Detection of Regional Variation in Selection Intensity within Protein-Coding Genes Using DNA Sequence Polymorphism and Divergence

Zhao, Zi-Ming; Campbell, Michael C.; Li, Ning; Lee, Daniel S.W.; Zhang, Zhang; Townsend, Jeffrey P.

doi:10.1093/molbev/msx213

Cited by 10 publications

(4 citation statements)

References 92 publications

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“…To compare relationships of positive selection to phylogenetic support more broadly across Zan and other molecular markers, we constructed individual Bayesian phylogenies and performed corresponding PAML selection analyses for all reliable sequences of all eutherian genes (n = 40) previously shown to have evolved by positive selection (as of June 2022; [47,51,[67][68][69][70][71][72][73][74][75][76][77][78][79][80][81][82][83]). Annotated gene functions ranged from reproduction (n = 23) to sensory perception (n = 7), immunity (n = 5), metabolism (n = 3), the nervous system (n = 1), and the cell cycle (n = 1), and the genes' compared sequence lengths ranged from 394 nt (for S100a2) to 8016 (for Cr2) nt (Table 1), collectively encompassing >104,000 nt of gene coding sequence.…”

Section: Testing the Phylogenetic Utility Of Zanmentioning

confidence: 99%

Gamete Recognition Gene Divergence Yields a Robust Eutherian Phylogeny across Taxonomic Levels

Roberts,

Wright,

Worsham

et al. 2023

Diversity

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The extraordinary morphological diversity among extant mammals poses a challenge for studies of speciation, adaptation, molecular evolution, and reproductive isolation. Despite the recent wealth of molecular studies on mammalian phylogenetics, uncertainties remain surrounding both ancestral and more recent divergence events that have proven difficult to resolve. Multi-gene datasets, especially including genes that are highly divergent, often provide increased support for higher-level affinities within Mammalia; however, such analyses require vast amounts of genomic sequence data and at times, intensive, high-performance computational effort. Furthermore, despite the large-scale efforts dedicated to comprehensive, multi-gene phylogenetic analyses using a combination of mitochondrial, nuclear, and other sequences (e.g., tRNA, ultra-conserved elements, and transposable elements), many relationships across Mammalia remain highly controversial. To offer another approach and provide a phylogenetic solution to this longstanding issue, here we present a phylogenetic tool based on a single reproductive molecular marker, zonadhesin (gene: Zan), one of two known mammalian speciation genes, which encodes the rapidly evolving sperm protein zonadhesin that mediates species-specific adhesion to the egg and thereby promotes reproductive isolation among placental mammals (Eutheria). Topological comparison of Zan Maximum Likelihood phylogenies to a nearly complete mammalian supertree confirmed Zan’s striking phylogenetic utility and resolution at both deeper and more terminal nodes in the placental mammalian phylogeny. This single gene marker yielded an equivalent and/or superiorly supported topology in comparison to a supertree generated using DNA sequences from a supermatrix of 31 genes from 5911 species (extinct and extant). Resolution achieved with this new phylogenetic approach provides unique insights into the divergence of both early and recent mammalian radiations. Finally, and perhaps most importantly, the utility of zonadhesin as a singular molecular marker was especially useful in clades where sufficient taxon sampling is impossible to achieve, and where only a subset of members of the mammalian species tree is available. The eutherian relationships presented here provide a foundation for future studies in the reconstruction of mammalian classifications, including reproductive isolation, hybridization, and biodiversification of species.

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Section: Testing the Phylogenetic Utility Of Zanmentioning

confidence: 99%

Gamete Recognition Gene Divergence Yields a Robust Eutherian Phylogeny across Taxonomic Levels

Roberts,

Wright,

Worsham

et al. 2023

Diversity

View full text Add to dashboard Cite

show abstract

“…To assess relationships of positive selection to phylogenetic support more broadly, we retrieved all reliable sequences of all genes previously shown to have evolved by positive selection [24,91,95,100,[107][108][109][110][111][112][113][114][115][116][117][118][119][120][121][122] and conducted Bayesian and selection analyses on individually constructed gene trees. Excluding 12 genes with too little taxonomic representation (either fewer than nine Orders total or no basal Orders), the analysis yielded Bayesian (>95% posterior support) and M7 and M8 model selection data (magnitude = dN/dS = ω, and frequency= f) for 40 positively selected genes with widely ranging functions, including 23 genes that function in reproduction, seven in sensory perception, five in immunity, three in metabolism, and one each in the nervous system and the cell cycle.…”

Section: Divergence Comparisonsmentioning

confidence: 99%

Rapid divergence of a gamete recognition gene promoted macroevolution of Eutheria

et al. 2022

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Background Speciation genes contribute disproportionately to species divergence, but few examples exist, especially in vertebrates. Here we test whether Zan, which encodes the sperm acrosomal protein zonadhesin that mediates species-specific adhesion to the egg’s zona pellucida, is a speciation gene in placental mammals. Results Genomic ontogeny reveals that Zan arose by repurposing of a stem vertebrate gene that was lost in multiple lineages but retained in Eutheria on acquiring a function in egg recognition. A 112-species Zan sequence phylogeny, representing 17 of 19 placental Orders, resolves all species into monophyletic groups corresponding to recognized Orders and Suborders, with <5% unsupported nodes. Three other rapidly evolving germ cell genes (Adam2, Zp2, and Prm1), a paralogous somatic cell gene (TectA), and a mitochondrial gene commonly used for phylogenetic analyses (Cytb) all yield trees with poorer resolution than the Zan tree and inferior topologies relative to a widely accepted mammalian supertree. Zan divergence by intense positive selection produces dramatic species differences in the protein’s properties, with ordinal divergence rates generally reflecting species richness of placental Orders consistent with expectations for a speciation gene that acts across a wide range of taxa. Furthermore, Zan’s combined phylogenetic utility and divergence exceeds those of all other genes known to have evolved in Eutheria by positive selection, including the only other mammalian speciation gene, Prdm9. Conclusions Species-specific egg recognition conferred by Zan’s functional divergence served as a mode of prezygotic reproductive isolation that promoted the extraordinary adaptive radiation and success of Eutheria.

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“…(2) If population sequence data that spans multiple time points is available then it is possible to identify positively selected sites by assessing the change in mutant frequency over time (Henn et al 2012;Foll et al 2014). (3) More recently it has been demonstrated that it is possible to determine nucleotide sites under selection by analyzing the distribution of those sites across a gene (Zhang, Townsend 2009;Zhao et al 2017).…”

Section: Introductionmentioning

confidence: 99%

Convergent evolution as an indicator for selection during acute HIV-1 infection

Bertels¹,

Metzner²,

Regoes³

2021

Peer Community Journal

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Convergent evolution describes the process of different populations acquiring similar phenotypes or genotypes. Complex organisms with large genomes only rarely and only under very strong selection converge to the same genotype. In contrast, independent virus populations with very small genomes often acquire identical mutations. Here we test the hypothesis of whether convergence in early HIV-1 infection is common enough to serve as an indicator for selection. To this end, we measure the number of convergent mutations in a well-studied dataset of full-length HIV-1envgenes sampled from HIV-1 infected individuals during early infection. We compare this data to a neutral model and find an excess of convergent mutations. Convergent mutations are not evenly distributed across the env gene, but more likely to occur in gp41, which suggests that convergent mutations provide a selective advantage and hence are positively selected. In contrast, mutations that are only found in an HIV-1 population of a single individual are significantly affected by purifying selection. Our analysis suggests that comparisons between convergent and private mutations with neutral models allow us to identify positive and negative selection in small viral genomes. Our results also show that selection significantly shapes HIV-1 populations even before the onset of the adaptive immune system.

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Detection of Regional Variation in Selection Intensity within Protein-Coding Genes Using DNA Sequence Polymorphism and Divergence

Cited by 10 publications

References 92 publications

Gamete Recognition Gene Divergence Yields a Robust Eutherian Phylogeny across Taxonomic Levels

Gamete Recognition Gene Divergence Yields a Robust Eutherian Phylogeny across Taxonomic Levels

Rapid divergence of a gamete recognition gene promoted macroevolution of Eutheria

Convergent evolution as an indicator for selection during acute HIV-1 infection

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