Adaptive radiation of gobies in the interstitial habitats of gravel beaches accompanied by body elongation and excessive vertebral segmentation

Abstract Background The seacoasts of the Japanese Arc are fringed by many gravel beaches owing to active tectonic uplift and intense denudation caused by heavy rainfall. These gravel beaches are inhabited by gobies of the genus Luciogobius that burrow into the gravel sediment and live interstitially. Although their habitat and morphology (e. g., reduced fins, elongated, scale-less body, and highly segmented vertebral column) are highly unusual among fishes, little is known on how their morphological evolution has facilitated the colonization of interstitial habitats and promoted extensive diversification. We conducted thorough sampling of Luciogobius and related species throughout Japan, and performed molecular phylogenetic analysis to explore the patterns of morphological evolution associated with gravel beach colonization. Results An analysis of the mitochondrial cytochrome b gene suggested a remarkable diversity of previously unrecognized species. The species-level phylogeny based on six protein-coding nuclear genes clearly indicated that interstitial species cluster into two distinct clades, and that transitions from benthic or demersal habits to interstitial habits are strongly correlated with an increase in vertebral number. Colonization of gravel beach habitats is estimated to have occurred ca. 10 Ma, which coincides with the period of active orogenesis of the Japanese landmass. Different species of interstitial Luciogobius inhabit sediments with different granulometric properties, suggesting that microhabitat partitioning has been an important mechanism facilitating speciation in these fishes. Conclusion This is the first study to document the adaptation to interstitial habitats by a vertebrate. Body elongation and excessive vertebral segmentation had been the key aspects enhancing body flexibility and fishes' ability to burrow into the gravel sediment. The rich diversity of coastal gravel habitats of the Japanese Arc has likely promoted the adaptive radiation of these unique gravel-dwelling fishes.