Abstract
Internal organs of ectotherms have melanin‐containing cells that confer different degrees of coloration to them. Previous experimental studies analyzed their developmental origin, role in immunity, and hormonal regulation. For example, melanin increases with ultraviolet radiation (UV) and temperature in frogs and fish. However, little is known about how environmental variables influence the amount of coloration on organs among amphibian species over a large spatial extent. Here, we tested how climatic variables (temperature, UV, and photoperiod) influence the coloration of internal organs of anurans. We recorded the level of melanin pigmentation using four categories on 12 internal organs and structures of 388 specimens from 43 species belonging to six anuran families. Then, we tested which climatic variables had the highest covariation with the pigmentation on each organ after controlling for spatial autocorrelation in climatic variables and phylogenetic signal in organ coloration using the extended version of the RLQ ordination. Coloration in all organs was correlated with the phylogeny. However, the coloration of different organs was affected by different variables. Specifically, the coloration of the heart, kidneys, and rectum of hylids, Rhinella schneideri, some Leptodactylus, and Proceratophrys strongly covaried with temperature and photoperiod, whereas that of the testicle, lumbar parietal peritoneum, lungs, and mesenterium of Leiuperinae, Hylodidae, Adenomera, and most Leptodactylus had highest covariation with UV‐B and temperature. Our results support the notion that melanin pigmentation on the surface of organs of amphibians has an adaptive function conferred by the protective functions of the pigment. But most importantly, internal melanin seems to respond differently to climatic variables depending on the lineage and locality in which species occur.
Highlights
Vertebrates have a wide variety of body color patterns whose evolution is shaped by both natural and sexual selection (Cuthill et al., 2017)
Previous experimental studies have established a link between the amount and distribution of melanin pigmentation on organs to temperature variation (Santos, Franco-Belussi, Zieri, Borges, & Oliveira, 2014), ultraviolet B (UV-B) radiation (Franco-Belussi, Sköld, & Oliveira, 2016), bacterial infections (Franco-Belussi et al, 2013), and the joint effect of ultraviolet radiation (UV)-B and bacteria
We found a large intraspecific variation in coloration intensity in some lineages, mainly the Dendropsophryni tribe (Dendropsophus and Scinax). Both diurnal and annual thermal ranges had a high covariation with the coloration on the testicle, lumbar parietal peritoneum, lungs, and mesenterium
Summary
Vertebrates have a wide variety of body color patterns whose evolution is shaped by both natural and sexual selection (Cuthill et al., 2017). No study has tested the effects of UV on the coloration of internal organs of multiple species (but see Franco- Belussi et al, 2016 for Physalaemus nattereri), which could potentially play a role in determining amphibian declines Another environmental variable that alters the skin coloration of fish and anurans is photoperiod. We build upon our previous study (Provete et al, 2012) to test which climatic variables (temperature, UV, and photoperiod) have the highest covariation with coloration on the surface of internal organs in anurans using a three-table ordination method called RLQ (R- mode Linked to Q-mode; Dolédec, Chessel, ter Braak, & Champely, 1996; Pavoine, Vela, Gachet, Belair, & Bonsall, 2011). Diurnal species tend to have a great amount of internal melanin, because during this period the UV incidence and temperature are higher
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