Explore the vast range of titles available.

Transgenerational plasticity (TGP) occurs when the environment experienced by a parent influences the development of their offspring. In this article, we develop a framework for understanding the mechanisms and multigenerational consequences of TGP. First, we conceptualize the mechanisms of TGP in the context of communication between parents (senders) and offspring (receivers) by dissecting the steps between an environmental cue received by a parent and its resulting effects on the phenotype of one or more future generations. Breaking down the problem in this way highlights the diversity of mechanisms likely to be involved in the process. Second, we review the literature on multigenerational effects and find that the documented patterns across generations are diverse. We categorize different multigenerational patterns and explore the proximate and ultimate mechanisms that can generate them. Throughout, we highlight opportunities for future work in this dynamic and integrative area of study.

A molecular signature found in the brains of monogamous prairie voles begins to decay after prolonged separation from their partner.A molecular signature found in the brains of monogamous prairie voles begins to decay after prolonged separation from their partner.

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.

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.

Significance In some cases similar molecular programs (i.e., conserved genes and gene networks) underlie the expression of phenotypic traits that evolve repeatedly across diverse species. We investigated this possibility in the context of social behavioral response, using a comparative genomics approach for three distantly related species: house mouse ( Mus musculus ), stickleback fish ( Gasterosteus aculeatus ), and honey bee ( Apis mellifera ). An experience of territory intrusion modulated similar brain functional processes across species, including hormone-mediated signal transduction, neurodevelopment, chromosome organization, and energy metabolism. Several homologous transcription factors also responded consistently to territory intrusion, suggesting that shared neuronal effects may involve transcriptional cascades of evolutionarily conserved genes. These results indicate that conserved genetic “toolkits” are involved in independent evolutions of social behavior. Certain complex phenotypes appear repeatedly across diverse species due to processes of evolutionary conservation and convergence. In some contexts like developmental body patterning, there is increased appreciation that common molecular mechanisms underlie common phenotypes; these molecular mechanisms include highly conserved genes and networks that may be modified by lineage-specific mutations. However, the existence of deeply conserved mechanisms for social behaviors has not yet been demonstrated. We used a comparative genomics approach to determine whether shared neuromolecular mechanisms could underlie behavioral response to territory intrusion across species spanning a broad phylogenetic range: house mouse ( Mus musculus ), stickleback fish ( Gasterosteus aculeatus ), and honey bee ( Apis mellifera ). Territory intrusion modulated similar brain functional processes in each species, including those associated with hormone-mediated signal transduction and neurodevelopment. Changes in chromosome organization and energy metabolism appear to be core, conserved processes involved in the response to territory intrusion. We also found that several homologous transcription factors that are typically associated with neural development were modulated across all three species, suggesting that shared neuronal effects may involve transcriptional cascades of evolutionarily conserved genes. Furthermore, immunohistochemical analyses of a subset of these transcription factors in mouse again implicated modulation of energy metabolism in the behavioral response. These results provide support for conserved genetic “toolkits” that are used in independent evolutions of the response to social challenge in diverse taxa.

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.

There is growing evidence for nongenetic effects of maternal experience on offspring. For example, previous studies have shown that female threespined stickleback fish (Gasterosteus aculeatus) exposed to predation risk produce offspring with altered behavior, metabolism and stress physiology. Here, we investigate the effect of maternal exposure to predation risk on the embryonic transcriptome in sticklebacks. Using RNA-sequencing we compared genome-wide transcription in three day post-fertilization embryos of predator-exposed and control mothers. There were hundreds of differentially expressed transcripts between embryos of predator-exposed mothers and embryos of control mothers including several non-coding RNAs. Gene Ontology analysis revealed biological pathways involved in metabolism, epigenetic inheritance, and neural proliferation and differentiation that differed between treatments. Interestingly, predation risk is associated with an accelerated life history in many vertebrates, and several of the genes and biological pathways that were identified in this study suggest that maternal exposure to predation risk accelerates the timing of embryonic development. Consistent with this hypothesis, embryos of predator-exposed mothers were larger than embryos of control mothers. These findings point to some of the molecular mechanisms that might underlie maternal effects.

Parental care can increase the fitness of parents through increased offspring survival but can also reduce reproductive output by limiting time and energy allocated to additional mating opportunities. The evolutionary origin of parental care is often associated with shifts in life‐history traits (e.g., high investment in few, large offspring, slow offspring growth), but little is known about whether the evolutionary loss of care is associated with reciprocal shifts in the same life‐history traits. Here, we capitalize on the divergence of parental care between ecotypes of three‐spined stickleback (Gasterosteus aculeatus) to test for associations between parental care and life‐history traits. While males from most stickleback populations provide care, an unusual “white” ecotype has recently lost paternal care. We found support for the hypothesis that the evolutionary loss of paternal care is associated with shifts in female life‐history traits; relative to females of the ecotype with paternal care, females of the white ecotype that lack paternal care produced clutches with a similar overall mass and a greater number of smaller eggs, despite their smaller body size, suggesting lower per‐offspring investment. We did not detect an ecotypic difference in embryonic development rate, metabolic rate, or offspring age at hatching, contrary to the ‘safe harbor hypothesis’. These results support the theory that behavioral traits such as parental care co‐evolve with other life‐history traits and highlight opportunities for future study of the underlying causal mechanisms. Parental care has evolved independently multiple times and is often associated with shifts in additional life‐history traits, such as increased egg size, but what happens when care is lost? Here, we show that an unusual population of sticklebacks that evolved a loss of typical paternal care also exhibit changes in maternal life‐history traits, including decreased egg size. These results highlight that male and female life‐history traits evolve in a coordinated way during both evolutionary gains and losses of parental care in one sex.

A behavioural syndrome occurs when individuals behave in a consistent way through time or across contexts and is analogous to 'personality' or 'temperament'. Interest is accumulating in behavioural syndromes owing to their important ecological and evolutionary consequences. There are plenty of opportunities in this burgeoning young field to integrate proximate and functional approaches to studying behaviour, but there are few guidelines about where to start or how to design a study on behavioural syndromes. After summarizing what we do and do not know, this brief review aims to act as a general guide for studying behavioural syndromes. Although the array of possible behavioural combinations can seem overwhelming, there are at least four different strategies that can be used to choose which behaviours or contexts to study in a behavioural syndromes view. I describe the strengths and weaknesses of these non-exclusive strategies, and then discuss the methodological and statistical issues raised by such studies.

Eco‐evolutionary experiments are typically conducted in semi‐unnatural controlled settings, such as mesocosms; yet inferences about how evolution and ecology interact in the real world would surely benefit from experiments in natural uncontrolled settings. Opportunities for such experiments are rare but do arise in the context of restoration ecology—where different “types” of a given species can be introduced into different “replicate” locations. Designing such experiments requires wrestling with consequential questions. (Q1) Which specific “types” of a focal species should be introduced to the restoration location? (Q2) How many sources of each type should be used—and should they be mixed together? (Q3) Which specific source populations should be used? (Q4) Which type(s) or population(s) should be introduced into which restoration sites? We recently grappled with these questions when designing an eco‐evolutionary experiment with threespine stickleback (Gasterosteus aculeatus) introduced into nine small lakes and ponds on the Kenai Peninsula in Alaska that required restoration. After considering the options at length, we decided to use benthic versus limnetic ecotypes (Q1) to create a mixed group of colonists from four source populations of each ecotype (Q2), where ecotypes were identified based on trophic morphology (Q3), and were then introduced into nine restoration lakes scaled by lake size (Q4). We hope that outlining the alternatives and resulting choices will make the rationales clear for future studies leveraging our experiment, while also proving useful for investigators considering similar experiments in the future. Opportunities for eco‐evolutionary experiments are rare but they do arise in the context of restoration ecology. Designing such experiments requires wrestling with several consequential questions. We recently grappled with these questions when designing an eco‐evolutionary experiment with threespine stickleback (Gasterosteus aculeatus) introduced into nine small lakes and ponds on the Kenai Peninsula in Alaska that required restoration. We ended up using benthic versus limnetic ecotypes from a mixture of four source populations per ecotype (selected based on trophic morphology) that were then introduced in various combinations into the nine restoration lakes.