Conserved Genes Underlie Phenotypic Plasticity in an Incipiently Social Bee.

Sandra M Rehan, Karl M Glastad, Michael A Steffen, Cameron R Fay, Brendan G Hunt, Amy L Toth
Author Information
  1. Sandra M Rehan: Department of Biological Sciences, University of New Hampshire.
  2. Karl M Glastad: Department of Cell & Developmental Biology, University of Pennsylvania.
  3. Michael A Steffen: Department of Biological Sciences, University of New Hampshire.
  4. Cameron R Fay: Department of Ecology, Evolution and Organismal Biology, Iowa State University.
  5. Brendan G Hunt: Department of Entomology, University of Georgia.
  6. Amy L Toth: Department of Ecology, Evolution and Organismal Biology, Iowa State University.

Abstract

Despite a strong history of theoretical work on the mechanisms of social evolution, relatively little is known of the molecular genetic changes that accompany transitions from solitary to eusocial forms. Here, we provide the first genome of an incipiently social bee that shows both solitary and social colony organization in sympatry, the Australian carpenter bee Ceratina australensis. Through comparative analysis, we provide support for the role of conserved genes and cis-regulation of gene expression in the phenotypic plasticity observed in nest-sharing, a rudimentary form of sociality. Additionally, we find that these conserved genes are associated with caste differences in advanced eusocial species, suggesting these types of mechanisms could pave the molecular pathway from solitary to eusocial living. Genes associated with social nesting in this species show signatures of being deeply conserved, in contrast to previous studies in other bees showing novel and faster-evolving genes are associated with derived sociality. Our data provide support for the idea that the earliest social transitions are driven by changes in gene regulation of deeply conserved genes.

References

  1. Neuron. 2000 Jul;27(1):145-58 [PMID: 10939338]
  2. Cell. 2014 Nov 20;159(5):1212-1226 [PMID: 25416956]
  3. Proc Natl Acad Sci U S A. 2011 Sep 20;108(38):15936-41 [PMID: 21911372]
  4. Proc Natl Acad Sci U S A. 2008 Sep 23;105(38):14620-5 [PMID: 18794533]
  5. Prog Lipid Res. 1990;29(3):167-227 [PMID: 2131463]
  6. Development. 2001 Apr;128(8):1359-67 [PMID: 11262236]
  7. Mol Biol Evol. 2015 Feb;32(2):456-71 [PMID: 25425561]
  8. Proc Natl Acad Sci U S A. 2014 Feb 18;111(7):2614-9 [PMID: 24488971]
  9. BMC Genomics. 2011 Mar 29;12:164 [PMID: 21447185]
  10. Development. 2007 Jan;134(1):55-64 [PMID: 17164414]
  11. Neuron. 1992 Nov;9(5):789-803 [PMID: 1418995]
  12. Annu Rev Entomol. 2017 Jan 31;62:419-442 [PMID: 27912247]
  13. Philos Trans R Soc Lond B Biol Sci. 2011 Jul 27;366(1574):2155-70 [PMID: 21690132]
  14. Integr Comp Biol. 2017 Sep 1;57(3):640-648 [PMID: 28662576]
  15. Nature. 1995 Mar 16;374(6519):227-32 [PMID: 7885442]
  16. Genome Biol. 2010;11(10):R106 [PMID: 20979621]
  17. Genome Res. 2003 Sep;13(9):2178-89 [PMID: 12952885]
  18. Development. 2010 Jan;137(2):191-201 [PMID: 20040486]
  19. Genome Res. 2013 Aug;23(8):1235-47 [PMID: 23636946]
  20. Horm Behav. 2000 Feb;37(1):1-14 [PMID: 10712853]
  21. Proc Natl Acad Sci U S A. 2009 Sep 8;106(36):15400-5 [PMID: 19706434]
  22. Mol Ecol. 2014 Jan;23(1):151-61 [PMID: 24118315]
  23. Mol Biol Evol. 2010 Mar;27(3):497-500 [PMID: 20110264]
  24. Reproduction. 2006 Jan;131(1):11-22 [PMID: 16388004]
  25. Trends Ecol Evol. 1999 May;14(5):202-205 [PMID: 10322535]
  26. Cell Stem Cell. 2011 May 6;8(5):580-93 [PMID: 21549331]
  27. Trends Ecol Evol. 2015 Jul;30(7):426-33 [PMID: 26051561]
  28. Insect Mol Biol. 2006 Oct;15(5):703-14 [PMID: 17069641]
  29. Cold Spring Harb Symp Quant Biol. 2009;74:419-26 [PMID: 19850850]
  30. Proc Natl Acad Sci U S A. 2015 Nov 10;112(45):13970-5 [PMID: 26483466]
  31. Nucleic Acids Res. 2009 Jul;37(Web Server issue):W202-8 [PMID: 19458158]
  32. Bioinformatics. 2005 Sep 15;21(18):3674-6 [PMID: 16081474]
  33. Curr Biol. 2015 Mar 30;25(7):897-900 [PMID: 25772447]
  34. BMC Genomics. 2015 Mar 25;16:235 [PMID: 25880983]
  35. Cell Mol Life Sci. 2004 Apr;61(7-8):737-49 [PMID: 15094999]
  36. Evolution. 2017 Dec;71(12):2871-2884 [PMID: 28875541]
  37. PLoS One. 2013 Aug 15;8(8):e72434 [PMID: 23977298]
  38. Nat Commun. 2014 May 20;5:3636 [PMID: 24845553]
  39. Mol Ecol. 2011 Oct;20(19):4070-84 [PMID: 21902748]
  40. BMC Genomics. 2013 Dec 19;14:903 [PMID: 24350621]
  41. BMC Genomics. 2014 Jan 28;15:75 [PMID: 24472515]
  42. Genome Biol. 2013 Feb 26;14(2):R20 [PMID: 23442883]
  43. Comp Biochem Physiol B Biochem Mol Biol. 1995 Jul;111(3):503-14 [PMID: 7613772]
  44. Nat Rev Genet. 2002 Feb;3(2):137-44 [PMID: 11836507]
  45. J Insect Physiol. 1998 Jul;44(7-8):597-603 [PMID: 12769942]
  46. Science. 2015 Jun 5;348(6239):1139-43 [PMID: 25977371]
  47. Brain Behav Evol. 2015;85(2):117-24 [PMID: 25925014]
  48. Mol Ecol. 2007 Nov;16(22):4837-48 [PMID: 17927707]
  49. Mol Biol Evol. 2011 Apr;28(4):1381-92 [PMID: 21172833]
  50. Genome Biol Evol. 2016 May 13;8(5):1401-10 [PMID: 27048475]
  51. Proc Natl Acad Sci U S A. 2014 Dec 16;111(50):17929-34 [PMID: 25453090]
  52. Genome Biol Evol. 2017 Sep 1;9(9):2395-2402 [PMID: 28957466]
  53. Cell. 2008 Jul 11;134(1):25-36 [PMID: 18614008]
  54. Trends Genet. 2007 Jul;23(7):350-8 [PMID: 17499383]
  55. Nature. 2004 Jul 1;430(6995):85-8 [PMID: 15229602]
  56. PLoS Genet. 2012;8(3):e1002596 [PMID: 22479195]

MeSH Term

Adaptation, Biological
Animals
Base Sequence
Bees
Biological Evolution
Brain
Conserved Sequence
Female
Gene Expression
Genome, Insect
Social Behavior
Transcription Factors

Chemicals

Transcription Factors

Word Cloud

Created with Highcharts 10.0.0socialconservedgenessolitaryeusocialprovideassociatedmechanismsmolecularchangestransitionsbeesupportgenesocialityspeciesGenesdeeplyDespitestronghistorytheoreticalworkevolutionrelativelylittleknowngeneticaccompanyformsfirstgenomeincipientlyshowscolonyorganizationsympatryAustraliancarpenterCeratinaaustralensiscomparativeanalysisrolecis-regulationexpressionphenotypicplasticityobservednest-sharingrudimentaryformAdditionallyfindcastedifferencesadvancedsuggestingtypespavepathwaylivingnestingshowsignaturescontrastpreviousstudiesbeesshowingnovelfaster-evolvingderiveddataideaearliestdrivenregulationConservedUnderliePhenotypicPlasticityIncipientlySocialBee

Similar Articles

Cited By (16)