How do genomes create novel phenotypes Insights from the loss of the worker caste in ant social parasites

Molecular Biology and Evolution

Volumn 32, Issue 11, 2015, Pages 2919-2931

  Smith, Chris R ^a   Helms Cahan, Sara ^b   Kemena, Carsten ^c   Brady, Seán G ^d   Yang, Wei ^e   Bornberg Bauer, Erich ^c   Eriksson, Ti ^f   Gadau, Juergen ^f   Helmkampf, Martin ^f   Gotzek, Dietrich ^g,h   Okamoto Miyakawa, Misato ⁱ   Suarez, Andrew V ^h   Mikheyev, Alexander ⁱ  

^a EARLHAM COLLEGE   (United States)

^b UNIVERSITY OF VERMONT   (United States)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d DEPARTMENT OF PALEOBIOLOGY   (United States)

^e University of Illinois at Urbana Champaign   (United States)

^f ARIZONA STATE UNIVERSITY   (United States)

^g UNIVERSITY OF GEORGIA   (United States)

^h UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

ⁱ OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

Author keywords

ant; caste; genome; phenotypic plasticity; social parasite

Indexed keywords

ADULT; ANT; ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GENE EXPRESSION; GENE LOSS; GENE MUTATION; GENOME; GENOME ANALYSIS; HOST; LAST COMMON ANCESTOR; MALE; MOLECULAR EVOLUTION; NONHUMAN; PARASITISM; PHENOTYPE; PHYLOGENY; QUEEN (INSECT); SOCIAL BEHAVIOR; SOCIAL PARASITISM; WORKER (INSECT); ANIMAL; ANIMAL BEHAVIOR; CLASSIFICATION; EVOLUTION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION STUDY; GENETIC SELECTION; GENETICS; PHYSIOLOGY; REPRODUCTION;

TRANSCRIPTOME;

ANIMALS; ANTS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; FEMALE; GENE EXPRESSION PROFILING; GENES, INSECT; GENETIC ASSOCIATION STUDIES; GENOME COMPONENTS; MALE; REPRODUCTION; SELECTION, GENETIC; SOCIAL BEHAVIOR; TRANSCRIPTOME;

EID: 84946124058     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msv165     Document Type: Article

References (83)

1. Aird SD, Watanabe Y, Villar-Briones A, Roy MC, Terada K, Mikheyev AS. 2013. Quantitative high-Dhroughput profiling of snake venom gland transcriptomes and proteomes (Ovophis okinavensis and Protobothrops flavoviridis). BMC Genomics 14:790.
2. Amdam GV, Csondes A, Fondrk MK, Page RE. 2006. Complex social behaviour derived from maternal reproductive traits. Nature 439:76-78.
3. Anderson KE, Gadau J, Mott BM, Johnson RA, Altamirano A, Strehl C, Fewell JH. 2006. Distribution and evolution of genetic caste determination in Pogonomyrmex seed-harvester ants. Ecology 87:2171-2184.
4. Anderson KE, Linksvayer TA, Smith CR. 2008. The causes and consequences of genetic caste determination in ants (Hymenoptera: Formicidae). Myrmecol News 11:119-132.
5. Anderson KE, Smith CR, Linksvayer TA, Mott BM, Gadau J, Fewell JH. 2009. Modeling themaintenance of a dependent lineage system: the influence of positive frequency-dependent selection on sex ratio. Evolution 63:2142-2152.
6. Anholt RR, Mackay TF. 2004. Quantitative genetic analyses of complex behaviours in Drosophila. Nat Rev Genet. 5:838-849.
7. Berens AJ, Hunt JH, Toth AL. 2015. Comparative transcriptomics of convergent evolution: different genes but conserved pathways underlie caste phenotypes across lineages of eusocial insects. Mol Biol Evol. 32:690-703.
8. Bonasio R, Zhang G, Ye C, Mutti NS, Fang X, Qin N, Donahue G, Yang P, Li Q, Li C. 2010. Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329:1068-1071.
9. Buschinger A. 1986. Evolution of social parasitism in ants. Trends Ecol Evol. 1:155-160.
10. Buschinger A. 2009. Social parasitism among ants: a review (Hymenoptera: Formicidae). Myrmecol News 12:219-235.
11. Cantarel BL, Korf I, Robb SMC, ParraG, Ross E, Moore B, Holt C, S-Anchez Alvarado A, Yandell M. 2008. MAKER: An easy-Do-use annotation pipeline designed for emerging model organism genomes. Genome Res. 18:188-196.
12. Carpenter FM. 1930. The fossil ants of North America. Bull Mus Comp Zool. 70:1-66.
13. Cini A, Patalano S, Segonds-Pichon A, Busby GBJ, Cervo R, Sumner S. 2015. Social parasitism and the molecular basis of phenotypic evolution. Front Genet. 6:32.
14. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, et al. 2011. A framework for variation discovery and genotyping using nextgeneration DNA sequencing data. Nat Genet. 43:491-498.
15. Domazet-Loso T, Tautz D. 2003. An evolutionary analysis of orphan genes in Drosophila. Genome Res. 13:2213-2219.
16. Drummond AJ, Ho SY, Phillips MJ, Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4:e88.
17. Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 29:1969-1973.
18. Feldmeyer B, Elsner D, Foitzik S. 2014. Gene expression patterns associated with caste and reproductive status in ants: worker-specific genes are more derived than queen-specific ones. Mol Ecol. 23:151-161.
19. Evans JD. 1993. Parentage analyses in ant colonies using simple sequence repeat loci. Mol Ecol. 2:393-397.
20. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, et al. 2014. Pfam: the protein families database. Nucleic Acids Res. 42:D222-D230.
21. Foitzik S, Haberl M, Gadau J, Heinze J. 1997. Mating frequency of Leptothorax nylanderi ant queens determined bymicrosatellite analysis. Insect Soc. 44: 219-227.
22. Gadagkar R. 1997. The evolution of caste polymorphism in social insects: genetic release followed by diversifying evolution. J Genet. 76:167-179.
23. Gadau J, Helmkampf M, Nygaard S, Roux J, Simola DF, Smith CR, Suen G, Wurm Y, Smith CD. 2012. The genomic impact of 100 million years of social evolution in seven ant species. Trends Genet. 28:14-21.
24. Gadau J, Strehl CP, Oettler J, Heolldobler B. 2003. Determinants of intracolonial relatedness in Pogonomyrmex rugosus (Hymenoptera: Formicidae): mating frequency and brood raids. Mol Ecol. 12: 1931-1938.
25. Grozinger CM, Sharabash NM, Whitfield CW, Robinson GE. 2003. Pheromone-mediated gene expression in the honey bee brain. Proc Natl Acad Sci. 100:14519-14525.
26. Hall DW, Soojin VY, Goodisman MA. 2013. Kin selection, genomics and caste-Antagonistic pleiotropy. Biol Lett. 9:20130309.
27. Helanterea H, Uller T. 2014. Neutral and adaptive explanations for an association between caste-biased gene expression and rate of sequence evolution. Front Genet. 5: 297.
28. Helms Cahan SH, Julian GE, Rissing SW, Schwander T, Parker JD, Keller L. 2004. Loss of phenotypic plasticity generates genotype-caste association in harvester ants. Curr Biol. 14:2277-2282.
29. Helms Cahan SH, Keller L. 2003. Complex hybrid origin of genetic caste determination in harvester ants. Nature 424:306-309.
30. Hoeulldobler B, Wilson EO. 1990. The ants. Cambridge (MA): Belknap Press of Harvard University Press.
31. Holt C, Yandell M. 2011. MAKER2: an annotation pipeline and genomedatabase management tool for second-generation genome projects. BMC Bioinformatics 12:491.
32. Hunt BG, Ometto L, Wurm Y, Shoemaker D, Soojin VY, Keller L, Goodisman MA. 2011. Relaxed selection is a precursor to the evolution of phenotypic plasticity. Proc Natl Acad Sci. 108:15936-15941.
33. Jasper WC, Linksvayer TA, Atallah J, Friedman D, Chiu JC, Johnson BR. 2015. Large scale coding sequence change underlies the evolution of post-developmental novelty in honey bees. Mol Biol Evol. 32: 334-346.
34. Johnson BR, Tsutsui ND. 2011. Taxonomically restricted genes are associated with the evolution of sociality in the honey bee. BMC Genomics 12:164.
35. Johnson RA, Parker JD, Rissing SW. 1996. Rediscovery of the workerless inquiline ant Pogonomyrmex colei and additional notes on natural history (Hymenoptera: Formicidae). Insectes Sociaux 43:69-76.
36. Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, Swofford R, Pirun M, Zody MC, White S. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55-61.
37. Kinomura K, Yamauchi K. 1992. A new workerless socially parasitic species of the genus Vollenhovia (Hymenoptera: Formicidae) from Japan. Jpn J Entomol. 60:203-206.
38. Lahti DC, Johnson NA, Ajie BC, Otto SP, Hendry AP, Blumstein DT, Coss RG, Donohue K, Foster SA. 2009. Relaxed selection in the wild. Trends Ecol Evol. 24:487-496.
39. Lanfear R, Calcott B, Ho SY, Guindon S. 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol. 29:1695-1701.
40. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357-359.
41. Leek JT. 2014. svaseq: removing batch effects and other unwanted noise from sequencing data. Nucleic Acids Res. 42:e161.
42. Leek JT, Johnson WE, Parker HS, Fertig EJ, Jaffe AE, Storey JD. 2015. sva: Surrogate Variable Analysis. R package version 3.14.0. Available from: http://www.bioconductor.org/packages/release/bioc/html/sva.htm.l.
43. Leichty AR, Pfennig DW, Jones CD, Pfennig KS. 2012. Relaxed genetic constraint is ancestral to the evolution of phenotypic plasticity. Int Comp Biol. 52:16-30.
44. Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323.
45. Libbrecht R, Schwander T, Keller L. 2011. Genetic components to caste allocation in a multiple-queen ant species. Evolution 65:2907-2915.
46. Linksvayer TA, Busch JW, Smith CR. 2013. Social supergenes of superorganisms: do supergenes play important roles in social evolution? BioEssays News Rev Mol Cell Dev Biol 35:683-689.
47. Linksvayer TA, Wade MJ. 2009. Genes with social effects are expected to harbor more sequence variation within and between species. Evolution 63:1685-1696.
48. Maynard Smith J, Szathm-Ary E. 1995. The major transitions in evolution. Nature 374:227-232.
49. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, et al. 2010. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20:1297-1303.
50. Mikheyev AS, Linksvayer TA. 2015. Genes associated with ant social behavior show distinct transcriptional and evolutionary patterns. eLife 4:e04775.
51. Monteiro A. 2012. Gene regulatory networks reused to build novel traits. BioEssays 34:181-186.
52. Ohkawara K, Nakayama M, Satoh A, Trindl A, Heinze J. 2006. Clonal reproduction and genetic caste differences in a queen-polymorphic ant, Vollenhovia emeryi. Biol Lett. 2:359-363.
53. Ohno S. 1970. Evolution by gene duplication. New York. Springer Science and Business Media.
54. Okamoto M, Kobayashi K, Hasegawa E, Ohkawara K. 2015. Sexual and asexual reproduction of queens in a myrmicine ant, Vollenhovia emeryi (Hymenoptera: Formicidae). Myrmecol News 21:13-17.
55. Page RE, Amdam GV. 2007. The making of a social insect: developmental architectures of social design. Bioessays 29:334-343.
56. Parker JD, Rissing SW. 2002. Molecular evidence for the origin of workerless social parasites in the ant genus Pogonomyrmex. Evolution 56:2017-2028.
57. Purandare SR, Bickel RD, Jaquiery J, Rispe C, Brisson JA. 2014. Accelerated evolution of morph-biased genes in pea aphids. Mol Biol Evol. 31:2073-2083.
58. Rajakumar R, San Mauro D, Dijkstra MB, Huang MH, Wheeler DE, Hiou-Dim F, Khila A, Cournoyea M, Abouheif E. 2012. Ancestral developmental potential facilitates parallel evolution in ants. Science 335:79-82.
59. Rambaut A, Grassly NC. 1997. Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Comput Appl Biosci. 13:235-238.
60. Robinson GE, Grozinger CM, Whitfield CW. 2005. Sociogenomics: social life in molecular terms. Nat Rev Genet. 6:257-270.
61. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140.
62. Robinson MD, Oshlack A. 2010. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11:R25.
63. Schrader L, Simola DF, Heinze J, Oettler J. 2015. Sphingolipids, transcription factors, and conserved toolkit genes: developmental plasticity in the ant Cardiocondyla obscurior. Mol Biol Evol. 32:1474-1486.
64. Schwander T, Helms Cahan S, Keller L. 2007. Characterization and distribution of Pogonomyrmex harvester ant lineages with genetic caste determination. Mol Ecol. 16:367-387.
65. Schwander T, Keller L, Helms Cahan S. 2007. Two alternate mechanisms contribute to the persistence of interdependent lineages in Pogonomyrmex harvester ants. Mol Ecol. 16:3533-3543.
66. 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.
67. Simola DF, Wissler L, Donahue G, Waterhouse RM, Helmkampf M, Roux J, Nygaard S, Glastad KM, Hagen DE, Viljakainen L. 2013. Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality. Genome Res. 23:1235-1247.
68. Smith CR, Mutti NS, Jasper WC, Naidu A, Smith CD, Gadau J. 2012. Patterns of DNA methylation in development, division of labor and hybridization in an ant with genetic caste determination. PloS One 7:e42433.
69. Smith CR, Smith CD, Robertson HM, Helmkampf M, Zimin A, Yandell M, Holt C, Hu H, Abouheif E, Benton R. 2011. Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc Natl Acad Sci. 108:5667-5672.
70. 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.
71. Strope CL, Scott SD, Moriyama EN. 2007. indel-Seq-Gen: a new protein family simulator incorporating domains, motifs, and indels. Mol Biol Evol. 24:640-649.
72. Sumner S. 2014. The importance of genomic novelty in social evolution. Mol Ecol. 23:26-28.
73. Toth AL, Varala K, Newman TC, Miguez FE, Hutchison SK, Willoughby DA, Simons JF, Egholm M, Hunt JH, Hudson ME. 2007. Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318: 441-444.
74. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111.
75. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 7:562-578.
76. True JR, Carroll SB. 2002. Gene co-option in physiological and morphological evolution. Annu Rev Cell Dev Biol. 18:53-80.
77. Tsai IJ, Zarowiecki M, Holroyd N, Garciarrubio A, Sanchez-Flores A, Brooks KL, Tracey A, Bobes RJ, Fragoso G, Sciutto E. 2013. The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496:57-63.
78. Van der Auwera GA, Carneiro MO, Hartl C, Poplin R, del Angel G, Levy-Moonshine A, Jordan T, Shakir K, Roazen D, Thibault J, et al. 2002. From FastQ data to high-confidence variant calls: the genome analysis toolkit best practices pipeline. Current Protocols in Bioinformatics. 11:11.10:11.10.111.10.33.
79. Volny VP, Gordon DM. 2002. Characterization of polymorphic microsatellite loci in the red harvester ant, Pogonomyrmex barbatus. Mol Ecol Notes 2:302-303.
80. Ward PS, Brady SG, Fisher BL, Schultz TR. 2015. The evolution of myrmicine ants: phylogeny and biogeography of a hyperdiverse ant clade (Hymenoptera: Formicidae). Syst Entomol. 40:61-81.
81. West-Eberhard MJ. 1987. Flexible strategy and social evolution. In: Ito Y, Brown JL, Kikkawa J, editors. Animal societies: theories and facts. Tokyo: Japan Scientific Societies Press. p. 35-51.
82. Wissler L, Gadau J, Simola DF, Helmkampf M, Bornberg-Bauer E. 2013. Mechanisms and dynamics of orphan gene emergence in insect genomes. Genome Biol Evol. 5:439-455.
83. Wurm Y, Wang J, Riba-Grognuz O, Corona M, Nygaard S, Hunt BG, Ingram KK, Falquet L, Nipitwattanaphon M, Gotzek D. 2011. The genome of the fire ant Solenopsis invicta. Proc Natl Acad Sci. 108:5679-5684.