No evidence for the ‘expensive‐tissue hypothesis’ from an intraspecific study in a highly variable species

Abstract

The 'expensive-tissue hypothesis' states that investment in one metabolically costly tissue necessitates decreased investment in other tissues and has been one of the keystone concepts used in studying the evolution of metabolically expensive tissues. The trade-offs expected under this hypothesis have been investigated in comparative studies in a number of clades, yet support for the hypothesis is mixed. Nevertheless, the expensive-tissue hypothesis has been used to explain everything from the evolution of the human brain to patterns of reproductive investment in bats. The ambiguous support for the hypothesis may be due to interspecific differences in selection, which could lead to spurious results both positive and negative. To control for this, we conduct a study of trade-offs within a single species, Thalassoma bifasciatum, a coral reef fish that exhibits more intraspecific variation in a single tissue (testes) than is seen across many of the clades previously analysed in studies of tissue investment. This constitutes a robust test of the constraints posited under the expensive-tissue hypothesis that is not affected by many of the factors that may confound interspecific studies. However, we find no evidence of trade-offs between investment in testes and investment in liver or brain, which are typically considered to be metabolically expensive. Our results demonstrate that the frequent rejection of the expensive-tissue hypothesis may not be an artefact of interspecific differences in selection and suggests that organisms may be capable of compensating for substantial changes in tissue investment without sacrificing mass in other expensive tissues.