Effects of ploidy and sex-locus genotype on gene expression patterns in the fire ant Solenopsis invicta

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1797, 2014, Pages

  Nipitwattanaphon, Mingkwan ^a,g   Wang, John ^a,b   Ross, Kenneth G ^c   Riba Grognuz, Oksana ^a,d   Wurm, Yannick ^a,d,e   Khurewathanakul, Chitsanu ^f   Keller, Laurent ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b BIODIVERSITY RESEARCH CENTER   (Taiwan)

^c UNIVERSITY OF GEORGIA   (United States)

^d SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^e QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^f EPFL   (Switzerland)

^g KASETSART UNIVERSITY   (Thailand)

Author keywords

Complementary sex determination; Diploid male; Doublesex; Hymenoptera; Microarray; Sex determination

Indexed keywords

ANT; BEE; EGG; GENE EXPRESSION; GENETIC ANALYSIS; GENOTYPE; PLOIDY; PUPA; SEX DETERMINATION; STERILITY; WASP;

HYMENOPTERA; SOLENOPSIS GEMINATA; SOLENOPSIS INVICTA;

EID: 84908374950     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.1776     Document Type: Article

References (51)

1. Beukeboom LW, Perrin N. 2014 The evolution of sex determination. New York, NY: Oxford University Press.
2. Bull JJ. 1983 Evolution of sex determining mechanisms. New York, NY: Benjamin.
3. Beye M, Hasselmann M, Fondrk MK, Page RE, Omholt SW. 2003 The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114, 419–429. (doi:10.1016/S0092-8674(03)00606-8)
4. Whiting P. 1943 Multiple alleles in complementary sex determination of habrobracon. Genetics 28, 365–382.
5. Cowan DP, Stahlhut JK. 2004 Functionally reproductive diploid and haploid males in an inbreeding hymenopteran with complementary sex determination. Proc. Natl Acad. Sci. USA 101, 10374–10379. (doi:10.1073/pnas.0402481101)
6. Bostian CH. 1935 Biparental males and hatchability of eggs in habrobracon. Genetics 20, 280–285.
7. Herrmann M, Trenzcek T, Fahrenhorst H, Engels W. 2005 Characters that differ between diploid and haploid honey bee (Apis mellifera) drones. Genet. Mol. Res. 4, 624–641.
8. Ross KG, Fletcher DJC. 1985 Genetic origin of male diploidy in the fire ant, Solenopsis invicta (Hymenoptera: Formicidae), and its evolutionary significance. Evolution (N. Y). 39, 888–903. (doi:10.2307/2408688)
9. 9. Van Wilgenburg E, Driessen G, Beukeboom LW. 2006 Single locus complementary sex determination in Hymenoptera: an ‘unintelligent’ design? Front. Zool. 3, 1. (doi:10.1186/1742-9994-3-1)
10. 10. Tavares MG, Teixeira Irsigler AS, De Oliveira Campos LA. 2003 Testis length distinguishes haploid from diploid drones in Melipona quadrifasciata (Hymenoptera: Meliponinae). Apidologie 34, 449–455. (doi:10.1051/apido:2003045)
11. 11. Woyke J. 1974 Genic balance, heterozygosity and inheritance of testis size in diploid drone honeybees. J. Apic. Res. 13, 77–85.
12. Hung ACF, Vinson SB, Summerlin JW. 1974 Male sterility in the red imported fire ant, Solenopsis invicta. Ann. Entomol. Soc. Am. 67, 4.
13. Ayabe T, Hoshiba H, Ono M. 2004 Cytological evidence for triploid males and females in the bumblebee, Bombus terrestris. Chromosom. Res. 12, 215–223. (doi:10.1023/B:CHRO.0000021880.83639.4b)
14. 14. Krieger MJB, Ross KG, Chang CWY, Keller L. 1999 Frequency and origin of triploidy in the fire ant Solenopsis invicta. Heredity (Edinb). 82, 142–150. (doi:10.1038/sj.hdy.6884600)
15. 15. De Boer JG, Ode PJ, Vet LEM, Whitfield JB, Heimpel GE. 2007 Diploid males sire triploid daughters and sons in the parasitoid wasp Cotesia vestalis. Heredity (Edinb). 99, 288–294. (doi:10.1038/sj.hdy.6800995)
16. 16. Yamauchi K, Yoshida T, Ogawa T, Itoh S, Ogawa Y, Jimbo S, Imai HT. 2001 Spermatogenesis of diploid males in the formicine ant, Lasius sakagamii. Insectes Soc. 48, 28–32. (doi:10.1007/PL00001741)
17. 17. Woyke J, Kro´l-Paluch W. 1985 Changes in tissue polyploidization during development of worker, queen, haploid and diploid drone honeybees. J. Apic. Res. 24, 214–224.
18. Aron S, de Menten L, Van Bockstaele DR, Blank SM, Roisin Y. 2005 When hymenopteran males reinvented diploidy. Curr. Biol. 15, 824–827. (doi:10.1016/j.cub.2005.03.017)
19. Leeb M, Wutz A. 2013 Haploid genomes illustrate epigenetic constraints and gene dosage effects in mammals. Epigenetics Chromatin 6, 41. (doi:10.1186/1756-8935-6-41)
20. Scholes DR, Suarez AV, Paige KN. 2013 Can endopolyploidy explain body size variation within and between castes in ants? Ecol. Evol. 3, 2128–2137. (doi:10.1002/ece3.623)
21. Borges AA, Humann FC, Oliveira Campos LA, Tavares MG, Hartfelder K. 2011 Transcript levels of ten caste-related genes in adult diploid males of Melipona quadrifasciata (Hymenoptera, Apidae)—a comparison with haploid males, queens and workers. Genet. Mol. Biol. 34, 698–706. (doi:10.1590/S1415-475720 11005000050)
22. Borges AA, Humann FC, Tavares MG, Campos LAO, Hartfelder K. 2012 Gene copy number and differential gene expression in haploid and diploid males of the stingless bee, Melipona quadrifasciata. Insectes Soc. 59, 587–598. (doi:10.1007/s00040- 012-0259-1)
23. Ellegren H, Parsch J. 2007 The evolution of sexbiased genes and sex-biased gene expression. Nat. Rev. Genet. 8, 689–698. (doi:10.1038/nrg2167)
24. Ross KG, Fletcher DJC. 1986 Diploid male production: a significant colony mortality factor in the fire ant Solenopsis invicta (Hymenoptera: Formicidae). Behav. Ecol. Sociobiol. 19, 283–291. (doi:10.1007/BF00300643)
25. Passera L, Keller L. 1992 The period of sexual maturation and the age at mating in Iridomyrmex humilis, an ant with intranidal mating. J. Zool. 228, 141–153. (doi:10.1111/j.1469-7998.1992.tb04438.x)
26. Wang J, Jemielity S, Uva P, Wurm Y, Gräff J, Keller L. 2007 An annotated cDNA library and microarray for large-scale gene-expression studies in the ant Solenopsis invicta. Genome Biol. 8, R9. (doi:10.1186/ gb-2007-8-1-r9)
27. Jouvenaz DP, Allen GE, Banks WA, Wojcik DP, Entomologist TF, Dec N. 1977 A survey for pathogens of fire ants, Solenopsis spp., in the Southeastern United States. Florida Entomol. 60, 275–279. (doi:10.2307/3493922)
28. Krieger MJB, Ross KG. 2002 Identification of a major gene regulating complex social behavior. Science 295, 328–332. (doi:10.1126/science.1065247)
29. Ross KG, Vargo EL, Keller L, Trager JC. 1993 Effect of a founder event on variation in the genetic sexdetermining system of the fire ant Solenopsis invicta. Genetics 135, 843–854.
30. Wang J, Wurm Y, Nipitwattanaphon M, Riba- Grognuz O, Huang Y-C, Shoemaker D, Keller L. 2013 A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493, 664–668. (doi:10.1038/nature11832)
31. Krieger MJB, Keller L. 1997 Polymorphism at dinucleotide microsatellite loci in fire ant Solenopsis invicta populations. Mol. Ecol. 6, 997–999. (doi:10.1046/j.1365-294X.1997.00264.x)
32. 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. (doi:10.1093/molbev/ msq322)
33. R Development Core Team. 2010 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
34. Saeed AI et al. 2006 TM4 microarray software suite. Methods Enzymol. 411, 134–193. (doi:10.1016/ S0076-6879(06)11009-5)
35. Götz S et al. 2008 High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 36, 3420–3435. (doi:10.1093/nar/gkn176)
36. Alexa A, Rahnenführer J. 2010 topGO: Enrichment analysis for Gene Ontology. Bioconductor Packag. version 2.6.0. See www.bioconductor.org/packages/ release/bioc/
37. Nipitwattanaphon M, Wang J, Dijkstra MB, Keller L. 2013 A simple genetic basis for complex social behaviour mediates widespread gene expression differences. Mol. Ecol. 22, 3797–3813. (doi:10.1111/mec.12346)
38. Stupar RM et al. 2007 Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics 176, 2055–2067. (doi:10.1534/genetics.107.074286)
39. Galitski T, Saldanha AJ, Styles CA, Lander ES, Fink GR. 1999 Ploidy regulation of gene expression. Science 285, 251–254. (doi:10.1126/science.285.5425.251)
40. Wurm Y et al. 2011 The genome of the fire ant Solenopsis invicta. Proc. Natl Acad. Sci. USA 108, 5679–5684. (doi:10.1073/pnas.1009690108)
41. 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. (doi:10.1371/journal.pone.0042433)
42. Glastad KM, Hunt BG, Yi SV, Goodisman MAD. 2014 Epigenetic inheritance and genome regulation: is DNA methylation linked to ploidy in haplodiploid insects? Proc. R. Soc. B 281, 1–7. (doi:10.1098/ rspb.2014.0411)
43. Tanaka K, Barmina O, Sanders LE, Arbeitman MN, Kopp A. 2011 Evolution of sex-specific traits through changes in HOX-dependent doublesex expression. PLoS Biol. 9, e1001131. (doi:10.1371/journal.pbio.1001131)
44. Tschinkel WR. 2006 The fire ants. Cambridge, MA: Belknap Press.
45. Fischer BE, Wasbrough E, Meadows LA, Randlet O, Dorus S, Karr TL, Russell S. 2012 Conserved properties of Drosophila and human spermatozoal mRNA repertoires. Proc. R. Soc. B 279, 2636–2644. (doi:10.1098/rspb.2012.0153)
46. Keisman EL, Christiansen AE, Baker BS. 2001 The sex determination gene doublesex regulates the A/P organizer to direct sex-specific patterns of growth in the Drosophila genital imaginal disc. Dev. Cell 1, 215–225. (doi:10.1016/S1534-5807(01)00027-2)
47. Cho S, Huang ZY, Zhang J. 2007 Sex-specific splicing of the honeybee doublesex gene reveals 300 million years of evolution at the bottom of the insect sexdetermination pathway. Genetics 177, 1733–1741. (doi:10.1534/genetics.107.078980)
48. Baker DA, Nolan T, Fischer B, Pinder A, Crisanti A, Russell S. 2011 A comprehensive gene expression atlas of sex- and tissue-specificity in the malaria vector, Anopheles gambiae. BMC Genomics 12, 296. (doi:10.1186/1471-2164-12-296)
49. Ranz JM, Castillo-Davis CI, Meiklejohn CD, Hartl DL. 2003 Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300, 1742–1745. (doi:10.1126/science.1085881)
50. Bermejo-Alvarez P, Rizos D, Rath D, Lonergan P, Gutierrez-Adan A. 2010 Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc. Natl Acad. Sci. USA 107, 3394–3399. (doi:10.1073/pnas.0913843107)
51. Hahn MW, Lanzaro GC. 2005 Female-biased gene expression in the malaria mosquito Anopheles gambiae. Curr. Biol. 15, R192–R193. (doi:10.1016/j.cub.2005.03.005)