Evolutionary trends in adaptation of Drosophila melanogaster fruit flies and their symbiotic microbiome to growth mediums with different NaCl concentrations

封面

如何引用文章

全文:

开放存取 开放存取
受限制的访问 ##reader.subscriptionAccessGranted##
受限制的访问 订阅或者付费存取

详细

Many experimental evolution studies have shown the ability of model animal species, such as Drosophila melanogaster, to adapt quickly to various adverse conditions such as unfavorable growth medium. It is usually assumed by default that such adaptation is due to changes in the genes of the studied macroorganisms. However, it is also known that microbiome can influence various biological processes in macroorganisms. Here we performed an evolutionary experiment in which some D. melanogaster lines were reared on a growth medium with two regimes of high NaCl concentration (4% and 7%), while the others were reared on the standard (favourable) medium. We evaluated the reproductive efficiency of experimental lines on the same two different unfavourable growth mediums five years after the experiment started. Our tests confirmed that the lines reared on the salty substrate became more tolerant to high NaCl concentration, with lines reared on 7% being overall better than lines reared on 4%, especially when tested on 7% medium. Moreover, we found that pre-inoculation of the high salt medium with homogenized salt-tolerant flies tended to improve reproductive efficiency on this medium (compared to pre-inoculation with homogenized control flies). Besides, we found out that individual laboratory line history is also an important factor that affect evolutionary experiment results. Finally, we show that general adaptive traits (overall number of mature offsprings and their development speed) can change linearly (number of mature offsprings) and non-linearly (development speed) when fruit flies progressively adapt to growing NaCl concentration (0 → 4% → 7%).

全文:

受限制的访问

作者简介

P. Panchenko

Lomonosov Moscow State University

编辑信件的主要联系方式.
Email: 15Panha@rambler.ru

Faculty of Biology, Department of Biological Evolution

俄罗斯联邦, Leninskiye gory, 1, Moscow, 119991

K. Perfilieva

Lomonosov Moscow State University

Email: 15Panha@rambler.ru

Faculty of Biology, Department of Biological Evolution

俄罗斯联邦, Leninskiye gory, 1, Moscow, 119991

M. Kornilova

Lomonosov Moscow State University

Email: 15Panha@rambler.ru

Faculty of Biology, Department of Biological Evolution

俄罗斯联邦, Leninskiye gory, 1, Moscow, 119991

参考

  1. Дмитриева А.С., Ивницкий С.Б., Марков А.В., 2016. Адаптация Drosophila melanogaster к неблагоприятному кормовому субстрату сопровождается расширением трофической ниши // Журн. общ. биологии. Т. 77. № 4. С. 249–261.
  2. Ивницкий С.Б., Максимова И.А., Панченко П.Л., Дмитриева А.С., Качалкин А.В. и др., 2018. Роль микробиома в адаптации Drosophila melanogaster к кормовому субстрату с повышенной концентрацией NaCl // Журн. общ. биологии. Т. 79. № 5. С. 393–403.
  3. Марков А.В., Ивницкий С.Б., Корнилова М.Б., Наймарк Е.Б., Широкова Н.Г., Перфильева К.С., 2015. Материнский эффект маскирует адаптацию к неблагоприятным условиям и затрудняет дивергенцию у Drosophila melanogaster // Журн. общ. биологии. Т. 76. № 6. С. 429–437.
  4. Панченко П.Л., Корнилова М.Б., Перфильева К.С., Марков А.В., 2017. Симбиотическая микробиота вносит вклад в адаптацию Drosophila melanogaster к неблагоприятной среде // Изв. РАН. Сер. биол. № 4. С. 341–351.
  5. Полуэктова Е.В., Митрофанов В.Г., Бурыченко Г.М., Мяснянкина Е.Н., Бакулина Э.Д., 1975. Дрозофила Drosophila // Объекты биологии развития. М.: Наука. С. 128–146.
  6. Шапошников Г.Х., 1961. Специфичность и возникновение адаптаций к новым хозяевам у тлей (Homoptera, Aphidoidea) в процессе естественного отбора (экспериментальные исследования) // Энтомол. обозр. Т. 40. № 4. С. 739–762.
  7. Akman Gündüz E., Douglas A.E., 2009. Symbiotic bacteria enable insect to use a nutritionally inadequate diet // Proc. Biol. Sci. V. 276. P. 987–991.
  8. Alberch P., Gale E.A., 1985. A developmental analysis of an evolutionary trend: Digital reduction in amphibians // Evolution. V. 39. № 1. Р. 8–23.
  9. Anagnostou C., Dorsch M., Rohlfs M., 2010. Influence of dietary yeasts on Drosophila melanogaster life-history traits // Entomol. Exp. Appl. V. 136. P. 1–11.
  10. Arbuthnott D., Rundle H.D., 2014. Misalignment of natural and sexual selection among divergently adapted Drosophila melanogaster populations // Anim. Behav. V. 87. P. 45–51.
  11. Bäckhed F., Ley R.E., Sonnenburg J.L., Peterson D.A., Gordon J.I., 2005. Host-bacterial mutualism in the human intestine // Science. V. 307. № 5717. Р. 1915–1920.
  12. Blum J.E., Fischer C.N., Miles J., Handelsman J., 2013. Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster // mBio. V. 4. Art. e00860.
  13. Bonfili L., Cecarini V., Berardi S., Scarpona S., Suchodolski J.S., et al., 2017. Microbiota modulation counteracts Alzheimer’s disease progression influencing neuronal proteolysis and gut hormones plasma levels // Sci. Rep. V. 7. № 1. Art. 2426.
  14. Bordenstein S.R., Theis K.R., 2015. Host biology in light of the microbiome: Ten principles of holobionts and hologenomes // PLoS Biol V. 13. № 8. Art. e1002226.
  15. Brummel T., Ching A., Seroude L., Simon A.F., Benzer S., 2004. Drosophila lifespan enhancement by exogenous bacteria // Proc. Natl. Acad. Sci. USA. V. 101. P. 12974–12979.
  16. Carpenter F.W., 1905. The reactions of the pomace fly (Drosophila ampelophila Loew) to light, gravity, and mechanical stimulation // Am. Nat. V. 39. P. 157–171.
  17. Castle W.E., 1906. Inbreeding, cross‐breeding and sterility in Drosophila // Science. V. 23. P. 153.
  18. Chandler J.A., Eisen J.A., Kopp A., 2012. Yeast communities of diverse Drosophila species: Comparison of two symbiont groups in the same hosts // Appl. Environ. Microbiol. V. 78. № 20. P. 7327–7336.
  19. Chirgwin S.R., Coleman S.U., Porthouse K.H. et al., 2003. Removal of Wolbachia from Brugia pahangi is closely linked to worm death and fecundity but does not result in altered lymphatic lesion formation in Mongolian gerbils (Meriones unguiculatus) // Infect. Immun. V. 71. № 12. P. 6986–6994.
  20. Cumming G., 2008. Replication and p intervals: p values predict the future only vaguely, but confidence intervals do much better // Perspect. Psychol. Sci. V. 3. № 4. P. 286–300.
  21. Dmitrieva A.S., Ivnitsky S.B., Maksimova I.A., Panchenko P.L., Kachalkin A.V., Markov A.V., 2019. Yeasts affect tolerance of Drosophila melanogaster to food substrate with high NaCl concentration // PLoS One. V. 14. № 11. Art. e0224811. https://doi.org/10.1371/journal.pone.0224811
  22. Dudley S.A., 1996. Differing selection on plant physiological traits in response to environmental water availability: A test of adaptive hypotheses // Evolution. V. 50. № 1. P. 92–102. https://doi.org/10.1111/j.1558-5646.1996.tb04475.x
  23. Erkosar B., Storelli G., Defaye A., Leulier F., 2013. Host-intestinal microbiota mutualism: ‘‘Learning on the fly’’ // Cell Host Microbe. V. 13. P. 8–14.
  24. Fry J.D., 2003. Detecting ecological trade-offs using selection experiments // Ecology. V. 84. P. 1672–1678.
  25. Guerrero R., Margulis L., Berlanga M., 2013. Symbiogenesis: The holobiont as a unit of evolution // Int. Microbiol. V. 16. P. 133–143.
  26. Halsey L., Curran-Everett D., Vowler S., Drummond G.B., 2015. The fickle P value generates irreproducible results // Nat. Methods. V. 12. P. 179–185.
  27. Hass J.W., 2000. The Reverend Dr William Henry Dallinger, F.R.S. (1839–1909) // Notes Rec. R. Soc. Lond. V. 54. № 1. P. 53–65.
  28. Hehemann J.H., Correc G., Barbeyron T., Helbert W., Czjzek M., Michel M., 2010. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota // Nature. V. 464. P. 908–912.
  29. Janeček Š., Patáčová E., Bartoš M., Padyšáková E., Spitzer L., Tropek R., 2010. Hovering sunbirds in the Old World: Occasional behaviour or evolutionary trend? // Oikos. V. 120. № 2. P. 178–183. https://doi.org/10.1111/j.1600-0706.2010.18612.x
  30. Johansson T., 2010. Hail the impossible: p-values, evidence, and likelihood // Scand. J. Psychol. V. 52. № 2. P. 113–125.
  31. Kautz S., Rubin B.E.R., Moreau C.S., 2013. Bacterial infections across the ants: Frequency and prevalence of Wolbachia, Spiroplasma, and Asaia // Psyche: J. Entomol. V. 2013. Art. 936341. https://doi.org/10.1155/2013/936341
  32. Kawecki T.J., Lenski R.E., Ebert D., Hollis B., Olivieri I., Whitlock M.C., 2012. Experimental evolution // Trends Ecol. Evol. V. 27. № 10. P. 547–560.
  33. Kohl K.D., Sadowska E.T., Rudolf A.M., Dearing M.D., Koteja P., 2016. Experimental еvolution on a wild mammal species results in modifications of gut microbial communities // Front. Microbiol. V. 7. https://doi.org/10.3389/fmicb.2016.00634
  34. Lenski R.E., 2004. Phenotypic and genomic evolution during a 20000-generation experiment with the bacterium Escherichia coli // Plant Breed. Rev. V. 24. P. 225–265.
  35. Long T.A.F., Rowe L., Agrawal A.F., 2013. The effects of selective history and environmental heterogeneity on inbreeding depression in experimental populations of Drosophila melanogaster // Am. Nat. V. 181. P. 532–544.
  36. Margulis L., Fester R., 1991. Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis. Boston: MIT Press. 454 p.
  37. McFall-Ngai M.J., 2002. Unseen forces: The influence of bacteria on animal development // Develop. Biol. V. 242. P. 1–14.
  38. Meyer J.R., Dobias D.T., Weitz J.S., Barrick J.E., Quick R.T., Lenski R.E., 2012. Repeatability and contingency in the evolution of a key innovation in phage lambda // Science. V. 335. № 6067. P. 428–432. https://doi.org/10.1126/science.1214449
  39. Milocco L., Salazar‐Ciudad I., 2020. Is evolution predictable? Quantitative genetics under complex genotype‐phenotype maps // Evolution. V. 74. № 2. Р. 230–244. https://doi.org/10.1111/evo.13907
  40. Morey R., 2017. Putting p’s into lmer: mixed-model regression and statistical significance // Psychonomic Society Featured Content. https://featuredcontent.psychonomic.org/putting-ps-into-lmer-mixed-model-regression-and-statistical-significance/
  41. Munkacsi A.B., Pan J.J., Villesen P., Mueller U.G., Blackwell M., McLaughlin D.J., 2004. Convergent coevolution in the domestication of coral mushrooms by fungus-growing ants // Proc. Biol. Sci. V. 271. P. 1777–1782.
  42. Nuzzo R., 2014. Scientific method: Statistical errors // Nature. V. 506. P. 150–152. https://doi.org/10.1038/506150a
  43. Odierna G., Olmo E., Caprigilone T., Kupriyanova L.A., 1993. Further data on sex chromosomes of Lacertidae and a hypothesis on their evolutionary trend // Amphibia-Reptilia. V. 14. № 1. P. 1–11. https://doi.org/10.1163/156853893x00147
  44. Roff D.A., Fairbairn D.J., 2007. The evolution of trade-offs: Where are we? // J. Evol. Biol. V. 20. P. 433–447.
  45. Rosenberg E., Koren O., Reshef L., Efrony R., Zilber-Rosenberg I., 2007. The role of microorganisms in coral health, disease and evolution // Nat. Rev. Microbiol. V. 5. № 5. P. 355–362.
  46. Rosenberg E., Sharon G., Zilber-Rosenberg I., 2009. The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework // Environ. Microbiol. V. 11. № 12. P. 2959–2962.
  47. Rosenberg E., Zilber-Rosenberg I., 2011. Symbiosis and development: The hologenome concept // Birth Defects Res. C. Embryo Today. V. 93. № 1. P. 56–66. https://doi.org/10.1002/bdrc.20196
  48. Sapolsky R., Balt S., 1996. Reductionism and variability in data: A meta-analysis // Perspect. Biol. Med. V. 39. № 2. P. 193–203. https://doi.org/10.1353/pbm.1996.0057
  49. Saxer G., Doebeli M., Travisano M., 2010. The repeatability of adaptive radiation during long-term experimental evolution of Escherichia coli in a multiple nutrient environment // PLoS One. V. 5. № 12. Art. e14184. https://doi.org/10.1371/journal.pone.0014184
  50. Shin S.C., Kim S.H., You H., Kim B., Kim A.C., et al., 2011. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling // Science. V. 334. P. 670–674.
  51. Silver N., 2012. The Signal and the Noise: Why So Many Predictions Fail – but Some Don’t. N.Y.: Penguin. 534 p.
  52. Starmer W.T., 1981. A comparison of Drosophila habitats according to the physiological attributes of the associated yeast communities // Evolution. V. 35. № 1. P. 38–52.
  53. Starmer W.T., Barker J.S.F., Phaff H.J., Fogleman J.C., 1986. Adaptations of Drosophila and yeasts: their Interactions with the Volatile 2-propanol in the Cactus–Microorganism–Drosophila model system // Aust. J. Biol. Sci. V. 39. P. 69–77.
  54. Stergiopoulos K., Cabrero P., Davies S.A., Dow J.A., 2009. Salty dog, an SLC5 symporter, modulates Drosophila response to salt stress // Physiol. Genomics. V. 37. P. 1–11.
  55. Stern D.L., Orgogozo V., 2008. The loci of evolution: how predictable is genetic evolution? // Evolution. V. 62. № 9. P. 2155–2177. https://doi.org/10.1111/j.1558-5646.2008.00450.x
  56. Stern D.L., Orgogozo V., 2009. Is genetic evolution predictable? // Science. V. 323. № 5915. P. 746–751. https://doi.org/10.1126/science.1158997
  57. Storelli G., Defaye A., Erkosar B., Hols P., Royet J., Leulier F., 2011. Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing // Cell Metabolism. V. 14. P. 403–414.
  58. Te Velde J.H., Molthoff C.F.M., Scharloo W., 1988. The function of anal papillae in salt adaptation of Drosophila melanogaster larvae // J. Evol. Biol. V. 2. P. 139–153.
  59. Waddington C.H., 1959. Canalization of development and genetic assimilation of acquired characters // Nature. V. 183. P. 1654–1655.
  60. Yang J., Yang Y., Wu W.M., Zhao J., Jiang L., 2014. Evidence of polyethylene biodegradation by bacterial strains from the guts of plastic-eating waxworms // Environ. Sci. Technol. V. 48. № 23. P. 13776–13784.
  61. Yang Y., Yang J., Wu W.M., Zhao J., Song Y., et al., 2015. Biodegradation and mineralization of polystyrene by plastic-eating mealworms: Part 2. Role of gut microorganisms // Environ. Sci. Technol. V. 49. № 20. P. 12087–12093.
  62. Zilber-Rosenberg I., Rosenberg E., 2008. Role of microorganisms in the evolution of animals and plants: The hologenome theory of evolution // FEMS Microbiol. Rev. V. 32. P. 723–735.

补充文件

附件文件
动作
1. JATS XML
下载
2. Fig. 1. Experimental scheme for testing the flies' adaptability to an unfavorable environment.

下载 (60KB)
索引源数据

版权所有 © Russian Academy of Sciences, 2025