Matrotrophy limits a female's ability to adaptively adjust offspring size and fecundity in fluctuating environments

1. The ability to adjust the allocation of energy to maintenance, growth and reproduction in response to fluctuations in resource availability, in a way that enhances fitness, is thought to depend on the mode of maternal provisioning. 2. We manipulated food availability in the matrotrophic, livebearing fish Phalloptychus januarius (Poeciliidae) to examine patterns of allocation under fluctuating resource conditions. 3. We observed an asynchrony in the adjustment of offspring traits in response to changes in food availability. A reduction in food availability caused an immediate reduction in allocation of energy to offspring size and lipid content at birth, but a delayed reduction in offspring number (fecundity). Similarly, an increase in food availability caused an immediate increase in offspring size and lipid content and a delayed increase in fecundity. This asynchrony is thought to be inherent to matrotrophy, limiting a female's ability to attain an optimal fitness in fluctuating resource environments, regardless of whether food availability changes from high to low, or low to high. 4. We found no evidence for embryo abortion under low food conditions. All developing offspring were retained, yet were smaller at birth. Furthermore, although females carried large fat reserves, these were rapidly depleted during low food conditions and were not sufficient to fully buffer gestating females or their developing offspring against the detrimental effects of reduced food availability. 5. Our study shows that matrotrophy is likely to be a maladaptive strategy in environments that are characterized by fluctuations in resource availability. It further suggests that matrotrophy is most likely to evolve in high and stable resource environments.