The evolutionary dynamics of major regulators for sexual development among Hymenoptera species

Frontiers in Genetics

Volumn 6, Issue MAR, 2015, Pages

  Biewer, Matthias ^a,b   Schlesinger, Francisca ^a,c   Hasselmann, Martin ^a,b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF HOHENHEIM   (Germany)

^c Institute of Bee Research   (Germany)

Author keywords

Adaptive evolution; Gene duplications; Pathway evolution; Regulatory changes; Sex determination

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; BIOINFORMATICS; DROSOPHILA MELANOGASTER; EVOLUTION; FEM GENE; GENE; GENE DUPLICATION; GENE SEQUENCE; GENETIC DISTANCE; HYMENOPTERA; NONHUMAN; ONCOGENE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEX DETERMINATION; SEXUAL DEVELOPMENT;

APIS; APIS MELLIFERA; APOIDEA; FORMICIDAE; HEXAPODA; HYMENOPTERA;

EID: 84927127945     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2015.00124     Document Type: Article

References (60)

1. Abouheif E and Wray GA. 2002. Evolution of the gene network underlying wing polyphenism in ants. Science 297: 249-52.
2. Bailey TB, M; Buske, FA; Frith, M; Grant, CE; Clementi, L; Ren, J; Li, WW; Noble, WS. 2009. MEME SUITE: tools for motif discovery and searching. Nucleid Acids Research 37.
3. Baker BS. 1989. Sex in flies: the splice of life. Nature 340: 521-524.
4. Beukeboom LW, Kamping A, Louter M, et al. 2007. Haploid females in the parasitic wasp Nasonia vitripennis. Science 315: 206.
5. Beye M, Gattermeier I, Hasselmann M, et al. 2006. Exceptionally high levels of recombination across the honey bee genome. Genome Res 16: 1339-1344.
6. Beye M, Hasselmann M, Fondrk MK, et al. 2003. The Gene csd is the Primary Signal for Sexual Development in the Honey Bee and Encodes a SR-Type Protein. Cell 114: 419-429.
7. Bopp D, Saccone G and Beye M. 2014. Sex determination in insects: variations on a common theme. Sexual development: genetics, molecular biology, evolution, endocrinology, embryology, and pathology of sex determination and differentiation 8: 20-8.
8. Bull JJ. 1983. Evolution of sex determining mechanisms. Menlo Park, CA: Cummings Publishing Company.
9. Burtis KC and Baker BS. 1989. Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56: 997-1010.
10. Butler B, Pirrotta V, Irminger-Finger I, et al. 1986. The sex-determining gene tra of Drosophila: molecular cloning and transformation studies. The EMBO Journal 5: 3607-3613.
11. Cardinal S and Danforth BN. 2013. Bees diversified in the age of eudicots. P Roy Soc B-Biol Sci 280.
12. Carvalho GA. 2001. The number of sex alleles (CSD) in a Bee population and its practical importance (Hymenoptera: Apidae). J Hym Res 10: 10-15.
13. Chandler D, McGuffin ME, Piskur J, et al. 1997. Evolutionary conservation of regulatory strategies for the sex determination factor transformer-2. Molecular and cellular biology 17: 2908-19.
14. Cho S, Huang ZY and Zhang J. 2007. Sex-specific splicing of the honeybee doublesex gene reveals 300 million years of evolution at the bottom of the insect sex-determination pathway. Genetics 177: 1733-1741.
15. Cline TW and Meyer BJ. 1996. Vive la difference: males vs females in flies vs worms. Annu Rev Genet 30: 637- 702.
16. Davidson EH. 2010. Emerging properties of animal gene regulatory networks. Nature 468: 911-20.
17. Dodds PN, Lawrence GJ, Catanzariti AM, et al. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci U S A 103: 8888-93.
18. Eddy SR. 1998. Profile hidden Markov models. Bioinformatics 14: 755-763.
19. Eddy SR. 2009. A new generation of homology search tools based on probabilistic inference. Genome informatics International Conference on Genome Informatics 23: 205-11.
20. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
21. Fairbrother WG, Yeh RF, Sharp PA, et al. 2002. Predictive identification of exonic splicing enhancers in human genes. Science 297: 1007-13.
22. Fani R and Fondi M. 2009. Origin and evolution of metabolic pathways. Physics of life reviews 6: 23-52.
23. Force A, Cresko WA, Pickett FB, et al. 2005. The origin of subfunctions and modular gene regulation. Genetics 170: 433-446.
24. Fraser HB, Hirsh AE, Wall DP, et al. 2004. Coevolution of gene expression among interacting proteins. Proc Natl Acad Sci U S A 101: 9033-9038.
25. Gadau J, Helmkampf M, Nygaard S, et al. 2012. The genomic impact of 100 million years of social evolution in seven ant species. Trends Genet 28: 14-21.
26. Gempe T, Hasselmann M, Schioett M, et al. 2009. Sex determination in honeybees: Two separate mechanisms induce and maintain the female pathway. PLoS Biol 7: e1000222.
27. Grimaldi D and Engel MS. 2005. Evolution of the Insects Cambridge, UK: Cambridge University Press.
28. Hasselmann M and Beye M. 2004. Signatures of selection among sex-determining alleles of the honey bee. Proc Natl Acad Sci U S A 101: 4888-4893.
29. Hasselmann M, Gempe T, Schiott M, et al. 2008. Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature 454: 519-522.
30. Hasselmann M, Lechner S, Schulte C, et al. 2010. Origin of a function by tandem gene duplication limits the evolutionary capability of its sister copy. Proc Natl Acad Sci USA 107: 13378-13383.
31. Hediger M, Henggeler C, Meier N, et al. 2010. Molecular characterization of the key switch F provides a basis for understanding the rapid divergence of the sex-determining pathway in the housefly. Genetics 184: 155-70.
32. Hunter S, Jones P, Mitchell A, et al. 2012. InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res 40: D306-12.
33. Innan H and Kondrashov F. 2010. The evolution of gene duplications: classifying and distinguishing between models. NatRevGenet 11: 97-108.
34. Kerr WE. 1987. Sex determination in bees. XXI. Number of XO-heteroalleles in a natural population of Melipona compressipes fasciculata (Apidae). Insectes Sociaux 34.
35. Koch V, Nissen I, Schmitt BD, et al. 2014. Independent evolutionary origin of fem paralogous genes and complementary sex determination in hymenopteran insects. PLoS One 9: e91883.
36. Lechner S, Ferretti L, Schoning C, et al. 2014. Nucleotide Variability at Its Limit? Insights into the Number and Evolutionary Dynamics of the Sex-Determining Specificities of the Honey Bee Apis mellifera. Mol Biol Evol 31: 272-287.
37. Lonnig WE and Saedler H. 2002. Chromosome rearrangements and transposable elements. Annu Rev Genet 36: 389-410.
38. Marchler-Bauer A, Lu S, Anderson JB, et al. 2011. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: D225-9.
39. Meznar ER, Gadau J, Koeniger N, et al. 2010. Comparative linkage mapping suggests a high recombination rate in all honeybees. The Journal of heredity 101 Suppl 1: S118-26.
40. Nahmad M, Glass L and Abouheif E. 2008. The dynamics of developmental system drift in the gene network underlying wing polyphenism in ants: a mathematical model. Evol Dev 10: 360-74.
41. Nissen I, Muller M and Beye M. 2012. The Am-tra2 gene is an essential regulator of female splice regulation at two levels of the sex determination hierarchy of the honeybee. Genetics 192: 1015-1026.
42. Pane A, Salvemini M, Delli BP, et al. 2002. The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development 129: 3715-3725.
43. Peter IS and Davidson EH. 2011. Evolution of gene regulatory networks controlling body plan development. Cell 144: 970-85.
44. Pires-daSilva A and Sommer RJ. 2003. The evolution of signalling pathways in animal development. Nat Rev Genet 4: 39-49.
45. Posada D and Crandall KA. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817- 818.
46. Privman E, Wurm Y and Keller L. 2013. Duplication and concerted evolution in a master sex determiner under balancing selection. Proc Biol Sci 280: 20122968.
47. Ruiz MF, Eirin-Lopez JM, Stefani RN, et al. 2007. The gene doublesex of Anastrepha fruit flies (Diptera, Tephritidae) and its evolution in insects. Development genes and evolution 217: 725-31.
48. Sadd B, Barribeau SM, Bloch G et al. 2015. The genomes of two key bumblebee species with primitive eusocial organisation. in press Salvemini M, Robertson M, Aronson B, et al. 2009. Ceratitis capitata transformer-2 gene is required to establish and maintain the autoregulation of Cctra, the master gene for female sex determination. International Journal of Developmental Biology 53: 109-120.
49. Sarno F, Ruiz MF, Eirin-Lopez JM, et al. 2010. The gene transformer-2 of Anastrepha fruit flies (Diptera, Tephritidae) and its evolution in insects. BMC Evol Biol 10: 140.
50. Schmieder S, Colinet D and Poirie M. 2012. Tracing back the nascence of a new sex-determination pathway to the ancestor of bees and ants. NatCommun 3: 895.
51. Sirvio A, Gadau J, Rueppell O, et al. 2006. High recombination frequency creates genotypic diversity in colonies of the leaf-cutting ant Acromyrmex echinatior. J Evol Biol 19: 1475-85.
52. Tamura K, Stecher G, Peterson D, et al. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-9.
53. Thompson JN and Burdon JJ. 1992. Gene-for-Gene Coevolution between Plants and Parasites. Nature 360: 121-125.
54. True JR and Haag ES. 2001. Developmental system drift and flexibility in evolutionary trajectories. Evolution & Development 3: 109-119.
55. van de Zande L and Verhulst EC. 2014. Genomic Imprinting and Maternal Effect Genes in Haplodiploid Sex Determination. Sexual Development 8: 74-82
56. Verhulst EC, Beukeboom LW and van de Zande L. 2010. Maternal control of haplodiploid sex determination in the wasp Nasonia. Science 328: 620-3
57. Verhulst EC, Lynch JA, Bopp D, et al. 2013. A new component of the Nasonia sex determining cascade is maternally silenced and regulates transformer expression. PLoS One 8: e63618.
58. Werren JH, Richards S, Desjardins CA, et al. 2010. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327: 343-348.
59. Wilkins AS. 1995. Moving up the hierarchy: A hypothesis on the evolution of a genetic sex dermination pathway. BioEssays 17: 71-77.
60. Wilkins AS. 2007. Between "design" and "bricolage": genetic networks, levels of selection, and adaptive evolution. Proc Natl Acad Sci U S A 104 Suppl 1: 8590-6.