Phylogenomic analysis of Syngnathidae reveals novel relationships, origins of endemic diversity and variable diversification rates

Abstract Background Seahorses, seadragons, pygmy pipehorses, and pipefishes (Syngnathidae, Syngnathiformes) are among the most recognizable groups of fishes because of their derived morphology, unusual life history, and worldwide distribution. Despite previous phylogenetic studies and recent new species descriptions of syngnathids, the evolutionary relationships among several major groups within this family remain unresolved. Results Here, we provide a reconstruction of syngnathid phylogeny based on genome-wide sampling of 1314 ultraconserved elements (UCEs) and expanded taxon sampling to assess the current taxonomy and as a basis for macroevolutionary insights. We sequenced a total of 244 new specimens across 117 species and combined with published UCE data for a total of 183 species of Syngnathidae, about 62% of the described species diversity, to compile the most data-rich phylogeny to date. We estimated divergence times using 14 syngnathiform fossils, including nine fossils with newly proposed phylogenetic affinities, to better characterize current and historical biogeographical patterns, and to reconstruct diversification through time. We present a phylogenetic hypothesis that is well-supported and provides several notable insights into syngnathid evolution. We found nine non-monophyletic genera, evidence for seven cryptic species, five potentially invalid synonyms, and identified a novel sister group to the seahorses, the Indo-Pacific pipefishes Halicampus macrorhynchus and H. punctatus. In addition, the morphologically distinct southwest Pacific seahorse Hippocampus jugumus was recovered as the sister to all other non-pygmy seahorses. As found in many other groups, a high proportion of syngnathid lineages appear to have originated in the Central Indo-Pacific and subsequently dispersed to adjoining regions. Conversely, we also found an unusually high subsequent return of lineages from southern Australasia to the Central Indo-Pacific. Diversification rates rose abruptly during the Middle Miocene Climate Transition and peaked after the closure of the Tethys Sea. Conclusions Our results reveal a previously underappreciated diversity of syngnathid lineages. The observed biogeographic patterns suggest a significant role of the southern Australasian region as a source and sink of lineages. Shifts in diversification rates imply possible links to declining global temperatures, the separation of the Atlantic and Pacific faunas, and the environmental changes associated with these events.