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Comparative Study
. 2020 Sep 1;12(9):1493-1503.
doi: 10.1093/gbe/evaa138.

Excessive Parallelism in Protein Evolution of Lake Baikal Amphipod Species Flock

Valentina Burskaia  1 , Sergey Naumenko  2   3 , Mikhail Schelkunov  1   2 , Daria Bedulina  4   5 , Tatyana Neretina  2   6   7 , Alexey Kondrashov  7   8 , Lev Yampolsky  9 , Georgii A Bazykin  1   2
Affiliations
Comparative Study

Excessive Parallelism in Protein Evolution of Lake Baikal Amphipod Species Flock

Valentina Burskaia et al. Genome Biol Evol. .

Erratum in

Abstract

Repeated emergence of similar adaptations is often explained by parallel evolution of underlying genes. However, evidence of parallel evolution at amino acid level is limited. When the analyzed species are highly divergent, this can be due to epistatic interactions underlying the dynamic nature of the amino acid preferences: The same amino acid substitution may have different phenotypic effects on different genetic backgrounds. Distantly related species also often inhabit radically different environments, which makes the emergence of parallel adaptations less likely. Here, we hypothesize that parallel molecular adaptations are more prevalent between closely related species. We analyze the rate of parallel evolution in genome-size sets of orthologous genes in three groups of species with widely ranging levels of divergence: 46 species of the relatively recent lake Baikal amphipod radiation, a species flock of very closely related cichlids, and a set of significantly more divergent vertebrates. Strikingly, in genes of amphipods, the rate of parallel substitutions at nonsynonymous sites exceeded that at synonymous sites, suggesting rampant selection driving parallel adaptation. At sites of parallel substitutions, the intraspecies polymorphism is low, suggesting that parallelism has been driven by positive selection and is therefore adaptive. By contrast, in cichlids, the rate of nonsynonymous parallel evolution was similar to that at synonymous sites, whereas in vertebrates, this rate was lower than that at synonymous sites, indicating that in these groups of species, parallel substitutions are mainly fixed by drift.

Keywords: convergence; parallelism; positive selection; speciation.

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Figures

Fig. 1
Fig. 1
Phylogenetics of lake Baikal amphipods and analysis of parallelism. (A) Phylogenetic tree of lake Baikal amphipods. Dots indicate bootstrap values above 80%. (B, C) Parallel versus divergent substitutions in amphipods. Each dot corresponds to one species quartet. (B) Quartets were selected only from the closely related group originating from the second invasion. (C) Quartets consist of two species from the first invasion and two species from the second invasion; these pairs are genetically more distant. Slopes of linear regression models differ significantly (Analysis of variance test, P value <2.2e-16) for synonymous and nonsynonymous substitutions at both panels.
Fig. 2
Fig. 2
The P test for excess parallelism. (A) A schematic representation of the calculation of the level of parallelism dP. In a quartet of species with the depicted topology, green and red colors identify evolutionary paths I and II, respectively. dP measures the probability that a substitution that has occurred along path I has also occurred along path II. P is the ratio of dP values at nonsynonymous and synonymous sites. (B) P for quartets of cichlids, amphipods, and vertebrates. Each point represents the mean value of P for a species quartet across the six mutation types; only those 642 out of the 900 quartets for which sufficient data are available for each mutation type are shown (see Materials and Methods). The horizontal axis shows the phylogenetic distance between the last common ancestors of pairs I and II, measured in number of substitutions per nucleotide site (note the logarithmic axis). (C) dN/dS values for two species in path I, calculated for three groups of species. (D) Distribution of values of the P statistic in all the 300 analyzed quartets (cyan) and in the 40 quartets with evidence of parallel phenotypic adaptations to abyssal environment (blue). The mean values of the two distributions are similar (Wilcoxon test, P = 0.2709).
Fig. 3
Fig. 3
Polymorphism at sites of parallel substitutions. (A–D) Proportion of sites carrying a SNP among those with a nucleotide substitution between species in path I (A, C) or among sites with parallel substitutions (B, D). (A, B) Individual-based polymorphism test. (C, D) Population-based polymorphism test. (E, F) Ratio of proportions of sites carrying a SNP between nonsynonymous and synonymous sites (pN/pS). (E): Individual-based polymorphism test (paired t-test, P = 0.0031; unpaired t-test, P = 0.0033). (F) Population-based polymorphism test (paired t-test, P = 0.0091; unpaired t-test, P = 0.0100).
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