Immune challenges and visual signalling in tree frogs

Abstract

In animals, mate-choice is often based on sexual signals that carry information and help the receiver make the best choice to improve the receiver's fitness. Orange visual sexual signals have been hypothesised to carry immune information because they are often due to carotenoid pigments which are also involved in immunity response. Although many studies have focused on the direct relationships between coloration and immunocompetence, few studies have simultaneously studied immunocompetent response and coloration variation after an immune challenge. We tested this hypothesis on starved and ad libitum-fed males of the European tree frog Hyla arborea. Our results show that male coloration is not a reliable indicator of its immune response capacity in this species. However, after an immune challenge induced by a PHA (Phaseolus vulgaris phytohaemagglutinin) injection, starved males presented a significant coloration loss and this alteration was related to the immune response intensity. Taken together, these results suggest that the brighter (lighter) coloration may be used as a cue by female to exclude males with a recent immune challenge, due to diseases or parasites for example.

Critical review of the phytohemagglutinin assay for assessing amphibian immunity

“… Murillo-Rincón et al (2017) found that when performed on larvae, the PHA assay increased the larval period, which is potentially problematic given that development time has been a long-standing measure of fitness and can impact survival in ephemeral environments. Desprat et al (2017) observed that the PHA assay caused a lightening of the vocal sac in starved males proportional to the PHA response, which the authors suggested may be an indicator to females that a male recently encountered a disease agent, reducing chances of breeding success. Finally, histological analysis by Clulow et al (2015) found evidence of damage to the muscle fibers and fibrosis in some specimens injected with PHA.…”

“…However, previous studies have found minimal differences in immunocompetence both among sexes and individuals of the same sex exhibiting variation in reproductive morphology and behavior during the mating season ( Saad, 1992 ; Zapata et al , 1992 ; Cornuau et al , 2014 ; Thomas and Woodley, 2017 ). While some amphibian PHA studies looked at only males ( de Assis et al , 2015 ; Desprat et al , 2015 , 2017 ; Josserand et al , 2015 ; Madelaire et al , 2017 ; Troïanowski et al , 2017 ; Iglesias-Carrasco et al , 2018 ; Titon et al , 2019 , 2021 ; Wang et al , 2019 ) or females ( Fites et al , 2014 ) to avoid confounding sex-related effects, several other studies specifically investigated sex-related differences in PHA swelling responses ( Bakewell et al , 2021 ; Zamora-Camacho et al , 2022 ).…”

“…Injection sites should be tailored to the specimen type to generate an easily measurable swelling response ( Clulow et al , 2015 ). However, many studies do not provide an adequate description of the injection site for proper duplication, using unspecific terms such as ‘tail’, ‘leg’ and ‘hind leg’ ( Szuroczki et al , 2016 ; Desprat et al , 2017 ; Troïanowski et al , 2017 ). Still, some overall patterns can be observed.…”

“…Many studies used the approach adopted by Brown et al (2015) and Zhang et al (2017) , reporting a proportion as change in thickness over starting thickness ( Brown et al , 2011 , 2015 ; Brown and Shine, 2014 ; Clulow et al , 2015 ; de Assis et al , 2015 ; Abu Bakar et al , 2016 ; Szuroczki et al , 2016 ; Madelaire et al , 2017 , 2019 ; Murillo-Rincón et al , 2017 ; Brannelly et al , 2019 ; Titon et al , 2019 ; Cassettari et al , 2022 ; Vasconcelos-Teixeira et al , 2022 ; Venesky and Laskey, 2022 ). Meanwhile, many other studies reported millimetres of swelling without providing a starting or ending thickness measure to allow comparison with percentage-based reporting ( Gilbertson et al , 2003 ; Gervasi and Foufopoulos, 2008 ; Seiter, 2009 ; Venesky et al , 2012 ; Young et al , 2014 ; Desprat et al , 2015 , 2017 ; Ceccato et al , 2016 ; Szuroczki et al , 2016 , 2019 ; Titon et al , 2016 ; Troïanowski et al , 2017 ; Wang et al , 2019 ; Zamora-Camacho, 2019 ; Zamora-Camacho et al , 2022 ). Other methodologies have been used less often; for example, Zamora-Camacho and Comas (2018) calculated the ‘area under the curve’, by integrating swelling response measurements over multiple time points.…”

Selection and population demography shape evolution of two long-lived ectotherms

“…Physiological stress is associated with changes in characteristics of color (e.g., brightness and hue) across animals, including birds (Mougeot et al 2010), fish (Sefc et al 2014), amphibians (Desprat et al 2017), and reptiles (Cote et al 2010a). Brightness, or how light or dark a color appears (i.e., overall achromatic intensity) is generally hypothesized to be inversely related to stress, such that stressed organisms are duller (e.g., San-Jose and Fitze 2013).…”