Comparative transcriptomics reveals the conserved building blocks involved in parallel evolution of diverse phenotypic traits in ants

Genome Biology

Volumn 17, Issue 1, 2016, Pages

  Morandin, Claire ^a,b   Tin, Mandy M Y ^c   Abril, Sílvia ^d   Gómez, Crisanto ^d   Pontieri, Luigi ^e   Schiøtt, Morten ^e   Sundström, Liselotte ^a,b   Tsuji, Kazuki ^f   Pedersen, Jes Søe ^e   Helanterä, Heikki ^a,b   Mikheyev, Alexander S ^c,g  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^d UNIVERSITY OF GIRONA   (Spain)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f UNIVERSITY OF THE RYUKYUS   (Japan)

^g AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Caste differentiation; Gene co expression network; Gene expression; Parallel evolution; Phenotypic plasticity; Social insects

Indexed keywords

DIFFERENTIATION; GENE EXPRESSION; HUMAN; HUMAN EXPERIMENT; INSECT; PHENOTYPE; SPECIES; TRANSCRIPTOMICS; WORKER; ANIMAL; ANIMAL BEHAVIOR; ANT; GENETICS; MOLECULAR EVOLUTION; REPRODUCTION;

TRANSCRIPTOME;

ANIMALS; ANTS; BEHAVIOR, ANIMAL; EVOLUTION, MOLECULAR; PHENOTYPE; REPRODUCTION; TRANSCRIPTOME;

EID: 84962141674     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-016-0902-7     Document Type: Article

References (93)

1. Stearns SC. The evolutionary significance of phenotypic plasticity. Bioscience. 1989;39:436-45.
2. West-Eberhard MJ. Developmental plasticity and evolution. Oxford: Oxford University Press; 2003.
3. West-Eberhard MJ. Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst. 1989;20:249-78.
4. Zhang J, Kumar S. Detection of convergent and parallel evolution at the amino acid sequence level. Mol Biol Evol. 1996;14:527-36.
5. Stern DL. The genetic causes of convergent evolution. Nat Rev Genet. 2013;14:751-64.
6. Rodríguez-Verdugo A, Gaut BS, Tenaillon O. Evolution of Escherichia coli rifampicin resistance in an antibiotic-free environment during thermal stress. BMC Evol Biol. 2013;13:50.
7. Jackson DJ, McDougall C, Woodcroft B, Moase P, Rose R, Kube M, et al. Parallel evolution of nacre building gene sets in molluscs. Mol Biol Evol. 2010;27:591-608.
8. Saenko S, French V, Brakefield PM, Beldade P. Conserved developmental processes and the formation of evolutionary novelties: examples from butterfly wings. Philos Trans R Soc Lond B Biol Sci. 2008;363:1549-55.
9. True JR, Carroll SB. Gene co-option in physiological and morphological evolution. Annu Rev Cell Dev Biol. 2002;18:53-80.
10. Page R, Amdam G. The making of a social insect: developmental architectures of social design. Bioessays. 2007;29:334-43.
11. Kuraku S, Usuda R, Kuratani S. Comprehensive survey of carapacial ridge-specific genes in turtle implies co-option of some regulatory genes in carapace evolution. Evol Dev. 2005;17:3-17.
12. Beldade P, Brakefield PM, Long AD. Generating phenotypic variation: prospects from "evo-devo" research on Bicyclus anynana wing patterns. Evol Dev. 2005;7:101-7.
13. Galant R, Skeath JB, Paddock S, Lewis DL, Carroll SB. Expression pattern of a butterfly achaete-scute homolog reveals the homology of butterfly wing scales and insect sensory bristles. Curr Biol. 1998;8:807-13.
14. Stuart JM, Segal E, Koller D, Kim SK. A gene-coexpression network for global discovery of conserved genetic modules. Science. 2003;302:249-55.
15. Lynch M. The evolution of genetic networks by non-adaptive processes. Nat Rev Genet. 2007;8:803-13.
16. Wilson EO. The insect societies. Cambridge, Massachusetts, USA: Harvard University Press; 1971.
17. Szathmáry E, Smith JM. The major evolutionary transitions. Nature. 1995;374:227-32.
18. Bourke AF. Principles of social evolution. Oxford: Oxford University Press; 2011.
19. Morandin C, Dhaygude K, Paviala J, Trontti K, Wheat C, Helanterä H. Caste-biases in gene expression are specific to developmental stage in the ant Formica exsecta. J Evol Biol. 2015;28:1705-18.
20. Toth AL, Robinson GE. Evo-devo and the evolution of social behavior. Trends Genet. 2007;23:334-41.
21. Toth AL, Varala K, Henshaw MT, Rodriguez-Zas SL, Hudson ME, Robinson GE. Brain transcriptomic analysis in paper wasps identifies genes associated with behaviour across social insect lineages. Proc Biol Sci. 2010;277:2139-48.
22. Toth AL, Tooker JF, Radhakrishnan S, Minard R, Henshaw MT, Grozinger CM. Shared genes related to aggression, rather than chemical communication, are associated with reproductive dominance in paper wasps (Polistes metricus). BMC Genomics. 2014;15:75.
23. Daugherty T, Toth AL, Robinson GE. Nutrition and division of labor: Effects on foraging and brain gene expression in the paper wasp Polistes metricus. Mol Ecol. 2011;20:5337-47.
24. Berens AJ, Hunt JH, Toth AL. Comparative transcriptomics of convergent evolution: different genes but conserved pathways underlie caste phenotypes across lineages of eusocial insects. Mol Biol Evol. 2014;32:690-703.
25. Feldmeyer B, Elsner D, Foitzik S. Gene expression patterns associated with caste and reproductive status in ants: worker-specific genes are more derived than queen-specific ones. Mol Ecol. 2014;23:151-61.
26. Hall DW, Goodisman MAD. The effects of kin selection on rates of molecular evolution in social insects. Evolution. 2012;66:2080-93.
27. Linksvayer TA, Wade MJ. Genes with social effects are expected to harbor more sequence variation within and between species. Evolution. 2009;63:1685-96.
28. Hunt BG, Ometto L, Wurm Y, Shoemaker D, Yi S, Keller L, et al. Relaxed selection is a precursor to the evolution of phenotypic plasticity. Proc Natl Acad Sci U S A. 2011;108:15936-41.
29. Harpur BA, Kent CF, Molodtsova D, Lebon JMD, Alqarni AS, Owayss AA, et al. Population genomics of the honey bee reveals strong signatures of positive selection on worker traits. Proc Natl Acad Sci U S A. 2014;111:2614-9.
30. Hahn MW, Kern AD. Comparative genomics of centrality and essentiality in three eukaryotic protein-interaction networks. Mol Biol Evol. 2005;22:803-6.
31. Kim PM, Korbel JO, Gerstein MB. Positive selection at the protein network periphery: Evaluation in terms of structural constraints and cellular context. Proc Natl Acad Sci U S A. 2007;104:20274-9.
32. Krylov DM, Wolf YI, Rogozin IB, Koonin E. Gene loss, protein sequence divergence, gene dispensability, expression level, and interactivity are correlated in eukaryotic evolution. Genome Res. 2003;13:2229-35.
33. Mikheyev AS, Linksvayer T. Genes associated with ant social behavior show distinct transcriptional and evolutionary patterns. Elife. 2015;4:e04775.
34. Jasper WC, Linksvayer TA, Atallah J, Friedman D, Chiu JC, Johnson BR. Large-scale coding sequence change underlies the evolution of postdevelopmental novelty in honey bees. Mol Biol Evol. 2014;32:334-46.
35. Wilkins AS. "The genetic tool-kit": the life-history of an important metaphor. In: Streelman JT, editor. Advances in evolutionary developmental biology. Hoboken, NJ: John Wiley & Sons, Inc.; 2013. doi: 10.1002/9781118707449.ch12014.
36. Woodard SH, Fischman BJ, Venkat A, Hudson ME, Varala K, Cameron SA, et al. Genes involved in convergent evolution of eusociality in bees. Proc Natl Acad Sci U S A. 2011;108:7472-7.
37. Fischman BJ, Woodard SH, Robinson GE. Molecular evolutionary analyses of insect societies. Proc Natl Acad Sci U S A. 2011;108:10847-54.
38. Oldham MC, Konopka G, Iwamoto K, Langfelder P, Kato T, Horvath S, et al. Functional organization of the transcriptome in human brain. Nat Neurosci. 2008;11:1271-82.
39. Zhang B, Horvath S. A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol. 2005;4:17.
40. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9:559.
41. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8:1494-512.
42. Grabherr M, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol. 2013;29:644-52.
43. Hornett EA, Wheat CW. Quantitative RNA-Seq analysis in non-model species: assessing transcriptome assemblies as a scaffold and the utility of evolutionary divergent genomic reference species. BMC Genomics. 2012;13:361.
44. Ravasz E, Somera AL, Mongru DA, Oltvai ZN, Barabási AL. Hierarchical organization of modularity in metabolic networks. Science. 2002;297:1551-5.
45. Hadfield JD. MCMC methods for multi-respoinse generalized linear mixed models: The MCMCglmm R package. J Stat Softw. 2010;33:1-22.
46. Allen JD, Xie Y, Chen M, Girard L, Xiao G. Comparing statistical methods for constructing large scale gene networks. PLoS One. 2012;7:e29348.
47. Helmkampf M, Cash E, Gadau J. Evolution of the insect desaturase gene family with an emphasis on social hymenoptera. Mol Biol Evol. 2014;32:456-71.
48. Jovelin R, Phillips PC. Evolutionary rates and centrality in the yeast gene regulatory network. Genome Biol. 2009;10:R35.
49. Helanterä H, Strassmann JE, Carrillo J, Queller DC. Unicolonial ants: where do they come from, what are they and where are they going? Trends Ecol Evol. 2009;24:341-9.
50. Lowe S, Browne M, Boudjelas S. 100 of the world's worst invasive alien species: a selection from the global species database. Aliens Invasive Species Bull. 2000;12:12. http://www.issg.org/pdf/publications/worst_100/english_100_worst.pdf.
51. Huang MH, Wheeler DE, Fjerdingstad EJ. Mating system evolution and worker caste diversity in Pheidole ants. Mol Ecol. 2013;22:1998-2010.
52. Fournier D, Estoup A, Orivel J, Foucaud J, Jourdan H, Le Breton J, et al. Clonal reproduction by males and females in the little fire ant. Nature. 2005;435:1230-4.
53. Gruber M, Hoffmann BD, Ritchie PA, Lester PJ. The conundrum of the yellow crazy ant (Anoplolepis gracilipes) reproductive mode: No evidence for dependent lineage genetic caste determination. Insectes Soc. 2013;60:135-45.
54. Espadaler X, Rey S. Biological constraints and colony founding in the polygynous invasive ant Lasius neglectus (Hymenoptera, Formicidae). Insectes Soc. 2001;48:159-64.
55. Ellegren H, Parsch J. The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet. 2007;8:689-98.
56. Hunt BG, Wyder S, Elango N, Werren JH, Zdobnov EM, Yi S, et al. Sociality is linked to rates of protein evolution in a highly social insect. Mol Biol Evol. 2010;27:497-500.
57. Lemos B, Bettencourt BR, Meiklejohn CD, Hartl DL. Evolution of proteins and gene expression levels are coupled in Drosophila and are independently associated with mRNA abundance, protein length, and number of protein-protein interactions. Mol Biol Evol. 2005;22:1345-54.
58. Meisel RP. Towards a more nuanced understanding of the relationship between sex-biased gene expression and rates of protein-coding sequence evolution. Mol Biol Evol. 2011;28:1893-900.
59. Molodtsova D, Harpur BA, Kent CF, Seevananthan K, Zayed A. Pleiotropy constrains the evolution of protein but not regulatory sequences in a transcription regulatory network influencing complex social behaviors. Front Genet. 2014;5:431.
60. Harrison MC, Hammond RL, Mallon EB. Reproductive workers show queenlike gene expression in an intermediately eusocial insect, the buff-tailed bumble bee Bombus terrestris. Mol Ecol. 2015;24:3043-63.
61. Hoffman EA, Goodisman MAD. Gene expression and the evolution of phenotypic diversity in social wasps. BMC Biol. 2007;5:23.
62. Waterhouse RM, Zdobnov EM, Tegenfeldt F, Li J, Kriventseva E. OrthoDB: the hierarchical catalog of eukaryotic orthologs in 2011. Nucleic Acids Res. 2011;39:D283-8.
63. Khalturin K, Anton-Erxleben F, Sassmann S, Wittlieb J, Hemmrich G, Bosch TCG. A novel gene family controls species-specific morphological traits in Hydra. PLoS Biol. 2008;6:2436-49.
64. Ferreira PG, Patalano S, Chauhan R, Ffrench-Constant R, Gabaldón T, Guigó R, et al. Transcriptome analyses of primitively eusocial wasps reveal novel insights into the evolution of sociality and the origin of alternative phenotypes. Genome Biol. 2013;14:R20.
65. Simola DF, Wissler L, Donahue G, Waterhouse RM, Helmkampf M, Roux J, et al. Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality. Genome Res. 2013;21:1339-48.
66. Sumner S. The importance of genomic novelty in social evolution. Mol Ecol. 2014;23:26-8.
67. Bot ANM, Boomsma JJ. Variable metapleural gland size-allometries in Acromyrmex leafcutter ants (Hymenoptera: Formicidae). J Kansas Entomol Soc. 1996;69:375-83.
68. Sen Sarma M, Rodriguez-Zas SL, Hong F, Zhong S, Robinson GE. Transcriptomic profiling of central nervous system regions in three species of honey bee during dance communication behavior. PLoS One. 2009;4:e6408.
69. Miller JA, Horvath S, Geschwind DH. Divergence of human and mouse brain transcriptome highlights Alzheimer disease pathways. Proc Natl Acad Sci U S A. 2010;107:12698-703.
70. Voineagu I, Wang X, Johnston P, Lowe JK, Tian Y, Horvath S, et al. Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature. 2011;474:380-4.
71. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10-2.
72. Cox MP, Peterson DA, Biggs PJ. SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics. 2010;11:485.
73. Johansson H, Dhaygude K, Lindström S, Helanterä H, Sundström L, Trontti K. A metatranscriptomic approach to the identification of microbiota associated with the ant Formica exsecta. PLoS One. 2013;8:e79777.
74. Min XJ, Butler G, Storms R, Tsang A. OrfPredictor: predicting protein-coding regions in EST-derived sequences. Nucleic Acids Res. 2005;33:W677-80.
75. Gouzy J, Carrere S, Schiex T. FrameDP: sensitive peptide detection on noisy matured sequences. Bioinformatics. 2009;25:670-1.
76. Löytynoja A, Goldman N. Phylogeny-aware gap placement prevents errors in sequence alignment and evolutionary analysis. Science. 2008;320:1632-5.
77. Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005;33:511-8.
78. Ebersberger I, Strauss S, von Haeseler A. HaMStR: profile hidden markov model based search for orthologs in ESTs. BMC Evol Biol. 2009;9:157.
79. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011;12:323.
80. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139-40.
81. Penn O, Privman E, Ashkenazy H, Landan G, Graur D, Pupko T. GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Res. 2010;38:W23-8.
82. Gil M, Zanetti MS, Zoller S, Anisimova M. CodonPhyML: fast maximum likelihood phylogeny estimation under codon substitution models. Mol Biol Evol. 2013;30:1270-80.
83. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24:1586-91.
84. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21:3674-6.
85. Beissbarth T, Speed TP. GOstat: find statistically overrepresented Gene Ontologies within a group of genes. Bioinformatics. 2004;20:1464-5.
86. Langfelder P, Luo R, Oldham MC, Horvath S. Is my network module preserved and reproducible? PLoS Comput Biol. 2011;7:e1001057.
87. Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312-3.
88. Team RC. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2012.
89. Sanderson MJ. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol. vh2002;19:101-9.
90. Paradis E, Claude J, Strimmer K. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics. 2004;20:289-90.
91. Wurm Y, Uva P, Ricci F, Wang J, Jemielity S, Iseli C, et al. Fourmidable: a database for ant genomics. BMC Genomics. 2009;10:5.
92. He X, Zhang J. Why do hubs tend to be essential in protein networks? PLoS Genet. 2006;2:0826-34.
93. Yu G, Li F, Qin Y, Bo X, Wu Y, Wang S. GOSemSim: an R package for measuring semantic similarity among GO terms and gene products. Bioinformatics. 2010;26:976-8.