Colonization Dynamics Explain the Decoupling of Species Richness and Morphological Disparity in Syngnatharian Fishes across Oceans

AbstractA clear longitudinal gradient in species richness across oceans is observed in extant marine fishes, with the Indo-Pacific exhibiting the greatest diversity. Three non-mutually-exclusive evolutionary hypotheses have been proposed to explain this diversity gradient: time for speciation, center of accumulation, and in situ diversification rates. Using the morphologically disparate syngnatharians (seahorses, dragonets, goatfishes, and relatives) as a study system, we tested these hypotheses and additionally assessed whether patterns of morphological diversity are congruent with species richness patterns. We used well-sampled phylogenies and a suite of phylogenetic comparative methods (including a novel phylogenetically corrected Kruskal-Wallis test) that account for various sources of uncertainty to estimate rates of lineage diversification and morphological disparity within all three major oceanic realms (Indo-Pacific, Atlantic, and eastern Pacific), as well as within the Indo-Pacific region. We find similar lineage diversification rates across regions, indicating that increased syngnatharian diversity in the Indo-Pacific is due to earlier colonizations from the Tethys Sea followed by in situ speciation and more frequent colonizations during the Miocene coinciding with the formation of coral reefs. These results support both time for speciation and center of accumulation hypotheses. Unlike species richness unevenness, shape disparity and evolutionary rates are similar across oceans because of the early origin of major body plans and their subsequent spread via colonization rather than in situ evolution. Our results illustrate how species richness patterns became decoupled from morphological disparity patterns during the formation of a major biodiversity hot spot.