Abstract
BackgroundThe 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.ResultsAn 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.ConclusionThis 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.
Highlights
The seacoasts of the Japanese Arc are fringed by many gravel beaches owing to active tectonic uplift and intense denudation caused by heavy rainfall
Luciogobius elongatus had the highest number of clades, while L. guttatus was separated into three clades, and the others were each grouped into two clades
The divergent clades within each species formed a monophyletic group, except for L. guttatus, which was not recovered as monophyletic in the cytochrome b (Cyt b) tree
Summary
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. Gobies of the East Asian genus Luciogobius have elongated, flexible bodies and are adapted to inhabit the dynamic sediment of gravel beaches (Figure 1) [6,7,8,9,10,11]. 11 Luciogobius species have been described from the Japanese Arc, Taiwan, Hainan Island, Hong Kong, and the southernmost seacoasts of the Russian Far East and Korean Peninsula (Figure 2). Five of the 11 species are strongly associated with well-sorted gravel beach sediment and are strictly interstitial [11,16,17,18,19] (Table 1); they reside within the gravel throughout their life after a pelagic larval stage and prey on interstitial invertebrates [16,17,18,19]
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