In a wide range of organisms, including humans, mothers can influence offspring via the care they provide. Comparatively little is known about the effects of fathering on offspring. Here, we test the hypothesis that fathers are capable of programming their offspring for the type of environment they are likely to encounter. Male threespine sticklebacks, Gasterosteus aculeatus, were either exposed to predation risk while fathering or not. Fathers altered their paternal behaviour when exposed to predation risk, and consequently produced adult offspring with phenotypes associated with strong predation pressure (smaller size, reduced body condition, reduced behavioural activity). Moreover, more attentive fathers produced offspring that showed stronger antipredator responses. These results are consistent with behaviourally mediated paternal programming: fathers can alter offspring phenotypes to match their future environment and influence offspring traits well into adulthood.
There is growing evidence that individual animals show consistent differences in behavior. For example, individual threespined stickleback fish differ in how they react to predators and how aggressive they are during social interactions with conspecifics. A relatively unexplored but potentially important axis of variation is parental behavior. In sticklebacks, fathers provide all of the parental care that is necessary for offspring survival; therefore paternal care is directly tied to fitness. In this study, we assessed whether individual male sticklebacks differ consistently from each other in parental behavior. We recorded visits to nest, total time fanning, and activity levels of 11 individual males every day throughout one clutch, and then allowed the males to breed again. Half of the males were exposed to predation risk while parenting during the first clutch, and the other half of the males experienced predation risk during the second clutch. We detected dramatic temporal changes in parental behaviors over the course of the clutch: for example, total time fanning increased six-fold prior to eggs hatching, then decreased to approximately zero. Despite these temporal changes, males retained their individually-distinctive parenting styles within a clutch that could not be explained by differences in body size or egg mass. Moreover, individual differences in parenting were maintained when males reproduced for a second time. Males that were exposed to simulated predation risk briefly decreased fanning and increased activity levels. Altogether, these results show that individual sticklebacks consistently differ from each other in how they behave as parents.
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.
Expertise in the broader impacts of scientific research is an increasingly important aspect of professional development, particularly because federal grant proposals are commonly reviewed using both the Intellectual Merit and the Broader Impacts Criteria. Unfortunately, training in broader impacts, such as science communication and outreach, is not typically part of undergraduate or graduate curricula. We initiated one of the first graduate-level biology courses on broader impacts, focusing on giving graduate students firsthand, authentic experiences with grant writing, science communication, and educational outreach. Students in this interdisciplinary course learned from experts, wrote for a broad audience about their own research, and proposed and implemented outreach in collaboration with local organizations. We outline our approach, discuss outcomes from each activity, assess our impact, and finally consider how future programs might expand on this model.
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 this field study we measured consistent individual differences in parenting behavior and evaluated correlations between parenting and other behaviors in threespine stickleback (Gasterosteus aculeatus). We repeatedly measured male parenting behavior and male behavior in the presence of three different types of live intruders: a female, a conspecific male, and a predator, meant to provoke courtship, aggressive and antipredator behavior, respectively. While males plastically adjusted their reactions to different types of intruders, we found consistent individual differences in behavior (behavioral types) both within and across contexts, even after accounting for variation in body size and nest characteristics. Males that performed more parenting behavior responded faster to all types of intruders. These results suggest that in nature, individual male stickleback exhibit robust parental behavioral types, and highly parental males are more attentive to their surroundings. Future studies are needed to examine the potential causes of individual variation in parental behavior in the field.
Stressors experienced by parents can influence the behavioral development of their offspring. Here, we review recent studies in threespined sticklebacks (a species in which males are the sole providers of parental care) showing that when parents are exposed to an ecologically relevant stressor (predation risk), there are consequences for offspring. For example, female sticklebacks exposed to predation risk produce eggs with higher concentrations of cortisol, a stress hormone, and offspring with altered behavior and physiology. Male sticklebacks exposed to predation risk produce offspring that are less active, smaller, and in poorer condition. The precise mechanisms by which maternal and paternal experiences with predators affect offspring phenotypes are under investigation, and could include steroid hormones, olfactory cues and/or parental behavior. As in other species, some of the consequences of parental exposure to predation risk for offspring in sticklebacks might be adaptive, but depend on the stressor, the reliability of the parental and offspring environments and the evolutionary history of the population.
Summary1. Environmental factors such as temperature, humidity and partial oxygen pressure can affect avian eggshell structure because gas exchange across the shell must allow sufficient water loss while preventing dehydration of the embryo. Studies of species with known chronology of colonization of novel environments provide a powerful insight into the relative importance of ecological factors shaping the evolution of eggshell structure. 2. Here, we examined changes in eggshell structure that accompanied rapid range expansion of house finches (Carpodacus mexicanus) across North America. We analysed thickness and pore density in eggshells from three ecologically distinct populations: the native desert population in southwestern Arizona and two 30-year-old populations in the northwestern (north-west Montana) and southeastern (south-east Alabama) parts of the species' range. We also conducted cross-foster exchanges of freshly laid eggs within and between the northwestern and southeastern populations to examine consequences of population differences in eggshell structure on embryo development. 3. Eggshell structure was most distinct in a recently established population inhabiting higher humidity environment (southeastern Alabama), where eggs were the largest, eggshells the thickest and pore density the lowest. Populations that experienced highly distinct ambient temperatures (southwestern Arizona and northwestern Montana) nevertheless had similar eggshell structure. These results were corroborated by experiments where humidity differences between cross-fostered nests had twice the effect on embryo survival compared to the effect of change in ambient temperature. Correspondingly, experimental egg exchanges between southeastern. Alabama and northwestern Montana populations were associated with fourfold increase in embryo mortality compared to within-population egg exchanges. 4. We document rapid evolution of eggshell structure in response to colonization of novel environments and establish the relative importance of environmental factors on avian eggshells. We discuss these results in relation to population variation in incubation behaviour and its ability to shield eggshell structure from the selection exerted by novel environments.
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.
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