Adaptation and conservation throughout the drosophila melanogaster life-cycle

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  • Marta Coronado-Zamora, Universitat Autònoma de Barcelona
  • ,
  • Irepan Salvador-Martınez, University of Helsinki Institute of Biotechnology, UCL
  • ,
  • David Castellano
  • ,
  • Antonio Barbadilla, Universitat Autònoma de Barcelona
  • ,
  • Isaac Salazar-Ciudad, Universitat Autònoma de Barcelona, University of Helsinki Institute of Biotechnology, Centre de Recerca Matematica

Previous studies of the evolution of genes expressed at different life-cycle stages of Drosophila melanogaster have not been able to disentangle adaptive from nonadaptive substitutions when using nonsynonymous sites. Here, we overcome this limitation by combining whole-genome polymorphism data from D. melanogaster and divergence data between D. melanogaster and Drosophila yakuba. For the set of genes expressed at different life-cycle stages of D. melanogaster, as reported in modENCODE, we estimate the ratio of substitutions relative to polymorphism between nonsynonymous and synonymous sites (a) and then a is discomposed into the ratio of adaptive (xa) and nonadaptive (xna) substitutions to synonymous substitutions. We find that the genes expressed in mid- and late-embryonic development are the most conserved, whereas those expressed in early development and postembryonic stages are the least conserved. Importantly, we found that low conservation in early development is due to high rates of nonadaptive substitutions (high xna), whereas in postembryonic stages it is due, instead, to high rates of adaptive substitutions (high xa). By using estimates of different genomic features (codon bias, average intron length, exon number, recombination rate, among others), we also find that genes expressed in mid- and late-embryonic development show the most complex architecture: they are larger, have more exons, more transcripts, and longer introns. In addition, these genes are broadly expressed among all stages. We suggest that all these genomic features are related to the conservation of mid- and late-embryonic development. Globally, our study supports the hourglass pattern of conservation and adaptation over the life-cycle.

Original languageEnglish
JournalGenome Biology and Evolution
Pages (from-to)1463-1482
Number of pages20
Publication statusPublished - May 2019

    Research areas

  • Adaptation, Conservation, DFE-alpha, Evo-devo, Hourglass hypothesis, Natural selection

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