Recombination is associated with the evolution of genome structure and worker behavior in honey bees

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

Volumn 109, Issue 44, 2012, Pages 18012-18017

  Kent, Clement F ^a   Minaei, Shermineh ^a   Harpur, Brock A ^a   Zayed, Amro ^a  

^a YORK UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA BASE COMPOSITION; EVOLUTIONARY RATE; GC RICH SEQUENCE; GENE CONVERSION; GENE FREQUENCY; GENE MUTATION; GENETIC RECOMBINATION; GENETIC VARIABILITY; HONEYBEE; INSECT GENOME; INSECT SOCIETY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; POPULATION GENETICS; PRIORITY JOURNAL; WORKER (INSECT);

ANIMALS; BEES; BEHAVIOR, ANIMAL; EVOLUTION, MOLECULAR; MOLECULAR SEQUENCE DATA; RECOMBINATION, GENETIC;

APIS MELLIFERA; APOIDEA; HEXAPODA; HYMENOPTERA;

EID: 84868088496     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1208094109     Document Type: Article

References (56)

1. Wilson EO, Hölldobler B (2005) Eusociality: Origin and consequences. Proc Natl Acad Sci USA 102(38):13367-13371.
2. Nowak MA, Tarnita CE, Wilson EO (2010) The evolution of eusociality. Nature 466 (7310):1057-1062.
3. Strassmann JE, Page RE, Jr., Robinson GE, Seeley TD (2011) Kin selection and eusociality. Nature 471(7339):E5-E6, author reply E9-E10.
4. Hamilton WD (1964) The genetical evolution of social behaviour. I. J Theor Biol 7(1): 1-16.
5. Wilfert L, Gadau J, Schmid-Hempel P (2007) Variation in genomic recombination rates among animal taxa and the case of social insects. Heredity (Edinb) 98(4):189-197.
6. Sirviö A, Johnston JS, Wenseleers T, Pamilo P (2011) A high recombination rate in eusocial Hymenoptera: Evidence from the common wasp Vespula vulgaris. BMC Genet 12:95.
7. Meznar ER, Gadau J, Koeniger N, Rueppell O (2010) Comparative linkage mapping suggests a high recombination rate in all honeybees. J Hered 101(Suppl 1):S118-S126.
8. Bessoltane N, Toffano-Nioche C, Solignac M, Mougel F (2012) Fine scale analysis of crossover and non-crossover and detection of recombination sequence motifs in the honeybee (Apis mellifera). PLoS ONE 7(5):e36229.
9. Solignac M, Mougel F, Vautrin D, Monnerot M, Cornuet JM (2007) A third-generation microsatellite-based linkage map of the honey bee, Apis mellifera, and its comparison with the sequence-based physical map. Genome Biol 8(4):R66.
10. Beye M, et al. (2006) Exceptionally high levels of recombination across the honey bee genome. Genome Res 16(11):1339-1344.
11. Gadau J, et al. (2012) The genomic impact of 100 million years of social evolution in seven ant species. Trends Genet 28(1):14-21.
12. Weinstock GM, et al.; Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443(7114): 931-949.
13. Joørgensen FG, Schierup MH, Clark AG (2007) Heterogeneity in regional GC content and differential usage of codons and amino acids in GC-poor and GC-rich regions of the genome of Apis mellifera. Mol Biol Evol 24(2):611-619.
14. Duret L, Galtier N (2009) Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet 10:285-311.
15. Eyre-Walker A (1999) Evidence of selection on silent site base composition in mammals: potential implications for the evolution of isochores and junk DNA. Genetics 152(2):675-683.
16. Eyre-Walker A, Hurst LD (2001) The evolution of isochores. Nat Rev Genet 2(7): 549-555.
17. Lercher MJ, Smith NGC, Eyre-Walker A, Hurst LD (2002) The evolution of isochores: Evidence from SNP frequency distributions. Genetics 162(4):1805-1810.
18. Duret L, Arndt PF (2008) The impact of recombination on nucleotide substitutions in the human genome. PLoS Genet 4(5):e1000071.
19. Ratnakumar A, et al. (2010) Detecting positive selection within genomes: The problem of biased gene conversion. Philos Trans R Soc Lond B Biol Sci 365(1552): 2571-2580.
20. Meunier J, Duret L (2004) Recombination drives the evolution of GC-content in the human genome. Mol Biol Evol 21(6):984-990.
21. Hodgkinson A, Eyre-Walker A (2011) Variation in the mutation rate across mammalian genomes. Nat Rev Genet 12(11):756-766.
22. Spencer CCA, et al. (2006) The influence of recombination on human genetic diversity. PLoS Genet 2(9):e148.
23. Peters AD, Otto SP (2003) Liberating genetic variance through sex. Bioessays 25(6): 533-537.
24. Comeron JM, Kreitman M (2002) Population, evolutionary and genomic consequences of interference selection. Genetics 161(1):389-410.
25. Crow JF, Kimura M (1965) Evolution in sexual and asexual populations. Am Nat 99: 439-450.
26. Smith JM, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genet Res 23(1):23-35.
27. Otto SP, Barton NH (2005) Evolution of recombination due to random drift. Genetics 169(4):2353-2370.
28. Keightley PD, Otto SP (2006) Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443(7107):89-92.
29. Zayed A, Whitfield CW (2008) A genome-wide signature of positive selection in ancient and recent invasive expansions of the honey bee Apis mellifera. Proc Natl Acad Sci USA 105(9):3421-3426.
30. Kent CF, Issa A, Bunting AC, Zayed A (2011) Adaptive evolution of a key gene affecting queen and worker traits in the honey bee, Apis mellifera. Mol Ecol 20(24): 5226-5235.
31. Harpur BA, Minaei S, Kent CF, Zayed A (2012) Management increases genetic diversity of honey bees via admixture. Mol Ecol 21(18):4414-4421.
32. Whitfield CW, et al. (2006) Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera. Science 314(5799):642-645.
33. Grozinger CM, Fan Y, Hoover SE, 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(22):4837-4848.
34. Zayed A, Naeger NL, Rodriguez-Zas SL, Robinson GE (2012) Common and novel transcriptional routes to behavioral maturation in worker and male honey bees. Genes Brain Behav 11(3):253-261.
35. Lyko F, et al. (2010) The honey bee epigenomes: Differential methylation of brain DNA in queens and workers. PLoS Biol 8(11):e1000506.
36. Myers S, et al. (2010) Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327(5967):876-879.
37. Coop G, Wen X, Ober C, Pritchard JK, Przeworski M (2008) High-resolution mapping of crossovers reveals extensive variation in fine-scale recombination patterns among humans. Science 319(5868):1395-1398.
38. Coop G, Myers SR (2007) Live hot, die young: Transmission distortion in recombination hotspots. PLoS Genet 3(3):e35.
39. Stumpf MP, McVean GA (2003) Estimating recombination rates from populationgenetic data. Nat Rev Genet 4(12):959-968.
40. Clark AG, Wang X, Matise T (2010) Contrasting methods of quantifying fine structure of human recombination. Annu Rev Genomics Hum Genet 11:45-64.
41. 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(27):11206-11211.
42. Ashburner M, et al.; The Gene Ontology Consortium (2000) Gene ontology: Tool for the unification of biology. Nat Genet 25(1):25-29.
43. Benjamini Y, Hochsberg Y (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J Roy Stat Soc Ser B (Stat Method) 57(1): 289-300.
44. Sinha S, Ling X, Whitfield CW, Zhai CX, Robinson GE (2006) Genome scan for cisregulatory DNA motifs associated with social behavior in honey bees. Proc Natl Acad Sci USA 103(44):16352-16357.
45. Chandrasekaran S, et al. (2011) Behavior-specific changes in transcriptional modules lead to distinct and predictable neurogenomic states. Proc Natl Acad Sci USA 108(44): 18020-18025.
46. Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet 76(3):449-462.
47. Team RDC (2008) R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna)
48. Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451-1452.
49. Huerta-Sanchez E, Durrett R, Bustamante CD (2008) Population genetics of polymorphism and divergence under fluctuating selection. Genetics 178(1):325-337.
50. Hernandez RD, Williamson SH, Zhu L, Bustamante CD (2007) Context-dependent mutation rates may cause spurious signatures of a fixation bias favoring higher GCcontent in humans. Mol Biol Evol 24(10):2196-2202.
51. Morton BR, Dar VU, Wright SI (2009) Analysis of site frequency spectra from Arabidopsis with context-dependent corrections for ancestral misinference. Plant Physiol 149(2):616-624.
52. Zar JH (1999) Biostatistical Analysis (Prentice Hall, Upper Saddle River, NJ), 4th Ed
53. Kent CF, Daskalchuk T, Cook L, Sokolowski MB, Greenspan RJ (2009) The Drosophila foraging gene mediates adult plasticity and gene-environment interactions in behaviour, metabolites, and gene expression in response to food deprivation. PLoS Genet 5(8):e1000609.
54. Niehuis O, et al. (2010) Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia. PLoS ONE 5(1):e8597.
55. Sirviö A, et al. (2006) High recombination frequency creates genotypic diversity in colonies of the leaf-cutting ant Acromyrmex echinatior. J Evol Biol 19(5):1475-1485.
56. Sirviö A, Pamilo P, Johnson RA, Page RE, Jr., Gadau J (2011) Origin and evolution of the dependent lineages in the genetic caste determination system of Pogonomyrmex ants. Evolution 65(3):869-884.