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Fischer, E. K.

Publications and source records attributed to Fischer, E. K..

At least 19 recordsLinked to original sources

Partner cues and individual variation underlie sex-reversed parental care in poison frogs

Flexible parental care strategies are widespread in nature and factor into conflict between the sexes and the realization of sex roles. While adaptive explanations abound, the mechanisms underlying flexible sex-reversal of care are less clear. We enlist a biparental frog (Ranitomeya imitator) with flexible parental care to investigate the extrinsic and intrinsic mechanisms underpinning parental decisions. Using mate removal experiments in the laboratory, we show that members of the primary caregiving sex (males) show less variation than the flexible sex (females) in their propensity to provide care, and that care propensity in females is affected by extrinsic partner cues as well as individual variability. Indeed, individual repeatability in parental effort is high in both typically caregiving and flexible parents. To investigate the underpinnings of differences in care propensity, we sequenced RNA from whole brains of caregiving and non-caregiving frogs of both sexes. While actively caregiving females showed minimal differential gene expression compared to actively caregiving males, females that failed to provide care showed distinct patterns of gene expression. Our findings offer an initial glimpse into the environmental and genetic regulation of individual variation in sex-reversed parental care.

animal behavior and cognition↗

Flexibility in Gene Coexpression at Developmental and Evolutionary Timescales

The explosion of next-generation sequencing technologies has allowed researchers to move from studying single genes to thousands of genes, and thereby to also consider the relationships within gene networks. Like others, we are interested in understanding how developmental and evolutionary forces shape the expression of individual genes, as well as the interactions among genes. In pursuing these questions, we confronted the central challenge that standard approaches fail to control the Type I error and/or have low power in the presence of high dimensionality (i.e., large number of genes) and small sample size, as in many gene expression studies. To overcome these challenges, we used random projection tests and correlation network comparisons to characterize differences in network connectivity and density. We detail central challenges, discuss sample size guidelines, and provide rigorous statistical approaches for exploring coexpression differences with small sample sizes. We apply these approaches in a species known for rapid adaptation - the Trinidadian guppy (Poecilia reticulata). Our findings provide evidence for coexpression network differences at developmental and evolutionary timescales and suggest that flexibility in gene coexpression relationships could promote evolvability.

evolutionary biology↗

Early development of the glucocorticoid stress response in poison frog tadpoles

In vertebrates, the glucocorticoid "stress" response (corticosterone or cortisol) through the hypothalamic-pituitary-adrenal (HPA) axis influences many essential functions, including behavior, metabolism, immunity, and ontogenetic transitions. During development, stress responses can be adaptive if they facilitate antipredator behavior and modulate developmental speed to adjust to environmental conditions; however, these same responses can be maladaptive when energetic costs become too high and developmental speed trades-off with size and health at maturity. Thus, the timing of HPA-axis development may be aligned with specific developmental challenges and opportunities presented by a species life history strategy. In anurans (frogs and toads), corticosterone plays critical roles in development and behavior, and concentrations can fluctuate in response to environmental stressors. Given the role of corticosterone in ontogenetic changes and behaviors, we studied the development of the glucocorticoid stress response in tadpoles of the dyeing poison frog (Dendrobates tinctorius), a species with a unique life history that includes transport to water after hatching on land and aggressive and cannibalistic behavior. We measured the excretion rate and whole-body concentration of corticosterone and the corticosterone response to adrenocorticotropic hormone (ACTH) in free-swimming tadpoles after transport and throughout metamorphosis. We found no significant differences across development in excretion rates or whole-body concentration of corticosterone, nor corticosterone response to ACTH, indicating that that the glucocorticoid response develops early in ontogeny. This pattern differs from those in other species, suggesting the unique ecological pressures faced by D. tinctorius have shaped the development of the glucocorticoid stress response in this species. More broadly, this study illustrates how life history strategies and tradeoffs impact the timing of the development of stress responsivity.

physiology↗

Timing-dependent effects of elevated maternal glucocorticoids on offspring brain gene expression in a wild small mammal

An increase in maternal stress during offspring development can have cascading, life-long impacts on offspring behavior and physiology, which can vary depending on the timing of exposure to the stressor. By responding to stressors through increasing production of glucocorticoids (GCs), the hypothalamic-pituitary-adrenal (HPA) axis is a key mediator of maternal effects - both on the side of the mother and the offspring. At a molecular level, maternal effects are thought to be mediated through modifying transcription of genes, particularly in the brain. To better understand the evolutionary implications of maternal effects, more studies are needed on mechanisms of maternal effects in wild populations. To test how the timing of maternal stress impacts gene expression in the brains of offspring, we treated free-ranging North American red squirrels (Tamiasciurus hudsonicus) with GCs during late pregnancy or early lactation and collected brains from offspring around weaning. We used RNA-sequencing to measure gene expression in the hypothalamus and hippocampus. We found small differences in gene expression between GC-treated and control individuals suggesting long-term effects of the GC treatment on neural gene transcription. The general patterns of gene regulation across the transcriptome were consistent between the pregnancy and lactation-treated individuals. However, the number of significantly differentially expressed genes was higher in the lactation treatment group. These results support the idea that maternal stress affects neural gene expression in offspring, and these effects are dependent on timing. Our findings add valuable insight into the impact of maternal hormones on neural transcriptomics in a wild population.

ecology↗

Fortune may favor the flexible: Environment-dependent behavioral shifts in invasive coqui frogs

Biological invasions are a major driver of global biodiversity loss, impacting endemic species, ecosystems, and economies. While the influence of life history traits on invasive success is well-established, the role of behavior in the invasive potential of animals is less studied. The common coqui frog, Eleutherodactylus coqui, is a highly successful invader in Hawaii. We build on previous research characterizing changes in physiology and morphology to explore behavioral variation across the invasive range of coqui in Hawaii. We hypothesized that behavioral traits contributing to invasion expansion would be reflected in behavioral differences at the invasive center versus invasive edge. To investigate whether differences in the field represent local adaptation or behavioral plasticity, we additionally evaluated behavior following acclimation to a shared laboratory environment. While we identified only subtle behavioral variation among populations in the field, we found that individuals from all populations became less bold, active, and exploratory in the laboratory, converging on a similar behavioral phenotype. Alongside previous work, our results suggest that coqui adjust their behavior to local environmental conditions across their invasive range, and that behavioral flexibility may contribute to invasive success.

animal behavior and cognition↗

Individual Behavioral Variability Across Time and Contexts in Dendrobates tinctorius Poison Frogs

Consistent individual differences in behavior ("animal personality") have consequences for individual fitness, evolutionary trajectories, and species persistence. Such differences have been documented across a wide range of animals, though amphibians are generally underrepresented in this research area. The aim of our study was to examine consistent individual differences in Dyeing poison frogs, Dendrobates tinctorius. We evaluated repeatability in behaviors including activity, exploration, and boldness to assess consistency of behaviors across different temporal, experimental, and environmental contexts. We found repeatability in activity and exploration across time and contexts. In contrast, we observed context-specific behavior for our metrics of boldness, with consistent individual differences only for some measures. Further, while activity and exploration displayed consistent correlations across contexts, relationships between activity and boldness were context dependent. Our findings document the presence of consistent individual differences in behavior in D. tinctorius poison frogs, and also reveal context-dependent behavioral differences, highlighting the complex relationship between consistent individual differences and context-specific responses in animal behavior. Statement of SignificanceThe concept of animal personality centers on the existence of consistent individual differences in behavior. However, behavioral responses can depend on context, and consistent individual differences in one context do not guarantee consistent differences in another. To address this question, we assessed activity, exploration, and boldness in captive-bred poison frogs (Dendrobates tinctorius) across time and environmental contexts. Our comprehensive approach revealed consistent individual differences in some behaviors and context-specificity in others. While activity and exploration were generally repeatable and correlated with one another, boldness was not. Especially in view of the emphasis on measures of boldness in the animal personality literature, our findings emphasize the importance of reiterative and holistic approaches in the study of animal behavior.

animal behavior and cognition↗

Evidence for individual vocal recognition in a pair bonding poison frog? Insights from no-choice and two-choice paradigms

Individually distinctive vocalizations are widespread in nature, although the ability of receivers to discriminate these signals has only been studied through limited taxonomic and social lenses. Here we ask whether anuran advertisement calls, typically studied for their role in territory defense and mate attraction, facilitate recognition and preferential association with partners in a pair bonding poison frog. Combining no- and two-stimulus choice playback experiments, we evaluated behavioral and physiological responses of females to male acoustic stimuli. Virgin females oriented to and approached speakers broadcasting male calls independent of caller identity, implying that females are generally attracted to male acoustic stimuli outside the context of a pair bond. When pair bonded females were presented with calls of a mate and a stranger, they showed a slight preference for calls of their mate. Moreover, behavioral responses varied with breeding status: females with eggs were faster to approach stimuli and spent more time in the mate arm than females that were pair bonded but did not currently have eggs. Our study suggests a potential role for individual vocal recognition in the formation and maintenance of pair bonds in a poison frog and raises new questions about how acoustic signals are perceived in the context of monogamy and biparental care.

animal behavior and cognition↗

Tap Dancing Frogs: Posterior Toe Tapping and Feeding Behavior in Dendrobates tinctorius

Animals have myriad adaptations to help them hunt and feed in the most efficient and effective manner. One mysterious behavior related to hunting and feeding is the posterior toe tapping behavior of some frogs. Biologists and hobbyists alike have long noticed this behavior, but there is little empirical data to explain its causes and consequences. To test the hypothesis that tapping is related to feeding and modulated by environmental context, we conducted a series of related experiments in the Dyeing poison frog, Dendrobates tinctorius. We first confirmed that tap rate was higher during feeding as has been observed in other species. Interestingly, this effect was heightened in the presence of a conspecific. We next asked whether frogs tapped less under conditions when prey were visible, but inaccessible. Finally, we asked whether D. tinctorius adjusted tap rate based on substrate characteristics and whether prey capture success was higher when tapping. In addition to confirming an association between tapping and feeding, our work demonstrates modulation of toe tapping based on social context, prey accessibility, and substrate characteristics. Based on our findings, we suggest that tapping could act to induce prey movement and thereby facilitate prey detection and capture by frogs. Significance StatementThe toe tapping of some amphibians is an intriguing behavior that has attracted attention from researchers and hobbyists, yet the functional role of toe tapping remains poorly understood. Previous studies have noted an association between toe tapping and feeding in other species, and our work does so quantitatively and experimentally in Dyeing poison frogs, Dendrobates tinctorius. We demonstrate that frogs modulate tap rate based on the presence of conspecifics, prey accessibility, and substrate type. We speculate that - alongside other potential functions - toe tapping may act as a vibrational stimulus to facilitate prey detection and capture.

animal behavior and cognition↗

Why not both? A case study measuring cortisol and corticosterone in poison frogs

A general tenet in stress physiology is that the hypothalamic-pituitary-adrenal (HPA) axis predominantly produces one glucocorticoid (GC) in response to stressors. However, most vertebrates produce both cortisol and corticosterone, and these steroids show variation across species in absolute levels, relative proportions, and stress responsivity and regulate much more than just stress physiology. Therefore, focusing on a single GC within a species may not capture the whole story. In the present study, we set out to validate non-invasive waterborne hormone measurements in our focal species, the dyeing poison frog Dendrobates tinctorius. In pursuing this goal, we uncovered unexpected patterns of GC abundance within and across species of poison frogs. D. tinctorius had higher amounts of corticosterone than cortisol in both plasma and waterborne samples, and corticosterone was responsive to adrenocorticotropic hormone (ACTH) as canonically assumed. However, corticosterone and cortisol levels were surprisingly similar in D. tinctorius, and cortisol was more abundant than corticosterone in water samples from four additional poison frog species. These results challenge the broadly accepted assumption that corticosterone is always more abundant in amphibians and add to the growing literature highlighting the importance of measuring both GCs to understand (stress) physiology.

physiology↗

Co-option of ancestral signal elements in the evolution of a cooperative parental behavior

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.

animal behavior and cognition↗

Neural correlates of winning and losing fights in poison frog tadpoles

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.

neuroscience↗

Hormonal and neural correlates of care in active versus observing poison frog parents

The occasional reversal of sex-typical behavior 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 will take over parental care duties when males disappear. We investigated hormonal and neural correlates 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 care. Surprisingly, hormonal changes and brain gene expression differences associated with active parental behavior in males were mirrored in their non-caregiving female partners. To further explore the disconnect between neuroendocrine patterns 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 active and observing parents are related to females ability to flexibly take over parental care in the absence of their male partners. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=131 SRC="FIGDIR/small/765503v2_ufig1.gif" ALT="Figure 1"> View larger version (50K): org.highwire.dtl.DTLVardef@18f4b87org.highwire.dtl.DTLVardef@a7b6ecorg.highwire.dtl.DTLVardef@da7394org.highwire.dtl.DTLVardef@1da19c8_HPS_FORMAT_FIGEXP M_FIG Graphical abstract C_FIG

neuroscience↗

Non-parallel transcriptional divergence during parallel adaptation

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.

evolutionary biology↗

Land use impacts poison frog chemical defenses through changes in leaf litter ant communities

Much of the worlds 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.

ecology↗

Mechanisms of convergent egg-provisioning in poison frogs

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.

neuroscience↗

The neural basis of tadpole transport in poison frogs

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.

animal behavior and cognition↗

Seasonal changes in diet and toxicity in the Climbing Mantella frog (Mantella laevigata)

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.

ecology↗

Untangling the role of selection and drift in population divergence via transcriptional network simulations: Extended analysis of Ghalambor et al. (2015)

Introduction Introduction Literature Cited A long-standing question in evolutionary biology is whether phenotypic plasticity influences adaptive evolutionary change (e.g. Waddington 1961; Price et al. 2003; Ghalambor et al. 2007; Lande 2009; Wund 2012). The same genotype can produce different phenotypes in response to different environments, but whether such plasticity constrains or facilitates evolutionary change remains an unresolved and controversial problem (Ghalambor et al. 2007). Theoretical models to date have made diverse predictions on the role of plasticity in evolutionary divergence (e.g. Ancel 2000; Paenke et al. 2007; Thibert-Plante and Hendry 2011), and empirical studies have largely been limited to retrospective approaches that infer the role of plasticity long-after popu ...

evolutionary biology↗