What doesn't kill you makes you stronger: Detoxification ability as a mechanism of honesty in a sexually selected signal

• Published in: Functional ecology 2021-08, Vol.35 (8), p.1666-1678
• Main Authors: G‐Santoyo, Isaac, González‐Tokman, Daniel, Tapia‐Rodríguez, Miguel, Córdoba‐Aguilar, Alex
• Format: Article
• Language: English
• Subjects: Byproducts; Confocal microscopy; Detoxification; detoxification ability; Evolution; Hetaerina americana; kynurenine; Lethal effects; Males; Metabolic pathways; Natural selection; odonata; Ommochromes; Pigments; Sexual selection; sexually selected colouration; Signal transduction; storage excretion; Survival; Toxicity; Tryptophan
• ISSN: 0269-8463; 1365-2435
• DOI: 10.1111/1365-2435.13798

Sexual selection leads to the expression and maintenance of colourful signals. The metabolic pathways to produce such signals often involve toxic byproducts that can reduce survival. However, rather than discarding these otherwise harmful byproducts, animals may use them by integrating them into sexually selected traits. We tested this using the damselfly Hetaerina americana, where males bear a red wing spot (RWS) that has evolved by intrasexual competition. By using confocal microscopy and several biochemical techniques, we determined that the RWS are generated by ommochrome pigments derived from tryptophan metabolism. Second, we injected a group of males with the toxic precursor of these ommochromes, 3‐hydroxy‐kynurenine (3‐Hk), confirming the toxicity of this compound in adult males. Finally, we showed that adult males injected with a median lethal concentration of 3‐Hk had more ommochromes in their RWS than controls but similar survival, suggesting that the deposition of ommochrome pigment in the wing counteracts the 3‐HK toxicity. Thus, we report that sexually selected pigmented signals may involve the co‐option of excreted compounds that could otherwise have lethal effects, a hypothesis we call ‘detoxifying ability signalling’. Our results provide new insights about the evolution of sexual signals, elucidating a mechanism for the evolution of honest indicators of quality that could have arisen due to natural selection. Resumen La selección sexual es uno de los mecanismos que permite la expresión de múltiples señales coloridas en los animales. La producción y mantenimiento de estasseñales puede involucrar la síntesis de diferentes subproductos tóxicos que afectanla supervivencia de quien los produce. Interesantemente, en vez de eliminarlos,los animales podrían inactivarlos, almacenarlos e integrarlos como parte deestas señales sexuales. Probamos esta idea en la libélula Hetaerina americana. Aquí, los machos presentanun pigmento rojo en la base de sus alas que ha evolucionado como una señal sexual por competencia intrasexual. Con el uso de técnicas bioquímicas y demicroscopia confocal, determinamos que estos pigmentos son omocromos,producidos por el metabolito del triptófano 3‐hidroxy‐Kinurenina (3‐Hk), y observamos que este metabolito es tóxico para los adultos de H.americana. Finalmente, demostramos que los adultos a los que se les administro una dosis letal mediade 3‐Hk, lograron contrarrestarsu toxicidad sintetizando más omocromos y depositándolos