Convergent evolution of extreme snout elongation in deep-sea fishes reveals constrained trajectories

Abstract

Phenotypic extremes are scattered across the Tree of Life, suggesting that evolutionary constraints often limit their emergence. Yet striking departures from standard body plans, such as elongate snouts, have evolved convergently across deep time. We investigate extreme morphologies in two distantly related deep-sea fish clades: spikefishes (pufferfish relatives) and snipefishes (seahorse relatives). Using spikefishes as a study system, including all 24 living and fossil species, we integrated genome-wide phylogenomic data with a fossil and extant morphological character matrix, skull shape and dentition analyses from 64 CT scans, phenotypic and divergence matrices from >200 X-rays, functional manipulations of freshly collected and cleared-and-stained specimens, and formal convergence test across 300 percomorph species. We show that snout elongation evolved independently twice within spikefishes, reaching intermediate and extreme conditions along one predictable, ordered trajectory of additive skeletal rearrangements. Snout bones form a highly integrated, semi-autonomous module that channels evolutionary change along intrinsic lines of least resistance, coinciding with accelerated cranial evolution and expanded morphospaces in a clade with enhanced cranial mobility. Snipefishes converge on the same body plan through largely non-homologous elements and distinct linkage mechanics, except for near-identical vomer convergence. Extreme morphologies can emerge when phenotypic integration aligns with functional innovation, guiding evolution along repeatable trajectories.