Relaxed selection is a precursor to the evolution of phenotypic plasticity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 38, 2011, Pages 15936-15941

  Hunt, Brendan G ^a   Ometto, Lino ^b,e   Wurm, Yannick ^b,c,f   Shoemaker, DeWayne ^d   Yi, Soojin V ^a   Keller, Laurent ^b   Goodisman, Michael A D ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^d CENTER FOR MEDICAL   (United States)

^e RESEARCH AND INNOVATION CENTRE   (Italy)

^f QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Eusociality; Protein evolution; Sex biased gene expression; Sexual dimorphism; Social insect

Indexed keywords

ANIMAL EXPERIMENT; ANT; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EVOLUTIONARY RATE; FEMALE; GENE EXPRESSION; HONEYBEE; INSECT CASTE; INSECT DEVELOPMENT; INSECT GENETICS; MALE; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NONHUMAN; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; SEXUAL DEVELOPMENT; SOLENOPSIS INVICTA;

ANIMALS; ANTS; BEES; EVOLUTION, MOLECULAR; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSECT PROTEINS; MALE; PHENOTYPE; PHYLOGENY; PRINCIPAL COMPONENT ANALYSIS; PUPA; SELECTION, GENETIC; SEX FACTORS; SOCIAL BEHAVIOR; SPECIES SPECIFICITY;

APIS MELLIFERA; APOIDEA; HEXAPODA; SOLENOPSIS GEMINATA; SOLENOPSIS INVICTA;

EID: 80053169442     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1104825108     Document Type: Article

References (70)

1. West-Eberhard MJ (2003) Developmental Plasticity and Evolution (Oxford Univ Press, New York).
2. Nijhout HF (2003) Development and evolution of adaptive polyphenisms. Evol Dev 5:9-18.
3. Moran NA (1992) The evolutionary maintenance of alternative phenotypes. Am Nat 139:971-989.
4. Moczek AP, Emlen DJ (1999) Proximate determination of male horn dimorphism in the beetle Onthophagus taurus (Coleoptera: Scarabaeidae). J Evol Biol 12:27-37. (Pubitemid 29033105)
5. Müller CB, Williams IS, Hardie J (2001) The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecol Entomol 26:330-340. (Pubitemid 32501093)
6. Hölldobler B, Wilson EO (1990) The Ants (Belknap Press of Harvard Univ Press, Cambridge, MA).
7. Wilson EO (1971) The Insect Societies (Harvard University Press, Cambridge, MA).
8. Pfennig DW, et al. (2010) Phenotypic plasticity's impacts on diversification and speciation. Trends Ecol Evol 25:459-467.
9. Smith CR, Toth AL, Suarez AV, Robinson GE (2008) Genetic and genomic analyses of the division of labour in insect societies. Nat Rev Genet 9:735-748.
10. Ellegren H, Parsch J (2007) The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet 8:689-698. (Pubitemid 47281991)
11. Ayroles JF, et al. (2009) Systems genetics of complex traits in Drosophila melanogaster. Nat Genet 41:299-307.
12. Graveley BR, et al. (2011) The developmental transcriptome of Drosophila melanogaster. Nature 471:473-479.
13. Gibson G (2008) The environmental contribution to gene expression profiles. Nat Rev Genet 9:575-581.
14. Connallon T, Clark AG (2011) Association between sex-biased gene expression and mutations with sex-specific phenotypic consequences in Drosophila. Genome Biol Evol 3:151-155.
15. Ometto L, Shoemaker D, Ross KG, Keller L (2011) Evolution of gene expression in fire ants: The effects of developmental stage, caste, and species. Mol Biol Evol 28:1381-1392.
16. Snell-Rood EC, Van Dyken JD, Cruickshank T, Wade MJ, Moczek AP (2010) Toward a population genetic framework of developmental evolution: The costs, limits, and consequences of phenotypic plasticity. Bioessays 32:71-81.
17. Van Dyken JD, Wade MJ (2010) The genetic signature of conditional expression. Genetics 184:557-570.
18. Gadagkar R (1997) The evolution of caste polymorphism in social insects: Genetic release followed by diversifying evolution. J Genet 76:167-179.
19. Mank JE, Ellegren H (2009) Are sex-biased genes more dispensable? Biol Lett 5:409-412.
20. Hunt BG, et al. (2010) Sociality is linked to rates of protein evolution in a highly social insect. Mol Biol Evol 27:497-500.
21. Snell-Rood EC, et al. (2011) Developmental decoupling of alternative phenotypes: Insights from the transcriptomes of horn-polyphenic beetles. Evolution 65:231-245.
22. Brisson JA, Nuzhdin SV (2008) Rarity of males in pea aphids results in mutational decay. Science 319:58.
23. Barker MS, Demuth JP, Wade MJ (2005) Maternal expression relaxes constraint on innovation of the anterior determinant, bicoid. PLoS Genet 1:e57.
24. Mank JE, Hultin-Rosenberg L, Zwahlen M, Ellegren H (2008) Pleiotropic constraint hampers the resolution of sexual antagonism in vertebrate gene expression. Am Nat 171:35-43. (Pubitemid 351226026)
25. Good JM, Hayden CA, Wheeler TJ (2006) Adaptive protein evolution and regulatory divergence in Drosophila. Mol Biol Evol 23:1101-1103. (Pubitemid 43781583)
26. Khaitovich P, et al. (2005) Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 309:1850-1854. (Pubitemid 41325094)
27. Schwander T, Lo N, Beekman M, Oldroyd BP, Keller L (2010) Nature versus nurture in social insect caste differentiation. Trends Ecol Evol 25:275-282.
28. Heimpel GE, De Boer JG (2008) Sex determination in the Hymenoptera. Annu Rev Entomol 53:209-230. (Pubitemid 351341939)
29. Wurm Y, et al. (2011) The genome of the fire ant Solenopsis invicta. Proc Natl Acad Sci USA 108:5679-5684.
30. Smith CR, et al. (2011) Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc Natl Acad Sci USA 108:5667-5672.
31. Smith CD, et al. (2011) Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile). Proc Natl Acad Sci USA 108:5673-5678.
32. Drummond DA, Wilke CO (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134:341-352. (Pubitemid 352010328)
33. Wall DP, et al. (2005) Functional genomic analysis of the rates of protein evolution. Proc Natl Acad Sci USA 102:5483-5488. (Pubitemid 40530284)
34. Pál C, Papp B, Lercher MJ (2006) An integrated view of protein evolution. Nat Rev Genet 7:337-348.
35. Grozinger CM, Fan YL, Hoover SER, Winston ML (2007) Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera). Mol Ecol 16:4837-4848. (Pubitemid 350135217)
36. Zhang J, Nielsen R, Yang Z (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22:2472-2479. (Pubitemid 41661383)
37. Fletcher W, Yang Z (2010) The effect of insertions, deletions, and alignment errors on the branch-site test of positive selection. Mol Biol Evol 27:2257-2267.
38. Hirsh AE, Fraser HB (2001) Protein dispensability and rate of evolution. Nature 411:1046-1049.
39. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654. (Pubitemid 21896661)
40. Parsch J, Zhang Z, Baines JF (2009) The influence of demography and weak selection on the McDonald-Kreitman test: An empirical study in Drosophila. Mol Biol Evol 26:691-698.
41. Stoletzki N, Eyre-Walker A (2011) Estimation of the neutrality index. Mol Biol Evol 28:63-70.
42. Linksvayer TA, Wade MJ (2009) Genes with social effects are expected to harbor more sequence variation within and between species. Evolution 63:1685-1696.
43. Zhang Y, Sturgill D, Parisi M, Kumar S, Oliver B (2007) Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 450:233-237. (Pubitemid 350100545)
44. Duret L, Mouchiroud D (2000) Determinants of substitution rates in mammalian genes: Expression pattern affects selection intensity but not mutation rate. Mol Biol Evol 17:68-74. (Pubitemid 30056993)
45. Meisel RP (2011) Towards a more nuanced understanding of the relationship between sex-biased gene expression and rates of protein-coding sequence evolution. Mol Biol Evol 28:1893-1900.
46. Foret S, Kucharski R, Pittelkow Y, Lockett GA, Maleszka R (2009) Epigenetic regulation of the honey bee transcriptome: Unravelling the nature of methylated genes. BMC Genomics 10:472.
47. Bonduriansky R, Chenoweth SF (2009) Intralocus sexual conflict. Trends Ecol Evol 24:280-288.
48. Bonasio R, et al. (2010) Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329:1068-1071.
49. Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931-949.
50. Werren JH, et al., Nasonia Genome Working Group (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327:343-348.
51. Crosby MA, Goodman JL, Strelets VB, Zhang P, Gelbart WM; FlyBase Consortium (2007) FlyBase: Genomes by the dozen. Nucleic Acids Res 35(Database issue):D486-D491. (Pubitemid 46056256)
52. Wurm Y, et al. (2009) Fourmidable: A database for ant genomics. BMC Genomics 10:5.
53. Munoz-Torres MC, et al. (2011) Hymenoptera Genome Database: Integrated community resources for insect species of the order Hymenoptera. Nucleic Acids Res 39 (Database issue, Suppl 1):D658-D662.
54. Altschul SF, et al. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25:3389-3402. (Pubitemid 27359211)
55. Stajich JE, et al. (2002) The Bioperl toolkit: Perl modules for the life sciences. Genome Res 12:1611-1618. (Pubitemid 35175100)
56. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797.
57. Suyama M, Torrents D, Bork P (2006) PAL2NAL: Robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34 (Web Server issue):W609-W612.
58. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564-577. (Pubitemid 47171631)
59. Löytynoja A, Goldman N (2005) An algorithm for progressive multiple alignment of sequences with insertions. Proc Natl Acad Sci USA 102:10557-10562. (Pubitemid 41061593)
60. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696-704. (Pubitemid 37365050)
61. Yang ZH (2007) PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586-1591. (Pubitemid 47236688)
62. Ning Z, Cox AJ, Mullikin JC (2001) SSAHA: A fast search method for large DNA databases. Genome Res 11:1725-1729. (Pubitemid 33040499)
63. Li H, et al.; 1000 Genome Project Data Processing Subgroup (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079.
64. Wurm Y, Wang J, Keller L (2010) Changes in reproductive roles are associated with changes in gene expression in fire ant queens. Mol Ecol 19:1200-1211.
65. Wang J, et al. (2007) An annotated cDNA library and microarray for large-scale gene-expression studies in the ant Solenopsis invicta. Genome Biol 8:R9.
66. Townsend J, Hartl D (2002) Bayesian analysis of gene expression levels: Statistical quantification of relative mRNA level across multiple strains or treatments. Genome Biol 3:RESEARCH0071-RESEARCH0071.0016.
67. Wu TD, Watanabe CK (2005) GMAP: A genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21:1859-1875. (Pubitemid 40668022)
68. Elango N, Hunt BG, Goodisman MAD, Yi SV (2009) DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proc Natl Acad Sci USA 106:11206-11211.
69. Hunt BG, Brisson JA, Yi SV, Goodisman MAD (2010) Functional conservation of DNA methylation in the pea aphid and the honeybee. Genome Biol Evol 2:719-728.
70. Zemach A, McDaniel IE, Silva P, Zilberman D (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916-919.