A Single Origin for Nymphalid Butterfly Eyespots Followed by Widespread Loss of Associated Gene Expression

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Understanding how novel complex traits originate involves investigating the time of origin of the trait, as well as the origin of its underlying gene regulatory network in a broad comparative phylogenetic framework. The eyespot of nymphalid butterflies has served as an example of a novel complex trait, as multiple genes are expressed during eyespot development. Yet the origins of eyespots remain unknown. Using a dataset of more than 400 images of butterflies with a known phylogeny and gene expression data for five eyespot-associated genes from over twenty species, we tested origin hypotheses for both eyespots and eyespot-associated genes. We show that eyespots evolved once within the family Nymphalidae, approximately 90 million years ago, concurrent with expression of at least three genes associated with early eyespot development. We also show multiple losses of expression of most genes from this early three-gene cluster, without corresponding losses of eyespots. We propose that complex traits, such as eyespots, may have originated via co-option of a large pre-existing complex gene regulatory network that was subsequently streamlined of genes not required to fulfill its novel developmental function.

Vyšlo v časopise: A Single Origin for Nymphalid Butterfly Eyespots Followed by Widespread Loss of Associated Gene Expression. PLoS Genet 8(8): e32767. doi:10.1371/journal.pgen.1002893
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002893

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1. CarrollSB, GatesJ, KeysDN, PaddockSW, PanganibanGEF, et al. (1994) Pattern formation and eyespot determination in butterfly wings. Science 265 : 109–114.

2. BrakefieldPM, GatesJ, KeysD, KesbekeF, WijngaardenPJ, et al. (1996) Development, plasticity and evolution of butterfly eyespot patterns. Nature 384 : 236–242.

3. KeysDN, LewisDL, SelegueJE, PearsonBJ, GoodrichLV, et al. (1999) Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283 : 532–534.

4. BeldadeP, BrakefieldPM (2002) The genetics and evo-devo of butterfly wing patterns. Nat Rev Genet 3 : 442–452.

5. ReedRD, SerfasMS (2004) Butterfly wing pattern evolution is associated with changes in a Notch/Distal-less temporal pattern formation process. Curr Biol 14 : 1159–1166.

6. MonteiroA, GlaserG, StockslagerS, GlansdorpN, RamosD (2006) Comparative insights into questions of lepidopteran wing pattern homology. BMC Dev Biol 6 : 52.

7. SaenkoSV, MarialvaMSP, BeldadeP (2011) Involvement of the conserved Hox gene Antennapedia in the development and evolution of a novel trait. EvoDevo 2 : 9.

8. ShiraiLT, SaenkoSV, KellerRA, JeronimoMA, BrakefieldPM, 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.

9. MonteiroA, PodlahaO (2009) Wings, horns, and butterfly eyespots: how do complex traits evolve? PLoS Biol 7: e1000037 doi:10.1371/journal.pbio.1000037.

10. MonteiroA, PrudicKL (2010) Multiple approaches to study color pattern evolution in butterflies. Trends Evol Biol 2: e2.

11. Mayr E (1982) The Growth of Biological Thought. Cambridge, MA: Harvard Univ Press.

12. Abouheif A (1999) Establishing homology criteria for regulatory gene networks: prospects and challenges. In: Bock GR, Cardew G, editors. Homology. Novartis Foundation Symposium 222. Chichester: Wiley. pp. 207–225.

13. MonteiroA (2012) Gene regulatory networks reused to build novel traits: Co-option of an eye-related gene regulatory network in eye-like organs and red wing patches on insect wings is suggested by optix expression. Bioessays 34 : 181–186.

14. WakeDB, WakeMH, SpechtCD (2011) Homoplasy: from detecting pattern to determining process and mechanism of evolution. Science 331 : 1032–1035.

15. WahlbergN, LeneveuJ, KodandaramaiahU, PeñaC, NylinS, et al. (2009) Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proc R Soc B 276 : 4295–4302.

16. ReedRD, ChenP-H, NijhoutHF (2007) Cryptic variation in butterfly eyespot development: the importance of sample size in gene expression studies. Evol Dev 9 : 2–9.

17. AbouheifE, WrayGA (2002) Evolution of the gene network underlying wing polyphenism in ants. Science 297 : 249–252.

18. ForceA, LynchM, PickettFB, AmoresA, YanY, et al. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151 : 1531–1545.

19. TrueJR, HaagES (2001) Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3 : 109–119.

20. BrunettiCR, SelegueJE, MonteiroA, FrenchV, BrakefieldPM, et al. (2001) The generation and diversification of butterfly eyespot color patterns. Curr Biol 11 : 1578–1585.

21. HaywardDC, PatelNH, RehmEJ, GoodmanCS, BallEE (1995) Sequence and expression of grasshopper Antennapedia: comparison to Drosophila. Dev Biol 172 : 452–465.

22. FehonRG, KoohPJ, RebayI, ReganCL, XuT, et al. (1990) Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell 61 : 523–534.

23. PatelNH, Martin-BlancoE, ColemanKG, PooleSJ, EllisMC, et al. (1989) Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58 : 955–968.

24. PanganibanG, SebringA, NagyL, CarrollS (1995) The development of crustacean limbs and the evolution of arthropods. Science 270 : 1363–1366.

25. Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis, version 2.75. Available: http://mesquiteproject.org. Accessed 3 October 2011.

26. HeikkiläM, KailaL, MutanenM, PeñaC, WahlbergN (2012) Cretaceous origin and repeated tertiary diversification of the redefined butterflies. Proc R Soc B 279 : 1093–1099.

27. Pagel M, Meade A (2007) BayesTraits, version 1.0. Available: http://www.evolution.reading.ac.uk/BayesTraits.html. Accessed 28 July 2011.

28. PagelM (1999) The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst Biol 48 : 612–622.

29. BrowerAVZ (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci U S A 91 : 6491–6495.

30. MinasC, WaddellSJ, MontanaG (2011) Distance-based differential analysis of gene curves. Bioinformatics 27 : 3135–3141.

31. R Development Core Team (2011) R: a language and environment for statistical computing, Available: http://www.R-project.org.Accessed 20 December 2011.