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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. 

Abstract Maternal age can influence reproductive success and offspring fitness, but the timing, magnitude and direction of those impacts are not well understood. Evolutionary theory predicts that selection on fertility senescence is stronger than maternal effect senescence, and therefore, the rate of maternal effect senescence will be faster than fertility senescence.We used a 36‐year study of northern elephant seals (Mirounga angustirostris) to investigate reproductive senescence. Our dataset included 103,746 sightings of 1203 known‐age female northern elephant seals.We hypothesized that fertility (maternal reproductive success), offspring survival and recruitment into the breeding population, and male offspring production would decline with advanced maternal age. Furthermore, we hypothesized that older females would shorten their moulting haul out to allow for more time spent foraging.We found evidence for both fertility and maternal effect senescence, but no evidence for senescence impacting offspring recruitment or sex ratio. Breeding probability declined from 96.4% (95% CI: 94.8%–97.5%) at 11 years old to 89.7% (81.9%–94.3%) at 19 years old, and the probability of offspring survival declined from 30.3% (23.6%–38.0%) at 11 years old to 9.1% (3.2%–22.9%) at 19 years old.The rates of decline for fertility and maternal effect senescence were not different from each other. However, maternal effect senescence had a substantially greater impact on the number of offspring surviving to age 1 compared to fertility senescence. Compared to a hypothetical non‐senescent population, maternal effect senescence resulted in 5.3% fewer surviving pups, whereas fertility senescence resulted in only 0.3% fewer pups produced per year. These results are consistent with evolutionary theory predicting weaker selection on maternal effect than fertility senescence. Maternal effect senescence may therefore be more influential on population dynamics than fertility senescence in some systems.