Integrating biogeography and behavioral ecology to rapidly address biodiversity loss.

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.

Venom and Social Behavior: The Potential of Using Spiders to Evaluate the Evolution of Sociality under High Risk.

Risks of sociality, including competition and conspecific aggression, are particularly pronounced in venomous invertebrates such as arachnids. Spiders show a wide range of sociality, with differing levels of cannibalism and other types of social aggression. To have the greatest chance of surviving interactions with conspecifics, spiders must learn to assess and respond to risk. One of the major ways risk assessment is studied in spiders is via venom metering, in which spiders choose how much venom to use based on prey and predator characteristics. While venom metering in response to prey acquisition and predator defense is well-studied, less is known about its use in conspecific interactions. Here we argue that due to the wide range of both sociality and venom found in spiders, they are poised to be an excellent system for testing questions regarding whether and how venom use relates to the evolution of social behavior and, in return, whether social behavior influences venom use and evolution. We focus primarily on the widow spiders, Latrodectus, as a strong model for testing these hypotheses. Given that successful responses to risk are vital for maintaining sociality, comparative analysis of spider taxa in which venom metering and sociality vary can provide valuable insights into the evolution and maintenance of social behavior under risk.

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

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.

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

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.

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

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.

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

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.

Do reproduction and parenting influence personality traits? Insights from threespine stickleback.

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.

Consistent individual differences in paternal behavior: a field study of threespine stickleback.

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.

Paternal programming in sticklebacks.

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.

Consistent individual differences in fathering in threespined stickleback Gasterosteus aculeatus.

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.