Proteomic Differences Reveal Early Development of Contrasting Energetic Strategies Between Divergent Migratory Ecotypes in Three-Spined Stickleback

Abstract

Divergence in migratory behaviour represents a striking and common axis of life-history variation in animals. Plastic changes in adult animals in preparation for migration are well known, but the differences in early development between migratory and non-migratory forms are not well documented. These differences might contribute to reproductive isolation because of the potentially substantial divergence in metabolism and physiology. Here we document substantial differences between migratory ecotypes in sarcomeric development and energetic pathways from immediately after hatching. On North Uist (Scottish Western Isles), migratory and non-migratory (‘resident’) three-spined stickleback (Gasterosteus aculeatus) ecotypes breed in sympatry in brackish lagoons, providing an ideal system for investigating early developmental and energetic strategies associated with migration. Using relative-quantitative proteomics, we compared protein abundance in migratory, resident and reciprocal hybrid crosses of the three-spined stickleback 2 days after hatching. Migratory stickleback exhibited higher abundance of muscle, metabolic and collagen-associated proteins, indicating early investment in growth and preparation for the energetic demands of migration and sustained swimming. In contrast, resident stickleback showed increased abundance of maternal provisioning proteins, delayed hatching and higher hatching success, consistent with a strategy of producing fewer but high-quality offspring. Hybrids generally exhibited intermediate protein abundances, but there was some evidence of negative transgression in proteins related to mitochondrial function which might contribute to reduced fitness through mitonuclear incompatibility. Together, these results reveal early biochemical differences consistent with divergent energy allocation and reproductive strategies between migratory and resident stickleback.