Tapia, E. E. | Search bioRxiv

bioRxiv2019

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↗

bioRxiv2019

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↗

bioRxiv2019

Molecular physiology of chemical defenses in a poison frog

Poison frogs sequester small molecule lipophilic alkaloids from their diet of leaf litter arthropods for use as chemical defenses against predation. Although the dietary acquisition of chemical defenses in poison frogs is well-documented, the physiological mechanisms of alkaloid sequestration has not been investigated. Here, we used RNA sequencing and proteomics to determine how alkaloids impact mRNA or protein abundance in the Little Devil Frog (Oophaga sylvatica) and compared wild caught chemically defended frogs to laboratory frogs raised on an alkaloid-free diet. To understand how poison frogs move alkaloids from their diet to their skin granular glands, we focused on measuring gene expression in the intestines, skin, and liver. Across these tissues, we found many differentially expressed transcripts involved in small molecule transport and metabolism, as well as sodium channels and other ion pumps. We then used proteomic approaches to quantify plasma proteins, where we found several protein abundance differences between wild and laboratory frogs, including the amphibian neurotoxin binding protein saxiphilin. Finally, because many blood proteins are synthesized in the liver, we used thermal proteome profiling as an untargeted screen for soluble proteins that bind the alkaloid decahydroquinoline. Using this approach, we identified several candidate proteins that interact with this alkaloid, including saxiphilin. These transcript and protein abundance patterns suggest the presence of alkaloids influences frog physiology and that small molecule transport proteins may be involved in toxin bioaccumulation in dendrobatid poison frogs.\n\nResumenLas ranas venenosas obtienen moleculas lipofilicas a partir de su dieta de artropodos que luego usan como una defensa quimica contra depredadores. Mientras que la acumulacion de toxinas dieteticas ha sido bien documentada, el mecanismo fisiologico de obtencion de alcaloides no ha sido investigado. En este estudio usamos secuenciacion de RNA y proteomica para determinar como la presencia de alcaloides afecta la abundancia de mRNA y proteinas en ranas diablito (Oophaga sylvatica) silvestres con defensas quimicas en comparacion a ranas diablito criadas en laboratorio con una dieta sin alcaloides. Para entender como las ranas venenosas mueven los alcaloides de su dieta a las glandulas granulares en su piel, nos enfocamos en medir la expresion de genes en tres tejidos: intestinos, piel e higado. En estos tejidos, encontramos varios transcriptomas regulados diferencialmente que tienen actividades involucradas con el transporte y metabolismo de pequenas moleculas, ademas de canales de sodio y bombas de iones. Luego usamos metodos proteomicos para cuantificar proteinas en plasma, donde encontramos varias diferencias en abundancia de proteinas entre las ranas silvestres y de laboratorio, incluyendo la proteina anfibia de fijacion de toxinas, saxifilina. Finalmente, debido a que muchas proteinas encontradas en la sangre se sintetizan en el higado, usamos la tecnica de perfilacion proteomica termal para seleccionar imparcialmente las proteinas solubles que fijan el alcaloide decahydroquinolina. Usando este metodo, identificamos varias posibles proteinas que interactuan con este alcaloide, incluyendo saxifilina. Estos patrones de cambios en abundancia de transcriptomas y proteinas en ranas con y sin defensas quimicas sugieren que la presencia de alcaloides influye en la fisiologia de las ranas y que moleculas proteicas pequenas de transporte podrian estar involucradas en la bioacumulacion de toxinas en ranas venenosas dendrobatidos.\n\nSummary StatementChemically defended wild poison frogs have gene expression and protein abundance differences across several tissue systems compared to poison frogs reared on an alkaloid-free diet.

physiology↗