Convergence and molecular evolution of floral fragrance after independent transitions to self-fertilization

Studying the independent evolution of similar traits provides valuable insights into the ecological and genetic factors driving phenotypic evolution.1Blount Z.D. Lenski R.E. Losos J.B. Contingency and determinism in evolution: replaying life's tape.Science. 2018; 362eaam5979https://doi.org/10.1126/science.aam5979Crossref PubMed Scopus (311) Google Scholar The transition from outcrossing to self-fertilization is common in plant evolution2Barrett S.C.H. The evolution of plant sexual diversity.Nat. Rev. Genet. 2002; 3: 274-284https://doi.org/10.1038/nrg776Crossref PubMed Scopus (985) Google Scholar and is often associated with a reduction in floral attractive features such as display size, chemical signals, and pollinator rewards.3Sicard A. Lenhard M. The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants.Ann. Bot. 2011; 107: 1433-1443https://doi.org/10.1093/aob/mcr023Crossref PubMed Scopus (265) Google Scholar These changes are believed to result from the reallocation of the resources used for building attractive flowers, as the need to attract pollinators decreases.2Barrett S.C.H. The evolution of plant sexual diversity.Nat. Rev. Genet. 2002; 3: 274-284https://doi.org/10.1038/nrg776Crossref PubMed Scopus (985) Google Scholar,3Sicard A. Lenhard M. The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants.Ann. Bot. 2011; 107: 1433-1443https://doi.org/10.1093/aob/mcr023Crossref PubMed Scopus (265) Google Scholar We investigated the similarities in the evolution of flower fragrance following independent transitions to self-fertilization in Capsella.4Guo Y.-L. Bechsgaard J.S. Slotte T. Neuffer B. Lascoux M. Weigel D. Schierup M.H. Recent speciation of Capsella rubella from Capsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck.Proc. Natl. Acad. Sci. USA. 2009; 106: 5246-5251https://doi.org/10.1073/pnas.0808012106Crossref PubMed Scopus (174) Google Scholar,5Foxe J.P. Slotte T. Stahl E.A. Neuffer B. Hurka H. Wright S.I. Recent speciation associated with the evolution of selfing in Capsella.Proc. Natl. Acad. Sci. USA. 2009; 106: 5241-5245https://doi.org/10.1073/pnas.0807679106Crossref PubMed Scopus (204) Google Scholar,6Koenig D. Hagmann J. Li R. Bemm F. Slotte T. Neuffer B. Wright S.I. Weigel D. Long-term balancing selection drives evolution of immunity genes in Capsella.eLife. 2019; 8: 1-27https://doi.org/10.7554/eLife.43606Crossref Scopus (50) Google Scholar,7Bachmann J.A. Tedder A. Laenen B. Fracassetti M. Désamoré A. Lafon-Placette C. Steige K.A. Callot C. Marande W. Neuffer B. et al.Genetic basis and timing of a major mating system shift in Capsella.bioRxiv. 2018; (Preprint at)https://doi.org/10.1101/425389Crossref Scopus (0) Google Scholar,8Hurka H. Friesen N. German D.A. Franzke A. Neuffer B. "Missing link" species Capsella orientalis and Capsella thracica elucidate evolution of model plant genus Capsella (Brassicaceae).Mol. Ecol. 2012; 21: 1223-1238https://doi.org/10.1111/j.1365-294X.2012.05460.xCrossref PubMed Scopus (70) Google Scholar,9Slotte T. Hazzouri K.M. Ågren J.A. Koenig D. Maumus F. Guo Y.-L. Steige K. Platts A.E. Escobar J.S. Newman L.K. et al.The Capsella rubella genome and the genomic consequences of rapid mating system evolution.Nat. Genet. 2013; 45: 831-835https://doi.org/10.1038/ng.2669Crossref PubMed Scopus (288) Google Scholar We identified several compounds that exhibited similar changes in different selfer lineages, such that the flower scent composition reflects mating systems rather than evolutionary history within this genus. We further demonstrate that the repeated loss of β-ocimene emission, one of the compounds most strongly affected by these transitions, was caused by mutations in different genes. In one of the Capsella selfing lineages, the loss of its emission was associated with a mutation altering subcellular localization of the ortholog of TERPENE SYNTHASE 2. This mutation appears to have been fixed early after the transition to selfing through the capture of variants segregating in the ancestral outcrossing population. The large extent of convergence in the independent evolution of flower scent, together with the evolutionary history and molecular consequences of a causal mutation, suggests that the emission of specific volatiles evolved as a response to changes in ecological pressures rather than resource limitation.