Adaptation to warm environments with a fast pace of life in a marine predatory snail

Understanding how latitudinal temperature variation shapes local adaptation of life-history strategies is crucial for predicting future responses to warming. Contrasting predictive frameworks explain how growth and other life-history traits may respond to differing selective pressures across latitude. However, these frameworks have rarely been explored within the context of fluctuating environmental temperatures across longer (i.e., seasonal) time scales experienced in nature. Furthermore, consequences of growth differences for other aspects of fitness, including reproductive output, remain unclear. Here, we conducted a long-term (17-month) laboratory experiment to examine local adaptation in two populations of the predatory marine snail Urosalpinx cinerea separated by 8.6° latitude (1000 km). We reared F1 offspring in a common-garden design under two seasonally fluctuating temperature regimes (“warm” and “cold”, simulating field thermal conditions experienced by low- and high-latitude populations, respectively), quantifying temporal patterns in growth, maturation, and reproductive output. We identified striking divergence in life-history strategies between populations in the warm regime, with offspring from the low-latitude population achieving greater growth in their first year, and high reproductive output coupled with reduced growth in their second year. In contrast, the high-latitude population grew slower in their first year, but eventually attained larger sizes in their second year, at the expense of reduced reproductive output. Responses in the cold regime followed similar population-specific life-history patterns to those in the warm regime, although growth and reproductive output was reduced in both populations. Our data provide support for adaptive divergence across latitude consistent with the pace-of-life syndrome hypothesis, with the low-latitude population selected for a fast-paced life characterized by rapid development and early reproduction. In contrast, the high-latitude population exhibited slower growth and delayed maturation. Our results highlight the potential limitations of short-term comparisons of growth that do not account for longer term processes, such as seasonal temperature variation and ontogenetic shifts in energy allocation, and imply a radical reshaping of physiological performance and life-history traits across populations under climate change.