Accelerated evolution of morph-biased genes in pea aphids

Molecular Biology and Evolution

Volumn 31, Issue 8, 2014, Pages 2073-2083

  Purandare, Swapna R ^a   Bickel, Ryan D ^b   Jaquiery, Julie ^c   Rispe, Claude ^c,d   Brisson, Jennifer A ^b  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

^c Universite Rennes 1   (France)

^d Epidemiology and Risk Analysis in Animal Health   (France)

Author keywords

aphid; gene expression; morph bias; phenotypic plasticity; polyphenism; relaxed purifying selection

Indexed keywords

ACCELERATION; ADULT; ARTICLE; ENVIRONMENTAL FACTOR; FEMALE; GENE EXPRESSION; GENE MUTATION; GENETIC SELECTION; GENOTYPE; MALE; MOLECULAR EVOLUTION; NONHUMAN; PEA APHID; PHENOTYPIC PLASTICITY; PURIFYING SELECTION; ANATOMY AND HISTOLOGY; ANIMAL; APHID; CLASSIFICATION; EVOLUTION; GENE; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; INSECT CHROMOSOME; MUTATION RATE; PHENOTYPE; SPECIES DIFFERENCE;

ANIMALS; APHIDS; BIOLOGICAL EVOLUTION; CHROMOSOMES, INSECT; FEMALE; GENE EXPRESSION REGULATION; GENES, INSECT; GENETIC VARIATION; MALE; MUTATION RATE; PHENOTYPE; SELECTION, GENETIC; SPECIES SPECIFICITY;

EID: 84904992253     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu149     Document Type: Article

References (76)

1. Achaz G. 2008. Testing for neutrality in samples with sequencing errors. Genetics 179:1409-1424
2. Aguade M. 1998. Different forces drive the evolution of the Acp26Aa and Acp26Ab accessory gland genes in the Drosophila melanogaster species complex. Genetics 150:1079-1089
3. Altschul SF, Gish W, Miller W, Myers W, Lipman DJ. 1990. Basic local alignment search tool. J Mol Evol. 215:403-410
4. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol. 11:R106
5. Barker MS, Demuth JP, Wade MJ. 2005. Maternal expression relaxes constraint on innovation of the anterior determinant, bicoid. PLoS Genet. 1:e57
6. Bickel RD, Dunham JP, Brisson JA. 2013. Widespread selection across coding and noncoding DNA in the pea aphid genome. G3 3: 993-1001
7. Blackman RL. 1974. Aphids. London: Ginn and Company Ltd
8. Blackman RL. 1987. Reproduction, cytogenetics and development. In: Minks AK, Harrewijn P, editors. Aphids: Their biology, natural enemies & control, Vol. 2A. Amsterdam: Elsevier. p. 163-195
9. Braendle C, Caillaud MC, Stern DL. 2005. Genetic mapping of aphicarus-A sex-linked locus controlling a wing polymorphism in the pea aphid (Acyrthosiphon pisum). Heredity 94:435-442
10. Brisson JA, Davis GK, Stern DL. 2007. Common genome-wide transcription patterns underlying the wing polyphenism and polymorphism in the pea aphid (Acyrthosiphon pisum). Evol Dev. 9:338-346
11. Brisson JA, Nuzhdin SV. 2008. Rarity of males in pea aphids results in mutational decay. Science 319:58
12. Caillaud MC, Boutin M, Braendle C, Simon J-C. 2002. A sex-linked locus controls wing polymorphism in males of the pea aphid, Acyrthosiphon pisum (Harris). Heredity 89:346-352
13. Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 17: 540-552
14. Connallon T, Clark AG. 2011. Associations between sex-biased gene expression and mutations with sex-specific phenotypic consequences in Drosophila. Genome Biol Evol. 3:151-155
15. Dixon AFG. 1997. Aphid ecology: An optimization approach, 2nd ed. London: Chapman & Hall
16. 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
17. Ellegren H, Parsch J. 2007. The evolution of sex-biased genes and sexbiased gene expression. Nat Rev Genet. 8:689-698
18. Frantz A, Plantegenest M, Simon J-C. 2010. Host races of the pea aphid Acyrthosiphon pisum differ in male wing phenotypes. Bull Entomol Res. 100:59-66
19. Fu X, FuN, Guo SW, Yan Z, Xu Y, Hu H, Menzel C, Chen W, Li Y, Zeng R, et al. 2009. Estimating accuracy of RNA-Seq and microarrays with proteomics. BMC Genomics 10:161
20. Grozinger CM, Fan Y, 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
21. Hales DF, Wilson ACC, Sloane MA, Simon J-C, Legallic J-F, Sunnucks P. 2002. Lack of detectable genetic recombination on the X chromosome during the parthenogenetic production of female and male aphids. Genet Res (Camb). 79:203-209
22. Hambuch TM, Parsch J. 2005. Patterns of synonymous codon usage in Drosophila melanogaster genes with sex-biased expression. Genetics 2005:1691-1700
23. Hebenstreit D, Fang M, Gu M, Charoensawan V, Van Oudenaarden A, Teichmann SA. 2011. RNA sequencing reveals two major classes of gene expression levels in metazoan cells. Mol Syst Biol. 7:497
24. Hirsh AE, Fraser HB. 2001. Protein dispensability and rate of evolution. Nature 411:1046-1049
25. Hunt BG, Ometto L, Wurm Y, Shoemaker D, Yi SV, Keller L, Goodisman MAD. 2011. Relaxed selection is a precursor to the evolution of phenotypic plasticity. Proc Natl Acad Sci U S A. 108:15936-15941
26. Hunt BG, Wyder S, Elango N, Werren JH, Zdobnov EM, Yi SV, Goodisman MAD. 2010. Sociality is linked to rates of protein evolution in a highly social insect. Mol Biol Evol. 27:497-500
27. Hunt J, Simmons LW. 1997. Patterns of fluctuating asymmetry in beetle horns: An experimental examination of the honest signalling hypothesis. Behav Ecol Sociogiol. 41:109-114
28. Jaquiery J, Rispe C, Roze D, Legeai F, Le Trionnaire G, Stoeckel S, Mieuzet L, Da Silva C, Poulain J, Prunier-Leterme N, et al. 2013. Masculinization of the X chromosome in the pea aphid. PLoS Genet. 9:e1003690
29. Jordan IK, Rogozin IB, Wolf YI, Koonin EV. 2002. Essential genes aremore evolutionarily conserved than are nonessential genes in bacteria. Genome Res. 12:962-968
30. Kawecki TJ. 1994. Accumulation of deleterious mutations and the evolutionary cost of being a generalist. Am Nat. 144:833-838
31. Kawecki TJ, Barton NH, Fry JD. 1997. Mutational collapse of fitness in marginal habitats and the evolution of ecological specialisation. J Evol Biol. 10:407-429
32. Kingsolver JG. 1995. Viability selection on seasonally polyphenic traits: Wing melanin pattern in Western White Butterflies. Evolution 49: 932-941
33. Lees AD. 1966. The control of polymorphism in aphids. Adv Insect Physiol. 3:207-277
34. Leichty AR, Pfennig DW, Jones CD, Pfennig KS. 2012. Relaxed genetic constraint is ancestral to the evolution of phenotypic plasticity. Integr Comp Biol. 52:16-30
35. Lemos B, Bettencourt BR, Meiklejohn CD, Hartl DL. 2005. 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. 22:1345-1354
36. MacKay PA. 1989. Clonal variation in sexual morph production in Acyrthosiphon pisum (Homoptera: Aphididae). Environ Entomol. 18:558-562
37. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y. 2008. RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 18:1509-1517
38. McDonald JH, KreitmanM. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654
39. Meisel RP. 2011. Towards a more nuances understanding of the relationship between sex-biased gene expression and rates of proteincoding sequence evolution. Mol Biol Evol. 28:1893-1900
40. Moczek AP, Emlen DJ. 1999. Proximate determination of male horn dimorphism in the beetle Onthophagus taurus (Coleoptera: Scarabaeidae). J Evol Biol. 12:27-37
41. Moran NA. 1992. The evolution of aphid life cycles. Annu Rev Entemol. 37:321-348
42. Nijhout HF. 2003. Development and evolution of adaptive polyphenisms. Evol Dev. 5:9-18
43. Notredame C, Higgins DG, Heringa J. 2000. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol. 302: 205-217
44. Ollivier M, Legeai F, Rispe C. 2010. Comparative analysis of the Acyrthosiphon pisum genome and expressed sequence tag-based gene sets from other aphid species. Insect Mol Biol. 19:33-45
45. Orlando E. 1974. Sex determination in Megoura viciae Buckton (Homoptera, Aphididae). Monitore Zool Ital (NS). 8:61-70
46. Pal C, Papp B, Hurst LD. 2001. Highly expressed genes in yeast evolve slowly. Genetics 158:927-931
47. Parisi M, Nuttal R, Naiman D, Bouffard GG, Malley J, Andrews J, Eastman S, Oliver B. 2003. Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299:697-700
48. Parsch J, Ellegren H. 2013. The evolutionary causes and consequences of sex-biased gene expression. Nat Rev Genet. 14:83-87
49. Pfennig DW. 1992. Polyphenism in spadefoot toad tadpoles as a locally-Adjusted evolutionarily stable strategy. Evolution 46: 1408-1420
50. Pointer MA, Harrison PW, Wright AE, Mank JE. 2013. Masculinization of gene expression is associated with exaggeration of male sexual dimorphism. PLoS Genet. 9:e1003697
51. Proschel M, Zhang Z, Parsch J. 2006. Widespread adaptive evolution of Drosophila genes with sex-biased expression. Genetics 174:893-900
52. R Development Core Team. 2012. R: A language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing
53. Ranz JM, Castillo-Davis CD, Meiklejohn CM, Hartl DL. 2003. Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300:1742-1745
54. Rocha EPC, Danchin A. 2004. An analysis of determinants of amino acids substitution rates in bacterial proteins. Mol Biol Evol. 21:108-116
55. Scheiner SM. 1993. Genetics and evolution of phenotypic plasticity. Annu Rev Ecol Syst. 24:35-68
56. Schiex T, Gouzy J, Moisan A, De Oliveira Y. 2003. FrameD: A flexible program for quality check and gene prediction in prokaryotic genomes and noisy matured eukaryotic sequences. Nucl Acids Res. 31: 3738-3741
57. 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
58. Snell-Rood EC, Cash A, Han MV, Kijimoto T, Andrews J, Moczek AP. 2011. Developmental decoupling of alternative phenotypes: Insights from the transcriptomes of horn-polyphenic beetles. Evolution 65: 231-245
59. 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
60. Sutherland ORW. 1969. The role of crowding in the production of winged forms by two strains of the pea aphid, Acyrthosiphon pisum. J Insect Physiol. 15:1385-1410
61. Swanson WJ, Clark AG, Waldrip-Dail HM, Wolfner MF, Aquadro CF. 2001. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc Natl Acad Sci U S A. 98: 7375-7379
62. Swanson WJ, Vacquier VD. 2002. The rapid evolution of reproductive proteins. Nat Rev Genet. 3:137-144
63. Swanson WJ, Wong A, Wolfner MF, Aquadro CF. 2004. Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection. Genetics 168: 1457-1465
64. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595
65. Thomas C. 1878. A list of the species of the tribe Aphidini, family Aphidae, found in the United States, which have heretofore been named, with descriptions of some new species. Bull Ill State Lab Nat Hist. 1:3-16
66. Van Dyken JD, Wade MJ. 2010. The genetic signature of conditional expression. Genetics 184:557-570
67. Via S. 1992. Inducing the sexual forms and hatching the eggs of pea aphids. Entomol Exp Appl. 65:119-127
68. West-Eberhard MJ. 1989. Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst. 20:249-278
69. West-Eberhard MJ. 2003. Developmental plasticity and evolution. New York: Oxford University Press
70. Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, Goodhead I, Penkett CJ, Rogers J, Bahler J. 2008. Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453:1239-1243
71. Wilson ACC, Sunnucks P, Hales DF. 1997. Random loss of X chromosome at male determination in an aphid, Sitobion near fragariae, detected using an X-linked polymorphic microsatellite marker. Genet Res. 69:233-236
72. Wilson EO. 1971. The insect societies. Cambridge (MA): Harvard University Press
73. Wright F. 1990. The 'effective number of codons' used in a gene. Gene 87: 23-29
74. Yanai I, Benjamin H, Shmoish M, Chalifa-Caspi V, Shklar M, Ophir R, Bar-Even A, Horn-Saban S, Safran M, Domany E, et al. 2005. Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics 21: 650-659
75. Yang ZH. 1997. PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13:555-556
76. Zhang Z, Hambuch RM, Parsch J. 2004. Molecular evolution of sexbiased genes in Drosophila. Mol Biol Evol. 21:2130-2139.