Fluctuating salinity during development impacts fish life histories

Climate change and human activities are elevating the level and variability of salinity in freshwater ecosystems. Consequently, many aquatic species now experience more extreme developmental environments. Resultant shifts in developmental trajectories could change key life-history traits that persist into adulthood. The 'silver spoon' hypothesis posits that favourable developmental conditions lead to faster growth, earlier maturation and greater reproductive success. In contrast, the 'predictable adaptive response' hypothesis suggests that faster growth and earlier reproduction should be selected for under stressful developmental conditions because stress provides cues about a higher risk of mortality in future environments. To understand life-history responses to salinity during development, we reared a global pest, mosquitofish (Gambusia holbrooki), from birth in either freshwater control (0‰), stable-saline (10‰), or fluctuating-saline environments (0‰-20‰; mean = 10‰) until maturation. We then monitored their performance in early and late adulthood in a common garden setting. Fish in fluctuating salinity grew more slowly and had a reduced reproductive output (lower sperm count, smaller eggs) than those in stable elevated salinity. These differences are consistent with a more stable environment providing a 'silver spoon' effect. Conversely, fish in stable elevated salinity grew faster and matured earlier than those in freshwater, supporting a 'predictive adaptive response' whereby salinity is a stressor triggering faster development and accelerates reproduction. In addition, fluctuations in salinity altered the effect of higher salinity on self-maintenance. Stable elevated salinity caused a decrease in male telomere length and female gut length, but fluctuating salinity caused an increase in female gut length. Our results suggest that fluctuating versus stable salinity during development leads to distinct fish life histories. The effect sizes for some traits differed significantly between males and females, suggesting sex-specific responses to climate fluctuations.