Horizontally Transferred Carotenoid Genes Associated with Light-Driven ATP Synthesis to Promote Cold Adaptation in...

The pea aphid, Acyrthosiphon pisum, possesses horizontally acquired fungal carotenoid biosynthesis genes, enabling de novo production of carotenoids. Although carotenoids are known to contribute to photo-protection and coloration, their potential role in energy metabolism and population fitness under thermal stress is still unclear. This study investigated the interactive effects of temperature and light intensity on energy homeostasis and life-history traits in A. pisum. Using controlled environmental regimes, we demonstrate that light intensity significantly influenced the ATP content, development, and reproductive output of A. pisum at 12 °C, but not at 22 °C. Under cold stress (12 °C), high light intensity (5000 lux) increased ATP content by 240%, shortened the pre-reproductive period by 46%, extended reproductive duration by 62%, and enhanced the net reproductive rate (R₀) and intrinsic rate of increase (rₘ) compared to low light intensity (200 lux). These effects were abolished at the optimal temperature (22 °C), indicating a temperature-gated, light-dependent mechanism. Demographic analyses revealed that carotenoid-associated solar energy harvesting significantly improves fitness under cold conditions, likely compensating for metabolic depression. Our findings reveal a novel ecological adaptation in aphids, where horizontally transferred genes may enable light-driven energy supplementation during thermal stress. This study provides new insights into the physiological mechanisms underlying insect resilience to climate variability and highlights the importance of light as a key environmental factor in shaping life-history strategies in temperate agroecosystems.