Revisiting the ‘Marine Speciation Paradox’ using genomic, morphometric,
and ecological evidence in pipefish
Abstract
General theory predicts that ecological specialization should be rare in
marine ecosystems, given that barriers to dispersal are less effective
in the vastness of the sea compared to terrestrial settings. This
paradigm, however, hardly fits with classical theories of local
adaptation, leaving the question open of as to how marine diversity
could originate at a restricted spatial scale. We tackled this so-called
“Marine Speciation Paradox” by investigating how local specialization
could arise in a widely distributed marine species, the seaweed pipefish
Syngnathus schlegeli. We integrated morphological, genomic, and
niche-based evidences to unravel geographical structuring in S.
schlegeli populations. 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. The
north-to-south phylogeographical structuring was further corroborated by
ecological analyses. 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. We showed that the
effect of this historical segregation, in concert with niche-driven
ecological differentiation, lead to establishment of three distinct
clades across the widely distributed marine pipefish. Ultimately, our
study demonstrates that even the sea environment maintains the potential
for adaptive radiation and ecological specialization, suggesting that
‘marine speciation’ may actually be far from being ‘paradoxical’.