Molecular Evolution in Small Steps under Prevailing Negative Selection: A Nearly Universal Rule of Codon Substitution

Chen, Qingjian; Lan, Ao; Shen, Xu; Wu, Chung‐I

doi:10.1093/gbe/evz192

Cited by 17 publications

(11 citation statements)

References 45 publications

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“…The rank order of Ki's is nearly constant across a wide range of species from Drosophila , primates to yeast and rodents [ 54 ]. The constancy, determined by the physico-chemical properties of the AAs, permits the calculation of the expected Ki's [E(Ki)’s] between any pair of closely related species [ 57 ].…”

Section: Resultsmentioning

confidence: 99%

Convergent adaptation of the genomes of woody plants at the land–sea interface

He¹,

Xu²,

Zhang³

et al. 2020

National Science Review

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Sequencing multiple species that share the same ecological niche may be a new frontier for genomic studies. While such studies should shed light on molecular convergence, genomic-level analyses have been unsuccessful, due mainly to the absence of empirical controls. Woody plant species that colonized the global tropical coasts, collectively referred to as mangroves, are ideal for convergence studies. Here, we sequenced the genomes/transcriptomes of 16 species belonging in three major mangrove clades. To detect convergence in a large phylogeny, a CCS+ model is implemented, extending the more limited CCS method (convergence at conservative sites). Using the empirical control for reference, the CCS+ model reduces the noises drastically, thus permitting the identification of 73 convergent genes with Ptrue (probability of true convergence) > 0.9. Products of the convergent genes tend to be on the plasma membrane associated with salinity tolerance. Importantly, convergence is more often manifested at a higher level than at amino-acid (AA) sites. Relative to >50 plant species, mangroves strongly prefer 4 AAs and avoid 5 others across the genome. AA substitutions between mangrove species strongly reflect these tendencies. In conclusion, the selection of taxa, the number of species and, in particular, the empirical control are all crucial for detecting genome-wide convergence. We believe this large study of mangroves is the first successful attempt at detecting genome-wide site convergence.

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Section: Resultsmentioning

confidence: 99%

Convergent adaptation of the genomes of woody plants at the land–sea interface

He¹,

Xu²,

Zhang³

et al. 2020

National Science Review

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show abstract

“…Finally, the strengths of positive selection and negative selection are strongly correlated (partly because both are functions of N e ). For example, large-step mutations, when measured by the physicochemical distances between amino acids, are both more deleterious and more beneficial than small-step mutations [21,22]. Therefore, the working of negative selection would be informative about the operation of positive selection and vice versa.…”

Section: Discussionmentioning

confidence: 99%

“…The results of analyses between species can be qualitatively different from the analyses of polymorphism data within species. The two approaches are complementary, rather than redundant (see Discussion) [20][21][22]. There are several challenges in correctly inferring positive selection since DNA sequences are simultaneous influenced by multiple forces that may include mutation, genetic drift, positive selection and negative selection.…”

Section: Introductionmentioning

confidence: 99%

Two decades of suspect evidence for adaptive molecular evolution – Negative selection confounding positive selection signals

Chen

Yang

Feng

et al. 2021

Preprint

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There is a large literature in the last two decades affirming adaptive DNA sequences evolution between species. The main lines of evidence are from i) the McDonald-Kreitman (MK) test, which compares divergence and polymorphism data, and ii) the PAML test, which analyzes multi-species divergence data. Here, we apply these two tests concurrently on the genomic data of Drosophila and Arabidopsis. To our surprise, the >100 genes identified by the two tests do not overlap beyond random expectation. Because the non-concordance could be due to low powers leading to high false-negatives, we merge every 20 - 30 genes into a “supergene”. At the supergene level, the power of detection is large but the calls still do not overlap. We rule out methodological reasons for the non-concordance. In particular, extensive simulations fail to find scenarios whereby positive selection can only be detected by either MK or PAML, but not both. Since molecular evolution is governed by positive and negative selection concurrently, a fundamental assumption for estimating one (say, positive selection) is that the other is constant. However, in a broad survey of primates, birds, Drosophila and Arabidopsis, we found that negative selection rarely stays constant for long in evolution. As a consequence, the variation in negative selection is often mis-construed as signals of positive selection. In conclusion, MK, PAML or any method that examines genomic sequence evolution has to explicitly address the variation in negative selection before estimating positive selection. In a companion study, we propose a possible path forward in two stages – first, by mapping out the changes in negative selection and then using this map to estimate positive selection. For now, the large literature on positive selection between species has to await the re-assessment.

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“…(2) shows. For example, large-step mutations, when measured by the physico-chemical distances between amino acids, are both more deleterious and more beneficial than small-step mutations 26,48 . Therefore, the working of negative selection would be informative about the operation of positive selection as well.…”

Section: Discussionmentioning

confidence: 99%

Two decades of suspect evidence for adaptive DNA-sequence evolution – Less negative selection misconstrued as positive selection

Chen

Feng

et al. 2020

Preprint

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Evidence for biological adaptation is often obtained by studying DNA sequence evolution. Since the analyses are affected by both positive and negative selection, studies usually assume constant negative selection in the time span of interest. For this reason, hundreds of studies that conclude adaptive evolution might have reported false signals caused by relaxed negative selection. We test this suspicion two ways. First, we analyze the fluctuation in population size, N, during evolution. For example, the evolutionary rate in the primate phylogeny could vary by as much as 2000 fold due to the variation in N alone. Second, we measure the variation in negative selection directly by analyzing the polymorphism data from four taxa (Drosophila, Arabidopsis, primates, and birds, with 64 species in total). The strength of negative selection, as measured by the ratio of nonsynonymous/synonymous polymorphisms, fluctuates strongly and at multiple time scales. The two approaches suggest that the variation in the strength of negative selection may be responsible for the bulk of the reported adaptive genome evolution in the last two decades. This study corroborates the recent report 1 on the inconsistent patterns of adaptive genome evolution. Finally, we discuss the path forward in detecting adaptive sequence evolution.

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Molecular Evolution in Small Steps under Prevailing Negative Selection: A Nearly Universal Rule of Codon Substitution

Cited by 17 publications

References 45 publications

Convergent adaptation of the genomes of woody plants at the land–sea interface

Convergent adaptation of the genomes of woody plants at the land–sea interface

Two decades of suspect evidence for adaptive molecular evolution – Negative selection confounding positive selection signals

Two decades of suspect evidence for adaptive DNA-sequence evolution – Less negative selection misconstrued as positive selection

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