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.

Immunogenetic losses co-occurred with seahorse male pregnancy and mutation in tlx1 accompanied functional asplenia

“…The family Syngnathidae is a large (>350 species) and diverse clade of morphologically unique teleosts. They can be divided into two subfamilies: the Nerophinae and the Syngnathinae 22 , 23 . When assessing the mutation’s locus also in all other available members of the subfamily Syngnathinae, we detected that all investigated members of the genus Syngnathus (all with quite derived, closed brooding organs and closely related to seahorses 8 ) share the described mutation.…”

“…For now our understanding of the intricate immune challenges syngnathids face at different stages of male pregnancy is still incomplete, our study sheds light on the genetic basis of a major adaptive immunological novelty putatively associated with the evolution of sex-role reversal and male pregnancy in seahorses. Considering the entire syngnathid phylogeny, there is still deep divergence between the Hippocampus and Syngnathus lineages 23 , and the splenic phenotype and tlx1 gene sequence information of lineages more closely related to Hippocampus , which are missing in our study, would improve the resolution of the dataset and thus allow us to formulate better informed conclusions. Therefore, we encourage further studies filling these gaps in genomic knowledge.…”

<i>Kyonemichthys rumengani</i> (Teleostei: Syngnathidae) is Sister Taxon to the Pipefish Genus <i>Urocampus</i>: Genetic and Morphological Evidence

“…The sister taxa Kyonemichthys and Urocampus share numerous morphological synapomorphies indicating that the two genera are closely related, including meristics, trunk and tail ridge configurations, placement of dorsal fin on the tail, and presence of anal fin (Table 2; Dawson 1985;Gomon 2007;Araki and Motomura 2022). Siokunichthys, which is phylogenetically distant from Kyonemichthys and Urocampus (Hamilton et al 2017;Stiller et al 2022; this study) differs from the latter genera in the well-developed caudal fin (vs. absent or vestigial) and the absence of an anal fin and dermal appendages (vs. present) (Table 2). Although Kyonemichthys and Urocampus are recovered as sister taxa in our phylogenetic hypothesis (Fig.…”

“…The family Syngnathidae contains more than 300 species within 57 genera of predominantly small-bodied and cryptic marine fish (Dawson 1985;Hamilton et al 2017;Stiller et al 2022). The family is widely distributed in temperate and tropical habitats among mostly shallow coastal areas of the Atlantic and Indo-Pacific Oceans, including soft sediment habitats, seagrass beds, estuaries, coral and rocky reefs, and mangroves (Dawson 1985).…”

“…Similarly, the dorsal-fin origin on the tail is also shared with the distinct worm-like Siokunichthys Herald, 1953. As K. rumengani was not included in the comprehensive molecular phylogenies of the family Syngnathidae by Hamilton et al (2017) and Stiller et al (2022), its phylogenetic placement remains unknown. We therefore investigated the evolutionary relationships of K. rumengani within Syngnathidae, using a specimen of K. rumengani collected from Okinawa Island in the Ryukyu Islands, a region exhibiting high levels of syngnathid biodiversity, including 48 species belonging to 17 genera of syngnathid fishes (Senou 2013;Matsunuma et al 2013;Yoshigou 2014;Wibowo and Motomura 2017;Araki et al 2020;Motomura and Uehara 2020;Araki and Motomura 2022).…”