Advertisement

Development Genes and Evolution

, Volume 225, Issue 1, pp 23–30 | Cite as

The comparative study of five sex-determining proteins across insects unveils high rates of evolution at basal components of the sex determination cascade

  • José M. Eirín-López
  • Lucas Sánchez
Original Article

Abstract

In insects, the sex determination cascade is composed of genes that interact with each other in a strict hierarchical manner, constituting a coadapted gene complex built in reverse order from bottom to top. Accordingly, ancient elements at the bottom are expected to remain conserved ensuring the correct functionality of the cascade. In the present work, we have studied the levels of variation displayed by five key components of the sex determination cascade across 59 insect species, including Sex-lethal, transformer, transformer-2, fruitless, doublesex, and sister-of-Sex-lethal (a paralog of Sxl encompassing sex-independent functions). Surprisingly, our results reveal that basal components of the cascade (doublesex, fruitless) seem to evolve more rapidly than previously suspected. Indeed, in the case of Drosophila, these proteins evolve more rapidly than the master regulator Sex-lethal. These results agree with the notion suggesting that genes involved in early aspects of development will be more constrained due to the large deleterious pleiotropic effects of mutations, resulting in increased levels of purifying selection at top positions of the cascade. The analyses of the selective episodes involved in the recruitment of Sxl into sex-determining functions further support this idea, suggesting the presence of bursts of adaptive selection in the common ancestor of drosophilids, followed by the onset of purifying selection preserving the master regulatory role of this protein on top of the Drosophila sex determination cascade. Altogether, these results underscore the importance of the position of sex determining genes in the cascade, constituting a major constraint shaping the molecular evolution of the insect sex determination pathway.

Keywords

Evolution Development Sex-specific genes Insects Evolutionary rates Selection 

Notes

Acknowledgments

The present work was supported by start-up funds from the College of Arts and Sciences at Florida International University (CAS-FIU) to J.M.E.-L. We thank two anonymous reviewers for helpful comments and suggestions on an earlier version of this work.

Supplementary material

427_2015_491_MOESM1_ESM.doc (220 kb)
Supplementary Table 1 (DOC 219 kb)
427_2015_491_MOESM2_ESM.xls (509 kb)
Supplementary Table 2 (XLS 509 kb)

References

  1. Artieri CG, Haerty W, Singh RS (2009) Ontogeny and phylogeny: molecular signatures of selection, constraint, and temporal pleiotropy in the development of Drosophila. BMC Biol 7:42. doi: 10.1186/1741-7007-7-42 PubMedCentralPubMedCrossRefGoogle Scholar
  2. Baker BS, Ridge KA (1980) Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics 94:383–423PubMedCentralPubMedGoogle Scholar
  3. Black DL (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72:291–336. doi: 10.1146/annurev.biochem.72.121801.161720 PubMedCrossRefGoogle Scholar
  4. Bopp D, Saccone G, Beye M (2014) Sex determination in insects: variations on a common theme. Sex Dev 8:20–28. doi: 10.1159/000356458 PubMedCrossRefGoogle Scholar
  5. Civetta A, Singh RS (1998) Sex-related genes, directional sexual selection, and speciation. Mol Biol Evol 15:901–909PubMedCrossRefGoogle Scholar
  6. Cline TW (1978) Two closely linked mutations in Drosophila melanogaster that are lethal to opposite sexes and interact with daughterless. Genetics 90:683–698PubMedCentralPubMedGoogle Scholar
  7. Cline TW, Dorsett M, Sun S, Harrison MM, Dines J, Sefton L, Megna L (2010) Evolution of the Drosophila feminizing switch gene Sex-lethal. Genetics 186:1321–1336. doi: 10.1534/genetics.110.121202 PubMedCentralPubMedCrossRefGoogle Scholar
  8. Delport W, Poon AF, Frost SD, Kosakovsky Pond SL (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455–2457. doi: 10.1093/bioinformatics/btq429 PubMedCentralPubMedCrossRefGoogle Scholar
  9. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973. doi: 10.1093/molbev/mss075 PubMedCentralPubMedCrossRefGoogle Scholar
  10. Gempe T, Beye M (2011) Function and evolution of sex determination mechanisms, genes and pathways in insects. Bioessays 33:52–60. doi: 10.1002/bies.201000043 PubMedCentralPubMedCrossRefGoogle Scholar
  11. Goldman N, Whelan S (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:681–699CrossRefGoogle Scholar
  12. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  13. Hedges SB, Dudley J, Kumar S (2006) TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22:2971–2972. doi: 10.1093/bioinformatics/btl505 PubMedCrossRefGoogle Scholar
  14. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282PubMedGoogle Scholar
  15. Kulathinal RJ, Skwarek L, Morton RA, Singh RS (2003) Rapid evolution of the sex-determining gene, transformer: structural diversity and rate heterogeneity among sibling species of Drosophila. Mol Biol Evol 20:441–452PubMedCrossRefGoogle Scholar
  16. Kunte K et al (2014) doublesex is a mimicry supergene. Nature 507:229–232. doi: 10.1038/nature13112 PubMedCrossRefGoogle Scholar
  17. McAllister BF, McVean GA (2000) Neutral evolution of the sex-determining gene transformer in Drosophila. Genetics 154:1711–1720PubMedCentralPubMedGoogle Scholar
  18. Mullon C, Pomiankowski A, Reuter M (2012) Molecular evolution of Drosophila Sex-lethal and related sex determining genes. BMC Evol Biol 12:5. doi: 10.1186/1471-2148-12-5 PubMedCentralPubMedCrossRefGoogle Scholar
  19. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764. doi: 10.1371/journal.pgen.1002764 PubMedCentralPubMedCrossRefGoogle Scholar
  20. Peñalva LO, Sánchez L (2003) RNA binding protein sex-lethal (Sxl) and control of Drosophila sex determination and dosage compensation. Microbiol Mol Biol Rev 67:343–359, table of contentsGoogle Scholar
  21. Pomiankowski A, Nothiger R, Wilkins A (2004) The evolution of the Drosophila sex-determination pathway. Genetics 166:1761–1773PubMedCentralPubMedCrossRefGoogle Scholar
  22. Pond SL, Frost SD (2005) A genetic algorithm approach to detecting lineage-specific variation in selection pressure. Mol Biol Evol 22:478–485. doi: 10.1093/molbev/msi031 PubMedCrossRefGoogle Scholar
  23. Pond SL, Frost SD, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679. doi: 10.1093/bioinformatics/bti079 PubMedCrossRefGoogle Scholar
  24. Poon AF, Frost SD, Pond SL (2009) Detecting signatures of selection from DNA sequences using Datamonkey. Methods Mol Biol 537:163–183. doi: 10.1007/978-1-59745-251-9_8 PubMedCrossRefGoogle Scholar
  25. Ruiz MF, Goday C, Gonzalez P, Sanchez L (2003) Molecular analysis and developmental expression of the Sex-lethal gene of Sciara ocellaris (Diptera order, Nematocera suborder). Gene Expr Patterns 3:341–346PubMedCrossRefGoogle Scholar
  26. Ruiz MF et al (2007) The gene transformer of anastrepha fruit flies (Diptera, tephritidae) and its evolution in insects. PLoS ONE 2:e1239PubMedCentralPubMedCrossRefGoogle Scholar
  27. Ruiz MF, Sarno F, Zorrilla S, Rivas G, Sanchez L (2013) Biochemical and functional analysis of Drosophila-sciara chimeric sex-lethal proteins. PLoS ONE 8:e65171. doi: 10.1371/journal.pone.0065171 PubMedCentralPubMedCrossRefGoogle Scholar
  28. Sánchez L (2008) Sex-determining mechanisms in insects. Int J Dev Biol 52:837–856. doi: 10.1387/ijdb.072396ls PubMedCrossRefGoogle Scholar
  29. Sarno F, Ruiz MF, Eirin-Lopez JM, Perondini AL, Selivon D, Sanchez L (2010) The gene transformer-2 of Anastrepha fruit flies (Diptera, Tephritidae) and its evolution in insects. BMC Evol Biol 10:140PubMedCentralPubMedCrossRefGoogle Scholar
  30. Serna E, Gorab E, Ruiz MF, Goday C, Eirín-López JM, Sánchez L (2004) The gene Sex-lethal of the Sciaridae family (order Diptera, suborder Nematocera) and its phylogeny in dipteran insects. Genetics 168:907–921PubMedCentralPubMedCrossRefGoogle Scholar
  31. Sobrinho IS Jr, de Brito RA (2010) Evidence for positive selection in the gene fruitless in Anastrepha fruit flies. BMC Evol Biol 10:293. doi: 10.1186/1471-2148-10-293 PubMedCentralPubMedCrossRefGoogle Scholar
  32. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi: 10.1093/molbev/mst197 PubMedCentralPubMedCrossRefGoogle Scholar
  33. Verhulst EC, van de Zande L, Beukeboom LW (2010) Insect sex determination: it all evolves around transformer. Curr Opin Genet Dev 20:376–383. doi: 10.1016/j.gde.2010.05.001 PubMedCrossRefGoogle Scholar
  34. Wheeler WC, Whiting M, Wheeler QD, Carpenter JM (2001) The phylogeny of the extant hexapod orders. Cladistics 12:113–169CrossRefGoogle Scholar
  35. Wiegmann BM et al (2011) Episodic radiations in the fly tree of life. Proc Natl Acad Sci U S A 108:5690–5695. doi: 10.1073/pnas.1012675108 PubMedCentralPubMedCrossRefGoogle Scholar
  36. Wilkins AS (1995) Moving up the hierarchy: a hypothesis on the evolution of a genetic sex determination pathway. Bioessays 17:71–77. doi: 10.1002/bies.950170113 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.CHROMEVOL Group, Department of Biological SciencesFlorida International University, Marine Sciences ProgramNorth MiamiUSA
  2. 2.Centro de Investigaciones Biológicas (C.S.I.C.)MadridSpain

Personalised recommendations