Evolution of the immune system influences speciation rates in teleost fishes

Abstract

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 ...

A cold-blooded view of adaptive immunity

“…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 .…”

“…1) but also (in some cases) have distinctive features that are found in subtaxa. Prominent in the bony fish, and consistent with the general rapid evolution of this vertebrate class, the immune system has unique features in different taxa such as the loss of an MHC class II system and certain immunoglobulin isotypes 16,17 . Cartilaginous fish have a distinctive immunoglobulin organization that has permitted the emergence of antigen receptor genes with novel functions 18,19 .…”

Targeted Sequencing of Venom Genes from Cone Snail Genomes Improves Understanding of Conotoxin Molecular Evolution

“…In addition, we found that variation in conotoxin diversity tracks changes in dietary breadth, suggesting that species with more generalist diets contain a greater number of conotoxin genes in their genome. Given that increased gene diversity is thought to confer an increased capacity for evolutionary change and species diversification (Kirschner and Gerhart 1998;Yang 2001;Malmstrøm et al 2016), generalist species may speciate at faster rates than species with specialist diets. The targeted sequencing technique presented in this paper provides the necessary methodological advancement to rapidly sequence toxin genes across diverse clades of species, allowing tests of the relationship between ecology, toxin gene diversity, and higher order biodiversity patterns to be realized in future work.…”

“…Past studies have described several genetic characteristics that seem to be associated with rapidly radiating clades or the evolution of novel phenotypes, including evidence for diversifying selection, gene gains and losses, and accelerated rates of sequence evolution (Floudas et al 2012;Brawand et al 2014;Guill en et al 2014;Cornetti et al 2015;Malmstrøm et al 2016;Pease et al 2016). Although large-scale comparative genomic studies have vastly increased our knowledge of the genetic changes associated with diversification, the link between genotype and ecologically relevant phenotypes frequently remains unclear.…”

Gene(s) and individual feeding behavior: Exploring eco‐evolutionary dynamics underlying left‐right asymmetry in the scale‐eating cichlid fish Perissodus microlepis

“…The immune system is known to contribute to animal diversification also in the absence of geographical boundaries (e.g., Eizaguirre, Lenz, Traulsen, & Milinski, 2009; Landry, Garant, Duchesne, & Bernatchez, 2001; Malmstrøm et al., 2016; discussed in Raffini et al., 2017). However, the immunoglobulin locus associated with the identified SNP might also have indirect effects on mouth shapes due to functional or physical association to the genomic locus (or loci) for asymmetry (e.g., Lehnert, Pitcher, Devlin, & Heath, 2016; Sacchi et al., 2007).…”