a territory to caring for offspring. Egr-1 expression peaked when the activities associated with fatherhood were greatest (when they were providing care to fry), and then returned to baseline levels once offspring were independent. The medial dorsal telencephalon (basolateral amygdala), lateral part of dorsal telencephalon (hippocampus) and anterior tuberal nucleus (ventral medial hypothalamus) exhibited high levels of Egr-1 expression during the breeding cycle. These results help to define the neural circuitry associated with fatherhood in fishes, and are consistent with the hypothesis that fatherhood - like motherhood - is a period of intense behavioral and neural activity.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.yhbeh.2017.11.002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5771839PMC
January 2018

Transgenerational and developmental plasticity at the molecular level: Lessons from Daphnia.

Mol Ecol 2017 10 11;26(19):4859-4861. Epub 2017 Sep 11.

Department of Biology, Colorado State University, Fort Collins, CO, USA.

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 of our ancestors' experience?). It is also a touchy subject within evolutionary biology because it provokes concerns about Lamarckianism and general scepticism about the importance of extra-genetic inheritance (Laland et al., ). Part of why the research in this area has been controversial is because it is difficult to study. For one, there is the problem of how long it takes to track changes across generations, making long-term, multi-generational studies especially tricky in long-lived species. Moreover, there are presently very few (if any) known molecular mechanisms by which environmental effects can be incorporated into the genome and persist for multiple successive generations, casting doubt on their evolutionary repercussions. Fortunately, you only have to look in your local pond to find the creatures that are teaching us a great deal about how and why the experiences of parents are passed down to their offspring. In this issue of Molecular Ecology, Hales et al. (Hales et al., ) illustrate the power of Daphnia ("water fleas") for making headway in this field.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1111/mec.14327DOI Listing
October 2017

Temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks.

PLoS Genet 2017 Jul 13;13(7):e1006840. Epub 2017 Jul 13.

Carl R. Woese Institute for Genomic Biology, University of Illinois, Urbana Champaign, Urbana, IL, United States of America.

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 transcription associated with distinct molecular functions in the brain of male threespined sticklebacks, a species famous for its behavioral repertoire and evolution. Some biological functions (e.g., hormone activity) peaked soon after a brief territorial challenge and then declined, while others (e.g., immune response) peaked hours afterwards. We identify transcription factors that are predicted to coordinate waves of transcription associated with different components of behavioral plasticity. Next, using H3K27Ac as a marker of chromatin accessibility, we show that a brief territorial intrusion was sufficient to cause rapid and dramatic changes in the epigenome. Finally, we integrate the time course brain gene expression data with a transcriptional regulatory network, and link gene expression to changes in chromatin accessibility. This study reveals rapid and dramatic epigenomic plasticity in response to a brief, highly consequential social interaction.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1371/journal.pgen.1006840DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5509087PMC
July 2017

Testing the predictions of coping styles theory in threespined sticklebacks.

Behav Processes 2017 Mar 23;136:1-10. Epub 2016 Dec 23.

Program in Ecology, Evolution, and Conservation Biology, School of Integrative Biology, University of Illinois, 505 S. Goodwin Ave., Urbana, IL 61801, United States; Institute for Genomic Biology, University of Illinois, Urbana, IL, United States.

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 more routinized than their reactive counterparts. A key tenet of coping styles theory is that variation in coping styles is maintained by tradeoffs with behavioral flexibility: proactive individuals excel in stable environments while more flexible, reactive individuals perform better in variable environments. Here, we assess evidence for coping styles within a natural population of threespined sticklebacks (Gasterosteus aculeatus). We developed a criterion-based learning paradigm to evaluate individual variation in initial and reversal learning. We observed strong individual differences in boldness, cortisol production, and learning performance. Consistent with coping styles, fish that released more cortisol were more timid in response to a predator attack and slower to learn a color discrimination task. However, there was no evidence that reactive individuals performed better when the environment changed (when the rewarded color was reversed). The failure to detect trade-offs between behavioral routinization and flexibility prompts other explanations for the maintenance of differing coping styles.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.beproc.2016.12.011DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5493480PMC
March 2017

Molecular mechanisms and the conflict between courtship and aggression in three-spined sticklebacks.

Mol Ecol 2016 09 26;25(17):4368-76. Epub 2016 Aug 26.

School of Integrative Biology, Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, 505 S. Goodwin Ave., 433 Morrill Hall, Urbana, IL, 61801, USA.

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 behavioural trade-offs are largely unknown. In this study, we compared the brain transcriptional responses of territorial male three-spined sticklebacks to a mating opportunity with a female and to a territorial challenge by a rival male. We focused on the diencephalon and the cerebellum, two regions of the brain implicated in courtship and aggression. There was a set of genes that were differentially expressed in response to both a courtship opportunity and a territorial challenge. Closer inspection of the direction of regulation revealed that genes that were downregulated in response to a courtship opportunity were upregulated in response to a territorial challenge and vice versa. Our study reveals some of the potential molecular mechanisms underlying behavioural trade-offs between sex and aggression, along with a possible solution to the conflict via social context-dependent gene regulation.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1111/mec.13766DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5021609PMC
September 2016

Stickleback embryos use ATP-binding cassette transporters as a buffer against exposure to maternally derived cortisol.

Proc Biol Sci 2016 Mar;283(1826):20152838

School of Integrative Biology, University of Illinois, Urbana, IL 61801, USA Carl R. Woese Institute for Genomic Biology, University of Illinois, Urbana, IL 61801, USA.

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, much less is known about how and whether egg-laying vertebrates can control their steroid environment during embryonic development. We tested the hypothesis that threespine stickleback (Gasterosteus aculeatus) embryos can regulate exposure to maternal steroids via active efflux of maternal steroids from the egg. Embryos rapidly (within 72 h) cleared intact steroids, but blocking ATP-binding cassette (ABC) transporters inhibited cortisol clearance. Remarkably, this efflux of cortisol was sufficient to prevent a transcriptional response of embryos to exogenous cortisol. Taken together, these findings suggest that, much like their placental counterparts, developing fish embryos can actively regulate their exposure to maternal cortisol. These findings highlight the fact that even in egg-laying vertebrates, the realized exposure to maternal steroids is mediated by both maternal and embryonic processes and this has important implications for understanding how maternal stress influences offspring development.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1098/rspb.2015.2838DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4810855PMC
March 2016
-->