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Roved, J.

Publications and source records attributed to Roved, J..

3 recordsLinked to original sources

Natural selection on synonymous genetic variation in the major histocompatibility complex

Protein coding DNA sequences harbor synonymous nucleotide variation that does not change amino acid sequences but influences phenotypes via multiple effects on the pathway from gene to protein. Synonymous variation has recently been shown to coevolve between viruses and their natural hosts, but its potential role in host immune defenses has not been explored. Here, I present evidence of natural selection on synonymous variation in the major histocompatibility complex (MHC), a highly polymorphic multigene locus that plays a crucial role in pathogen recognition by the adaptive immune system of vertebrate species. Using data from a wild population of Great Reed Warblers, I show that codon usage in exon 3 of MHC class I (MHC-I) genes is under strong purifying selection in 57 out of 87 codon sites. Scanning the Great Reed Warbler genome for tRNA genes revealed that, for most amino acids, bias towards preferred codons was associated with abundances of tRNA isotypes, indicating that the purifying selection is likely driven by selection for increased translational efficiency. However, spikes of synonymous variation appeared in 30 of the 87 sites in the MHC-I exon 3, and in those sites, codon usage bias and correlations with tRNA abundances were reduced. The distribution of the spikes of synonymous variation showed no consistent association with structural domains of the MHC-I protein, nor with sites under positive selection for amino acid change, which are considered important for antigen binding properties. Intriguingly, the amount of synonymous variation in genotypes showed a positive correlation with Darwinian fitness, indicating that important evolutionary forces are at play that neutralize purifying selection in the 30 sites. From an ultimate perspective, the release of purifying selection among certain sites in MHC genes may indicate an arms race with pathogens, and I propose that the spikes of synonymous variation reveal a footprint of natural selection to escape inhibitory molecular interactions targeting MHC mRNA. This interpretation is supported by the frequency spectrum of synonymous variants segregating among MHC-I haplotypes in the population, which is inconsistent with neutral drift and instead indicates that variation at these sites is actively maintained by selection. These results expose a previously unrecognized layer of selection in a key immune gene family and highlight the potential functional importance of synonymous variation in host-pathogen coevolution with direct implications for understanding susceptibility to infectious diseases.

evolutionary biology↗

Migration patterns and hybridization within the Asian stonechat complex in response to a major geographical barrier

Long-distance avian migration is thought to be under strong natural selection. Facing geographical barriers, migrants display various patterns considered to be adaptive. For example, they may detour along either side around the barrier or cross it, requiring specialized behavioral adaptations. Variations within closely related taxa are excellent sources for understanding the evolutionary background of migration and how barriers are shaping migration routes. In Asia, some species are assumed to have a migratory divide in response to the major geographical barrier, the Qinghai-Tibet Plateau (QTP), including the stonechat taxa (Siberian Stonechat Saxicola maurus maurus and Amur Stonechat S. stejnegeri). As they detour along either side of the QTP, these taxa are believed to disfavor a crossing over the highland. However, the more southernly distributed Tibetan Stonechat (S. m. przewalskii) breeds on the QTP, suggesting adaptation to high elevation. To investigate migration patterns and the potentially associated genetic differences, we studied migration routes and population genetics of four populations around the assumed migratory divide in Russia and Mongolia, and of one from the QTP in China. Our results confirmed the existence of a migratory divide between maurus and stejnegeri, albeit with extensive hybridization. We observed both the hypothesized western and eastern routes, but also found individuals employing intermediate routes crossing the QTP, of which two-thirds were clear hybrids. Meanwhile, przewalskii followed a highland-crossing route and was genetically differentiated from maurus and stejnegeri. The diverse migration routes among Asian stonechats show differential responses towards the geographical barrier. The intermediate route may be associated with hybridization, and its conditional viability may facilitate gene flow between maurus and stejnegeri. The Asian stonechat complex thus offers great opportunities for novel research of the genetics and evolution of migration. The specific evolutionary background associated with inhabiting and crossing the QTP can offer new perspectives in this field. Teaser textMigratory divides can arise in birds because alternative routes around migratory barriers would select for behaviors to restrict hybridization. Hybrids of parental types that employ alternative routes are hypothesized to embark on intermediate routes that would expose them to suboptimal conditions, resulting in post-zygotic reproductive isolation. However, this hypothesis is challenged when a sister taxon actually breeds on the geographical barrier. This is the case in the Asian stonechat complex that breeds near or on the Qinghai-Tibet Plateau (QTP), the roof of the world. We demonstrated a migratory divide in central Siberia to Mongolia for race maurus and stejnegeri, yet showed also evidence for extensive hybridization. Hybrids migrated along a newly discovered intermediate route, seemingly viable and overlaps with the migration trajectory of race przewalskii over the eastern part of the QTP. The Asian migratory divide relative to the QTP thus provided new insights to the evolution of landbird migration.

evolutionary biology↗

Non-random association of MHC-I alleles in favor of high diversity haplotypes in wild songbirds revealed by computer-assisted MHC haplotype inference using the R package MHCtools

Major histocompatibility complex (MHC) genes play a central role for pathogen recognition by the adaptive immune system. The MHC genes are often duplicated and tightly linked within a small genomic region. This structural organization suggests that natural selection acts on the combined property of multiple MHC gene copies in segregating haplotypes, rather than on single MHC genes. This may have important implications for analyses of patterns of selection on MHC genes. Here, we present a computer-assisted protocol to infer segregating MHC haplotypes from family data, based on functions in the R package MHCtools. We employed this method to identify 107 unique MHC class I (MHC-I) haplotypes in 116 families of wild great reed warblers (Acrocephalus arundinaceus). In our data, the MHC-I genes were tightly linked in haplotypes and inherited as single units, with only two observed recombination events among 334 offspring. We found substantial variation in the number of different MHC-I alleles per haplotype, and the divergence between alleles in MHC-I haplotypes was significantly higher than between randomly assigned alleles in simulated haplotypes. This suggests that selection has favored non-random associations of divergent MHC-I alleles in haplotypes to increase the range of pathogens that can be recognized by the adaptive immune system. Further studies of selection on MHC haplotypes in natural populations is an interesting avenue for future research. Moreover, inference and analysis of MHC haplotypes offers important insights into the structural organization of MHC genes, and may improve the accuracy of the MHC region in de novo genome assemblies.

evolutionary biology↗