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02 26, 2021;4 (1): 253.

Sociality sculpts similar patterns of molecular evolution in two independently evolved lineages of eusocial bees.

Wyatt A Shell, Michael A Steffen, Hannah K Pare, Arun S Seetharam, Andrew J Severin, Amy L Toth, Sandra M Rehan
Author Information
  1. Wyatt A Shell: Department of Biology, York University, Toronto, ON, Canada. ORCID
  2. Michael A Steffen: Department of Biological Sciences, University of New Hampshire, Durham, NH, 03924, USA.
  3. Hannah K Pare: Department of Biological Sciences, University of New Hampshire, Durham, NH, 03924, USA.
  4. Arun S Seetharam: Office of Biotechnology, Iowa State University, Ames, IA, 50011, USA. ORCID
  5. Andrew J Severin: Office of Biotechnology, Iowa State University, Ames, IA, 50011, USA. ORCID
  6. Amy L Toth: Department of Entomology, Iowa State University, Ames, IA, 50011, USA. ORCID
  7. Sandra M Rehan: Department of Biology, York University, Toronto, ON, Canada. sandra.rehan@gmail.com.
PMID: 33637860 DOI: 10.1038/s42003-021-01770-6

Abstract

While it is well known that the genome can affect social behavior, recent models posit that social lifestyles can, in turn, influence genome evolution. Here, we perform the most phylogenetically comprehensive comparative analysis of 16 bee genomes to date: incorporating two published and four new carpenter bee genomes (Apidae: Xylocopinae) for a first-ever genomic comparison with a monophyletic clade containing solitary through advanced eusocial taxa. We find that eusocial lineages have undergone more gene family expansions, feature more signatures of positive selection, and have higher counts of taxonomically restricted genes than solitary and weakly social lineages. Transcriptomic data reveal that caste-affiliated genes are deeply-conserved; gene regulatory and functional elements are more closely tied to social phenotype than phylogenetic lineage; and regulatory complexity increases steadily with social complexity. Overall, our study provides robust empirical evidence that social evolution can act as a major and surprisingly consistent driver of macroevolutionary genomic change.

References

  1. Sci Rep. 2018 Jul 10;8(1):10388 [PMID: 29991733]
  2. Mol Biol Evol. 2015 Mar;32(3):690-703 [PMID: 25492498]
  3. Bioinformatics. 2015 Oct 1;31(19):3210-2 [PMID: 26059717]
  4. Proc Natl Acad Sci U S A. 2012 Jun 26;109(26):E1801-10 [PMID: 22691501]
  5. Annu Rev Entomol. 2017 Jan 31;62:419-442 [PMID: 27912247]
  6. Proc Biol Sci. 2019 Dec 4;286(1916):20191815 [PMID: 31771475]
  7. Genes Brain Behav. 2020 Jan;19(1):e12597 [PMID: 31264771]
  8. Trends Ecol Evol. 2015 Jul;30(7):426-33 [PMID: 26051561]
  9. Insect Mol Biol. 2018 Feb;27(1):90-98 [PMID: 28987007]
  10. PLoS One. 2012;7(4):e34690 [PMID: 22511959]
  11. Proc Natl Acad Sci U S A. 2017 Jun 20;114(25):6569-6574 [PMID: 28533385]
  12. Front Genet. 2014 Dec 23;5:431 [PMID: 25566318]
  13. Mol Biol Evol. 2014 Oct;31(10):2689-96 [PMID: 25053804]
  14. Proc Natl Acad Sci U S A. 2011 May 3;108(18):7472-7 [PMID: 21482769]
  15. Trends Genet. 2007 Jul;23(7):334-41 [PMID: 17509723]
  16. Proc Natl Acad Sci U S A. 2012 Oct 30;109(44):18012-7 [PMID: 23071321]
  17. Bioinformatics. 2011 Feb 15;27(4):578-9 [PMID: 21149342]
  18. Annu Rev Entomol. 2007;52:127-50 [PMID: 16866635]
  19. Pest Manag Sci. 2001 Oct;57(10):958-67 [PMID: 11695190]
  20. Evolution. 2005 Oct;59(10):2063-72 [PMID: 16405152]
  21. BMC Bioinformatics. 2011 Dec 22;12:491 [PMID: 22192575]
  22. Annu Rev Entomol. 2018 Jan 7;63:105-123 [PMID: 28945976]
  23. Science. 2015 Jun 5;348(6239):1139-43 [PMID: 25977371]
  24. Genome Biol. 2014;15(12):550 [PMID: 25516281]
  25. BMC Genomics. 2011 Mar 29;12:164 [PMID: 21447185]
  26. Science. 2008 Nov 7;322(5903):896-900 [PMID: 18988841]
  27. Genome Biol Evol. 2018 Oct 1;10(10):2749-2758 [PMID: 30247544]
  28. Biol Lett. 2011 Apr 23;7(2):277-80 [PMID: 20943679]
  29. Heredity (Edinb). 2009 Sep;103(3):208-16 [PMID: 19436326]
  30. PLoS One. 2011;6(6):e21086 [PMID: 21695157]
  31. Mol Biol Evol. 2007 Aug;24(8):1586-91 [PMID: 17483113]
  32. Nat Rev Genet. 2005 Apr;6(4):257-70 [PMID: 15761469]
  33. Proc Natl Acad Sci U S A. 2005 Sep 20;102(38):13367-71 [PMID: 16157878]
  34. Genome Biol. 2012 Jun 25;13(6):R56 [PMID: 22731987]
  35. Genome Biol. 2010;11(10):R106 [PMID: 20979621]
  36. Genome Biol Evol. 2015 Aug 12;7(8):2407-16 [PMID: 26272716]
  37. Trends Ecol Evol. 2019 Sep;34(9):844-855 [PMID: 31130318]
  38. Bioinformatics. 2019 Oct 1;35(19):3617-3627 [PMID: 30873536]
  39. Genome Biol Evol. 2016 May 13;8(5):1401-10 [PMID: 27048475]
  40. Genome Res. 2013 Aug;23(8):1235-47 [PMID: 23636946]
  41. Integr Comp Biol. 2017 Sep 1;57(3):640-648 [PMID: 28662576]
  42. Genome Biol. 2015 Apr 24;16:76 [PMID: 25908251]
  43. BMC Evol Biol. 2014 Dec 17;14:260 [PMID: 25514967]
  44. Proc Natl Acad Sci U S A. 2014 Feb 18;111(7):2614-9 [PMID: 24488971]
  45. Nature. 1995 Mar 16;374(6519):227-32 [PMID: 7885442]
  46. Bioinformatics. 2006 May 15;22(10):1269-71 [PMID: 16543274]
  47. Nat Protoc. 2013 Aug;8(8):1494-512 [PMID: 23845962]
  48. Mol Phylogenet Evol. 2012 Dec;65(3):926-39 [PMID: 22982437]
  49. Proc Natl Acad Sci U S A. 2011 Nov 1;108(44):18020-5 [PMID: 21960440]
  50. Front Psychol. 2018 Jun 05;9:865 [PMID: 29928241]
  51. Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W555-9 [PMID: 16845069]
  52. Mol Phylogenet Evol. 2019 Jan;130:121-131 [PMID: 30326287]

MeSH Term

Animals
Bees
Behavior, Animal
Evolution, Molecular
Gene Expression Profiling
Gene Expression Regulation
Gene-Environment Interaction
Genes, Insect
Genome, Insect
Genomics
Phylogeny
Social Behavior
Species Specificity
Transcriptome
Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.
Article has an altmetric score of 142

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