Advertisement

Stick to the Bush

Can the underlying genetic changes driving the divergence of populations into new species be predicted or repeated? Soria-Carrasco et al. (p. 738) investigated the genetic changes observed after one generation when stick insect (Timema cristinae) populations were transplanted from their preferred host plants to alternative hosts. Diverged genetic regions were relatively small, with most loci showing divergence in a single population pair. However, the number of loci showing parallel divergence was greater than expected by chance. Thus, selection can drive parallel phenotypic evolution via parallel genetic changes.

Abstract

Natural selection can drive the repeated evolution of reproductive isolation, but the genomic basis of parallel speciation remains poorly understood. We analyzed whole-genome divergence between replicate pairs of stick insect populations that are adapted to different host plants and undergoing parallel speciation. We found thousands of modest-sized genomic regions of accentuated divergence between populations, most of which are unique to individual population pairs. We also detected parallel genomic divergence across population pairs involving an excess of coding genes with specific molecular functions. Regions of parallel genomic divergence in nature exhibited exceptional allele frequency changes between hosts in a field transplant experiment. The results advance understanding of biological diversification by providing convergent observational and experimental evidence for selection’s role in driving repeatable genomic divergence.

Get full access to this article

View all available purchase options and get full access to this article.

Already a subscriber or AAAS Member? Log In

Supplementary Material

Summary

Materials and Methods
Supplementary Text
Figs. S1 to S6
Tables S1 to S6
References (2680)

Resources

File (soria-carrasco.sm.pdf)

References and Notes

1
Stern D. L., The genetic causes of convergent evolution. Nat. Rev. Genet. 14, 751–764 (2013).
2
Barrett R. D. H., Hoekstra H. E., Molecular spandrels: Tests of adaptation at the genetic level. Nat. Rev. Genet. 12, 767–780 (2011).
3
Burke M. K., How does adaptation sweep through the genome? Insights from long-term selection experiments. Proc. R. Soc. London Ser. B 279, 5029–5038 (2012).
4
Weinreich D. M., Delaney N. F., Depristo M. A., Hartl D. L., Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312, 111–114 (2006).
5
Meyer J. R., Dobias D. T., Weitz J. S., Barrick J. E., Quick R. T., Lenski R. E., Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 335, 428–432 (2012).
6
J. B. Losos, Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of Anoles (Univ. California Press, Berkeley, CA, 2009).
7
Jones F. C., Grabherr M. G., Chan Y. F., Russell P., Mauceli E., Johnson J., Swofford R., Pirun M., Zody M. C., White S., Birney E., Searle S., Schmutz J., Grimwood J., Dickson M. C., Myers R. M., Miller C. T., Summers B. R., Knecht A. K., Brady S. D., Zhang H., Pollen A. A., Howes T., Amemiya C., Baldwin J., Bloom T., Jaffe D. B., Nicol R., Wilkinson J., Lander E. S., Di Palma F., Lindblad-Toh K., Kingsley D. M., The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55–61 (2012).
8
Conte G. L., Arnegard M. E., Peichel C. L., Schluter D., The probability of genetic parallelism and convergence in natural populations. Proc. R. Soc. London Ser. B 279, 5039–5047 (2012).
9
Heliconius Genome Consortium, Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487, 94–98 (2012).
10
Schluter D., Nagel L. M., Parallel speciation by natural selection. Am. Nat. 146, 292–301 (1995).
11
Feder J. L., Egan S. P., Nosil P., The genomics of speciation-with-gene-flow. Trends Genet. 28, 342–350 (2012).
12
Ellegren H., Smeds L., Burri R., Olason P. I., Backström N., Kawakami T., Künstner A., Mäkinen H., Nadachowska-Brzyska K., Qvarnström A., Uebbing S., Wolf J. B., The genomic landscape of species divergence in Ficedula flycatchers. Nature 491, 756–760 (2012).
13
Martin S. H., Dasmahapatra K. K., Nadeau N. J., Salazar C., Walters J. R., Simpson F., Blaxter M., Manica A., Mallet J., Jiggins C. D., Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Res. 23, 1817–1828 (2013).
14
Ellegren H., Genome sequencing and population genomics in non-model organisms. Trends Ecol. Evol. 29, 51–63 (2014).
15
Nosil P., Divergent host plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking sticks. Am. Nat. 169, 151–162 (2007).
16
Nosil P., Gompert Z., Farkas T. E., Comeault A. A., Feder J. L., Buerkle C. A., Parchman T. L., Genomic consequences of multiple speciation processes in a stick insect. Proc. R. Soc. London Ser. B 279, 5058–5065 (2012).
17
Nosil P., Crespi B. J., Sandoval C. P., Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature 417, 440–443 (2002).
18
Gompert Z., Comeault A. A., Farkas T. E., Feder J. L., Parchman T. L., Buerkle C. A., Nosil P., Experimental evidence for ecological selection on genome variation in the wild. Ecol. Lett. 17, 369–379 (2014).
19
Materials and methods are available as supplementary materials on Science Online.
20
Lawniczak M. K. N., Emrich S. J., Holloway A. K., Regier A. P., Olson M., White B., Redmond S., Fulton L., Appelbaum E., Godfrey J., Farmer C., Chinwalla A., Yang S. P., Minx P., Nelson J., Kyung K., Walenz B. P., Garcia-Hernandez E., Aguiar M., Viswanathan L. D., Rogers Y. H., Strausberg R. L., Saski C. A., Lawson D., Collins F. H., Kafatos F. C., Christophides G. K., Clifton S. W., Kirkness E. F., Besansky N. J., Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 330, 512–514 (2010).
21
Renaut S., Grassa C. J., Yeaman S., Moyers B. T., Lai Z., Kane N. C., Bowers J. E., Burke J. M., Rieseberg L. H., Genomic islands of divergence are not affected by geography of speciation in sunflowers. Nature Commun. 4, 1827 (2013).
22
Hofer T., Foll M., Excoffier L., Evolutionary forces shaping genomic islands of population differentiation in humans. BMC Genomics 13, 107 (2012).
23
van Ooik T., Rantala M. J., Local adaptation of an insect herbivore to a heavy metal contaminated environment. Ann. Zool. Fenn. 47, 215–222 (2010).
24
J. F. V. Vincent, Structural Biomaterials (Princeton Univ. Press, Princeton, NJ, 1990).
25
Dittmer N. T., Kanost M. R., Insect multicopper oxidases: diversity, properties, and physiological roles. Insect Biochem. Mol. Biol. 40, 179–188 (2010).
26
E. E. Hare, J. S. Johnston, “Genome size determination using flow cytometry of propidium iodide-stained nuclei,” in Molecular Methods for Evolutionary Genetics, V. Orgogozo, M. V. Rockman, Eds. (Humana, New York, 2011), vol. 772, pp. 3–12.
27
Li R., Zhu H., Ruan J., Qian W., Fang X., Shi Z., Li Y., Li S., Shan G., Kristiansen K., Li S., Yang H., Wang J., Wang J., De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 20, 265–272 (2010).
28
Gnerre S., Maccallum I., Przybylski D., Ribeiro F. J., Burton J. N., Walker B. J., Sharpe T., Hall G., Shea T. P., Sykes S., Berlin A. M., Aird D., Costello M., Daza R., Williams L., Nicol R., Gnirke A., Nusbaum C., Lander E. S., Jaffe D. B., High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc. Natl. Acad. Sci. U.S.A. 108, 1513–1518 (2011).
29
Comeault A. A., Sommers M., Schwander T., Buerkle C. A., Farkas T. E., Nosil P., Parchman T. L., De novo characterization of the Timema cristinae transcriptome facilitates marker discovery and inference of genetic divergence. Mol. Ecol. Resour. 12, 549–561 (2012).
30
Yandell M., Ence D., A beginner’s guide to eukaryotic genome annotation. Nat. Rev. Genet. 13, 329–342 (2012).
31
Holt C., Yandell M., MAKER2: An annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics 12, 491 (2011).
32
A. F. A. Smit, R. Hubley, P. Green, RepeatMasker Open-4.0, 1996-2013 (2013); www.repeatmasker.org.
33
Benson G., Tandem repeats finder: A program to analyze DNA sequences. Nucleic Acids Res. 27, 573–580 (1999).
34
Jurka J., Kapitonov V. V., Pavlicek A., Klonowski P., Kohany O., Walichiewicz J., Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110, 462–467 (2005).
35
Wheeler T. J., Clements J., Eddy S. R., Hubley R., Jones T. A., Jurka J., Smit A. F., Finn R. D., Dfam: A database of repetitive DNA based on profile hidden Markov models. Nucleic Acids Res. 41, D70–D82 (2013).
36
Korf I., Gene finding in novel genomes. BMC Bioinformatics 5, 59 (2004).
37
Ter-Hovhannisyan V., Lomsadze A., Chernoff Y. O., Borodovsky M., Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res. 18, 1979–1990 (2008).
38
Parra G., Bradnam K., Korf I., CEGMA: A pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23, 1061–1067 (2007).
39
Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., Madden T. L., BLAST+: Architecture and applications. BMC Bioinformatics 10, 421 (2009).
40
Birney E., Clamp M., Durbin R., GeneWise and Genomewise. Genome Res. 14, 988–995 (2004).
41
S. R. Eddy, “A new generation of homology search tools based on probabilistic inference,” in Genome Informatics 2009, S. Morishita et al., Eds. (Genome Informatics Series, Imperial College Press, London, 2009), vol. 23, pp. 205–211.
42
Parra G., Blanco E., Guigó R., GeneID in Drosophila. Genome Res. 10, 511–515 (2000).
43
Magrane M., Consortium U., UniProt Knowledgebase: A hub of integrated protein data. Database 2011, bar009 (2011).
44
Letsch H. O., Meusemann K., Wipfler B., Schütte K., Beutel R., Misof B., Insect phylogenomics: results, problems and the impact of matrix composition. Proc. Biol. Sci. 279, 3282–3290 (2012).
45
Falgueras J., Lara A. J., Fernández-Pozo N., Cantón F. R., Pérez-Trabado G., Claros M. G., SeqTrim: A high-throughput pipeline for pre-processing any type of sequence read. BMC Bioinformatics 11, 38 (2010).
46
Grabherr M. G., Haas B. J., Yassour M., Levin J. Z., Thompson D. A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q., Chen Z., Mauceli E., Hacohen N., Gnirke A., Rhind N., di Palma F., Birren B. W., Nusbaum C., Lindblad-Toh K., Friedman N., Regev A., Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).
47
Slater G. S. C., Birney E., Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6, 31 (2005).
48
Eilbeck K., Moore B., Holt C., Yandell M., Quantitative measures for the management and comparison of annotated genomes. BMC Bioinformatics 10, 67 (2009).
49
Quevillon E., Silventoinen V., Pillai S., Harte N., Mulder N., Apweiler R., Lopez R., InterProScan: Protein domains identifier. Nucleic Acids Res. 33 (suppl. 2), W116–W120 (2005).
50
Li R., Ye J., Li S., Wang J., Han Y., Ye C., Wang J., Yang H., Yu J., Wong G. K., Wang J., ReAS: Recovery of ancestral sequences for transposable elements from the unassembled reads of a whole genome shotgun. PLOS Comput. Biol. 1, e43 (2005).
51
Price A. L., Jones N. C., Pevzner P. A., De novo identification of repeat families in large genomes. Bioinformatics 21 (suppl. 1), i351–i358 (2005).
52
Edgar R. C., Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).
53
Feschotte C., Keswani U., Ranganathan N., Guibotsy M. L., Levine D., Exploring repetitive DNA landscapes using REPCLASS, a tool that automates the classification of transposable elements in eukaryotic genomes. Genome Biol. Evol. 1, 205–220 (2009).
54
Jurka J., Bao W., Kojima K. K., Families of transposable elements, population structure and the origin of species. Biol. Direct 6, 44 (2011).
55
Li H., Durbin R., Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
56
Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R.1000 Genome Project Data Processing Subgroup, The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
57
Jombart T., Devillard S., Balloux F., Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genet. 11, 94 (2010).
58
Tan Y. D., Fu Y. X., A novel method for estimating linkage maps. Genetics 173, 2383–2390 (2006).
59
A. Stamatakis, A. J. Aberer, paper presented at the 27th IEEE International on Parallel and Distributed Processing Symposium (IPDPS), Boston, MA, 20 to 24 May 2013.
60
Stamatakis A., RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006).
61
M. Simonsen, T. Mailund, C. N. Pedersen, in Algorithms in Bioinformatics: 8th International Workshop, WABI 2008, Karlsruhe, Germany, September 2008 Proceedings, K. Crandall, J. Lagergren, Eds. (vol. 5251 of Lecture Notes in Computer Science, Springer-Verlag, Berlin, 2008), pp. 113–122.
62
Price M. N., Dehal P. S., Arkin A. P., FastTree 2—approximately maximum-likelihood trees for large alignments. PLOS ONE 5, e9490 (2010).
63
Bergsten J., A review of long-branch attraction. Cladistics 21, 163–193 (2005).
64
Stamatakis A., RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312 –1313 (2014).
65
Shimodaira H., Hasegawa M., CONSEL: For assessing the confidence of phylogenetic tree selection. Bioinformatics 17, 1246–1247 (2001).
66
Shimodaira H., An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 51, 492–508 (2002).
67
R Development Core Team, R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2013); www.R-project.org.
68
Dray S., Dufour A.-B., The ade4 package: Implementing the duality diagram for ecologists. J. Stat. Softw. 22, 1–20 (2007).
69
Hudson R. R., Slatkin M., Maddison W. P., Estimation of levels of gene flow from DNA sequence data. Genetics 132, 583–589 (1992).
70
Bhatia G., Patterson N., Sankararaman S., Price A. L., Estimating and interpreting FST: The impact of rare variants. Genome Res. 23, 1514–1521 (2013).
71
Li H., A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27, 2987–2993 (2011).
72
Baum L. E., Petrie T., Soules G., Weiss N., A maximization technique occurring in statistical analysis of probabilistic functions of Markov chains. Ann. Math. Stat. 41, 164–171 (1970).
73
D. Harte, HiddenMarkov: Hidden Markov Models (2012); http://cran.r-project.org/web/packages/HiddenMarkov/index.html.
74
Nosil P., Crespi B. J., Experimental evidence that predation promotes divergence in adaptive radiation. Proc. Natl. Acad. Sci. U.S.A. 103, 9090–9095 (2006).
75
Sandoval C. P., The effects of relative geographical scales of gene flow and selection on morph frequencies in the walking-stick Timema cristinae. Evolution 48, 1866–1879 (1994).
76
Nosil P., Reproductive isolation caused by visual predation on migrants between divergent environments. Proc. R. Soc. London Ser. B 271, 1521–1528 (2004).
77
Sandoval C., Persistence of a walking-stick population (Phasmatoptera: Timematodea) after a wildfire. Southwest. Nat. 45, 123–127 (2000).
78
Gaggiotti O. E., Foll M., Quantifying population structure using the F-model. Mol. Ecol. Resour. 10, 821–830 (2010).
79
Falush D., Stephens M., Pritchard J. K., Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164, 1567–1587 (2003).
80
Nicholson G., Smith A. V., Jonsson F., Gustafsson O., Stefansson K., Donnelly P., Assessing population differentiation and isolation from single-nucleotide polymorphism data. J. R. Stat. Soc. Series B Stat. Methodol. 64, 695–715 (2002).
81
M. Galassi, J. Davies, J. Theiler, B. Gough, G. Jungman, M. Booth, F. Rossi, GNU Scientific Library Reference Manual (Network Theory Limited, Bristol, UK, ed. 3, 2009).

Information & Authors

Information

Published In

Science
Volume 344 | Issue 6185
16 May 2014

Submission history

Received: 12 February 2014
Accepted: 18 April 2014
Published in print: 16 May 2014

Permissions

Request permissions for this article.

Acknowledgments

The work was funded by the European Research Council (grant R/129639) and Utah State University start-up funds. We thank J. Slate, A. Beckerman, D. Schluter, and two anonymous reviewers for constructive feedback and the High-Throughput Genomics Group at the Wellcome Trust Centre for Human Genetics (funded by Wellcome Trust grant reference 090532/Z/09/Z and Medical Research Council Hub grant G0900747 91070) for generation of the sequencing data. O. Simakov and A. Kapusta provided scripts for transposable elements annotation. The data reported in this paper are tabulated in the supplementary materials and archived at the following databases. The raw sequencing reads are in the NCBI short read archive (BioProject ID: PRJNA243533), and the whole genome assembly and annotation at http://nosil-lab.group.shef.ac.uk/resources. Additional data and computer source code have been deposited in the Dryad repository, datadryad.org, and are also available from the authors upon request. The authors declare no conflicts of interest.

Authors

Affiliations

Víctor Soria-Carrasco*
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
Zachariah Gompert*
Department of Biology, Utah State University, Logan, UT 84322, USA.
Aaron A. Comeault
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
Timothy E. Farkas
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
Thomas L. Parchman
Deparment of Biology, University of Nevada, Reno, NV 89557, USA.
J. Spencer Johnston
Department of Entomology, Texas A&M University, College Station, TX 77843, USA.
C. Alex Buerkle
Department of Botany, University of Wyoming, Laramie, WY 82071, USA.
Jeffrey L. Feder
Department of Biology, Notre Dame University, South Bend, IN 46556, USA.
Jens Bast
J. F. Blumenbach Institute of Zoology and Anthropology, University of Göttingen, 37073 Göttingen, Germany.
Tanja Schwander
Department of Ecology and Evolution, University of Lausanne, Lausanne CH-1015, Switzerland.
Scott P. Egan
Department of Ecology and Evolutionary Biology, Rice University, Houston, TX 77005, USA.
Bernard J. Crespi
Department of Biological Sciences, Simon Fraser University, Burnaby, BC V5A 1S6, Canada.
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.

Notes

*
These authors contributed equally to this work.
Corresponding author. E-mail: [email protected]

Metrics & Citations

Metrics

Article Usage
Altmetrics

Citations

Export citation

Select the format you want to export the citation of this publication.

Cited by

  1. Convergent consequences of parthenogenesis on stick insect genomes, Science Advances, 8, 8, (2022)./doi/10.1126/sciadv.abg3842
    Abstract
  2. Selection on ancestral genetic variation fuels repeated ecotype formation in bottlenose dolphins, Science Advances, 7, 44, (2021)./doi/10.1126/sciadv.abg1245
    Abstract
  3. Large-scale mutation in the evolution of a gene complex for cryptic coloration, Science, 369, 6502, (460-466), (2021)./doi/10.1126/science.aaz4351
    Abstract
  4. Natural selection and the predictability of evolution in Timema stick insects, Science, 359, 6377, (765-770), (2021)./doi/10.1126/science.aap9125
    Abstract
  5. Convergent local adaptation to climate in distantly related conifers, Science, 353, 6306, (1431-1433), (2021)./doi/10.1126/science.aaf7812
    Abstract
  6. Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake, Science, 350, 6267, (1493-1498), (2015)./doi/10.1126/science.aac9927
    Abstract
Loading...

View Options

Get Access

Log in to view the full text

AAAS ID LOGIN

AAAS login provides access to Science for AAAS Members, and access to other journals in the Science family to users who have purchased individual subscriptions.

Log in via OpenAthens.
Log in via Shibboleth.
More options

Register for free to read this article

As a service to the community, this article is available for free. Login or register for free to read this article.

Purchase this issue in print

Buy a single issue of Science for just $15 USD.

View options

PDF format

Download this article as a PDF file

Download PDF

Media

Figures

Multimedia

Tables

Share

Share

Share article link

Share on social media