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The emergence of complex social interactions is predicted to be an important selective force in the diversification of communication systems. Parental care presents a key social context in which to study the evolution of novel signals, as care often requires communication and behavioral coordination between parents and is an evolutionary stepping-stone toward increasingly complex social systems. Anuran amphibians (frogs and toads) are a classic model of acoustic communication and the vocal repertoires of many species have been characterized in the contexts of advertisement, courtship, and aggression, yet quantitative descriptions of calls elicited in the context of parental care are lacking. The biparental poison frog, Ranitomeya imitator , exhibits a remarkable parenting behavior in which females, cued by the calls of their male partners, feed tadpoles unfertilized eggs. Here, we characterized and compared calls across three social contexts, for the first time including a parental care context. We found that egg-feeding calls share some properties with both advertisement and courtship calls but also had unique properties. Multivariate analysis revealed high classification success for advertisement and courtship calls but misclassified nearly half of egg feeding calls as either advertisement or courtship calls. Egg feeding and courtship calls both contained less identity information than advertisement calls, as expected for signals used in close-range communication where uncertainty about identity is low and additional signal modalities may be used. Taken together, egg-feeding calls likely borrowed and recombined elements of both ancestral call types to solicit a novel, context-dependent parenting response.

The emergence of complex social interactions is predicted to be an important selective force in the diversification of communication systems. Parental care presents a key social context in which to study the evolution of novel signals, as care often requires communication and behavioral coordination between parents and is an evolutionary stepping-stone towards increasingly complex social systems. Anuran amphibians (frogs and toads) are a classic model of acoustic communication and the vocal repertoires of many species have been characterized in the contexts of advertisement, courtship, and aggression; yet quantitative descriptions of calls elicited in the context of parental care are lacking. The biparental poison frog,Ranitomeya imitator, exhibits a remarkable parenting behavior in which females, cued by the calls of their male partners, feed tadpoles unfertilized eggs. Here, we characterized and compared calls across three social contexts, for the first time including a parental care context. We found that egg feeding calls share some properties with both advertisement and courtship calls but also had unique properties. Multivariate analysis revealed high classification success for advertisement and courtship calls but misclassified nearly half of egg feeding calls as either advertisement or courtship calls, suggesting additional signal modalities play a role in parental communication. Egg feeding and courtship calls both contained less identity information than advertisement calls, as expected for signals used in close-range communication where uncertainty about identity is low. Taken together, egg feeding calls likely borrowed and recombined elements of both ancestral call types to solicit a novel, context-dependent parenting response.Significance StatementParental care has evolved independently in every major animal lineage and represents a major step in the evolution of complex sociality. Communication systems may need to increase in complexity. To explore these ideas, we characterized calls associated with trophic egg feeding, a unique cooperative parental behavior in the biparental mimic poison frog and compared them to calls associated with mate attraction (advertisement and courtship calls). Our analysis revealed some distinct, but many shared properties of signals elicited during egg feeding, suggesting that signals deployed in a novel social context evolve via modification and recombination of existing signals. These findings deepen our understanding of the relationship between complexity of social and communication systems.

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.

The Puerto Rican coquí frog

Much of the world’s biodiversity is held within tropical rainforests, which are increasingly fragmented by agricultural practices. In these threatened landscapes, there are many organisms that acquire chemical defenses from their diet and are therefore intimately connected with their local food webs. Poison frogs (Family Dendrobatidae) are one such example, as they acquire alkaloid-based chemical defenses from their diet of leaf litter ants and mites. It is currently unknown how habitat fragmentation impacts chemical defense across trophic levels, from arthropods to frogs. We examined the chemical defenses and diets of the Diablito poison frog (Oophaga sylvatica), and the diversity of their leaf litter ant communities in secondary forest and reclaimed cattle pasture. Notably, this research was performed in collaboration with two high school science classrooms. We found that the leaf litter of forest and pasture frog habitats differed significantly in ant community structure. We also found that forest and pasture frogs differed significantly in diet and alkaloid profiles, where forest frogs contained more of specific alkaloids and ate more ants in both number and volume. Finally, ant species composition of frog diets resembled the surrounding leaf litter, but diets were less variable. This suggests that frogs tend to consume particular ant species within each habitat. To better understand how ants contribute to the alkaloid chemical profiles of frogs, we chemically profiled several ant species and found some alkaloids to be common across many ant species while others are restricted to a few species. At least one alkaloid (223H) found in ants from disturbed sites was also found in skins from pasture. Our experiments are the first to link anthropogenic land use changes to dendrobatid poison frog chemical defenses through variation in leaf litter communities, which has implications for conservation management of these threatened amphibians.

Parental care is critical for offspring survival in many species. However, parental behaviors have been lost in roughly 1% of avian species known as the obligate brood parasites. To shed light on molecular and neurobiological mechanisms mediating brood parasitic behavior, we compared brain gene expression patterns between two brood parasitic species and one closely related non-parasitic Icterid (blackbird) species. Our analyses focused on gene expression changes specifically in the preoptic area (POA), a brain region known to play a critical role in parental behavior across vertebrates. Using comparative transcriptomic approaches, we identified gene expression patterns associated with brood parasitism. We evaluated three non-mutually exclusive alternatives for the evolution of brood parasitism: (1) retention of juvenile-like (neotenic) gene expression, (2) reduced expression of maternal care-related genes in the POA, and/or (3) increased expression of genes inhibiting maternal care. We find evidence for neotenic expression patterns in both species of parasitic cowbirds as compared to maternal, non-parasites. In addition, we observed differential expression in a number of genes with previously established roles in mediating maternal care. Together, these results provide the first insight into transcriptomic and genetic mechanisms underlying the loss of maternal behavior in avian brood parasites.

How underlying mechanisms bias evolution toward predictable outcomes remains an area of active debate. In this study, we leveraged phenotypic plasticity and parallel adaptation across independent lineages of Trinidadian guppies (Poecilia reticulata) to assess the predictability of gene expression evolution during parallel adaptation. Trinidadian guppies have repeatedly and independently adapted to high- and low-predation environments in the wild. We combined this natural experiment with a laboratory breeding design to attribute transcriptional variation to the genetic influences of population of origin and developmental plasticity in response to rearing with or without predators. We observed substantial gene expression plasticity, as well as the evolution of expression plasticity itself, across populations. Genes exhibiting expression plasticity within populations were more likely to also differ in expression between populations, with the direction of population differences more likely to be opposite those of plasticity. While we found more overlap than expected by chance in genes differentially expressed between high- and low-predation populations from distinct evolutionary lineages, the majority of differentially expressed genes were not shared between lineages. Our data suggest alternative transcriptional configurations associated with shared phenotypes, highlighting a role for transcriptional flexibility in the parallel phenotypic evolution of a species known for rapid adaptation.

Aggressive competition for resources among juveniles is documented in many species, but the neural mechanisms regulating this behavior in young animals are poorly understood. In poison frogs, increased parental care is associated with decreased water volume of tadpole pools, resource limitation, and aggression. Indeed, the tadpoles of many poison frog species will attack, kill, and cannibalize other tadpoles. We examined the neural basis of conspecific aggression in Dyeing poison frog (Dendrobates tinctorius) tadpoles by comparing individuals that won aggressive encounters, lost aggressive encounters, or did not engage in a fight. We first compared patterns of generalized neural activity using immunohistochemical detection of phosphorylated ribosomes (pS6) as a proxy for neural activation associated with behavior. We found increased neural activity in the medial pallium and preoptic area of loser tadpoles, suggesting the amphibian homologs of the mammalian hippocampus and preoptic area may facilitate loser-associated behaviors. Nonapeptides (arginine vasotocin and mesotocin) and dopamine have been linked to aggression in other vertebrates and are located in the preoptic area. We next examined neural activity specifically in nonapeptide- and tyrosine-hydroxylase-positive cells using double-label immunohistochemistry. We found increased neural activity specifically in the preoptic area nonapeptide neurons of winners, whereas we found no differences in activity of dopaminergic cells among behavioral groups. Our findings suggest the neural correlates of aggression in poison frog tadpoles are similar to neural mechanisms mediating aggression in adults and juveniles of other vertebrate taxa.

Parental care is a key evolutionary innovation that influences the fitness of parents and offspring. How the brain coordinates such a complex behavior remains poorly understood. Kohl and colleagues recently uncovered the organizational principles of hypothalamic galanin neurons and their connections in mice. Their findings revealed a striking picture in which discrete neuronal pools control distinct aspects of parental behavior.

Prolactin is often referred to as the "parental hormone" but there are examples in which prolactin and parental behavior are disconnected. One intriguing example is in avian obligate brood parasites; species exhibiting high circulating prolactin but no parental care. To understand this disconnect, we examined transcriptional and behavioral responses to prolactin in brown-headed (Molothrus ater) and bronzed (M aeneus) brood parasitic cowbirds. We first examine prolactin-dependent regulation of transcriptome wide gene expression in the preoptic area (POA), a brain region associated with parental care across vertebrates. We next examined prolactin-dependent abundance of seven parental care-related candidate genes in hypothalamic regions that are prolactin-responsive in other avian species. We found no evidence of prolactin sensitivity in cowbirds in either case. To understand this prolactin insensitivity, we compared prolactin receptor transcript abundance between parasitic and nonparasitic species and between prolactin treated and untreated cowbirds. We observed significantly lower prolactin receptor transcript abundance in brown-headed but not bronzed cowbird POA compared with a nonparasite and no prolactin-dependent changes in either parasitic species. Finally, estrogen-primed female brown-headed cowbirds with or without prolactin treatment exhibited significantly greater avoidance of nestling begging stimuli compared with untreated birds. Taken together, our results suggest that modified prolactin receptor distributions in the POA and surrounding hypothalamic regions disconnect prolactin from parental care in brood parasitic cowbirds.

How underlying mechanisms bias evolution toward predictable outcomes remains an area of active debate. In this study, we leveraged phenotypic plasticity and parallel adaptation across independent lineages of Trinidadian guppies (Poecilia reticulata) to assess the predictability of gene expression evolution during parallel adaptation. Trinidadian guppies have repeatedly and independently adapted to high- and low-predation environments in the wild. We combined this natural experiment with a laboratory breeding design to attribute transcriptional variation to the genetic influences of population of origin and developmental plasticity in response to rearing with or without predators. We observed substantial gene expression plasticity as well as the evolution of expression plasticity itself across populations. Genes exhibiting expression plasticity within populations were more likely to also differ in expression between populations, with the direction of population differences more likely to be opposite those of plasticity. While we found more overlap than expected by chance in genes differentially expressed between high- and low-predation populations from distinct evolutionary lineages, the majority of differentially expressed genes were not shared between lineages. Our data suggest alternative transcriptional configurations associated with shared phenotypes, highlighting a role for transcriptional flexibility in the parallel phenotypic evolution of a species known for rapid adaptation.

Parental provisioning of offspring with physiological products occurs in many animals. Within amphibians, maternal provisioning has evolved multiple times, including in South American dendrobatid and Malagasy mantellid poison frogs. In some of these species, mothers feed unfertilized eggs to their developing tadpoles for several months until tadpoles complete metamorphosis. We conducted field studies in Ecuador and Madagascar to ask whether convergence at the behavioral level provides similar benefits to offspring and whether nursing behavior relies on shared neural mechanisms across frogs and vertebrates more broadly. At an ecological level, we found that nursing allows poison frog mothers to provide chemical defenses to their tadpoles in both species. At the level of brain regions, nursing behavior was associated with increased neural activity in the lateral septum and preoptic area in both species, demonstrating recruitment of shared brain regions in the convergent evolution of maternal care within frogs and across vertebrates. In contrast at a molecular level, only mantellids showed increased oxytocin neuron activity akin to that in nursing mammals. Taken together, our findings demonstrate that convergently evolved maternal provisioning behavior provides similar benefits to offspring and relies on similar brain regions. However, the molecular mechanisms underlying the convergence in nursing behavior may be different, suggesting evolutionary versatility in the mechanisms promoting maternal behavior.

Parental care has evolved repeatedly and independently across animals. While the ecological and evolutionary significance of parental behaviour is well recognized, underlying mechanisms remain poorly understood. We took advantage of behavioural diversity across closely related species of South American poison frogs (Family Dendrobatidae) to identify neural correlates of parental behaviour shared across sexes and species. We characterized differences in neural induction, gene expression in active neurons, and activity of specific neuronal types in three species with distinct parental care patterns: male uniparental, female uniparental, and biparental. We identified the medial pallium and preoptic area as core brain regions associated with parental care, independent of sex and species. Identification of neurons active during parental care confirms a role for neuropeptides associated with care in other vertebrates as well as identifying novel candidates. Our work is the first to explore neural and molecular mechanisms of parental care in amphibians and highlights the potential for mechanistic studies in closely related but behaviourally variable species to build a more complete understanding of how shared principles and species-specific diversity govern parental care and other social behaviour.

Adaptive trade-offs between foraging and social behavior intuitively explain many aspects of individual decision-making. Given the intimate connection between social behavior and feeding/foraging at the behavioral level, we propose that social behaviors are linked to foraging on a mechanistic level, and that modifications of feeding circuits are crucial in the evolution of complex social behaviors. In this Review, we first highlight the overlap between mechanisms underlying foraging and parental care and then expand this argument to consider the manipulation of feeding-related pathways in the evolution of other complex social behaviors. We include examples from diverse taxa to highlight that the independent evolution of complex social behaviors is a variation on the theme of feeding circuit modification.

When organisms are faced with new or changing environments, a central challenge is the coordination of adaptive shifts in many different phenotypic traits. Relationships among traits may facilitate or constrain evolutionary responses to selection, depending on whether the direction of selection is aligned or opposed to the pattern of trait correlations. Attempts to predict evolutionary potential in correlated traits generally assume that correlations are stable across time and space; however, increasing evidence suggests that this may not be the case, and flexibility in trait correlations could bias evolutionary trajectories. We examined genetic and environmental influences on variation and covariation in a suite of behavioural traits to understand if and how flexibility in trait correlations influences adaptation to novel environments. We tested the role of genetic and environmental influences on behavioural trait correlations by comparing Trinidadian guppies (Poecilia reticulata) historically adapted to high- and low-predation environments that were reared under native and non-native environmental conditions. Both high- and low-predation fish exhibited increased behavioural variance when reared under non-native vs. native environmental conditions, and rearing in the non-native environment shifted the major axis of variation among behaviours. Our findings emphasize that trait correlations observed in one population or environment may not predict correlations in another and that environmentally induced plasticity in correlations may bias evolutionary divergence in novel environments.

Aggressive competition for resources among juveniles is documented in many species, but the neural mechanisms regulating this behavior in young animals are poorly understood. In poison frogs, increased parental care is associated with decreased water volume of tadpole pools, resource limitation, and aggression. Indeed, the tadpoles of many poison frog species will attack, kill, and cannibalize other tadpoles. We examined the neural basis of conspecific aggression in Dyeing poison frog (Dendrobates tinctorius) tadpoles by comparing individuals that won aggressive encounters, lost aggressive encounters, or did not engage in a fight. We first compared patterns of generalized neural activity using immunohistochemical detection of phosphorylated ribosomes (pS6) as a proxy for neural activation associated with behavior. We found increased neural activity in the medial pallium and preoptic area of loser tadpoles, suggesting the amphibian homologs of the mammalian hippocampus and preoptic area may facilitate loser-associated behaviors. Nonapeptides (arginine vasotocin and mesotocin) and dopamine have been linked to aggression in other vertebrates and are located in the preoptic area. We next examined neural activity specifically in nonapeptide- and tyrosine-hydroxylase-positive cells using double-label immunohistochemistry. We found increased neural activity specifically in the preoptic area nonapeptide neurons of winners, whereas we found no differences in activity of dopaminergic cells among behavioral groups. Our findings suggest the neural correlates of aggression in poison frog tadpoles are similar to neural mechanisms mediating aggression in adults and juveniles of other vertebrate taxa.

The occasional reversal of sex-typical behavior across species suggests that many of the neural circuits underlying behavior are conserved between males and females and can be activated in response to the appropriate social condition or stimulus. Most poison frog species (Family Dendrobatidae) exhibit male uniparental care, but flexible compensation has been observed in some species, where females can perform parental care duties when males disappear. Here, we investigated hormonal and neural mechanisms of sex-typical and sex-reversed parental care in a typically male uniparental species, the Dyeing Poison Frog (Dendrobates tinctorius). We first characterized hormone levels and whole brain gene expression across parental care stages during sex-typical behavior. Surprisingly, hormonal changes and brain gene expression differences associated with parental care in males were mirrored in their non-caregiving female partners. To further explore the disconnect between underlying neuroendocrine mechanisms and behavior, we characterized hormone levels and neural activity patterns in females performing sex-reversed parental care. In contrast to hormone and gene expression patterns, we found that patterns of neural activity were linked to the active performance of parental behavior, with sex-reversed tadpole transporting females exhibiting neural activity patterns more similar to those of transporting males than non-caregiving females. We suggest that parallels in hormones and brain gene expression in parental males and non-caregiving females are related to females’ ability to flexibly take over parental care in the absence of their male partners. Highlights Dendrobates tinctorius is a typically male uniparental species, but females will sometimes show parental care in the absence of their male mates. Testosterone decreases while cortisol increases in tadpole transporting males and their non-transporting female partners. Parental males and their non-caregiving female partners exhibit parallel patterns in brain gene expression across parental care stages. Neural activity in tadpole transporting females reflects transporting males more than non-transporting females. Patterns in active versus observing parents may relate to flexible compensation in parental behavior in D. tinctorius.

Poison frogs acquire chemical defenses from the environment for protection against potential predators. These defensive chemicals are lipophilic alkaloid toxins that are sequestered by poison frogs from dietary arthropods and stored in skin glands. Despite decades of research focusing on identifying poison frog toxins, we know relatively little about how environmental variation and subsequent arthropod availability impacts toxicity in poison frogs. We investigated how seasonal environmental variation influences poison frog toxin profiles through changes in the diet of the Climbing Mantella (Mantella laevigata). We collected M. laevigata females on the Nosy Mangabe island reserve in Madagascar during the wet and dry seasons and tested the hypothesis that seasonal differences in rainfall is associated with changes in the diet and skin toxin profiles of M. laevigata. The arthropod diet of each frog was characterized into five groups (i.e. ants, termites, mites, insect larvae, or ‘other’) using visual identification and cytochrome oxidase 1 DNA barcoding. We found that frog diet differed between the wet and dry seasons, where frogs had a more diverse diet in the wet season and consumed a higher percentage of ants in the dry season. To determine if seasonality was associated with variation in frog defensive chemical composition, we used gas chromatography / mass spectrometry to quantify toxins from individual skin samples. Although the assortment of identified toxins was similar across seasons, we detected significant differences in the abundance of certain alkaloids, which we hypothesize reflects seasonal variation in the diet of M. laevigata. We suggest that these variations could originate from seasonal changes in either arthropod leaf litter composition or changes in frog behavioral patterns. Although additional studies are needed to understand the consequences of long-term environmental shifts, this work suggests that toxin profiles are relatively robust against short-term environmental perturbations.

The medicinal leech is one of the most venerated model systems for the study of fundamental nervous system principles, ranging from single-cell excitability to complex sensorimotor integration. Yet, molecular analyses have yet to be extensively applied to complement the rich history of electrophysiological study that this animal has received. Here, we generated the first de novo transcriptome assembly from the entire central nervous system of Hirudo verbana, with the goal of providing a molecular resource, as well as to lay the foundation for a comprehensive discovery of genes fundamentally important for neural function. Our assembly generated 107,704 contigs from over 900 million raw reads. Of these 107,704 contigs, 39,047 (36%) were annotated using NCBI’s validated RefSeq sequence database. From this annotated central nervous system transcriptome, we began the process of curating genes related to nervous system function by identifying and characterizing 126 unique ion channel, receptor, transporter, and enzyme contigs. Additionally, we generated sequence counts to estimate the relative abundance of each identified ion channel and receptor contig in the transcriptome through Kallisto mapping. This transcriptome will serve as a valuable community resource for studies investigating the molecular underpinnings of neural function in leech and provide a reference for comparative analyses.

Parental care for is critical for offspring survival in many species. However, parental behaviors have been lost in roughly 1% of avian species known as the obligate brood parasites. To shed light on molecular and neurobiological mechanisms mediating brood parasitic behavior, brain gene expression patterns between two brood parasitic species and one closely related non-parasitic Icterid (blackbird) species were compared. Our analyses focused on gene expression changes specifically in the preoptic area (POA), a brain region known to play a critical role in maternal behavior across vertebrates. Using comparative transcriptomic approaches, we identified gene expression patterns associated with brood parasitism and evaluated two alternative explanations for the evolution of brood parasitism: reduced expression of parental-related genes in the POA versus retention of juvenile (neotenic) gene expression. While we did not find evidence for large scale gene downregulation, expression patterns did reflect substantial evidence for neotenic POA gene expression in parasitic birds. Differentially expressed genes with previously established roles in parental care were identified. Targeted examination of these selected candidate genes in additional hypothalamic regions revealed species differences in gene expression patterns is not POA-specific. Together, these results provide new insights into neurogenomics underlying maternal behavior loss in avian brood parasites.

Animals are continually faced with the challenge of producing context-appropriate social behaviors. In many instances, appropriate behaviors differ by social situation. However, in some instances, the same behaviors are employed across different social contexts, albeit in response to distinct stimuli and with distinct purposes. We took advantage of behavioral similarities across mating and aggression contexts in guppies, Poecilia reticulata, to understand how patterns of neural activity differ across social contexts when behaviors are nonetheless shared. While there is growing interest in understanding behavioral mechanisms in guppies, resources are sparse. As part of this study, we developed a neuroanatomical atlas of the guppy brain as a research community resource. Using this atlas, we found that neural activity in the preoptic area reflected social context, whereas individual differences in behavioral motivation paralleled activity in the posterior tuberculum and ventral telencephalon (teleost homologs of the mammalian ventral tegmental area and lateral septum, respectively). Our findings suggest independent coding of social salience versus behavioral motivation when behavioral repertoires are shared across social contexts. Choosing behaviors appropriate to the current social situation is of central importance to animals. Interactions with different social partners (e.g., mates, competitors, or offspring) generally require distinct behavioral repertories. However, in some cases, similar behaviors are used across social contexts. The neural mechanisms underlying social behavior are particularly intriguing in these situations, where the same behaviors are produced in response to distinct social stimuli and for distinct purposes. We took advantage of behavioral similarities across mating and aggression interactions in Trinidadian guppies to explore how social information is reflected in the brain when fish perform a common set of behaviors across contexts. We found that activity in distinct brain regions reflects social context versus behavioral motivation, suggesting a means by which social inputs and behavioral outputs can be coded independently of one another.

Phenotypic plasticity is the capacity for an individual genotype to produce different phenotypes in response to environmental variation. Most traits are plastic, but the degree to which plasticity is adaptive or non-adaptive depends on whether environmentally induced phenotypes are closer or further away from the local optimum. Existing theories make conflicting predictions about whether plasticity constrains or facilitates adaptive evolution. Debate persists because few empirical studies have tested the relationship between initial plasticity and subsequent adaptive evolution in natural populations. Here we show that the direction of plasticity in gene expression is generally opposite to the direction of adaptive evolution. We experimentally transplanted Trinidadian guppies (Poecilia reticulata) adapted to living with cichlid predators to cichlid-free streams, and tested for evolutionary divergence in brain gene expression patterns after three to four generations. We find 135 transcripts that evolved parallel changes in expression within the replicated introduction populations. These changes are in the same direction exhibited in a native cichlid-free population, suggesting rapid adaptive evolution. We find 89% of these transcripts exhibited non-adaptive plastic changes in expression when the source population was reared in the absence of predators, as they are in the opposite direction to the evolved changes. By contrast, the remaining transcripts exhibiting adaptive plasticity show reduced population divergence. Furthermore, the most plastic transcripts in the source population evolved reduced plasticity in the introduction populations, suggesting strong selection against non-adaptive plasticity. These results support models predicting that adaptive plasticity constrains evolution, whereas non-adaptive plasticity potentiates evolution by increasing the strength of directional selection. The role of non-adaptive plasticity in evolution has received relatively little attention; however, our results suggest that it may be an important mechanism that predicts evolutionary responses to new environments.

Social context is a powerful mediator of behavioral decisions across animal taxa, as the presence of conspecifics comes with both costs and benefits. In risky situations, the safety conferred by the presence of conspecifics can outweigh the costs of competition for resources. How the costs and benefits of grouping influence decisions among alternative antipredator behaviors remains largely unexplored. We took advantage of the Trinidadian guppy (Poecilia reticulata) to examine the influence of social context on alternative behavioral responses to threats. We compared the frequency of active (startle) versus passive (freeze) responses to sudden acoustic stimuli in the presence and absence of conspecifics. We found that fish were relatively less likely to startle and more likely to freeze when in a group than when alone, indicating that immediate social context modulates predator evasion strategy in guppies. We suggest that these social context-dependent changes reflect trade-offs between survival and energy expenditure. To our knowledge, an effect of immediate social environment on startle probability has not been previously demonstrated in a teleost.

In vertebrates, glucocorticoids mediate a wide-range of responses to stressors. For this reason, they are implicated in adaptation to changes in predation pressure. Trinidadian guppies (Poecilia reticulata) from high-predation environments have repeatedly and independently colonized and adapted to low-predation environments, resulting in parallel changes in life history, morphology, and behavior. We validated methods for non-invasive waterborne hormone sample collection in this species, and used this technique to examine genetic and environmental effects of predation on basal glucocorticoid (cortisol) levels. To examine genetic differences, we compared waterborne cortisol levels in high- and low-predation fish from two distinct population pairs. We found that fish from high-predation localities had lower cortisol levels than their low-predation counterparts. To isolate environmental influences, we compared waterborne cortisol levels in genetically similar fish reared with and without exposure to predator chemical cues. We found that fish reared with predator chemical cues had lower waterborne cortisol levels than those reared without. Comparisons of waterborne and whole-body cortisol levels demonstrated that populations differed in overall cortisol levels in the body, whereas rearing conditions altered the release of cortisol from the body into the water. Thus, evolutionary history with predators and lifetime exposure to predator cues were both associated with lower cortisol release, but depended on distinct physiological mechanisms.

Affiliative behaviours have evolved many times across animals. Research on the mechanisms underlying affiliative behaviour demonstrates remarkable convergence across species spanning wide evolutionary distances. Shared mechanisms have been identified with genomic approaches analysing genetic variants and gene expression differences as well as neuroendocrine and molecular approaches exploring the role of hormones and signalling molecules. We review the genomic and neural basis of pair bonding and parental care across diverse taxa to shed light on mechanistic patterns that underpin the convergent evolution of affiliative behaviour. We emphasize that mechanisms underlying convergence in complex phenotypes like affiliation should be evaluated on a continuum, where signatures of convergence may vary across levels of biological organization. In particular, additional comparative studies within and across major vertebrate lineages will be essential in resolving when and why shared neural substrates are repeatedly targeted in the independent evolution of affiliation, and how similar mechanisms are evolutionarily tuned to give rise to species-specific variations in behaviour. This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions'.

Early life adversity and stress in humans have been related to a number of psychological disorders including anxiety, depression, and addiction. The present study used isolation rearing, a well-characterized animal model of early life adversity, to examine its effects on social behavior and immediate early gene (IEG) expression produced by exposure to a novel social experience. Male and female rats were housed in same-sex groups or in isolation for 4 weeks beginning at weaning and were tested during late adolescence. The protein products of the IEGs c-fos and Arc, as well as the neurotrophic factor BDNF were assessed in medial prefrontal cortex (mPFC) subregions (anterior cingulate, prelimbic and infralimbic) using immunohistochemistry. Aggressive and non-aggressive behaviors during novel social exposure were also assessed. Exposure to a novel conspecific produced increases in Arc and c-fos activation in the mPFC of group reared animals in a sex- and subregion-dependent fashion compared to no social exposure controls, but this increase was blunted or absent in isolated animals. Isolates engaged in more social interactions and more aggressive behavior than group reared rats. Sex differences in some behaviors as well as in Arc and BDNF expression were observed. These results indicate that isolation rearing alters IEG activation in the mPFC produced by exposure to a novel conspecific, in addition to changing social behavior, and that these effects depend in part on sex.

Poison frogs acquire chemical defenses from the environment for protection against potential predators. These defensive chemicals are lipophilic alkaloids that are sequestered by poison frogs from dietary arthropods and stored in skin glands. Despite decades of research focusing on identifying poison frog alkaloids, we know relatively little about how environmental variation and subsequent arthropod availability impacts alkaloid loads in poison frogs. We investigated how seasonal environmental variation influences poison frog chemical profiles through changes in the diet of the Climbing Mantella (Mantella laevigata). We collected M. laevigata females on the Nosy Mangabe island reserve in Madagascar during the wet and dry seasons and tested the hypothesis that seasonal differences in rainfall is associated with changes in diet composition and skin alkaloid profiles of M. laevigata. The arthropod diet of each frog was characterized into five groups (i.e. ants, termites, mites, insect larvae, or 'other') using visual identification and cytochrome oxidase 1 DNA barcoding. We found that frog diet differed between the wet and dry seasons, where frogs had a more diverse diet in the wet season and consumed a higher percentage of ants in the dry season. To determine if seasonality was associated with variation in frog defensive chemical composition, we used gas chromatography / mass spectrometry to quantify alkaloids from individual skin samples. Although the assortment of identified alkaloids was similar across seasons, we detected significant differences in the abundance of certain alkaloids, which we hypothesize reflects seasonal variation in the diet of M. laevigata. We suggest that these variations could originate from seasonal changes in either arthropod leaf litter composition or changes in frog behavioral patterns. Although additional studies are needed to understand the consequences of long-term environmental shifts, this work suggests that alkaloid profiles are relatively robust against short-term environmental perturbations.

Summary Fish and other aquatic vertebrates use their mechanosensory lateral line to detect objects and motion in their immediate environment. Differences in lateral line morphology have been extensively characterized among species, however intraspecific variation remains largely unexplored. In addition, little is known about how environmental factors modify development of lateral line morphology. Predation is one environmental factor that can act both as a selective pressure causing genetic differences between populations, and as a cue during development to induce plastic changes. Here, we test if variation in the risk of predation within and among populations of Trinidadian guppies (Poecilia reticulata) influences lateral line morphology. We compared neuromast arrangement in wild-caught guppies from distinct high- and low-predation population pairs to examine patterns associated with differences in predation pressure. To distinguish genetic and environmental influences, we compared neuromast arrangement in guppies from different source populations reared with and without exposure to predator chemical cues. We found that the distribution of neuromasts across the body varies between populations based on both genetic and environmental factors. To the best of our knowledge, this study is the first to demonstrate variation in lateral line morphology based on environmental exposure to an ecologically relevant stimulus.