1. A high rate of reproduction may be costly if ecological factors limit immediate reproductive output as a fast metabolism compromises own future survival. Individuals with more reserves need more time and opportunity to realize their reproductive potential. Theory therefore predicts that the reproductive rate, defined as the investment in early reproduction in proportion to total potential, should decrease with body size within species. 2. However, metabolic constraints on body size- and temperature-dependent biological rates may impede biophysical adaptation. Furthermore, the sequential manner resources that are allocated to somatic vs. reproductive tissue during ontogeny may, when juveniles develop in unpredictable environments, further contribute to non-adaptive variation in adult reproductive rates. 3. With a model on female egg laying in insects, we demonstrate how variation in body reserves is predicted to affect reproductive rate under different ecological scenarios. Small females always have higher reproductive rates but shorter lifespans. However, incorporation of female host selectivity leads to more similar reproductive rates among female size classes, and oviposition behaviour is predicted to co-evolve with reproductive rate, resulting in small females being more selective in their choice and gaining relatively more from it. 4. We fed simulations with data on the butterfly Pararge aegeria to compare model predictions with reproductive rates of wild butterflies. However, simulated reproductive allometry was a poor predictor of that observed. Instead, reproductive rates were better explained as a product of metabolic constraints on rates of egg maturation, and an empirically derived positive allometry between reproductive potential and size. However, fitness is insensitive to moderate deviations in reproductive rate when oviposition behaviour is allowed to co-evolve in the simulations, suggesting that behavioural compensation may mitigate putative metabolic and developmental constraints. 5. More work is needed to understand how physiology and development together with compensatory behaviours interact in shaping reproductive allometry. Empirical studies should evaluate adaptive hypotheses against proper null hypotheses, including prediction from metabolic theory, preferentially by studying reproductive physiology in combination with behaviour. Conversely, inferences of constraint explanations on reproductive rates must take into consideration that adaptive scenarios may predict similar allometric exponents.