Summary 1. Comparative evidence from several animal taxa suggests that juveniles hatching from larger eggs have fitness benefits when growing up in a harsh environment, whereas under benign conditions egg size should be of less importance. However, the physiological and behavioural mechanisms responsible for these context‐dependent fitness differences are as yet poorly understood. 2. We studied the interactions between the phenotype of developing offspring and their environment in the mouthbrooding cichlid Simochromis pleurospilus. We hand‐raised young from large and small eggs, and measured their initial body size and burst swimming speed. Thereafter we raised half of each egg‐size class on high and half on low food ration and followed their growth trajectories and behavioural development until the age of 12 weeks. 3. We found that larger eggs gave rise to larger young that had a higher burst swimming speed. Food ration greatly influenced long‐term growth, while egg size predominantly affected fish size during the first 2 weeks of life. However, large egg size caused a size advantage of juveniles persisting throughout the experimental period. 4. Egg size and food ration interactively affected the hiding and foraging behaviour of young. In the low‐food treatment, individuals from small eggs spent less time in shelter and showed a higher commitment to foraging than individuals from large eggs. In a natural setting, this should markedly increase predation risk of young originating from small eggs, particularly in poor environments. In contrast, when food was plentiful juveniles behaved similarly, irrespective of egg size. 5. Our results show that egg size affects juvenile growth trajectories and behaviour differently in different environments. While it is well‐established that a large egg size raises offspring fitness particularly in harsh environments, our study suggests that this advantage arises through risk‐averse behaviour being tightly linked to offspring size.
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