Phylogenomics and Historical Biogeography of Seahorses, Dragonets, Goatfishes, and Allies (Teleostei: Syngnatharia): Assessing Factors Driving Uncertainty in Biogeographic Inferences

Abstract

The charismatic trumpetfishes, goatfishes, dragonets, flying gurnards, seahorses, and pipefishes encompass a recently defined yet extraordinarily diverse clade of percomorph fishes—the series Syngnatharia. This group is widely distributed in tropical and warm-temperate regions, with a great proportion of its extant diversity occurring in the Indo-Pacific. Because most syngnatharians feature long-range dispersal capabilities, tracing their biogeographic origins is challenging. Here, we applied an integrative phylogenomic approach to elucidate the evolutionary biogeography of syngnatharians. We built upon a recently published phylogenomic study that examined ultraconserved elements by adding 62 species (total 169 species) and one family (Draconettidae), to cover ca. 25% of the species diversity and all 10 families in the group. We inferred a set of time-calibrated trees and conducted ancestral range estimations. We also examined the sensitivity of these analyses to phylogenetic uncertainty (estimated from multiple genomic subsets), area delimitation, and biogeographic models that include or exclude the jump-dispersal parameter (j). Of the three factors examined, we found that the j parameter has the strongest effect in ancestral range estimates, followed by number of areas defined, and tree topology and divergence times. After accounting for these uncertainties, our results reveal that syngnatharians originated in the ancient Tethys Sea ca. 87 Ma (84–94 Ma; Late Cretaceous) and subsequently occupied the Indo-Pacific. Throughout syngnatharian history, multiple independent lineages colonized the eastern Pacific (6–8 times) and the Atlantic (6–14 times) from their center of origin, with most events taking place following an east-to-west route prior to the closure of the Tethys Seaway ca. 12–18 Ma. Ultimately, our study highlights the importance of accounting for different factors generating uncertainty in macroevolutionary and biogeographic inferences.

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

“…The placement of Syngnathidae within Syngnathiformes, a taxonomically, morphologically, and ecologically diverse group (comprising the families Pegasidae, Callionymidae, Dactylopteridae, Draconettidae, Mullidae, Centriscidae, Fistulariidae, Aulostomidae, Solenostomidae, and Syngnathidae) is now well established [ 8 – 11 ]. Syngnathids share ovoviviparity with their sister group, the ghost pipefishes (Solenostomidae), though the female broods the eggs in modified pelvic fins in the latter clade.…”

“…The taxonomically best sampled phylogeny included 91 species of syngnathids [ 44 ]; however, only a few mitochondrial and nuclear genes were analyzed, resulting in low resolution of some principal branches. Phylogenomic studies using genome-wide ultraconserved elements (UCEs) across Syngnathiformes resulted in largely robust relationships but were limited in their taxon sampling of Syngnathidae [ 9 , 11 ]. A total of 57 syngnathid species were sampled by [ 9 ], to which 14 species were added [ 11 ] leaving ca.…”

“…Phylogenomic studies using genome-wide ultraconserved elements (UCEs) across Syngnathiformes resulted in largely robust relationships but were limited in their taxon sampling of Syngnathidae [ 9 , 11 ]. A total of 57 syngnathid species were sampled by [ 9 ], to which 14 species were added [ 11 ] leaving ca. 3/4 of the described species diversity unsampled.…”

“…This undersampling also concerns extinct species of Syngnathidae and Syngnathiformes, for which a relatively good fossil record exists particularly from the former Tethys Sea because their outer bony plates fossilize well [ 46 – 48 ]. However, prior attempts to estimate divergence times focused primarily on seahorse fossils from the Miocene for time calibration [ 11 , 49 ], omitting a substantial number of other fossil taxa.…”

Incorporating Topological and Age Uncertainty into Event-Based Biogeography of Sand Spiders Supports Paleo-Islands in Galapagos and Ancient Connections among Neotropical Dry Forests

“…Similar pipelines have been incorporated into RASP (S-DIVA; [23]) and BioGeoBEARS (using the run_bears_optim_on_multiple_trees function). These functions summarize estimates of ancestral ranges of several trees on a target tree, such as a majority-rule consensus (as output by e.g., MrBayes) or a maximum clade credibility tree (MCC tree; as output by e.g., BEAST) and are routinely employed by researchers interested in incorporating phylogenetic uncertainty (e.g., [24,25]). However, the results are summarized in a single tree, and the underlying variability in the estimates is difficult to grasp.…”