title: Adaptive sequence evolution is driven by biotic stress in a pair of orchid species (Dactylorhiza) with distinct ecological optima.
abstract: The orchid family is the largest in the angiosperms, but little is known about the molecular basis of the significant variation they exhibit. We investigate here the transcriptomic divergence between two European terrestrial orchids, Dactylorhiza incarnata and Dactylorhiza fuchsii, and integrate these results in the context of their distinct ecologies that we also document. Clear signals of lineage-specific adaptive evolution of protein-coding sequences are identified, notably targeting elements of biotic defence, including both physical and chemical adaptations in the context of divergent pools of pathogens and herbivores. In turn, a substantial regulatory divergence between the two species appears linked to adaptation/acclimation to abiotic conditions. Several of the pathways affected by differential expression are also targeted by deviating post-transcriptional regulation via sRNAs. Finally, D. incarnata appears to suffer from insufficient sRNA control over the activity of RNA-dependent DNA polymerase, resulting in increased activity of class I transposable elements and, over time, in larger genome size than that of D. fuchsii. The extensive molecular divergence between the two species suggests significant genomic and transcriptomic shock in their hybrids and offers insights into the difficulty of coexistence at the homoploid level. Altogether, biological response to selection, accumulated during the history of these orchids, appears governed by their microenvironmental context, in which biotic and abiotic pressures act synergistically to shape transcriptome structure, expression and regulation.
authors.affiliation: Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria.|Departamento de Biología Vegetal y Ecología, University of Seville, Sevilla, Spain.
authors.forename: Francisco
authors.identifier: http://orcid.org/0000-0003-2104-3846
authors.initials: F
authors.lastname: Balao
authors.affiliation: Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria.|Department of Life Sciences and Biotechnologies, University of Ferrara, Ferrara, Italy.
authors.forename: Emiliano
authors.initials: E
authors.lastname: Trucchi
authors.affiliation: Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria.|Vienna Graduate School of Population Genetics, Vienna, Austria.
authors.forename: Thomas M
authors.initials: TM
authors.lastname: Wolfe
authors.affiliation: Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria.
authors.forename: Bao-Hai
authors.initials: BH
authors.lastname: Hao
authors.affiliation: Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria.|Departamento de Biología Vegetal y Ecología, University of Seville, Sevilla, Spain.
authors.forename: Maria Teresa
authors.initials: MT
authors.lastname: Lorenzo
authors.affiliation: Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria.
authors.forename: Juliane
authors.initials: J
authors.lastname: Baar
authors.affiliation: Gregor Mendel Institute for Plant Molecular Biology, Vienna, Austria.
authors.forename: Laura
authors.initials: L
authors.lastname: Sedman
authors.affiliation: Institut für Populationsgenetik, Vetmeduni Vienna, Vienna, Austria.|Centre of Biological Diversity, School of Biology, University of St Andrews, St Andrews, UK.
authors.forename: Carolin
authors.initials: C
authors.lastname: Kosiol
authors.affiliation: Department of Chromosome Biology, University of Vienna, Vienna, Austria.
authors.forename: Fabian
authors.initials: F
authors.lastname: Amman
authors.affiliation: Royal Botanic Gardens Kew, Richmond, UK.|School of Plant Biology, University of Western Australia, Crawley, Perth, WA, Australia.
authors.forename: Mark W
authors.initials: MW
authors.lastname: Chase
authors.affiliation: Department of Biology, Lund University, Lund, Sweden.
authors.forename: Mikael
authors.initials: M
authors.lastname: Hedrén
authors.affiliation: Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria.
authors.forename: Ovidiu
authors.identifier: http://orcid.org/0000-0002-8295-4937
authors.initials: O
authors.lastname: Paun
mesh_terms: D000220:Adaptation, Biological / Q000235:genetics*; D005075:Biological Evolution; D004251:DNA Transposable Elements; D004463:Ecology; D004777:Environment; D018745:Genome, Plant; D023281:Genomics; D029595:Orchidaceae / Q000145:classification*; D059467:Transcriptome
chemical_list: D004251:DNA Transposable Elements
keywords: abiotic stress; defence; ecological divergence; positive selection; small RNAs; transcriptomics