1. Evolutionary Biology
  2. Plant Biology

Natural selection and repeated patterns of molecular evolution following allopatric divergence

  1. Yibo Dong
  2. Shichao Chen
  3. Shifeng Cheng
  4. Wenbin Zhou
  5. Qing Ma
  6. Zhiduan Chen
  7. Cheng-Xin Fu
  8. Xin Liu  Is a corresponding author
  9. Yun-peng Zhao  Is a corresponding author
  10. Pamela S Soltis  Is a corresponding author
  11. Gane Ka-Shu Wong  Is a corresponding author
  12. Douglas E Soltis  Is a corresponding author
  13. Jenny Xiang  Is a corresponding author
  1. North Carolina State University, United States
  2. Noble Research Institute, United States
  3. Florida Museum of Natural History, University of Florida, United States
  4. University of Florida, United States
  5. Tongji University, China
  6. Beijing Genomics Institute, China
  7. Institute of Botany, Chinese Academy of Sciences, China
  8. Zhejiang University, China
  9. University of Alberta, Canada
https://doi.org/10.7554/eLife.45199
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Cite this article
  1. Yibo Dong
  2. Shichao Chen
  3. Shifeng Cheng
  4. Wenbin Zhou
  5. Qing Ma
  6. Zhiduan Chen
  7. Cheng-Xin Fu
  8. Xin Liu
  9. Yun-peng Zhao
  10. Pamela S Soltis
  11. Gane Ka-Shu Wong
  12. Douglas E Soltis
  13. Jenny Xiang
(2019)
Natural selection and repeated patterns of molecular evolution following allopatric divergence
eLife 8:e45199.
https://doi.org/10.7554/eLife.45199
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29 figures, 3 tables and 13 additional files

Figures

Figure 1
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Frequency distribution of synonymous substitutions per synonymous site (Ks) of putative orthologs (POGs) from leaf transcriptomes of 20 species/variety pairs of angiosperms.
https://doi.org/10.7554/eLife.45199.003
Figure 2
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Frequency distribution of nonsynonymous substitutions per non-sysnonymous site (Ka) of putative orthologs (POGs) of leaf transcriptomes from 20 species/variety pairs of angiosperms.
https://doi.org/10.7554/eLife.45199.004
Figure 3
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Frequency distribution of Ka/Ks ratios of putative orthologs (POGs) from leaf transcriptomes of 20 species/variety pairs of angiosperms.
https://doi.org/10.7554/eLife.45199.005
Figure 4
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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.

https://doi.org/10.7554/eLife.45199.006
Figure 5 with 1 supplement
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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.

https://doi.org/10.7554/eLife.45199.008
Figure 5—figure supplement 1
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Divergence times of 20 taxon pairs estimated with 79 single copy orthologs present in 90% or more species using BEAST.
https://doi.org/10.7554/eLife.45199.009
Figure 6
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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.

https://doi.org/10.7554/eLife.45199.010
Figure 7 with 2 supplements
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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.
https://doi.org/10.7554/eLife.45199.012
Figure 7—figure supplement 1
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Relative abundance of Ka/Ks > 2 genes annotated to different functions in the Biological Process category; drawn from data in Supplementary file 5.
https://doi.org/10.7554/eLife.45199.013
Figure 7—figure supplement 2
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Relative abundance of Ka/Ks > 2 genes annotated to different functions of in the Molecular Function category; drawn from data in Supplementary file 5.
https://doi.org/10.7554/eLife.45199.014
Appendix 1—figure 1
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Phylogenetic positions of orders represented by species pairs sampled in the angiosperm phylogeny.

Phylogenetic tree was taken from Angiosperm phylogeny website.

https://doi.org/10.7554/eLife.45199.029
Appendix 1—figure 2
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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.

https://doi.org/10.7554/eLife.45199.030
Appendix 1—figure 3
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Acorus.

https://doi.org/10.7554/eLife.45199.031
Appendix 1—figure 4
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Calycanthus.

https://doi.org/10.7554/eLife.45199.032
Appendix 1—figure 5
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Campsis.

https://doi.org/10.7554/eLife.45199.033
Appendix 1—figure 6
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Convallaria.

https://doi.org/10.7554/eLife.45199.034
Appendix 1—figure 7
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Cornus-1.

https://doi.org/10.7554/eLife.45199.035
Appendix 1—figure 8
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Cornus-2.

https://doi.org/10.7554/eLife.45199.036
Appendix 1—figure 9
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Cotinus.

https://doi.org/10.7554/eLife.45199.037
Appendix 1—figure 10
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Croomia.

https://doi.org/10.7554/eLife.45199.038
Appendix 1—figure 11
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Dysosma.

https://doi.org/10.7554/eLife.45199.039
Appendix 1—figure 12
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Gelsemium.

https://doi.org/10.7554/eLife.45199.040
Appendix 1—figure 13
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Hamamelis.

https://doi.org/10.7554/eLife.45199.041
Appendix 1—figure 14
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Liquidarnbar.

https://doi.org/10.7554/eLife.45199.042
Appendix 1—figure 15
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Liriodendron.

https://doi.org/10.7554/eLife.45199.043
Appendix 1—figure 16
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Meehania.

https://doi.org/10.7554/eLife.45199.044
Appendix 1—figure 17
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Menispermum.

https://doi.org/10.7554/eLife.45199.045
Appendix 1—figure 18
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Nelumbo.

https://doi.org/10.7554/eLife.45199.046
Appendix 1—figure 19
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Penthorum.

https://doi.org/10.7554/eLife.45199.047
Appendix 1—figure 20
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Phryma.

https://doi.org/10.7554/eLife.45199.048
Appendix 1—figure 21
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Sassafras.

https://doi.org/10.7554/eLife.45199.049
Appendix 1—figure 22
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Plot of Ka and Ks values for each POG in 20 taxon pairs, in alphabetical order of genus names.

Saururus.

https://doi.org/10.7554/eLife.45199.050

Tables

Table 1
List of biogeographic pairs and number of examined putative single copy orthologs (POGs) (sum from two species), maximum length (MAL), minimum length (MIL), and average length (AL) of POGs, number of POGs mapped to single copy genes in seed plants (NSP) and number of POGs that were mapped to single copy genes in 20 angiosperm plants (NAP).
https://doi.org/10.7554/eLife.45199.002
GeneraSpeciesDistribution#of
POGs		MAL of POGs (bp)MIL of POGs (bp)AL of POGs (bp)NSP of POGsNAP of
POGs
AcorusA.calamus, A.gramineusEA-Asia/America17192/262131028747781
CalycanthusC.chinensis, C.occidentalisEA-WNA23116/2670510290896152
CampsisC.grandiflora, C.radicansEA-ENA20840/2569710273466112
ConvallariaC.majalis var. keiskei, C.majalisvar. MontanaEA-ENA30322/270411025025375
Cornus-1 C.ellipica, C.floridaEA-ENA24398/25682102800154259
Cornus-2C.alternifolia, C.controversaEA-ENA26490/27455102836210323
CotinusC.coggygria, C.obovatusEurasia-ENA26494/27374102889237361
CroomiaC.japonica,C.paueifloraEA-ENA23160/2648010281771112
DysosmaD.pleiantha, D.versipellisAsia*24270/211694102944132218
GelsemiumG.elegans, G.sempervirensEA-ENA22774/26801102980129194
HamamelisH.japonica, H.vernalisEA-ENA23052/27308102955221365
LiquidarnbarL.styraciflua, L.formosanaEA-ENA24844/27041102893196343
LiriodendronL.chinense, L.tulipiferaEA-ENA23060/2705310274877120
MeehaniaM.fargesii, M.cordataEA-ENA25622/2556210291997166
MenispermumM.canadense, M.dauricumEA-ENA27490/2734710244960121
NelumboN.lutea, N.nuciferaEA-ENA23988/27329102774138220
PenthorumP.chinense, P.sedoidesEA-ENA23288/215225102882161245
PhrymaP.aleptostachya, P.leptostachyaEA-ENA25096/211445102863106180
SassafrasS.albidum, S.tzumuEA-ENA25070/27524102809104153
SaururusS.cernuus, S.chinensisEA-ENA19386/263001028885384

  1. *Evergreen-deciduous forests pair.

Table 2
The number of POGs under strong positive selection (Ka/Ks > 2) in each taxon pair and results from Blast Search.
https://doi.org/10.7554/eLife.45199.007
GeneraTotalWith blast (without hits)With blast hitsWith mappingWith GO annotation
Acorus10118201746
Calycanthus11514202556
Campsis725151042
Convallaria12351121545
Cornus-112317162367
Cornus-21167122968
Cotinus12440111360
Croomia17032292089
Dysosma10836141840
Gelsemium67510844
Hamamelis11428152645
Liquidambar12223192159
Liriodendron781571937
Meehania851214752
Menispermum1061861963
Nelumbo18493239104
Penthorum93516963
Phryma1194241675
Sassafras15924273177
Saururus1027211658
Table 3
Number of genes with Ka/Ks > 2 ratios annotated to Integral Component of Membrane.
https://doi.org/10.7554/eLife.45199.011
GeneraIntegral component of membrane
Acorus12
Calycanthus13
Campsis12
Convallaria8
Cornus-120
Cornus-212
Cotinus18
Croomia26
Dysosma7
Gelsemium7
Hamamelis16
Liquidarnbar15
Liriodendron7
Meehania10
Menispermum14
Nelumbo26
Penthorum15
Phryma13
Sassafras21
Saururus16

Additional files

Supplementary file 1

Total number of orthologous gene families, number of putative single copy orthologous gene pairs (POGs) in each taxon pair, and the proportion of POGs.

https://doi.org/10.7554/eLife.45199.015
Supplementary file 2

Frequency of Ks values in 0.01 intervals of all pairs.

https://doi.org/10.7554/eLife.45199.016
Supplementary file 3

Number and relative abundance in percentage of POGs with Ka/Ks values distributed in different interval categories.

https://doi.org/10.7554/eLife.45199.017
Supplementary file 4

Information of divergence time estimated from BEAST using seven SCG genes shared by all 40 taxa on a global phylogeny, Ks value in peak frequency, and relative abundance of POGs in three Ka/Ks ratio ranges used in correlation analyses shown in Figures 5 and 6.

https://doi.org/10.7554/eLife.45199.018
Supplementary file 5

Results of gene annotation for genes with Ka/Ks > 2.

https://doi.org/10.7554/eLife.45199.019
Supplementary file 6

Results from Variation Cluster analysis of POGs with Ka/Ks > 2.

https://doi.org/10.7554/eLife.45199.020
Supplementary file 7

Data and results from scatter plot between divergence time and Ka/Ks ratio of 79 POGs shared by 90% or more taxon pairs.

https://doi.org/10.7554/eLife.45199.021
Supplementary file 8

Data and results for scatter plot of divergence time and Ka/Ks ratio (with Ka/Ks > 0.5 data points removed) of 79 POGs shared by 90% or more taxon pairs.

https://doi.org/10.7554/eLife.45199.022
Supplementary file 9

Functions of genes annotated as integral_compotent_of_membrane predicted from Blast2Go analysis.

https://doi.org/10.7554/eLife.45199.023
Supplementary file 10

Relationships among Ks in peak abundance, relative abundance of genes in different ranges of selection pressures (Ka/Ks ratios), and divergence time.

https://doi.org/10.7554/eLife.45199.024
Supplementary file 11

Source of leaf materials used for the study.

https://doi.org/10.7554/eLife.45199.025
Supplementary file 12

Number of genes with different category value of Ks and Ka/Ks in each species pair.

https://doi.org/10.7554/eLife.45199.026
Transparent reporting form
https://doi.org/10.7554/eLife.45199.027

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  1. Yibo Dong
  2. Shichao Chen
  3. Shifeng Cheng
  4. Wenbin Zhou
  5. Qing Ma
  6. Zhiduan Chen
  7. Cheng-Xin Fu
  8. Xin Liu
  9. Yun-peng Zhao
  10. Pamela S Soltis
  11. Gane Ka-Shu Wong
  12. Douglas E Soltis
  13. Jenny Xiang
(2019)
Natural selection and repeated patterns of molecular evolution following allopatric divergence
eLife 8:e45199.
https://doi.org/10.7554/eLife.45199