Early development is a critical bottleneck in egg-laying fish species, in part because temperature influences both the time embryos are reliant on yolk reserves supplied in the egg (development time) and the rate of embryo energy expenditure (metabolic rate). Population responses to warming may therefore depend not only on plasticity of development time and metabolic rate, but also on whether their thermal sensitivity can evolve.
We estimated heritability in development time, metabolic rate, and their thermal sensitivities using a North Carolina II breeding design in three-spined stickleback (Gasterosteus aculeatus). Embryos from each family were reared at 12, 16 or 20 °C. We measured development time from fertilisation to hatching, oxygen consumption at three stages of embryogenesis, and hatching success. Larvae were then reared at a common 12 °C and juvenile mitochondrial function was quantified.
As expected, warming strongly accelerated development and increased metabolic rates, however estimated total developmental energy expenditure declined from 16 mJ at 12 °C to 9 mJ at 20 °C because development time decreased more than metabolic rates increased. Hatching success remained high across treatments (92–96%). Narrow-sense heritability of metabolic rate increased through development (h² = 0.20 to 0.73), while maternal effects declined. Development time was only weakly heritable (h² = 0.17), and no trait showed detectable additive genetic variance in thermal sensitivity. Embryonic temperature had no lasting effect on juvenile mitochondrial function, although individuals reared at 16 or 20 °C were smaller as juveniles than those reared at 12 °C.
This experiment provides evidence that warming can therefore accelerate early development without reducing hatching success, but it also alters developmental energetics and later body size. Limited heritable variation in thermal sensitivity may constrain evolutionary responses at this early-life bottleneck.