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Variation in reproductive success is the basis of evolution and allows species to respond to the environment, but only when it is based on fixed individual variation that is heritable. Several recent studies suggest that observed variation in reproduction is due to chance, not inherent individual differences. Our aim was to quantify inherent versus neutral variation in fitness of northern elephant seal (Mirounga angustirostris (Gill, 1866)) females, including both quality and quantity of their offspring. Using 44 years of observations at Año Nuevo in California, we assembled lifetime pup production of 1065 individual females and mass at weaning for 2120 of their pups. Females varied significantly in mean lifetime mass of their pups, with 28% of the variance due to fixed individual differences among mothers. Variation was repeatable over 6 years of a mother’s lifetime and heritable (h = 0.48). Moreover, pup mass at weaning was associated with future lifetime fitness, since larger pups had a higher chance of surviving to breed. Larger pups, however, did not produce more offspring once breeding, and lifetime pup production was not heritable. Traits related to offspring quality in elephant seals were inherently different among females, but variation in pup production was neutral. 

The open ocean twilight zone holds most of the global fish biomass but is poorly understood owing to difficulties of measuring subsurface ecosystem processes at scale. We demonstrate that a wide-ranging carnivore—the northern elephant seal—can serve as an ecosystem sentinel for the twilight zone. We link ocean basin–scale foraging success with oceanographic indices to estimate twilight zone fish abundance five decades into the past, and into the future. We discovered that a small variation in maternal foraging success amplified into larger changes in offspring body mass and enormous variation in first-year survival and recruitment. Worsening oceanographic conditions could shift predator population trajectories from current growth to sharp declines. As ocean integrators, wide-ranging predators could reveal impacts of future anthropogenic change on open ocean ecosystems.