Why does the immune system of Atlantic cod lack MHC II?

Star, Bastiaan; Jentoft, Sissel

doi:10.1002/bies.201200005

Cited by 57 publications

(46 citation statements)

References 29 publications

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“…This is supported by higher extinction rates in the same period (Takashima et al 2006; Harnik et al 2012). The anoxic scenario fits with one of several mechanisms proposed to promote loss of MHCII —metabolic cost (Star and Jentoft 2012). Nevertheless, it could also be coupled to post extinction speciation in which new species invade habitats where maintaining MHCII and Mx , in this case, was less favorable.…”

Section: Resultsmentioning

confidence: 55%

Successive Losses of Central Immune Genes Characterize the Gadiformes’ Alternate Immunity

et al. 2016

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Great genetic variability among teleost immunomes, with gene losses and expansions of central adaptive and innate components, has been discovered through genome sequencing over the last few years. Here, we demonstrate that the innate Myxovirus resistance gene (Mx) is lost from the ancestor of Gadiformes and the closely related Stylephorus chordatus, thus predating the loss of Major Histocompatibility Complex class II (MHCII) in Gadiformes. Although the functional implication of Mx loss is still unknown, we demonstrate that this loss is one of several ancient events appearing in successive order throughout the evolution of teleost immunity. In particular, we find that the loss of Toll-like receptor 5 predates the loss of Mx involving the entire Paracanthopterygii lineage. Using a time-calibrated phylogeny, we show that loss of MHCII and Mx overlap with major paleoclimatic and geological events indicating that these genetic changes were adaptive responses to the changing environment at the time.

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Section: Resultsmentioning

confidence: 55%

Successive Losses of Central Immune Genes Characterize the Gadiformes’ Alternate Immunity

et al. 2016

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“…The Gadiformes order of teleost species has lost the MHC class II system, as first shown in the cod 16,121 and later in other species. It has been known for a long time that specific antibody responses cannot be generated in cod after immunization, essentially producing the same repertoire of IgM antibodies to each antigen 122 .…”

Section: Evolution Of the Mhcmentioning

confidence: 85%

A cold-blooded view of adaptive immunity

2018

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The adaptive immune system arose 500 million years ago in ectothermic (cold-blooded) vertebrates. Classically, the adaptive immune system has been defined by the presence of lymphocytes expressing recombination-activating gene (RAG)-dependent antigen receptors and the MHC. These features are found in all jawed vertebrates, including cartilaginous and bony fish, amphibians and reptiles and are most likely also found in the oldest class of jawed vertebrates, the extinct placoderms. However, with the discovery of an adaptive immune system in jawless fish based on an entirely different set of antigen receptors — the variable lymphocyte receptors — the divergence of T and B cells, and perhaps innate-like lymphocytes, goes back to the origin of all vertebrates. This Review explores how recent developments in comparative immunology have furthered our understanding of the origins and function of the adaptive immune system.

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“…This implies that MHC II functionality was not outcompeted by a preexisting alternative immunological strategy such as an expanded MHC I repertoire but may instead have been lost as a result of the metabolic costs associated with its maintenance 39 . The temporal relationship between the loss and expansions in Gadiformes and the identification of putative cross-presentation signaling motifs in Atlantic cod 6 , as well as in several other gadiform species, indicate that a number of genes in the expanded MHC I repertoire evolved to compensate for loss of MHC II.…”

Section: Discussionmentioning

confidence: 99%

“…4, Supplementary Table 12 and Supplementary Note). Two hypotheses have been put forward as possible explanations for the loss of MHC II: a metabolic gain by not maintaining a costly system or a functional shift in the immune gene repertoire, rendering it obsolete 39 . Whether the loss occurred before or following the expansion of MHC I genes is key in discriminating between these hypotheses.…”

Section: Loss Of Mhc II Pathway Genesmentioning

confidence: 99%

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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Why does the immune system of Atlantic cod lack MHC II?

Cited by 57 publications

References 29 publications

Successive Losses of Central Immune Genes Characterize the Gadiformes’ Alternate Immunity

Successive Losses of Central Immune Genes Characterize the Gadiformes’ Alternate Immunity

A cold-blooded view of adaptive immunity

Evolution of the immune system influences speciation rates in teleost fishes

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