Patterns of evolution of MHC Class II genes of crows (Corvus) suggest trans-species polymorphism

A distinguishing characteristic of genes that code for the major histocompatibility complex (MHC) is that alleles often share more similarity between, rather than within species. There are two likely mechanisms that can explain this pattern: convergent evolution and trans-species polymorphism (TSP), in which ancient allelic lineages are maintained by balancing selection and retained by descendant species. Distinguishing between these two mechanisms has major implications in how we view adaptation of immune genes. In this study we analyzed exon 2 of the MHC class IIB in three passerine bird species in the genus Corvus: jungle crows (Corvus macrorhynchos japonensis) American crows (C. brachyrhynchos) and carrion crows (C. corone orientalis). Carrion crows and American crows are recently diverged, but allopatric, sister species, whereas carrion crows and jungle crows are more distantly related but sympatric species, and possibly share pathogens linked to MHC IIB polymorphisms. These patterns of evolutionary divergence and current geographic ranges enabled us to test for trans-species polymorphism and convergent evolution of the MHC IIB in crows. Phylogenetic reconstructions of MHC IIB sequences revealed several well supported interspecific clusters containing all three species, and there was no biased clustering of variants among the sympatric carrion crows and jungle crows. The topologies of phylogenetic trees constructed from putatively selected sites were remarkably different than those constructed from putatively neutral sites. In addition, trees constructed non-synonymous substitutions from a continuous fragment of exon 2 had more, and generally more inclusive, supported interspecific MHC IIB variant clusters than those constructed from the same fragment using synonymous substitutions. These phylogenetic patterns suggest that recombination, especially gene conversion, has partially erased the signal of allelic ancestry in these species. While clustering of positively selected amino acids by supertyping revealed a single supertype shared by only jungle and carrion crows, a pattern consistent with convergence, the overall phylogenetic patterns we observed suggest that TSP, rather than convergence, explains the interspecific allelic similarity of MHC IIB genes in these species of crows.

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Species divergence, selection and polymorphism in the MHC of crows

10.7287/peerj.preprints.621v1 ◽

2014 ◽

Author(s):

John A Eimes ◽

Andrea K Townsend ◽

Irem Sepil ◽

Isao Nishiumi ◽

Yoko Satta

Keyword(s):

Mhc Class Ii ◽

Convergent Evolution ◽

Bird Species ◽

Passerine Bird ◽

Evolutionary Divergence ◽

Closely Related Species ◽

Geographic Ranges ◽

Histocompatibility Complex ◽

High Level ◽

Mhc Iib

The relatively high level of polymorphism usually found in the major histocompatibility complex (MHC) is usually attributed to pathogen mediated selection; however, the timescale of selection is often unclear. Here we describe the MHC class II (IIB) in three passerine bird species in the genus Corvus: American, carrion and jungle crows. Carrion and American crows are recently diverged, but allopatric, sister species, whereas carrion and jungle crows are more distantly related but sympatric, likely sharing pathogens linked to MHC IIB polymorphisms. These patterns of evolutionary divergence and current geographic ranges enabled us to examine evidence for ancient versus recent selection, trans-species polymorphism, and convergent evolution of the MHC in closely related species. Among the three species, the MHC IIB genes were highly duplicated (7-20 variants per individual) and polymorphic (an average of 79 variants per species; N = 18/species). Phylogenetic reconstructions of MHC IIB revealed patterns that were inconsistent with the evolutionary histories of the species. Several well supported interspecific clusters were observed, indicating trans-species polymorphism within this genus. Clustering of positively selected amino acids by supertyping revealed a single supertype shared by only jungle and carrion crows, whereas all other supertypes were shared among the three species, a pattern consistent with convergent evolution.

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MHC class II expression in skin biopsies from the franciscana dolphin Pontoporia blainvillei and the southern right whale Eubalaena australis

Journal of the Marine Biological Association of the United Kingdom ◽

10.1017/s0025315409003245 ◽

2009 ◽

Vol 89 (5) ◽

pp. 1009-1013 ◽

Cited By ~ 6

Author(s):

Larissa Heinzelmann ◽

Maurício Tavares ◽

Paulo H. Ott ◽

Ignacio M.B. Moreno ◽

José Artur B. Chies

Keyword(s):

Mhc Class Ii ◽

Balancing Selection ◽

Rna Extraction ◽

Exon 2 ◽

Right Whale ◽

Eubalaena Australis ◽

Skin Biopsies ◽

Pontoporia Blainvillei ◽

First Time ◽

Franciscana Dolphin

Presently, there is no information about the functionality of the immune system in the franciscana dolphin (Pontoporia blainvillei), a small dolphin from southern Brazil. As in the case of the franciscana, the population of southern right whale (Eubalaena australis) which inhabits Brazilian waters has not yet been surveyed in what concerns MHC expression. For the first time it was possible to observe the DQB gene expression in skin of these two species of cetacean using RT-PCR. Skin pieces of the animals were collected to RNA extraction. The fragment corresponding to DQB exon 2 was amplified, cloned and sequenced. A total of five alleles were found, one to franciscana and four to southern right whale. The observed dN/dS ratio of 2.77 (P = 0.03) suggests that this gene is under balancing selection pressure (positive Darwinian selection). The sequences indicate that, in both species analysed, the DQB gene is functional.

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Genetic variation and balancing selection at MHC class II exon 2 in cultured stocks and wild populations of orange-spotted grouper (Epinephelus coioides)

Genetics and Molecular Research ◽

10.4238/2012.november.12.4 ◽

2012 ◽

Vol 11 (4) ◽

pp. 3869-3881 ◽

Cited By ~ 2

Author(s):

Z.N. Meng ◽

S. Yang ◽

B. Fan ◽

L. Wang ◽

H.R. Lin

Keyword(s):

Genetic Variation ◽

Mhc Class Ii ◽

Balancing Selection ◽

Class Ii ◽

Epinephelus Coioides ◽

Wild Populations ◽

Exon 2

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Polymorphism of exon 2 of MHC Class II B gene in the Chinese concave- eared torrent frog (Odorrana tormota)

Biodiversity Science ◽

10.3724/sp.j.1003.2012.09211 ◽

2013 ◽

Vol 20 (2) ◽

pp. 184-192 ◽

Cited By ~ 1

Author(s):

Li Fang ◽

Shu Yilin ◽

Wu Hailong

Keyword(s):

Mhc Class Ii ◽

Class Ii ◽

Exon 2

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Plasmodium vivax Cysteine-Rich Protective Antigen Polymorphism at Exon-1 Shows Recombination and Signatures of Balancing Selection

Genes ◽

10.3390/genes12010029 ◽

2020 ◽

Vol 12 (1) ◽

pp. 29

Author(s):

Lilia González-Cerón ◽

José Cebrián-Carmona ◽

Concepción M. Mesa-Valle ◽

Federico García-Maroto ◽

Frida Santillán-Valenzuela ◽

...

Keyword(s):

Amino Acid ◽

B Cell ◽

Plasmodium Vivax ◽

Nucleotide Diversity ◽

Protective Antigen ◽

Balancing Selection ◽

Southern Mexico ◽

Exon 2 ◽

Exon 1 ◽

Tajima’S D

Plasmodium vivax Cysteine-Rich Protective Antigen (CyRPA) is a merozoite protein participating in the parasite invasion of human reticulocytes. During natural P. vivax infection, antibody responses against PvCyRPA have been detected. In children, low anti-CyRPA antibody titers correlated with clinical protection, which suggests this protein as a potential vaccine candidate. This work analyzed the genetic and amino acid diversity of pvcyrpa in Mexican and global parasites. Consensus coding sequences of pvcyrpa were obtained from seven isolates. Other sequences were extracted from a repository. Maximum likelihood phylogenetic trees, genetic diversity parameters, linkage disequilibrium (LD), and neutrality tests were analyzed, and the potential amino acid polymorphism participation in B-cell epitopes was investigated. In 22 sequences from Southern Mexico, two synonymous and 21 nonsynonymous mutations defined nine private haplotypes. These parasites had the highest LD-R2 index and the lowest nucleotide diversity compared to isolates from South America or Asia. The nucleotide diversity and Tajima’s D values varied across the coding gene. The exon-1 sequence had greater diversity and Rm values than those of exon-2. Exon-1 had significant positive values for Tajima’s D, β-α values, and for the Z (HA: dN > dS) and MK tests. These patterns were similar for parasites of different origin. The polymorphic amino acid residues at PvCyRPA resembled the conformational B-cell peptides reported in PfCyRPA. Diversity at pvcyrpa exon-1 is caused by mutation and recombination. This seems to be maintained by balancing selection, likely due to selective immune pressure, all of which merit further study.

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Fast skeletal muscle-specific expression of a quail troponin I gene in transgenic mice.

Molecular and Cellular Biology ◽

10.1128/mcb.8.12.5072 ◽

1988 ◽

Vol 8 (12) ◽

pp. 5072-5079 ◽

Cited By ~ 7

Author(s):

P L Hallauer ◽

K E Hastings ◽

A C Peterson

Keyword(s):

Skeletal Muscle ◽

Transgenic Mice ◽

Troponin I ◽

Fiber Type ◽

Regulatory Elements ◽

Evolutionary Divergence ◽

Mrna Levels ◽

Fast Skeletal Muscle ◽

Specific Expression ◽

Exon 2

We have produced seven lines of transgenic mice carrying the quail gene encoding the fast skeletal muscle-specific isoform of troponin I (TnIf). The quail DNA included the entire TnIf gene, 530 base pairs of 5'-flanking DNA, and 1.5 kilobase pairs of 3'-flanking DNA. In all seven transgenic lines, normally initiated and processed quail TnIf mRNA was expressed in skeletal muscle, where it accumulated to levels comparable to that in quail muscle. Moreover, in the three lines tested, quail TnIf mRNA levels were manyfold higher in a fast skeletal muscle (gastrocnemius) than in a slow skeletal muscle (soleus). We conclude that the cellular mechanisms directing muscle fiber type-specific TnIf gene expression are mediated by cis-regulatory elements present on the introduced quail DNA fragment and that they control TnIf expression by affecting the accumulation of TnIf mRNA. These elements have been functionally conserved since the evolutionary divergence of birds and mammals, despite the major physiological and morphological differences existing between avian (tonic) and mammalian (twitch) slow muscles. In lines of transgenic mice carrying multiple tandemly repeated copies of the transgene, an aberrant quail TnIf transcript (differing from normal TnIf mRNA upstream of exon 2) also accumulated in certain tissues, particularly lung, brain, spleen, and heart tissues. However, this aberrant transcript was not detected in a transgenic line which carries only a single copy of the quail gene.

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