Search

Addressing climate change and biodiversity loss will be the defining ecological, political, and humanitarian challenge of our time. Alarmingly, policymakers face a narrowing window of opportunity to prevent the worst impacts, necessitating complex decisions about which land to set aside for biodiversity preservation. Yet, our ability to make these decisions is hindered by our limited capacity to predict how species will respond to synergistic drivers of extinction risk. We argue that a rapid integration of biogeography and behavioral ecology can meet these challenges because of the distinct, yet complementary levels of biological organization they address, scaling from individuals to populations, and from species and communities to continental biotas. This union of disciplines will advance efforts to predict biodiversity’s responses to climate change and habitat loss through a deeper understanding of how biotic interactions and other behaviors modulate extinction risk, and how responses of individuals and populations impact the communities in which they are embedded. Fostering a rapid mobilization of expertise across behavioral ecology and biogeography is a critical step toward slowing biodiversity loss.

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., Compared to motherhood, the molecular changes associated with fatherhood are less understood. Here, the authors investigate gene expression changes associated with paternal care in male stickleback fish, and compare them with patterns in territorial aggression.

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., 2014). 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., 2017) illustrate the power of Daphnia (“water fleas”) for making headway in this 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.

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.

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 three-spined 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 sticklebacks 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.

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.

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.

Lake and stream habitats pose a variety of challenges to fishes due to differences in variables such as water velocity, habitat structure, prey community, and predator community. These differences can cause divergent selection on body size and/or shape. Here, we measured sex, age, length, and eight different morphological traits of the blackstripe topminnow, Fundulus notatus, from 19 lake and stream populations across four river drainages in central Illinois. Our goal was to determine whether size and shape differed consistently between lake and stream habitats across drainages. We also considered the effects of age and sex as they may affect size and morphology. We found large differences in body size of age 1 topminnows where stream fish were generally larger than lake fish. Body shape mainly varied as a function of sex. Adult male topminnows had larger morphological traits (with the exception of body width) than females, in particular longer dorsal and anal base lengths. Subtle effects of habitat were present. Stream fish had a longer dorsal fin base than lake fish. These phenotypic patterns may be the result of genetic and/or environmental variation. As these lakes are human-made, the observed differences, if genetic, would have had to occur relatively rapidly (within about 100 years). © 2013 The Linnean Society of London

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 con-specifics. 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.

Phenotypic plasticity is a widespread phenomenon in which one genotype produces different phenotypes under different environmental conditions. Whether plasticity is adaptive or not depends on the optimal phenotypic value in each environment (Via 1993). Adaptive plasticity is expected to align with the direction of selective gradients, moving traits closer to the optima (Fig. 1A). Likewise, if the optimal values are similar in both environments, plasticity may be non-adaptive, opposing the directions of selective gradients (Fig. 1B). Plasticity as a trait is also subject to selective pressures and can itself evolve. This article is protected by copyright. All rights reserved

Summary 1. 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.

Some phytophagous insects gain defense from natural enemies by associating with otherwise potentially harmful top predators. Many lycaenid butterfly caterpillars are involved in such interactions with ants: larvae provide carbohydrate rewards from the dorsal nectary organ (DNO) to associated ants in return for protection from natural enemies. The stability of these interactions involves signals that identify the lycaenid caterpillar as a mutualist. However, larvae of some lycaenid species, such as Lycaena xanthoides, are found in close association with ants but do not possess the reward producing DNO. Evaluating the relationship in a phylogenetic framework, we show that the association between L. xanthoides and ants likely evolved from a non-ant-associated ancestor. Behavioral trials also show that L. xanthoides larvae are capable of influencing ant behavior to increase ant tending when faced with a simulated predator attack, without providing DNO-derived rewards to ant associates. These results demonstrate that the DNO is not necessary to maintain associations between lycaenid larvae and ants. Third-party interactions may affect the evolution of mutualisms and consideration of underlying evolutionary history is necessary to understand contemporary species associations.

Male provisioning of incubating females can increase reproductive success by maintaining physiological condition of females and consistency of incubation. The effects of male provisioning on the maintenance of incu- bation temperature and embryo development should be particularly pronounced in environments where ambient temperature exceeds the tolerance of unincubated eggs and where consistency of female incubation might be particu- larly important for hatching success. Here, we investigated the reproductive consequences of incubation feeding in a desert population of House Finches (Carpodacus mexic- anus) in southwestern Arizona. We found that greater nest attentiveness by females was related to higher minimum incubation nest temperature, that in turn was closely associated with hatching success. Only 44% of males regularly provisioned their incubating females. Although provisioned females maintained higher incubation tem- perature and took fewer incubation breaks than non-pro- visioned females, overall, male provisioning did not influence incubation dynamics or hatching success. Fur- ther, a male's incubation feeding rate did not correlate with male provisioning of nestlings. These results corroborate the finding that, in male House Finches, neither provi- sioning of incubating females nor pre-incubation courtship feeding are associated with increases in circulating pitui- tary prolactin--the hormone regulating male provisioning of nestlings. We suggest that incubation provisioning by male might be a component of pair maintenance behavior and that variation in male incubation behavior is best understood in relation to asymmetries in residual repro- ductive values between the mates.

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 changes in response to the experience of parenting in male threespine sticklebacks, Gasterosteus aculeatus. Life history theory predicts that males should be less risk averse after successfully parenting, and the neuroendocrinology of parenting suggests that parenting could reorganize the hormonal landscape and behaviour of fathers. We randomly assigned males to either an experimental group (reproduced and parented) or a control group (did not reproduce and parent), and repeatedly measured a personality trait ('boldness') and 11-ketotestosterone levels (11-kT, the major androgen in fishes) in individual males. In the control group, males became bolder over time. However, in the experimental group, boldness did not change. Furthermore, 11-kT changed dramatically in the experimental group, and changes in 11-kT in parents were associated with boldness after parenting ceased. Our study is one of the first to assess proximate and ultimate explanations for changes in personality as a function of reproduction and parenting.

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.

Review of A Troublesome Inheritance: Genes, Race and Human History, by Nicholas Wade. New York: Penguin Press, 2013. x + 278 pp. 978-1-5942-0446-3 (hardcover). US $27.95.