Polyphenism of visual and chemical secondary sexually-selected wing traits in the butterfly Bicyclus anynana: How different is the intermediate phenotype?

English version

Autoři: Doriane Muller ^aff001; Benjamin Elias ^aff002; Laurent Collard ^aff002; Christophe Pels ^aff001; Marie-Jeanne Holveck ^aff001; Caroline M. Nieberding ^aff001
Působiště autorů: Group of Evolutionary Ecology and Genetics, Biodiversity Research Centre, Earth and Life Institute, Université Catholique de Louvain (UCLouvain), Louvain-la-Neuve, Belgium ^aff001; Institute of Condensed Matter and Nanosciences, Université catholique de Louvain (UCLouvain), Louvain-la-Neuve, Belgium ^aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0225003

Souhrn

Polyphenism is a type of phenotypic plasticity supposedly adaptive to drastic and recurrent changes in the environment such as seasonal alternation in temperate and tropical regions. The butterfly Bicyclus anynana shows polyphenism with well-described wet and dry seasonal forms in sub-Saharan Africa, displaying striking morphological, physiological and behavioural differences in response to higher or lower developmental temperatures. During the seasonal transition in the wild, the intermediate phenotype co-occurs with wet and dry phenotypes. In this study, we aimed to characterize the secondary sexually-selected wing traits of the intermediate form to infer its potential fitness compared to wet and dry phenotypes. Among the previously described wing morphological traits, we first showed that the area of the fifth eyespot on the ventral hindwing is the most discriminant trait to identify wet, dry and intermediate phenotypes in both sexes. Second, we characterized the intermediate form for two secondary sexually-selected wing traits: the area and UV reflectance of the dorsal forewing pupil and the composition of the male sex pheromone. We showed that values of these two traits are often between those of the wet and dry phenotypes. Third, we observed increasing male sex pheromone production in ageing dry and wet phenotypes. Our results contrast with previous reports of values for sexually-selected traits in wet and dry seasonal forms, which might be explained by differences in rearing conditions or sample size effects among studies. Wet, dry and intermediate phenotypes display redundant sexually dimorphic traits, including sexually-selected traits that can inform about their developmental temperature in sexual interactions.

Klíčová slova:

Phenotypes – Seasons – Larvae – Moths and butterflies – Pupil – Sexual selection – Sex pheromones

Zdroje

1. Botero CA, Weissing FJ, Wright J, Rubenstein DR. Evolutionary tipping points in the capacity to adapt to environmental change. Proceedings of the National Academy of Sciences. 2015;112: 184–189.

2. Fordyce JA. The evolutionary consequences of ecological interactions mediated through phenotypic plasticity. J Exp Biol. 2006;209: 2377–2383. doi: 10.1242/jeb.02271 16731814

3. Whitman DW, Agrawal AA. What is phenotypic plasticity and why is it important. Phenotypic plasticity of insects: Mechanisms and consequences. 2009; 1–63.

4. Stearns SC. The Evolutionary Significance of Phenotypic Plasticity. BioScience. 1989;39: 436–445. doi: 10.2307/1311135

5. Nijhout HF. Development and evolution of adaptive polyphenisms. Evolution & Development. 2003;5: 9–18. doi: 10.1046/j.1525-142X.2003.03003.x

6. Simpson SJ, Sword GA, Lo N. Polyphenism in Insects. Current Biology. 2011;21: R738–R749. doi: 10.1016/j.cub.2011.06.006 21959164

7. Brakefield PM, Reitsma N. Phenotypic plasticity, seasonal climate and the population biology of Bicyclus butterflies (Satyridae) in Malawi. Ecological Entomology. 1991;16: 291–303.

8. Janzen FJ, Paukstis GL. Environmental Sex Determination in Reptiles: Ecology, Evolution, and Experimental Design. The Quarterly Review of Biology. 1991;66: 149–179. doi: 10.1086/417143 1891591

9. Devlin RH, Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture. 2002;208: 191–364. doi: 10.1016/S0044-8486(02)00057-1

10. Simões PM, Ott SR, Niven JE. Environmental adaptation, phenotypic plasticity, and associative learning in insects: the desert locust as a case study. Oxford University Press; 2016.

11. Friberg M, Wiklund C. Generation-dependent female choice: behavioral polyphenism in a bivoltine butterfly. Behav Ecol. 2007;18: 758–763. doi: 10.1093/beheco/arm037

12. Levis NA, de la Serna Buzón S, Pfennig DW. An inducible offense: carnivore morph tadpoles induced by tadpole carnivory. Ecol Evol. 2015;5: 1405–1411. doi: 10.1002/ece3.1448 25897380

13. Canfield M, Greene E. Phenotypic plasticity and the semantics of polyphenism: a historical review and current perspectives. Phenotypic plasticity of insects: mechanisms and consequences. 2009; 65–80.

14. Moran N. The Evolutionary Maintenance of Alternative Phenotypes on JSTOR. The American Society of Naturalists. 1992;139: 971–989.

15. Prudic KL, Stoehr AM, Wasik BR, Monteiro A. Eyespots deflect predator attack increasing fitness and promoting the evolution of phenotypic plasticity. Proceedings of the Royal Society of London B: Biological Sciences. 2015;282: 20141531.

16. Fusco G, Minelli A. Phenotypic plasticity in development and evolution: facts and concepts. Philosophical Transactions of the Royal Society of London B: Biological Sciences. 2010;365: 547–556. doi: 10.1098/rstb.2009.0267 20083631

17. Brakefield PM, Beldade P, Zwaan BJ. The African Butterfly Bicyclus anynana: A Model for Evolutionary Genetics and Evolutionary Developmental Biology. Emerging Model Organisms: A Laboratory Manual [Internet]. Edited by: Behringer RR, Johnson AD, Krumlauf RE; 2009. Available: http://cshprotocols.cshlp.org/content/2009/5/pdb.emo122

18. Kooi RE, Brakefield PM. The critical period for wing pattern induction in the polyphenic tropical butterfly Bicyclus anynana (Satyrinae). Journal of insect physiology. 1999;45: 201–212. doi: 10.1016/s0022-1910(98)00093-6 12770367

19. Brakefield PM, Pijpe J, Zwaan BJ. Developmental plasticity and acclimation both contribute to adaptive responses to alternating seasons of plenty and of stress in Bicyclus butterflies. Journal of biosciences. 2007;32: 465–475. doi: 10.1007/s12038-007-0046-8 17536166

20. Bear A, Monteiro A. Male Courtship Rate Plasticity in the Butterfly Bicyclus anynana Is Controlled by Temperature Experienced during the Pupal and Adult Stages. PLoS ONE. 2013;8: e64061. doi: 10.1371/journal.pone.0064061 23717531

21. Oostra V, de Jong MA, Invergo BM, Kesbeke F, Wende F, Brakefield PM, et al. Translating environmental gradients into discontinuous reaction norms via hormone signalling in a polyphenic butterfly. Proceedings of the Royal Society of London B: Biological Sciences. 2011;278: 789–797.

22. Lyytinen A, Brakefield PM, Mappes J. Significance of butterfly eyespots as an anti-predator device in ground-based and aerial attacks. Oikos. 2003;100: 373–379.

23. Prudic KL, Jeon C, Cao H, Monteiro A. Developmental plasticity in sexual roles of butterfly species drives mutual sexual ornamentation. Science. 2011;331: 73–75. doi: 10.1126/science.1197114 21212355

24. De Jong MA, Kesbeke F, Brakefield PM, Zwaan BJ. Geographic variation in thermal plasticity of life history and wing pattern in Bicyclus anynana. Climate research. 2010;43: 91.

25. Madewell R, Moczek AP. Horn possession reduces maneuverability in the horn-polyphenic beetle, Onthophagus nigriventris. J Insect Sci. 2006;6. doi: 10.1673/2006_06_21.1 19537972

26. Rueffler C, Van Dooren TJM, Leimar O, Abrams PA. Disruptive selection and then what? Trends in Ecology & Evolution. 2006;21: 238–245.

27. Windig JJ, Brakefield PM, Reitsma N, Wilson JGM. Seasonal polyphenism in the wild: survey of wing patterns in five species of Bicyclus butterflies in Malawi. Ecological Entomology. 1994;19: 285–298. doi: 10.1111/j.1365-2311.1994.tb00420.x

28. Jennions MD, Petrie M. Variation in mate choice and mating preferences: a review of causes and consequences. Biological Reviews. 1997;72: 283–327. doi: 10.1017/s0006323196005014 9155244

29. Candolin U. The use of multiple cues in mate choice. Biological Reviews. 2003;78: 575–595. 14700392

30. Mateus ARA, Marques-Pita M, Oostra V, Lafuente E, Brakefield PM, Zwaan BJ, et al. Adaptive developmental plasticity: Compartmentalized responses to environmental cues and to corresponding internal signals provide phenotypic flexibility. BMC Biology. 2014;12: 97. doi: 10.1186/s12915-014-0097-x 25413287

31. San Martin G, Bacquet P, Nieberding C. Mate choice and sexual selection in a model butterfly species, Bicyclus anynana: state of the art. Proc Neth Entomol Soc Meet. 2011;22: 9–22.

32. Robertson KA, Monteiro A. Female Bicyclus anynana butterflies choose males on the basis of their dorsal UV-reflective eyespot pupils. Proceedings of the Royal Society of London B: Biological Sciences. 2005;272: 1541–1546.

33. Ng SY, Bhardwaj S, Monteiro A. Males Become Choosier in Response to Manipulations of Female Wing Ornaments in Dry Season Bicyclus anynana Butterflies. J Insect Sci. 2017;17. doi: 10.1093/jisesa/iex053 28973485

34. Nieberding CM, De Vos H, Schneider MV, Lassance J-M, Estramil N, Andersson J, et al. The male sex pheromone of the butterfly Bicyclus anynana: towards an evolutionary analysis. PLoS One. 2008;3: e2751–e2751. doi: 10.1371/journal.pone.0002751 18648495

35. Nieberding CM, Fischer K, Saastamoinen M, Allen CE, Wallin EA, Hedenström E, et al. Cracking the olfactory code of a butterfly: the scent of ageing. Ecology letters. 2012;15: 415–424. doi: 10.1111/j.1461-0248.2012.01748.x 22390373

36. Bergen E van, Brakefield PM, S Heuskin, BJ Zwaan, Nieberding CM. The scent of inbreeding: a male sex pheromone betrays inbred males. Proc R Soc B. 2013;280: 20130102. doi: 10.1098/rspb.2013.0102 23466986

37. Fischer K, Perlick J, Galetz T. Residual reproductive value and male mating success: older males do better. Proceedings of the Royal Society of London B: Biological Sciences. 2008;275: 1517–1524.

38. Nieberding CM, Holveck M-J. Commentary on Kehl et al. “Young male mating success is associated with sperm number but not with male sex pheromone titres”: Unnatural experimental conditions inflate the importance of male courtship activity on mating success in a butterfly. Front Zool. 2018;15: 18. doi: 10.1186/s12983-018-0256-y 29719561

39. Nieberding CM, Holveck M-J. Laboratory social environment biases mating outcome: a first quantitative synthesis in a butterfly. Behav Ecol Sociobiol. 2017;71: 117. doi: 10.1007/s00265-017-2346-9

40. Karl I, Fischer K. Old male mating advantage results from sexual conflict in a butterfly. Animal Behaviour. 2013;85: 143–149.

41. Westerman EL, Chirathivat N, Schyling E, Monteiro A. Mate preference for a phenotypically plastic trait is learned, and may facilitate preference-phenotype matching. Evolution. 2014;68: 1661–1670. doi: 10.1111/evo.12381 24528407

42. Costanzo K, Monteiro A. The use of chemical and visual cues in female choice in the butterfly Bicyclus anynana. Proceedings of the Royal Society of London B: Biological Sciences. 2007;274: 845–851.

43. Dion E, Monteiro A, Yew JY. Phenotypic plasticity in sex pheromone production in Bicyclus anynana butterflies. Scientific Reports. 2016;6: 39002. doi: 10.1038/srep39002 27966579

44. Heuskin S, Vanderplanck M, Bacquet P, Holveck M-J, Kaltenpoth M, Engl T, et al. The composition of cuticular compounds indicates body parts, sex and age in the model butterfly Bicyclus anynana (Lepidoptera). Frontiers in Ecology and Evolution. 2014;2: 37.

45. Nieberding CM, Martin GS, Saenko S, Allen CE, Brakefield PM, Visser B. Sexual selection contributes to partial restoration of phenotypic robustness in a butterfly. Scientific Reports. 2018;8: 14315. doi: 10.1038/s41598-018-32132-8 30254273

46. Van’t Hof AE, Zwaan BJ, Saccheri IJ, Daly D, Bot ANM, Brakefield PM. Characterization of 28 microsatellite loci for the butterfly Bicyclus anynana. Molecular Ecology Notes. 2005;5: 169–172. doi: 10.1111/j.1471-8286.2004.00870.x

47. Rasband WS. ImageJ [Internet]. Bethesda, Maryland, USA: U. S. National Institutes of Health; 1997. Available: https://imagej.nih.gov/ij/, 1997–2016

48. Roskam JC, Brakefield PM. A comparison of temperature-induced polyphenism in African Bicylus butterflies from a seasonal savannah-rainforest ecotone. Evolution. 1996; 2360–2372. doi: 10.1111/j.1558-5646.1996.tb03624.x 28565687

49. Wijngaarden PJ, Brakefield PM. Lack of response to artificial selection on the slope of reaction norms for seasonal polyphenism in the butterfly Bicyclus anynana. Heredity. 2001;87: 410–420. doi: 10.1046/j.1365-2540.2001.00933.x 11737288

50. Beldade P, Brakefield PM. Concerted evolution and developmental integration in modular butterfly wing patterns. Evol Dev. 2003;5: 169–179. 12622734

51. Troscianko J, Stevens M. Image calibration and analysis toolbox–a free software suite for objectively measuring reflectance, colour and pattern. Methods Ecol Evol. 2015;6: 1320–1331. doi: 10.1111/2041-210X.12439 27076902

52. White TE, Dalrymple RL, Noble DW, O’Hanlon JC, Zurek DB, Umbers KD. Reproducible research in the study of biological coloration. Animal Behaviour. 2015;106: 51–57.

53. Papke RS, Kemp DJ, Rutowski RL. Multimodal signalling: structural ultraviolet reflectance predicts male mating success better than pheromones in the butterfly Colias eurytheme L. (Pieridae). Animal Behavior, Animal behaviour. 2007;73: 47–54. doi: 10.1016/j.anbehav.2006.07.004

54. Holveck M-J, Grégoire A, Staszewski V, Guerreiro R, Perret P, Boulinier T, et al. Eggshell Spottiness Reflects Maternally Transferred Antibodies in Blue Tits. PLOS ONE. 2012;7: e50389. doi: 10.1371/journal.pone.0050389 23226272

55. Wickham H. ggplot2: Elegant Graphics for Data Analysis [Internet]. New York: Springer-Verlag; 2009. Available: //www.springer.com/us/book/9780387981413

56. R Core Team. R: A Language and Environment for Statistical Computing [Internet]. Vienna, Austria,R Foundation for Statistical Computing; 2017. Available: https://www.R-project.org/

57. Zuur AF, Ieno E, Elphick CS. A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution. 2010;1. Available: https://besjournals.onlinelibrary.wiley.com/doi/full/10.1111/j.2041-210X.2009.00001.x

58. Dawson R. How Significant is a Boxplot Outlier? Journal of Statistics Education. 2011;19: null. doi: 10.1080/10691898.2011.11889610

59. Burnham KP, Anderson DR. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer Science & Business Media; 2003.

60. Lessells CM, Boag PT. Unrepeatable Repeatabilities: A Common Mistake. The Auk. 1987;104: 116–121. doi: 10.2307/4087240

61. Becker WA. Manual of quantitative genetics. 4th edition. Pullman (WA): Academic Enterprises; 1984.

62. van Bergen E, Osbaldeston D, Kodandaramaiah U, Brattström O, Aduse-Poku K, Brakefield PM. Conserved patterns of integrated developmental plasticity in a group of polyphenic tropical butterflies. BMC Evolutionary Biology. 2017;17: 59. doi: 10.1186/s12862-017-0907-1 28241743

63. Everett A, Tong X, Briscoe AD, Monteiro A. Phenotypic plasticity in opsin expression in a butterfly compound eye complements sex role reversal. BMC Evolutionary Biology. 2012;12: 232. doi: 10.1186/1471-2148-12-232 23194112

64. Dion E, Pui LX, Monteiro A. Early-exposure to new sex pheromone blend alters mate preference in female butterflies and in their offspring. bioRxiv. 2017; 214635. doi: 10.1101/214635

65. Balmer AJ, Brakefield PM, Brattström O, Bergen E van. Developmental plasticity for male secondary sexual traits in a group of polyphenic tropical butterflies. Oikos. 2018;127: 1812–1821. doi: 10.1111/oik.05291

66. Roskam JC, Brakefield PM. Seasonal polyphenism in Bicyclus (Lepidoptera: Satyridae) butterflies: different climates need different cues. Biological Journal of the Linnean Society. 1999;66: 345–356.

67. Garcia JE, Greentree AD, Shrestha M, Dorin A, Dyer AG. Flower Colours through the Lens: Quantitative Measurement with Visible and Ultraviolet Digital Photography. PLOS ONE. 2014;9: e96646. doi: 10.1371/journal.pone.0096646 24827828

Polyphenism of visual and chemical secondary sexually-selected wing traits in the butterfly Bicyclus anynana: How different is the intermediate phenotype?

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