Energy Trade-off And Evolution Among Expensive-tissues In Anurans

In this paper, we studied energy trade-offs in eight energy expensive-tissues(including brain, digestive tract, heart, liver, lungs, kidneys, spleen and limb-muscles). The effects of spawning locations and habitats on these expensive-tissues were also researched using 30 anuran species. In addition, we explored the energy trade-offs by analyzing their relationships with average annual temperature and precipitation. The species used in this study were collected from 21 districts and counties in Hengduan Mountains and Sichuan Basin.“Energy trade-off hypothesis” predicts that the costs of larger brains may be met by a decreased investment in other expensive-tissues. Here, we analyzed the relationship among brain, digestive tract, heart, liver, lungs, kidneys, spleen and limb-muscles by controlling for the effect of shared ancestry and body size using phylogenetically controlled generalized least-squared(PGLS) regression analyses. The results revealed that there was a negative correlation between brain mass and the length of the digestive tract(brain mass: t =-3.355, P = 0.002; body size: t = 8.948, P < 0.001), which supports the energy trade-off hypothesis. But we found no significant correlation between brain mass and other expensive-tissues(i.e. heart, liver, lungs, kidneys, spleen and limb-muscles) after controlling for the effect of shared ancestry and body size(P > 0.0558). In addition, we also investigated how the other organs were associated and found positive correlations among heart, kidneys, digestive tract and limb muscles. But no significantly negative relationships were found among these expensive-tissues when controlling for the effect of shared ancestry and body size, indicating that there was only a trade-off between brain mass and digestive tract length rather than other expensive-tissues.We also researched the effects of different spawning locations and habitats on the eight expensive-tissues. The results showed that the anurans with lotic spawning had heavier limb-muscle weights than those with lentic spawning after controlling for the effect of body mass(P = 0.002). However, spawning locations influenced slightly on limb-muscle weights as a whole(P = 0.085). The limb-muscle weights of lentic spawning, terrestrial or arboreal spawning and lotic spawning, increased in sequence. But the spawning locations did not influence other expensive-tissues after controlling for the effect of body mass(P > 0.252). We inferred that the energy requirements in muscles decreased by the sequence of lotic aquatic > terrestrial or arboreal > lentic aquatic for successfully moving to spawning locations and the order of energy requirements may result from the significantly different environments of spawning locations. Habitats had significant effects on limb-muscles(P = 0.002), lungs(P = 0.043), spleen(P = 0.038), slight effects on heart(P = 0.057), and no significant effects on other expensive-tissues(brain, digestive tract, liver and kidney)(P > 0.621), when we controlled for body mass. Post-hoc tests reveal that semi-aquatic species had smaller heart than cave-dweller and arboreal species(cave-dweller: P = 0.034, arboreal: P = 0.012); cave-dweller and arboreal species had smaller limb-muscles than aquatic and semi-aquatic species(P < 0.006); terrestrial and cave-dweller species had heavier lung than aquatic and semi-aquatic species(P < 0.034); and cave-dweller species had significantly smaller spleen than other habitats(P < 0.030) and no significant difference was found among other habitats(P > 0.521).By analyzing the effects of average annual temperature and precipitation on the energy trade-offs in the expensive-tissues we found the brain size increased with average annual temperature(brain: slope = 0.545, t = 2.168, P = 0.039), but digestive tract length did not significantly decrease with average annual temperature(digestive tract: slope =-0.316, t =-1.198, P = 0.241), and the other expensive-tissues did not vary with average annual temperature(P > 0.0946), after controlling for the effect of shared ancestry and body size. Both brain size and digestive tract length did not vary with precipitation((brain: slope =-0.129, t =-0.517, P = 0.609; digestive tract: slope = 0.207, t = 0.841, P = 0.408), and the other expensive-tissues were also not varied with precipitation(P > 0.190). In addition, the interaction between average annual temperature and precipitation had no significant effect on all the expensive-tissues(P > 0.062). The results indicated that average annual temperature may regulate the energy cost in brain by influencing the complexity in their biotic and abiotic environment. That the cost in digestive tract did not significantly vary with average annual temperature may result from the more energy compensation of fat bodies or more digestible foods for digestive tract in colder places.