Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2019 Aug 2:8:e45199.
doi: 10.7554/eLife.45199.

Natural selection and repeated patterns of molecular evolution following allopatric divergence

Yibo Dong #  1   2 , Shichao Chen #  3   4   5 , Shifeng Cheng  6 , Wenbin Zhou  1 , Qing Ma  1 , Zhiduan Chen  7 , Cheng-Xin Fu  8 , Xin Liu  6 , Yun-Peng Zhao  8 , Pamela S Soltis  3 , Gane Ka-Shu Wong  6   9   10 , Douglas E Soltis  3   4 , Qiu-Yun Jenny Xiang  1
Affiliations

Natural selection and repeated patterns of molecular evolution following allopatric divergence

Yibo Dong et al. Elife. .

Abstract

Although geographic isolation is a leading driver of speciation, the tempo and pattern of divergence at the genomic level remain unclear. We examine genome-wide divergence of putatively single-copy orthologous genes (POGs) in 20 allopatric species/variety pairs from diverse angiosperm clades, with 16 pairs reflecting the classic eastern Asia-eastern North America floristic disjunction. In each pair, >90% of POGs are under purifying selection, and <10% are under positive selection. A set of POGs are under strong positive selection, 14 of which are shared by 10-15 pairs, and one shared by all pairs; 15 POGs are annotated to biological processes responding to various stimuli. The relative abundance of POGs under different selective forces exhibits a repeated pattern among pairs despite an ~10 million-year difference in divergence time. Species divergence times are positively correlated with abundance of POGs under moderate purifying selection, but negatively correlated with abundance of POGs under strong purifying selection.

Keywords: allopatric/geographic speciation; eastern Asia-eastern North America floristic disjunction; evolutionary biology; genetic divergence; molecular evolution; plant biology; positive selection; transcriptome sequencing.

PubMed Disclaimer

Conflict of interest statement

YD, SC, SC, WZ, QM, ZC, CF, XL, YZ, PS, GW, DS, JX No competing interests declared

Figures

Figure 1.
Figure 1.. Frequency distribution of synonymous substitutions per synonymous site (Ks) of putative orthologs (POGs) from leaf transcriptomes of 20 species/variety pairs of angiosperms.
Figure 2.
Figure 2.. Frequency distribution of nonsynonymous substitutions per non-sysnonymous site (Ka) of putative orthologs (POGs) of leaf transcriptomes from 20 species/variety pairs of angiosperms.
Figure 3.
Figure 3.. Frequency distribution of Ka/Ks ratios of putative orthologs (POGs) from leaf transcriptomes of 20 species/variety pairs of angiosperms.
Figure 4.
Figure 4.. Relative abundance of putative orthologs (POGs) with different categories of Ka/Ks values.
Numbers of genes in each category are provided in Supplementary file 3.
Figure 5.
Figure 5.. Dated global phylogeny of the 20 taxon pairs and correlations of divergence time with level of divergence at sysnonymous sites, withabundance of genes under moderate purifying selection (Ka/Ks = 0.1 - 0.5), and with abundance of genes under strong purifying selection (ka/Ks <0.1).
(a) Dated global phylogeny and divergence times of taxon pairs estimated using BEAST program and seven single-copy orthologs shared by all 40 taxa with no missing data. Number 1, 2, and 3 indicate the crown node of Magnoliidae, crown node of Monocotyledoneae, and crown node of Eudicotyledoneae, respectively. (b – d). Correlation between divergence time and (b) Ks value at peak frequency of each genus, (c) abundance of POGs with Ka/Ks values between 0.1–0.5, and (d) abundance of POGs with Ka/Ks values < 0.1. Data used for the analyses are available in Supplementary file 4.
Figure 5—figure supplement 1.
Figure 5—figure supplement 1.. Divergence times of 20 taxon pairs estimated with 79 single copy orthologs present in 90% or more species using BEAST.
Figure 6.
Figure 6.. Positive and negative relationships between relative abundance (Y-axis) of genes with Ka/Ks values in the indicated ranges and Ks values of peak abundance (X-axis) in the 20 taxon pairs.
The pattern remains when the modified Ks (see Materials and methods) is used. Data used for the analyses are available in Supplementary file 4.
Figure 7.
Figure 7.. Relative abundance of genes with Ka/Ks > 2 annotated to Cell Component category, drawn from data in Supplementary file 5. Genes annotated to integral component of membrane (ICM) are shown in dark brown.
Figure 7—figure supplement 1.
Figure 7—figure supplement 1.. Relative abundance of Ka/Ks > 2 genes annotated to different functions in the Biological Process category; drawn from data in Supplementary file 5.
Figure 7—figure supplement 2.
Figure 7—figure supplement 2.. Relative abundance of Ka/Ks > 2 genes annotated to different functions of in the Molecular Function category; drawn from data in Supplementary file 5.
Appendix 1—figure 1.
Appendix 1—figure 1.. Phylogenetic positions of orders represented by species pairs sampled in the angiosperm phylogeny.
Phylogenetic tree was taken from Angiosperm phylogeny website.
Appendix 1—figure 2.
Appendix 1—figure 2.. Flowchart of transcriptome sequence analyses for one species pair.
The process was repeated for 20 pairs. A customized pipeline of programs was developed for running these steps.
Appendix 1—figure 3.
Appendix 1—figure 3.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Acorus.
Appendix 1—figure 4.
Appendix 1—figure 4.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Calycanthus.
Appendix 1—figure 5.
Appendix 1—figure 5.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Campsis.
Appendix 1—figure 6.
Appendix 1—figure 6.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Convallaria.
Appendix 1—figure 7.
Appendix 1—figure 7.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Cornus-1.
Appendix 1—figure 8.
Appendix 1—figure 8.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Cornus-2.
Appendix 1—figure 9.
Appendix 1—figure 9.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Cotinus.
Appendix 1—figure 10.
Appendix 1—figure 10.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Croomia.
Appendix 1—figure 11.
Appendix 1—figure 11.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Dysosma.
Appendix 1—figure 12.
Appendix 1—figure 12.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Gelsemium.
Appendix 1—figure 13.
Appendix 1—figure 13.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Hamamelis.
Appendix 1—figure 14.
Appendix 1—figure 14.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Liquidarnbar.
Appendix 1—figure 15.
Appendix 1—figure 15.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Liriodendron.
Appendix 1—figure 16.
Appendix 1—figure 16.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Meehania.
Appendix 1—figure 17.
Appendix 1—figure 17.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Menispermum.
Appendix 1—figure 18.
Appendix 1—figure 18.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Nelumbo.
Appendix 1—figure 19.
Appendix 1—figure 19.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Penthorum.
Appendix 1—figure 20.
Appendix 1—figure 20.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Phryma.
Appendix 1—figure 21.
Appendix 1—figure 21.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Sassafras.
Appendix 1—figure 22.
Appendix 1—figure 22.. Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.
Saururus.
See this image and copyright information in PMC

Comment in

  • How predictable is genome evolution?
    Coathup MJ, Osborne OG, Savolainen V. Coathup MJ, et al. Elife. 2019 Sep 13;8:e50784. doi: 10.7554/eLife.50784. Elife. 2019. PMID: 31517601 Free PMC article.

Similar articles

See all similar articles

Cited by

References

    1. Altenhoff AM, Dessimoz C. Phylogenetic and functional assessment of orthologs inference projects and methods. PLOS Computational Biology. 2009;5:e1000262. doi: 10.1371/journal.pcbi.1000262. - DOI - PMC - PubMed
    1. Arnegard ME, McGee MD, Matthews B, Marchinko KB, Conte GL, Kabir S, Bedford N, Bergek S, Chan YF, Jones FC, Kingsley DM, Peichel CL, Schluter D. Genetics of ecological divergence during speciation. Nature. 2014;511:307–311. doi: 10.1038/nature13301. - DOI - PMC - PubMed
    1. Atkinson BA, Stockey RA, Rothwell GW. Cretaceous origin of dogwoods: an anatomically preserved Cornus (Cornaceae) fruit from the campanian of Vancouver island. PeerJ. 2016;4:e2808. doi: 10.7717/peerj.2808. - DOI - PMC - PubMed
    1. Barrett RD, Hoekstra HE. Molecular spandrels: tests of adaptation at the genetic level. Nature Reviews Genetics. 2011;12:767–780. doi: 10.1038/nrg3015. - DOI - PubMed
    1. Boufford DE, Spongberg SA. Eastern Asian-Eastern north american phytogeographical Relationships-A history from the time of linnaeus to the twentieth century. Annals of the Missouri Botanical Garden. 1983;70:423–439. doi: 10.2307/2992081. - DOI

Publication types