Absence of major histocompatibility complex class II mediated immunity in pipefish,
            <i>Syngnathus typhle</i>
            : evidence from deep transcriptome sequencing

Haase, David; Roth, Olivia; Kalbe, Martin; Schmiedeskamp, Gisela; Scharsack, Jörn P.; Rosenstiel, Philip; Reusch, Thorsten B. H.

doi:10.1098/rsbl.2013.0044

Cited by 73 publications

(65 citation statements)

References 26 publications

(36 reference statements)

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“…Furthermore, genes in KEGG pathways associated with the adaptive immune system, including “antigen processing and presentation,” “T cell receptor signaling pathway,” and “B cell receptor signaling pathway,” were transcriptionally less sensitive to pregnancy status than those in innate immunity KEGG pathways (Additional file 1: Figure S6b). Consistent with a characterization of the immune gene repertoire in Syngnathus typhle [51], we failed to detect MHC class II alpha and beta chain genes in the genome of S. scovelli , so the potential for some functionality of the adaptive immune system in this pipefish genus may be limited in general.…”

Section: Resultssupporting

confidence: 85%

“…Prior to our characterization of the Gulf pipefish genome, however, with the exception of a few transcriptomic resources [51, 52, 54], virtually no information existed for how key developmental genes and their modification might be responsible for derived syngnathid phenotypes. Now, with the availability of the genome of Syngnathus scovelli , and likely other related genomes soon to follow, we expect researchers interested in the developmental genetic underpinnings of novel vertebrate morphologies to make the critical experimental connections between genomic differences in syngnathids and their functional consequences.…”

Section: Discussionmentioning

confidence: 99%

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The genome of the Gulf pipefish enables understanding of evolutionary innovations

et al. 2016

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BackgroundEvolutionary origins of derived morphologies ultimately stem from changes in protein structure, gene regulation, and gene content. A well-assembled, annotated reference genome is a central resource for pursuing these molecular phenomena underlying phenotypic evolution. We explored the genome of the Gulf pipefish (Syngnathus scovelli), which belongs to family Syngnathidae (pipefishes, seahorses, and seadragons). These fishes have dramatically derived bodies and a remarkable novelty among vertebrates, the male brood pouch.ResultsWe produce a reference genome, condensed into chromosomes, for the Gulf pipefish. Gene losses and other changes have occurred in pipefish hox and dlx clusters and in the tbx and pitx gene families, candidate mechanisms for the evolution of syngnathid traits, including an elongated axis and the loss of ribs, pelvic fins, and teeth. We measure gene expression changes in pregnant versus non-pregnant brood pouch tissue and characterize the genomic organization of duplicated metalloprotease genes (patristacins) recruited into the function of this novel structure. Phylogenetic inference using ultraconserved sequences provides an alternative hypothesis for the relationship between orders Syngnathiformes and Scombriformes. Comparisons of chromosome structure among percomorphs show that chromosome number in a pipefish ancestor became reduced via chromosomal fusions.ConclusionsThe collected findings from this first syngnathid reference genome open a window into the genomic underpinnings of highly derived morphologies, demonstrating that de novo production of high quality and useful reference genomes is within reach of even small research groups.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1126-6) contains supplementary material, which is available to authorized users.

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Section: Resultssupporting

confidence: 85%

Section: Discussionmentioning

confidence: 99%

The genome of the Gulf pipefish enables understanding of evolutionary innovations

et al. 2016

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“…Their taxonomic diversity is matched by extensive genetic and phenotypic variation, including novel immunological strategies. Although the functionality of the adaptive immune system has been considered to be conserved since its emergence in the ancestor of all jawed vertebrates 2,3 , fundamental modifications of the immune gene repertoire have recently been reported in teleosts [4][5][6][7] . One of the most dramatic changes has occurred in Atlantic cod (Gadus morhua), involving complete loss of the MHC II pathway that is otherwise responsible for the detection of bacterial pathogens in vertebrates 4 .…”

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Evolution of the immune system influences speciation rates in teleost fishes

et al. 2016

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With over 32,000 extant species 1 , teleost fishes comprise the majority of vertebrate species. Their taxonomic diversity is matched by extensive genetic and phenotypic variation, including novel immunological strategies. Although the functionality of the adaptive immune system has been considered to be conserved since its emergence in the ancestor of all jawed vertebrates 2,3 , fundamental modifications of the immune gene repertoire have recently been reported in teleosts [4][5][6][7] . One of the most dramatic changes has occurred in Atlantic cod (Gadus morhua), involving complete loss of the MHC II pathway that is otherwise responsible for the detection of bacterial pathogens in vertebrates 4 . Moreover, this loss is accompanied by a substantially enlarged repertoire of MHC I genes, which normally encode molecules for protection against viral pathogens. It has thus been hypothesized that the expanded MHC I repertoire of cod evolved as a compensatory mechanism, whereby broader MHC I functionality makes up for the initial loss of MHC II (refs. 4,6). However, the questions of how and when MHC II was lost relative to the MHC I expansion, and whether these genomic modifications are causally related, have so far remained unresolved.As key components of the vertebrate adaptive immune system, the complex MHC pathways and their functionality are now well characterized 8-10 , but less is known about the causes of MHC copy number variation, which poses an immunological tradeoff 11,12 . Although an increase in the number of MHC genes facilitates pathogen detection, it will also decrease the number of circulating T cells [13][14][15][16] , resulting in an immune system that can detect a large number of pathogens at the expense of being less efficient in removing them. The evolution of MHC copy numbers is therefore likely driven toward intermediate optima determined by a tradeoff between detection and elimination of pathogens-as suggested by selection for 5-10 copies inferred in case studies of fish 17,18 and birds 19 . Because pathogen load and the associated selective pressures vary between habitats, the optimal number of MHC copies depends on the environment [20][21][22] . As a result, interbreeding between different locally adapted populations is expected to produce hybrids with excess (above optimal) MHC diversity that are characterized by T cell deprivation and low fitness. This process would introduce postzygotic reproductive isolation and promote reinforcement of premating isolation between the populations. Consequently, MHC genes have been suggested to have an important role in speciation 22,23 , but, to our knowledge, this role has never been tested comparatively in a macroevolutionary context.Here we report comparative analyses of 76 teleost species, of which 66 were sequenced to produce partial draft genome assemblies, including 27 representatives of cod-like fishes within the order Gadiformes. First, we use phylogenomic analysis to resolve standing controversy regarding early-teleost divergences and to firmly ...

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“…This is an indication that measuring cytokine responses will be valuable for determining vaccine efficacy, but there is still a long way to go to establish what Th populations exist in fish and whether they are really equivalent to Th1/Th2/Th17 etc cells. It is not clear when Th appeared in evolution with the uncertainty over the presence of a functional CD4 molecule in cartilaginous fish [21], but precedents exist even in bony fish for effective disease resistance in the putative absence of canonical Th cells in species lacking CD4 and MHC II genes (eg in Gadidae and Syngnathidae) [7,18].…”

Section: Contents Lists Available At Sciencedirectmentioning

confidence: 98%

What's new in fish cytokine research?

Secombes

2016

Fish & Shellfish Immunology

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Absence of major histocompatibility complex class II mediated immunity in pipefish, Syngnathus typhle : evidence from deep transcriptome sequencing

Cited by 73 publications

References 26 publications

The genome of the Gulf pipefish enables understanding of evolutionary innovations

The genome of the Gulf pipefish enables understanding of evolutionary innovations

Evolution of the immune system influences speciation rates in teleost fishes

What's new in fish cytokine research?

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