Leafy and weedy seadragon genomes connect genic and repetitive DNA features to the extravagant biology of syngnathid fishes

Abstract

Seadragons are a remarkable lineage of teleost fishes in the family Syngnathidae, renowned for having evolved male pregnancy. Comprising three known species, seadragons are widely recognized and admired for their fantastical body forms and coloration, and their specific habitat requirements have made them flagship representatives for marine conservation and natural history interests. Until recently, a gap has been the lack of significant genomic resources for seadragons. We have produced gene-annotated, chromosome-scale genome models for the leafy and weedy seadragon to advance investigations of evolutionary innovation and elaboration of morphological traits in seadragons as well as their pipefish and seahorse relatives. We identified several interesting features specific to seadragon genomes, including divergent noncoding regions near a developmental gene important for integumentary outgrowth, a high genome-wide density of repetitive DNA, and recent expansions of transposable elements and a vesicular trafficking gene family. Surprisingly, comparative analyses leveraging the seadragon genomes and additional syngnathid and outgroup genomes revealed striking, syngnathid-specific losses in the family of fibroblast growth factors (FGFs), which likely involve reorganization of highly conserved gene regulatory networks in ways that have not previously been documented in natural populations. The resources presented here serve as important tools for future evolutionary studies of developmental processes in syngnathids and hold value for conservation of the extravagant seadragons and their relatives.

Genome rearrangements, male pregnancy and immunological tolerance – the curious case of the syngnathid immune system

“…In the genomes of the leafy seadragon (Phycodurus eques) and "weedy" seadragon (Phyllopteryx taeniolatus) seven gene families related to innate immunity experienced contractions, among them contractions in tripartite motif-containing (TRIM), immune-associated nucleotide-binding (IAN), and mannose receptor (MRC) gene families were identified, confirming previous reports in syngnathids (Small et al, 2022). The TRIM family of proteins are involved in many cellular processes, including within the immune system.…”

“…The last decade has seen the release of several high quality syngnathid genomes. Most of the studies focused around the genetics underlying syngnathid unique morphology and male pregnancy evolution (Small et al, 2016;Roth et al, 2020;Zhang et al, 2020;He et al, 2021;Li et al, 2021;Qu et al, 2021;Small et al, 2022). The genomes were fundamental to linking the loss of particular genes to a number of morphological traits such as the loss of mineralized teeth (loss of P/Q-rich scpp genes), pelvic fins (loss of tbx4) and ribs (HOX gene losses) (Lin et al, 2016;Small et al, 2016;Zhang et al, 2020;Qu et al, 2021).…”

“…A number of genome studies have used similar approaches, casting a wide net and looking at enriched GO terms or expanded protein families, rather than at selected individual genes or groups of genes (Small et al, 2016;Zhang et al, 2020;Qu et al, 2021;Small et al, 2022). Such an approach helps to look at a broader picture of syngnathid genome evolution, but cannot substitute a more detailed investigation of immune system components.…”

A comparative analysis of the ontogeny of syngnathids (pipefishes and seahorses) reveals how heterochrony contributed to their diversification

“…Examples are the elongated, fin-reduced bodies of the pipefishes, 1 the leaf-mimicking appendages of the leafy seadragons, 2,3 the curved body posture that permits upright swimming in seahorses, 4 and of course male pregnancy-a unique trait shared amongst syngnathids. 5,6 These and other outlandish novelties of the syngnathid lineage attract an ever-increasing scientific attention.…”

A comparative analysis of the ontogeny of syngnathids (pipefishes & seahorses) reveals how heterochrony contributed to their diversification

“…Syngnathids (pipefishes, pipe-horses and seahorses) are a globally distributed taxon of highly derived fishes that evolved a plethora of bizarre and unique phenotypes. Examples are the elongated, fin-reduced bodies of the pipefishes , 1 the leaf-mimicking appendages of the leafy seadragons, 2,3 the curved body posture that permits upright swimming in seahorses 4 , and of course male pregnancy -a unique trait shared amongst syngnathids. 5,6 These and other outlandish novelties of the syngnathid lineage attract an ever-increasing scientific attention .…”