Exploring ecological specialization in pipefish using genomic, morphometric and ecological evidence

Aim Theory predicts that ecological specialization should be rare in marine ecosystems, given that dispersal barriers are less effective in the vastness of the sea compared with those in terrestrial settings. This paradigm, however, hardly fits with classical theories of local adaptation, raising the question of how marine diversity originates in a highly interconnected system. In the present study, we investigated how ecological specialization arises in a widely distributed marine species, the seaweed pipefish Syngnathus schlegeli . Location Chinese coastal waters. Methods We integrated morphological (geometric morphometry), genetic (RADseq) and ecological (species distribution models and n ‐dimensional hypervolumes) evidence to shed light on population structuring in S. schlegeli . Results We revealed the existence of a north‐to‐south phenotypic gradient in eye size among S. schlegeli populations. This morphological differentiation was paralleled by genetic divergence, with South China Sea populations emerging as relatively independent. We further investigated the ecological differentiation of S. schlegeli populations. We observed high niche differentiation among northern, central and southern populations, resulting from both niche expansion and niche shift processes. Projected habitat suitability onto the Last Glacial Maximum revealed the existence of historical barriers to dispersal between the South and East China seas. Main conclusions We showed that the effect of this historical segregation, in concert with niche‐driven ecological differentiation, might lead to the establishment of three distinct clades across the widely distributed marine pipefish. Ultimately, our study demonstrates that even the high connected sea environment maintains the potential for ecological specialization.