Understanding the mechanisms of biological responses to environmental change is a central theme in comparative and evolutionary physiology. Here, we analyzed variation in physiological responses to temperature, using 21 full-sibling larval families of the Pacific oyster, Crassostrea gigas. Pedigrees were confirmed with genetic markers for adult broodstock obtained from our breeding program. From these 21 larval families, 41 determinations of thermal sensitivity (Q10 values) were assayed for larvae of different sizes. For respiration, thermal sensitivity was consistent within a larval family during growth, but showed significant differences among families. Different Q10 values were evident among 21 larval families, with family accounting for 87% of variation. Specifically, four larval families maintained an increased thermal sensitivity for respiration (Q10 of 3). This physiology would confer resilience to rising temperature by matching the increased energy demand of protein synthesis (Q10 of 3 previously reported). For protein synthesis, differences in Q10 values were also observed. Notably, a family was identified that had a decreased thermal sensitivity for protein synthesis (Q10 of 1.7 cf. Q10 of 3 for other families), conferring an optimal energy allocation with rising temperature. Different thermal sensitivities across families for respiration (energy supply) and protein synthesis (energy demand) were integrated into models of energy allocation at the whole-organism level. The outcome of these analyses provides insights into the physiological bases of optimal energy allocation with rising temperature. These transgenerational (egg-to-egg) experiments highlight approaches to dissect components of phenotypic variance to address long-standing questions of genetic adaptation and physiological resilience to environmental change.

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