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This study used crosses of wild-caught dumpling squid (Euprymna tasmanica) males to multiple females with known behavioural types to evaluate patterns of additive and residual variance in behavioural traits from offspring under two contexts - a threat and a foraging test. Genetic contributions to behavioural expression were context-dependent. Threat context behaviour had significant heritability, while foraging context behaviour had lesser additive and greater residual components. Female trait variation was not correlated with fecundity. Female foraging boldness (which co-varied with size) explained some variation in brood hatching success. Positive assortion of mate pairs according to shy-bold phenotype determined fertilization success.