Advertisement

Development Genes and Evolution

, Volume 227, Issue 5, pp 297–307 | Cite as

The flexible stem hypothesis: evidence from genetic data

  • Jean-Michel GibertEmail author
Review

Abstract

Phenotypic plasticity, the ability of a given genotype to produce different phenotypes in response to distinct environmental conditions, is widely observed in the wild. It is believed to facilitate evolution and, under the “flexible stem hypothesis”, it is thought that an ancestral plastic species can be at the origin of sister lineages with divergent phenotypes fixed by genetic assimilation of alternative morphs. We review here the genetic mechanisms underlying such phenomenon. We show several examples in which the same gene shows transcriptional plasticity in response to environmental factors and divergence of expression within or between species. Thus, the same gene is involved both in the plasticity of a trait and in the evolution of that trait. In a few cases, it can be traced down to cis-regulatory variation in this gene and, in one case, in the very same regulatory sequence whose activity is modulated by the environment. These data are compatible with the “flexible stem hypothesis” and also suggest that the evolution of the plasticity of a trait and the evolution of the trait are not completely uncoupled as they often involve the same locus. Furthermore, the “flexible stem hypothesis” implies that it is possible to canalize initially plastic phenotypes. Several studies have shown that it was possible through modification of chromatin regulation or hormonal signalling/response. Further studies of phenotypic plasticity in an evolutionary framework are needed to see how much the findings described in this review can be generalized.

Keywords

Phenotypic plasticity Evolution Gene expression Review 

Notes

Acknowledgements

I thank Sophie Gournet for the drawings illustrating this review. I thank Frédérique Peronnet, Emmanuèle Mouchel-Vielh and Virginie Courtier-Orgogozo for critical reading of the manuscript and stimulating discussions. I thank the two anonymous reviewers for comments that significantly enriched the manuscript.

References

  1. Azevedo RBR, French V, Partridge L (2002) Temperature modulates epidermal cell size in Drosophila melanogaster. J Insect Physiol 48:231–237CrossRefPubMedGoogle Scholar
  2. Badyaev AV, Foresman KR (2000) Extreme environmental change and evolution: stress-induced morphological variation is strongly concordant with patterns of evolutionary divergence in shrew mandibles. Proc Biol Sci 267:371–377CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bastide H, Betancourt A, Nolte V et al (2013) A genome-wide, fine-scale map of natural pigmentation variation in Drosophila melanogaster. PLoS Genet 9:e1003534. doi: 10.1371/journal.pgen.1003534 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Beldade P, Brakefield PM, Long AD (2002) Contribution of distal-less to quantitative variation in butterfly eyespots. Nature 415:315–318. doi: 10.1038/415315a CrossRefPubMedGoogle Scholar
  5. Bento G, Ogawa A, Sommer RJ (2010) Co-option of the hormone-signalling module dafachronic acid-DAF-12 in nematode evolution. Nature 466:494–497. doi: 10.1038/nature09164 CrossRefPubMedGoogle Scholar
  6. Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. In: Thoday EWC and JM (ed) advances in genetics. Academic Press, pp 115–155Google Scholar
  7. Brakefield PM, Gates J, Keys D et al (1996) Development, plasticity and evolution of butterfly eyespot patterns. Nature 384:236–242CrossRefPubMedGoogle Scholar
  8. Cheng LY, Bailey AP, Leevers SJ et al (2011) Anaplastic lymphoma kinase spares organ growth during nutrient restriction in Drosophila. Cell 146:435–447. doi: 10.1016/j.cell.2011.06.040 CrossRefPubMedGoogle Scholar
  9. Dembeck LM, Huang W, Magwire MM et al (2015) Genetic architecture of abdominal pigmentation in Drosophila melanogaster. PLoS Genet 11:e1005163. doi: 10.1371/journal.pgen.1005163 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dworkin I (2005) Towards a genetic architecture of cryptic genetic variation and genetic assimilation: the contribution of K. G Bateman J Genet 84:223–226CrossRefGoogle Scholar
  11. Endler L, Betancourt AJ, Nolte V, Schlötterer C (2015) Reconciling differences in pool-GWAS between populations: a case study of female abdominal pigmentation in Drosophila melanogaster. Genetics. doi: 10.1534/genetics.115.183376
  12. Fedorka KM, Copeland EK, Winterhalter WE (2013) Seasonality influences cuticle melanization and immune defense in a cricket: support for a temperature-dependent immune investment hypothesis in insects. J Exp Biol 216:4005–4010. doi: 10.1242/jeb.091538 CrossRefPubMedGoogle Scholar
  13. Ghalambor CK, Hoke KL, Ruell EW et al (2015) Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525:372–375. doi: 10.1038/nature15256 CrossRefPubMedGoogle Scholar
  14. Gibert J-M, Mouchel-Vielh E, De Castro S, Peronnet F (2016) Phenotypic plasticity through transcriptional regulation of the evolutionary hotspot gene tan in Drosophila melanogaster. PLoS Genet 12:e1006218. doi: 10.1371/journal.pgen.1006218 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gibert J-M, Mouchel-Vielh E, Peronnet F (2017) Modulation of yellow expression contributes to thermal plasticity of female abdominal pigmentation in Drosophila melanogaster. Sci Rep 7:43370. doi: 10.1038/srep43370 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gibert P, Moreteau B, David JR (2000) Developmental constraints on an adaptive plasticity: reaction norms of pigmentation in adult segments of Drosophila melanogaster. Evol Dev 2:249–260CrossRefPubMedGoogle Scholar
  17. Gibson G, Hogness DS (1996) Effect of polymorphism in the Drosophila regulatory gene Ultrabithorax on homeotic stability. Science 271:200–203CrossRefPubMedGoogle Scholar
  18. Gilbert SF (2001) Ecological developmental biology: developmental biology meets the real world. Dev Biol 233:1–12. doi: 10.1006/dbio.2001.0210 CrossRefPubMedGoogle Scholar
  19. James AC, Azevedo RB, Partridge L (1995) Cellular basis and developmental timing in a size cline of Drosophila melanogaster. Genetics 140:659–666PubMedPubMedCentralGoogle Scholar
  20. Jeong S, Rebeiz M, Andolfatto P et al (2008) The evolution of gene regulation underlies a morphological difference between two Drosophila sister species. Cell 132:783–793CrossRefPubMedGoogle Scholar
  21. Johannsen W (1911) The genotype conception of heredity. Am Nat XLV:129–159Google Scholar
  22. Kiontke K, Fitch DHA (2010) Phenotypic plasticity: different teeth for different feasts. Curr Biol CB 20:R710–R712. doi: 10.1016/j.cub.2010.07.009 CrossRefPubMedGoogle Scholar
  23. Kucharski R, Maleszka J, Foret S, Maleszka R (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319:1827–1830CrossRefPubMedGoogle Scholar
  24. Kutch IC, Sevgili H, Wittman T, Fedorka KM (2014) Thermoregulatory strategy may shape immune investment in Drosophila melanogaster. J Exp Biol 217:3664–3669. doi: 10.1242/jeb.106294 CrossRefPubMedGoogle Scholar
  25. Laland K, Uller T, Feldman M et al (2014) Does evolutionary theory need a rethink? Nature 514:161–164. doi: 10.1038/514161a CrossRefPubMedGoogle Scholar
  26. Laland KN, Uller T, Feldman MW et al (2015) The extended evolutionary synthesis: its structure, assumptions and predictions. Proc Biol Sci 282:20151019. doi: 10.1098/rspb.2015.1019 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Leung A, Parks BW, Du J et al (2014) Open chromatin profiling in mice livers reveals unique chromatin variations induced by high fat diet. J Biol Chem. doi: 10.1074/jbc.M114.581439
  28. Martin A, Orgogozo V (2013) The loci of repeated evolution: a catalog of genetic hotspots of phenotypic variation. Evolution 67:1235–1250. doi: 10.1111/evo.12081 PubMedGoogle Scholar
  29. Michie LJ, Mallard F, Majerus ME, Jiggins FM (2010) Melanic through nature or nurture: genetic polymorphism and phenotypic plasticity in Harmonia axyridis. J Evol Biol 23:1699–1707. doi: 10.1111/j.1420-9101.2010.02043.x CrossRefPubMedGoogle Scholar
  30. Moczek AP, Sultan S, Foster S et al (2011) The role of developmental plasticity in evolutionary innovation. Proc Biol Sci. doi: 10.1098/rspb.2011.0971
  31. Monteiro A, Chen B, Ramos DM et al (2013) Distal-less regulates eyespot patterns and melanization in Bicyclus butterflies. J Exp Zoolog B Mol Dev Evol 320:321–331. doi: 10.1002/jez.b.22503 CrossRefGoogle Scholar
  32. Muschick M, Barluenga M, Salzburger W, Meyer A (2011) Adaptive phenotypic plasticity in the Midas cichlid fish pharyngeal jaw and its relevance in adaptive radiation. BMC Evol Biol 11:116. doi: 10.1186/1471-2148-11-116 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Pfennig DW, Wund MA, Snell-Rood EC, et al (2010) Phenotypic plasticity’s impacts on diversification and speciationGoogle Scholar
  34. Pigliucci M (2001) Phenotypic plasticity. Beyond Nature and Nurture, Baltimore and LondonGoogle Scholar
  35. Prud’homme B, Gompel N, Carroll SB (2007) Emerging principles of regulatory evolution. Proc Natl Acad Sci U A 104(Suppl 1):8605–8612CrossRefGoogle Scholar
  36. Ragsdale EJ, Müller MR, Rödelsperger C, Sommer RJ (2013) A developmental switch coupled to the evolution of plasticity acts through a sulfatase. Cell 155:922–933. doi: 10.1016/j.cell.2013.09.054 CrossRefPubMedGoogle Scholar
  37. Rajpurohit S, Richardson R, Dean J et al (2016) Pigmentation and fitness trade-offs through the lens of artificial selection. Biol Lett. doi: 10.1098/rsbl.2016.0625
  38. Scheiner SM (1993) Plasticity as a selectable trait: reply to via. Am Nat 142:371–373CrossRefGoogle Scholar
  39. Schlichting CD, Pigliucci M (1993) Control of phenotypic plasticity via regulatory genes. Am Nat 142:366–370. doi: 10.1086/285543 CrossRefPubMedGoogle Scholar
  40. Schmalhausen II (1949) Factors of evolution, the theory of stabilizing selection. The University of Chicago Press, Chicago and LondonGoogle Scholar
  41. Schneider RF, Meyer A (2017) How plasticity, genetic assimilation and cryptic genetic variation may contribute to adaptive radiations. Mol Ecol 26:330–350. doi: 10.1111/mec.13880 CrossRefPubMedGoogle Scholar
  42. Schwander T, Leimar O (2011) Genes as leaders and followers in evolution. Trends Ecol Evol 26:143–151. doi: 10.1016/j.tree.2010.12.010 CrossRefPubMedGoogle Scholar
  43. Serobyan V, Xiao H, Namdeo S et al (2016) Chromatin remodelling and antisense-mediated upregulation of the developmental switch gene eud-1 control predatory feeding plasticity. Nat Commun 7:12337. doi: 10.1038/ncomms12337 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Shirai LT, Saenko SV, Keller RA et al (2012) Evolutionary history of the recruitment of conserved developmental genes in association to the formation and diversification of a novel trait. BMC Evol Biol 12:21. doi: 10.1186/1471-2148-12-21 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Sicard A, Thamm A, Marona C et al (2014) Repeated evolutionary changes of leaf morphology caused by mutations to a homeobox gene. Curr Biol 24:1880–1886. doi: 10.1016/j.cub.2014.06.061 CrossRefPubMedGoogle Scholar
  46. Simola DF, Graham RJ, Brady CM et al (2016) Epigenetic (re)programming of caste-specific behavior in the ant Camponotus floridanus. Science. doi: 10.1126/science.aac6633
  47. Susoy V, Ragsdale EJ, Kanzaki N, Sommer RJ (2015) Rapid diversification associated with a macroevolutionary pulse of developmental plasticity. elife. doi: 10.7554/eLife.05463
  48. Suzuki Y, Nijhout HF (2006) Evolution of a polyphenism by genetic accommodation. Science 311:650–652CrossRefPubMedGoogle Scholar
  49. Tang HY, Smith-Caldas MS, Driscoll MV et al (2011) FOXO regulates organ-specific phenotypic plasticity in drosophila. PLoS Genet 7:e1002373. doi: 10.1371/journal.pgen.1002373 CrossRefPubMedPubMedCentralGoogle Scholar
  50. True JR, Yeh SD, Hovemann BT et al (2005) Drosophila tan encodes a novel hydrolase required in pigmentation and vision. PLoS Genet 1:e63CrossRefPubMedPubMedCentralGoogle Scholar
  51. Via S (1993) Adaptive phenotypic plasticity: target or by-product of selection in a variable environment? Am Nat 142:352–365. doi: 10.1086/285542 CrossRefPubMedGoogle Scholar
  52. Via S, Gomulkievicz R, de Jong G et al (1995) Adaptive phenotypic plasticity: consensus and controversy. TREE 10:212–217PubMedGoogle Scholar
  53. Waddington CH (1952) Selection of the genetic basis for an acquired character. Nature 169:278CrossRefPubMedGoogle Scholar
  54. Waddington CH (1956) Genetic assimilation of the Bithorax phenotype. Evolution 10:1–13. doi: 10.2307/2406091 CrossRefGoogle Scholar
  55. Waddington CH (1959) Canalization of development and genetic assimilation of acquired characters. Nature 183:1654–1655CrossRefPubMedGoogle Scholar
  56. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New YorkGoogle Scholar
  57. West-Eberhard MJ (2005) Developmental plasticity and the origin of species differences. Proc Natl Acad Sci U A 102(Suppl 1):6543–6549CrossRefGoogle Scholar
  58. Whitehead A, Roach JL, Zhang S, Galvez F (2011) Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient. Proc Natl Acad Sci U A 108:6193–6198. doi: 10.1073/pnas.1017542108 CrossRefGoogle Scholar
  59. Whitehead A, Roach JL, Zhang S, Galvez F (2012) Salinity- and population-dependent genome regulatory response during osmotic acclimation in the killifish (Fundulus Heteroclitus) gill. J Exp Biol 215:1293–1305. doi: 10.1242/jeb.062075 CrossRefPubMedGoogle Scholar
  60. Wittkopp PJ, Beldade P (2009) Development and evolution of insect pigmentation: genetic mechanisms and the potential consequences of pleiotropy. Semin Cell Dev Biol 20:65–71CrossRefPubMedGoogle Scholar
  61. Wittkopp PJ, Stewart EE, Arnold LL et al (2009) Intraspecific polymorphism to interspecific divergence: genetics of pigmentation in Drosophila. Science 326:540–544. doi: 10.1126/science.1176980 CrossRefPubMedGoogle Scholar
  62. Wittkopp PJ, Williams BL, Selegue JE, Carroll SB (2003) Drosophila pigmentation evolution: divergent genotypes underlying convergent phenotypes. Proc Natl Acad Sci U A 100:1808–1813CrossRefGoogle Scholar
  63. Woltereck R (1909) Weitere experimentelle unters¨uchungen ¨uber artver¨anderung, speziell ¨uber das wesen quantitativer artunterschiede bei daphniden. Verhandlungen Dtsch Zooligischen Ges:110–172Google Scholar
  64. Wund MA, Baker JA, Clancy B et al (2008) A test of the “flexible stem” model of evolution: ancestral plasticity, genetic accommodation, and morphological divergence in the threespine stickleback radiation. Am Nat 172:449–462. doi: 10.1086/590966 CrossRefPubMedGoogle Scholar
  65. Yassin A, Bastide H, Chung H et al (2016) Ancient balancing selection at tan underlies female colour dimorphism in Drosophila erecta. Nat Commun 7:10400. doi: 10.1038/ncomms10400 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Sorbonne Universités, UPMC Université Paris 06, CNRS, Biologie du Développement Paris Seine, Institut de Biologie Paris Seine (LBD-IBPS)ParisFrance

Personalised recommendations