Tarvin, R. D. | bioRxiv Science

bioRxiv2022

Diurnality shapes the visual opsin genes of colorful Neotropical frogs

Amphibians are ideal for studying visual system evolution because their biphasic (aquatic and terrestrial) life history and ecological diversity expose them to a broad range of visual conditions. Here we evaluate signatures of selection on visual opsin genes across Neotropical anurans and focus on three diurnal clades that are well-known for the concurrence of conspicuous colors and chemical defense (i.e., aposematism): poison frogs (Dendrobatidae), Harlequin toads (Bufonidae: Atelopus), and pumpkin toadlets (Brachycephalidae: Brachycephalus). We found evidence of positive selection on 44 amino acid sites in LWS, SWS1, SWS2, and RH1 opsin genes, of which one in LWS and two in RH1 have been previously identified as spectral tuning sites in other vertebrates. Given that anurans have mostly nocturnal habits, the patterns of selection revealed new sites that might be important in spectral tuning for frogs, potentially for adaptation to diurnal habits and for color-based intraspecific communication. Furthermore, we provide evidence that SWS2, normally expressed in rod cells in amphibians, has likely been lost in the ancestor of Dendrobatidae, suggesting that under low-light levels, dendrobatids have inferior wavelength discrimination compared to other frogs. This loss might follow the origin of diurnal activity in dendrobatids and could have implications for their chemical ecology, biodiversity, and behavior. Our analyses show that assessments of opsin diversification in understudied groups could expand our understanding of the role of sensory system evolution in ecological adaptation.

evolutionary biology↗

bioRxiv2022

Characterizing Potential Tetrodotoxin Resistance in Domain IV of the Voltage-Gated Sodium Channel Nav1.4 of Pacific Chorus Frogs, Pseudacris regilla

Animals that frequently encounter toxins often select for mechanisms of toxin resistance. Both predators that consume toxic prey and organisms in physical contact with a toxin or pollutant in their environment may experience natural selection for resistance. Based on field observations that Pacific Chorus Frogs (Pseudacris regilla) sometimes eat and mistakenly amplect tetrodotoxin (TTX)-defended Taricha newts, we predicted that P. regilla may possess resistance to TTX. We tested this prediction by comparing the amino acid sequences of the molecular target of TTX, the muscle voltage-gated sodium channel gene SCN4A (NaV1.4), in populations of P. regilla that are sympatric and allopatric with Taricha. We identified a single substitution in NaV1.4 of P. regilla in a conserved site near the pore loop where TTX binds. Although the role of this site in TTX resistance has not been functionally assessed, both allopatric and sympatric P. regilla had this substitution, suggesting that it may be unrelated to TTX exposure from Taricha. Thus, there is no conclusive evidence that P. regilla has selected for TTX resistance encoded by amino acid substitutions in this domain. In addition, California occurrence data from the last 50 years indicate that Taricha activity peaks in January while the activity of P. regilla peaks in April. These relatively distinct activity patterns suggest that P. regilla may not be exposed to levels of TTX from Taricha that are high enough to select for mutations in the sodium channel. Nevertheless, other unidentified mechanisms of TTX resistance could be present in P. regilla and other species that are sympatric with toxic newts. ResumenLos animales que tienen contacto frecuente con toxinas suelen desarrollar mecanismos de resistencia a las mismas. Tanto los depredadores que consumen presas toxicas como los organismos en contacto cercano con una toxina o contaminante en su entorno pueden experimentar una presion de seleccion que los lleva a evolucionar resistencia a toxinas. Basandose en las observaciones de que las ranas coro del Pacifico (Pseudacris regilla) a veces comen por error y/o amplexan salamandras del genero Taricha que poseen tetrodotoxina (TTX), se planteo la hipotesis de que P. regilla podria poseer resistencia a la TTX. Esta prediccion fue probada comparando las secuencias de aminoacidos en el loop del poro del dominio IV en el gen del canal de sodio voltaje dependiente muscular SCN4A (proteina NaV1.4) en poblaciones de P. regilla que son simpatricas y alopatricas con Taricha. Se identifico una unica sustitucion en el NaV1.4 de P. regilla en un sitio conservado cerca del loop del poro donde se une la TTX. Aunque el papel de este sitio en la resistencia a la TTX no ha sido evaluado funcionalmente, tanto el P. regilla alopatrico como el simpatrico tienen esta sustitucion, lo que sugiere que no esta relacionado con la exposicion a la TTX secretada por Taricha. Por lo tanto, no hay evidencias concluyentes de que P. regilla haya evolucionado resistencia a la TTX por medio de sustituciones de aminoacidos en este dominio. Por otro lado, los datos de ocurrencia en California de la actividad de Taricha en los ultimos 50 anos indican alcanza su maximo en enero, mientras que la de P. regilla lo hace en abril. Estos patrones de actividad relativamente distintos sugieren que P. regilla puede no estar expuesta a niveles de TTX provenientes de Taricha que sean lo suficientemente altos como para inducir la evolucion de mutaciones en el canal de sodio. Sin embargo, otros mecanismos no identificados de resistencia a la TTX podrian estar presentes en P. regilla y en otras especies simpaticas a los salamandras toxicas. Palabras clave: Resistencia a las toxinas; California; Toxinas ambientales; Insensibilidad en el sitio de union; Salamandras; Ecologia quimica

evolutionary biology↗

bioRxiv2021

Toxin breakdown does not preclude the potential for defensive toxin use in a fruit fly

Animals that ingest toxins can become unpalatable and even toxic to predators and parasites through toxin sequestration. Because most animals rapidly eliminate toxins to survive their ingestion, it is unclear how populations transition from susceptibility and toxin elimination to tolerance and accumulation as chemical defense emerges. Studies of chemical defense have generally focused on species with active toxin sequestration and target-site insensitivity mutations or toxin-binding proteins that permit survival without necessitating toxin elimination. Here, we investigate whether animals that presumably rely on toxin elimination for survival can utilize ingested toxins for defense. We use the A4 and A3 Drosophila melanogaster fly strains from the Drosophila Synthetic Population Resource (DSPR), which respectively possess elevated and reduced metabolic nicotine resistance amongst DSPR fly lines. We find that ingesting nicotine increased A4 but not A3 fly survival against Leptopilina heterotoma wasp parasitism.Further, we find that despite possessing genetic variants that enhance toxin elimination, A4 flies accrued more nicotine than A3 individuals likely by consuming more media. Our results suggest that enhanced toxin metabolism can allow for greater toxin intake by offsetting the cost of toxin ingestion. Passive toxin accumulation that accompanies increased toxin intake may underlie the early origins of chemical defense.

evolutionary biology↗