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Seahorses have a specialized morphology that includes a toothless tubular mouth, a body covered with bony plates, a male brood pouch, and the absence of caudal and pelvic fins. Here we report the sequencing and de novo assembly of the genome of the tiger tail seahorse, Hippocampus comes . Comparative genomic analysis identifies higher protein and nucleotide evolutionary rates in H. comes compared with other teleost fish genomes. We identified an astacin metalloprotease gene family that has undergone expansion and is highly expressed in the male brood pouch. We also find that the H. comes genome lacks enamel matrix protein-coding proline/glutamine-rich secretory calcium-binding phosphoprotein genes, which might have led to the loss of mineralized teeth. tbx4 , a regulator of hindlimb development, is also not found in H. comes genome. Knockout of tbx4 in zebrafish showed a ‘pelvic fin-loss’ phenotype similar to that of seahorses. Here, the genome sequence of the tiger tail seahorse is reported and comparative genomic analyses with other ray-finned fishes are used to explore the genetic basis of the unique morphology and reproductive system of the seahorse. Evolution at a gallop Seahorses are prime examples of the exuberance of evolution and are unique among bony fish on several counts, including their equine body shape and male brood pouch. An international collaboration reporting in this issue of Nature has determined the genome sequence of a seahorse ( Hippocampus comes , the tiger tail seahorse). They find it to be the most rapidly evolving fish genome studied so far. H. comes is among the most commonly traded seahorse species—dried for traditional medicines and live for the aquarium trade—and is on the IUCN Red List as a 'vulnerable' species. Analysis of the genomic sequence provides insights into the evolution of its unique morphology. Of note is the absence of a master control gene, tbx4 , which functions in the development of hindlimbs and pelvic fins. Pelvic fins are missing in seahorses, and tbx4 -knockout mutant zebrafish also lack pelvic fins.

Seahorses have a circum-global distribution in tropical to temperate coastal waters. Yet, seahorses show many adaptations for a sedentary, cryptic lifestyle: they require specific habitats, such as seagrass, kelp or coral reefs, lack pelvic and caudal fins, and give birth to directly developed offspring without pronounced pelagic larval stage, rendering long-range dispersal by conventional means inefficient. Here we investigate seahorses’ worldwide dispersal and biogeographic patterns based on a de novo genome assembly of Hippocampus erectus as well as 358 re-sequenced genomes from 21 species. Seahorses evolved in the late Oligocene and subsequent circum-global colonization routes are identified and linked to changing dynamics in ocean currents and paleo-temporal seaway openings. Furthermore, the genetic basis of the recurring “bony spines” adaptive phenotype is linked to independent substitutions in a key developmental gene. Analyses thus suggest that rafting via ocean currents compensates for poor dispersal and rapid adaptation facilitates colonizing new habitats. A new seahorse genome and the re-sequenced genomes of 21 other species shed new light on the evolutionary origin and global dispersal routes of seahorses, and show that bony spines—a key adaptation against predation—probably evolved multiple times via independent substitutions in the bmp3 gene.

Background The experimental approach to the evolution and development of the vertebrate skeleton has to a large extent relied on “direct-developing” amniote model organisms, such as the mouse and the chicken. These organisms can however only be partially informative where it concerns secondarily lost features or anatomical novelties not present in their lineages. The widely used anamniotes Xenopus and zebrafish are “indirect-developing” organisms that proceed through an extended time as free-living larvae, before adopting many aspects of their adult morphology, complicating experiments at these stages, and increasing the risk for lethal pleiotropic effects using genetic strategies. Results Here, we provide a detailed description of the development of the osteology of the African mouthbrooding cichlid Astatotilapia burtoni , primarily focusing on the trunk (spinal column, ribs and epicentrals) and the appendicular skeleton (pectoral, pelvic, dorsal, anal, caudal fins and scales), and to a lesser extent on the cranium. We show that this species has an extremely “direct” mode of development, attains an adult body plan within 2 weeks after fertilization while living off its yolk supply only, and does not pass through a prolonged larval period. Conclusions As husbandry of this species is easy, generation time is short, and the species is amenable to genetic targeting strategies through microinjection, we suggest that the use of this direct-developing cichlid will provide a valuable model system for the study of the vertebrate body plan, particularly where it concerns the evolution and development of fish or teleost specific traits. Based on our results we comment on the development of the homocercal caudal fin, on shared ontogenetic patterns between pectoral and pelvic girdles, and on the evolution of fin spines as novelty in acanthomorph fishes. We discuss the differences between “direct” and “indirect” developing actinopterygians using a comparison between zebrafish and A. burtoni development.

ABSTRACT Transgenerational immune priming (TGIP) adjusts offspring's immune responses based on parental immunological experiences. It is predicted to be adaptive when parent–offspring environmental conditions match, while mismatches negate those advantages, rendering TGIP potentially costly. We tested these cost–benefit dynamics in the pipefish Syngnathus typhle (Syngnathidae). Because of their unique male pregnancy, egg production and rearing occur in different sexes, providing both parents multiple avenues for TGIP. Parental bacteria exposure in our pipefish was simulated through vaccinations with heat‐killed Vibrio aestuarianus before mating the fish to each other or to controls. The resulting offspring were exposed to V. aestuarianus in control or heat stress environments, after which transcriptome and microbiome compositions were investigated. Transcriptomic TGIP effects were only observed in Vibrio‐exposed offspring at control temperatures, arguing for low costs of TGIP in non‐matching microbiota environments. Transcriptomic phenotypes elicited by maternal and paternal TGIP had limited overlap and were not additive. Parentally induced transcriptomic responses were associated with immune functions, and specifically, the paternal response to the innate immune branch, possibly hinting at trained immunity. TGIP of both parents reduced the relative abundance of the experimental Vibrio in exposed offspring, showcasing its ecological benefits. Despite TGIP's significance in matching biotic environments, no TGIP‐associated phenotypes were observed for heat‐treated offspring, illustrating its limitations. Heat spikes caused by climate change thus threaten TGIP benefits, potentially increasing susceptibility to emerging marine diseases. We demonstrate the urgent need to understand how animals cope with climate‐induced changes in microbial assemblages to assess their vulnerability in light of climate change. Transgenerational immune priming allows parents to prepare their offspring for the microbial environment they will be released into. Using transcriptomics and microbiome analyses, we show that the male pregnant pipefish Syngnathus typhle primes its offspring after parental vaccination with Vibrio bacteria, that priming is effective in reducing Vibrio abundance after a contact with the offspring after release, and that this priming is Vibrio‐specific and not costly if the specific Vibrio is not encountered by the offspring. We also show that this mechanism is losing its effectiveness under heat stress conditions, arguing for the threat heat waves pose for inhabitants of shallow coastal habitats, such as the seagrass meadows inhabited by S. typhle.

With over 18,000 species, the Acanthomorpha, or spiny-rayed fishes, form the largest and arguably most diverse radiation of vertebrates. One of the key novelties that contributed to their evolutionary success are the spiny rays in their fins that serve as a defense mechanism. We investigated the patterning mechanisms underlying the differentiation of median fin Anlagen into discrete spiny and soft-rayed domains during the ontogeny of the direct-developing cichlid fish Astatotilapia burtoni. Distinct transcription factor signatures characterize these two fin domains, whereby mutually exclusive expression of hoxa13a/b with alx4a/b and tbx2b marks the spine to soft-ray boundary. The soft-ray domain is established by BMP inhibition via gremlin1b, which synergizes in the posterior fin with shh secreted from a zone of polarizing activity. Modulation of BMP signaling by chemical inhibition or gremlin1b CRISPR/Cas9 knockout induces homeotic transformations of spines into soft rays and vice versa. The expression of spine and soft-ray genes in nonacanthomorph fins indicates that a combination of exaptation and posterior expansion of an ancestral developmental program for the anterior fin margin allowed the evolution of robustly individuated spiny and soft-rayed domains. We propose that a repeated exaptation of such pattern might underly the convergent evolution of anterior spinyfin elements across fishes.

The two toothed jaws of cichlid fishes provide textbook examples of convergent evolution. Tooth phenotypes such as enlarged molar-like teeth used to process hard-shelled mollusks have evolved numerous times independently during cichlid diversification. Although the ecological benefit of molar-like teeth to crush prey is known, it is unclear whether the same molecular mechanisms underlie these convergent traits. To identify genes involved in the evolution and development of enlarged cichlid teeth, we performed RNA-seq on the serially homologous-toothed oral and pharyngeal jaws as well as the fourth toothless gill arch of Astatoreochromis alluaudi. We identified 27 genes that are highly upregulated on both tooth-bearing jaws compared with the toothless gill arch. Most of these genes have never been reported to play a role in tooth formation. Two of these genes (unk, rpfA) are not found in other vertebrate genomes but are present in all cichlid genomes. They also cluster genomically with two other highly expressed tooth genes (odam, scpp5) that exhibit conserved expression during vertebrate odontogenesis. Unk and rpfA were confirmed via in situ hybridization to be expressed in developing teeth of Astatotilapia burtoni. We then examined expression of the cluster’s four genes in six evolutionarily independent and phylogenetically disparate cichlid species pairs each with a large- and a small-toothed species. Odam and unk commonly and scpp5 and rpfA always showed higher expression in larger toothed cichlid jaws. Convergent trophic adaptations across cichlid diversity are associated with the repeated developmental deployment of this genomic cluster containing conserved and novel cichlid-specific genes.

Cichlid fishes provide textbook examples of explosive phenotypic diversification and sympatric speciation, thereby making them ideal systems for studying the molecular mechanisms underlying rapid lineage divergence. Despite the fact that gene regulation provides a critical link between diversification in gene function and speciation, many genomic regulatory mechanisms such as microRNAs (miRNAs) have received little attention in these rapidly diversifying groups. Therefore, we investigated the posttranscriptional regulatory role of miRNAs in the repeated sympatric divergence of Midas cichlids (Amphilophus spp.) from Nicaraguan crater lakes. Using miRNA and mRNA sequencing of embryos from five Midas species, we first identified miRNA binding sites in mRNAs and highlighted the presences of a surprising number of novel miRNAs in these adaptively radiating species. Then, through analyses of expression levels, we identified putative miRNA/gene target pairs with negatively correlated expression level that were consistent with the role of miRNA in downregulating mRNA. Furthermore, we determined that several miRNA/gene pairs show convergent expression patterns associated with the repeated benthic/limnetic sympatric species divergence implicating these miRNAs as potential molecular mechanisms underlying replicated sympatric divergence. Finally, as these candidate miRNA/gene pairs may play a central role in phenotypic diversification in these cichlids, we characterized the expression domains of selected miRNAs and their target genes via in situ hybridization, providing further evidence that miRNA regulation likely plays a role in the Midas cichlid adaptive radiation. These results provide support for the hypothesis that extremely quickly evolving miRNA regulation can contribute to rapid evolutionary divergence even in the presence of gene flow.

MicroRNAs (miRNAs) play crucial roles in the post-transcriptional control of messenger RNA (mRNA). These miRNA-mRNA regulatory networks are present in nearly all organisms and contribute to development, phenotypic divergence, and speciation. To examine the miRNA landscape of cichlid fishes, one of the most species-rich families of vertebrates, we profiled the expression of both miRNA and mRNA in a diverse set of cichlid lineages. Among these, we found that conserved miRNAs differ from recently arisen miRNAs (i.e. lineage specific) in average expression levels, number of target sites, sequence variability, and physical clustering patterns in the genome. Furthermore, conserved miRNA target sites tend to be enriched at the 5′ end of protein-coding gene 3′ UTRs. Consistent with the presumed regulatory role of miRNAs, we detected more negative correlations between the expression of miRNA-mRNA functional pairs than in random pairings. Finally, we provide evidence that novel miRNA targets sites are enriched in genes involved in protein synthesis pathways. Our results show how conserved and evolutionarily novel miRNAs differ in their contribution to the genomic landscape and highlight their particular evolutionary roles in the adaptive diversification of cichlids.

Trans-generational immune priming (TGIP) adjusts offspring immune responses based on parental immunological experiences - a form of trans-generational plasticity predicted to be adaptive when parent-offspring environmental conditions match. In contrast, mis-matches between environmental conditions negate those advantages, rendering TGIP costly when mismatched immunological offspring phenotypes are induced. Particularly maternal TGIP was thought to shape offspring immunological preparedness: mothers’ eggs contain more substance than sperm and, in viviparous species, pregnancy provides additional avenues for immune priming of developing offspring. The syngnathids’ (pipefishes and seahorses) unique male pregnancy provides an unusual perspective to the ecological relevance of TGIP in a system where egg production and pregnancy occur in different sexes. We simulated parental bacteria exposure in broad nosed pipefish, Syngnathus typhle, through vaccinations with heat-killed Vibrio aestuarianus before mating the fish to each other or control individuals. Resulting offspring were raised, and some exposed to V. aestuarianus, in a control or heat-stress environment, after which transcriptome and microbiome compositions were investigated. Transcriptomic TGIP effects were only observed in Vibrio-exposed offspring at control temperatures, arguing for low costs of TGIP in non-matching environments. Transcriptomic phenotypes elicited by maternal and paternal TGIP had only limited overlap and were not additive. Both transcriptomic responses were significantly associated to immune functions, and specifically the paternal response to the innate immune branch. TGIP of both parents reduced the relative abundance of the experimental Vibrio in exposed offspring, showcasing its ecological effectiveness. Despite its significance in matching biotic environments, no TGIP-associated phenotypes were observed for heat-treated offspring. Heat-spikes caused by climate change thus threaten TGIP benefits, potentially increasing susceptibility to emerging marine diseases. This highlights the urgent need to understand how animals will cope with climate-induced changes in microbial assemblages by illustrating the importance – and limits - of TGIP in mitigating the impacts of environmental stressors on offspring vulnerability.

Immune cells at sites of inflammation are continuously activated by local antigens and cytokines, and regulatory mechanisms must be enacted to control inflammation. The stepwise hydrolysis of extracellular ATP by ectonucleotidases CD39 and CD73 generates adenosine, a potent immune suppressor. Here we report that human effector CD8 T cells contribute to adenosine production by releasing CD73-containing extracellular vesicles upon activation. These extracellular vesicles have AMPase activity, and the resulting adenosine mediates immune suppression independently of regulatory T cells. In addition, we show that extracellular vesicles isolated from the synovial fluid of patients with juvenile idiopathic arthritis contribute to T cell suppression in a CD73-dependent manner. Our results suggest that the generation of adenosine upon T cell activation is an intrinsic mechanism of human effector T cells that complements regulatory T cell-mediated suppression in the inflamed tissue. Finally, our data underscore the role of immune cell-derived extracellular vesicles in the control of immune responses. Ectonucleotidases associated to regulatory T cells are known modulators in the inflammatory environment. Here the authors describe CD8 T cell-derived extracellular vesicles bearing CD73 and suggest they function as an additional intrinsic modulator of immune responses.