Growth, body size and sexual maturation are linked with the ontogenetic development of aerobic metabolic scope in fish

Aquatic ectotherms are challenged by global warming and declining oxygen, but the physiological determinants of the associated earlier sexual maturation and reduced body size remain unknown. Several frameworks link the body-mass-scaling of metabolic rates with life-history traits, including growth, body size, maturation and reproduction, but it is debated whether the ontogenetic development of these traits is governed by hard physiological limits, such as oxygen limitation, or adaptive co-optimization. We quantified individual ontogenetic growth trajectories and metabolic scaling of 53 Trinidadian guppies (Poecilia reticulata) followed longitudinally from birth to adulthood. We also quantified timing of maturation for males. Standard (maintenance) metabolic rate (SMR) scaled more steeply with body mass than maximum metabolic rate (MMR) for both sexes, resulting in metabolic scope (factorial aerobic scope, FAS = MMR/SMR) declining through ontogeny. Individuals whose FAS decreased the most grew slowest and, for males, matured at older age but smaller body size and became smaller adults. Both males and females retained high FAS (>5) at the age of male maturation, inconsistent with oxygen limitation triggering maturation. Instead, male maturation occurred after maximal growth rate and coincided with growth deceleration, consistent with reallocation of energy towards reproduction. Overall, our findings link steep declines in metabolic scope to reduced body size at sexual maturation and reduced asymptotic size.