The Salient Aroma Hypothesis: host plant specialization is linked with plant volatile availability in Lepidoptera.

Po-An Lin, Wei-Ping Chan, Liming Cai, Yun Hsiao, Even Dankowicz, Kadeem J Gilbert, Naomi E Pierce, Gary Felton
Author Information
  1. Po-An Lin: Department of Entomology, National Taiwan University, Taipei, Taiwan.
  2. Wei-Ping Chan: Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA. ORCID
  3. Liming Cai: Department of Integrative Biology, The University of Texas at Austin, Austin, TX, USA.
  4. Yun Hsiao: Institute of Ecology and Evolutionary Biology, National Taiwan University, Taipei, Taiwan.
  5. Even Dankowicz: Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA.
  6. Kadeem J Gilbert: Department of Plant Biology, Michigan State University, W K Kellogg Biological Station, Hickory Corners, MI, USA. ORCID
  7. Naomi E Pierce: Museum of Comparative Zoology, Harvard University, Cambridge, MA, USA. ORCID
  8. Gary Felton: Department of Entomology, The Pennsylvania State University, University Park, PA, USA.

Abstract

Host plant use in Lepidoptera has been a primary focus in studies of ecological specialization, and multiple factors are likely to be involved in shaping the evolution of diet breadth. Here, we first describe the Salient Aroma Hypothesis, suggesting that the availability of chemical information, particularly host-associated aromas, plays a critical role in shaping dietary specialization. According to the Salient Aroma Hypothesis, herbivores active during periods when chemical information is abundant, particularly during the daytime hours when plant aromas are hypothesized to be more prevalent, are more likely to evolve specialized diets. First, with meta-analysis, we show that plants release more diverse and abundant volatile compounds during daylight hours, increasing the availability of chemical information. We found that diurnal Lepidoptera tend to have specialized diets, while nocturnal species are more generalized, consistent with the prediction of the Salient Aroma Hypothesis. We further observed that morphological differences in the antennae of female Lepidoptera are correlated with variation in diet breadth and diel activity patterns, indirectly supporting the Salient Aroma Hypothesis. While multiple factors influence host plant specialization, the Salient Aroma Hypothesis offers a useful framework linking chemical information availability (e.g. plant volatiles) and ecological specialization.

Keywords

References

  1. Neuron. 2011 Dec 8;72(5):698-711 [PMID: 22153368]
  2. Plant Cell Environ. 2015 Jan;38(1):23-34 [PMID: 24725255]
  3. Syst Biol. 2010 Jan;59(1):9-26 [PMID: 20525617]
  4. Phytochemistry. 2011 Sep;72(13):1605-11 [PMID: 21596403]
  5. Trends Plant Sci. 2004 Apr;9(4):180-6 [PMID: 15063868]
  6. Proc Natl Acad Sci U S A. 2015 Jul 7;112(27):8362-6 [PMID: 26100883]
  7. J Chem Ecol. 2021 Sep;47(8-9):799-809 [PMID: 34347233]
  8. Am J Bot. 2018 Mar;105(3):302-314 [PMID: 29746720]
  9. Microsc Microanal. 2016 Aug;22(4):913-21 [PMID: 27411894]
  10. Proc Natl Acad Sci U S A. 2017 Jun 20;114(25):6569-6574 [PMID: 28533385]
  11. Front Plant Sci. 2016 Apr 13;7:462 [PMID: 27148293]
  12. Trends Plant Sci. 2017 Sep;22(9):744-753 [PMID: 28789922]
  13. Yale J Biol Med. 2018 Dec 21;91(4):457-469 [PMID: 30588211]
  14. J Chem Ecol. 2024 Apr;50(3-4):129-142 [PMID: 38195852]
  15. Trends Ecol Evol. 1992 Jan;7(1):10-5 [PMID: 21235936]
  16. Integr Comp Biol. 2018 Sep 1;58(3):367-371 [PMID: 30239782]
  17. Evid Based Ment Health. 2019 Nov;22(4):153-160 [PMID: 31563865]
  18. Ecol Lett. 2014 Nov;17(11):1341-50 [PMID: 25168335]
  19. Ecology. 2012 May;93(5):981-91 [PMID: 22764485]
  20. Proc Natl Acad Sci U S A. 2015 Jan 13;112(2):442-7 [PMID: 25548168]
  21. Bioinformatics. 2010 Jun 1;26(11):1463-4 [PMID: 20395285]
  22. Nat Commun. 2018 Dec 4;9(1):5155 [PMID: 30514925]
  23. Nat Commun. 2011 Nov 15;2:542 [PMID: 22086342]
  24. Curr Biol. 2011 May 10;21(9):730-9 [PMID: 21497087]
  25. Proc Natl Acad Sci U S A. 2019 Nov 5;116(45):22657-22663 [PMID: 31636187]
  26. Trends Plant Sci. 2005 Jun;10(6):269-74 [PMID: 15949760]
  27. J Evol Biol. 2004 Jul;17(4):856-61 [PMID: 15271085]
  28. Proc Biol Sci. 2014 Nov 22;281(1795): [PMID: 25274368]
  29. Stat Med. 2002 Jun 15;21(11):1559-73 [PMID: 12111920]
  30. J Chem Ecol. 2021 Dec;47(12):1025-1041 [PMID: 34506004]
  31. PLoS One. 2013 Nov 25;8(11):e80875 [PMID: 24282557]
  32. Nature. 1999 Oct 28;401(6756):877-84 [PMID: 10553904]
  33. Philos Trans R Soc Lond B Biol Sci. 2022 Jun 20;377(1853):20210166 [PMID: 35491593]
  34. Front Plant Sci. 2013 Jun 11;4:185 [PMID: 23781224]
  35. Trends Plant Sci. 2012 May;17(5):293-302 [PMID: 22425020]
  36. Proc Natl Acad Sci U S A. 2007 Dec 18;104(51):20427-31 [PMID: 18077380]
  37. Curr Biol. 2013 Nov 18;23(22):R990-R994 [PMID: 24262832]
  38. Ecol Evol. 2012 Jan;2(1):227-46 [PMID: 22408739]
  39. BMC Plant Biol. 2021 Aug 30;21(1):401 [PMID: 34461825]
  40. J Environ Sci (China). 2019 Jul;81:102-118 [PMID: 30975314]
  41. Front Physiol. 2019 Aug 02;10:972 [PMID: 31427985]
  42. PLoS One. 2011;6(8):e24025 [PMID: 21901154]
  43. Science. 2024 Feb 9;383(6683):607-611 [PMID: 38330103]
  44. Plant Cell Environ. 2014 Aug;37(8):1892-904 [PMID: 24738697]
  45. Glob Chang Biol. 2022 Aug;28(15):4495-4505 [PMID: 35574993]
  46. Insects. 2021 Nov 22;12(11): [PMID: 34821847]
  47. Evolution. 2021 Jul;75(7):1594-1606 [PMID: 34166533]
  48. Proc Biol Sci. 2025 Mar;292(2042):20242426 [PMID: 40068825]
  49. Ann Bot. 2009 Jun;103(9):1435-43 [PMID: 19287014]
  50. Proc Natl Acad Sci U S A. 2017 Sep 5;114(36):E7499-E7505 [PMID: 28827317]
  51. Proc Biol Sci. 2018 Mar 14;285(1874): [PMID: 29540519]
  52. J Evol Biol. 2009 Apr;22(4):907-12 [PMID: 19220649]
  53. Curr Biol. 2009 Jun 9;19(11):881-90 [PMID: 19427209]
  54. Phytochemistry. 2003 Jun;63(3):265-84 [PMID: 12737977]
  55. Glob Chang Biol. 2016 Apr;22(4):1644-54 [PMID: 26546275]
  56. Curr Biol. 2020 Nov 16;30(22):4476-4482.e5 [PMID: 32916118]
  57. Naturwissenschaften. 2007 Sep;94(9):733-9 [PMID: 17479233]
  58. Q Rev Biol. 2016 Dec;91(4):389-418 [PMID: 29562117]
  59. Evolution. 1991 Aug;45(5):1065-1080 [PMID: 28564168]
  60. J Comp Neurol. 2013 Aug 15;521(12):2742-55 [PMID: 23359124]
  61. Evolution. 2024 May 29;78(6):1174-1182 [PMID: 38536734]
  62. Bioinformatics. 2004 Jan 22;20(2):289-90 [PMID: 14734327]
  63. Sci Rep. 2016 Sep 21;6:33851 [PMID: 27651113]

Grants

  1. /Ministry of Education of Taiwan
  2. /National Science and Technology Council
  3. /National Science Foundation of the USA
  4. /University of Texas at Austin

MeSH Term

Animals
Volatile Organic Compounds
Herbivory
Lepidoptera
Plants
Diet
Female
Odorants
Biological Evolution

Chemicals

Volatile Organic Compounds

Word Cloud

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