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. 2024 Jul 26;15(1):6308.
doi: 10.1038/s41467-024-50622-4.

Genome of the early spider-orchid Ophrys sphegodes provides insights into sexual deception and pollinator adaptation

Alessia Russo  1   2   3 , Mattia Alessandrini  4 , Moaine El Baidouri  5   6   7 , Daniel Frei  8 , Teresa Rosa Galise  9 , Lara Gaidusch  4 , Hannah F Oertel  4 , Sara E Garcia Morales  4 , Giacomo Potente  10 , Qin Tian  11   12 , Dmitry Smetanin  13 , Joris A M Bertrand  5   6   7 , Renske E Onstein  11   14 , Olivier Panaud  5   6   7 , Jürg E Frey  8 , Salvatore Cozzolino  9 , Thomas Wicker  13 , Shuqing Xu  15 , Ueli Grossniklaus  13 , Philipp M Schlüter  16   17
Affiliations

Genome of the early spider-orchid Ophrys sphegodes provides insights into sexual deception and pollinator adaptation

Alessia Russo et al. Nat Commun. .

Abstract

Pollinator-driven evolution of floral traits is thought to be a major driver of angiosperm speciation and diversification. Ophrys orchids mimic female insects to lure male pollinators into pseudocopulation. This strategy, called sexual deception, is species-specific, thereby providing strong premating reproductive isolation. Identifying the genomic architecture underlying pollinator adaptation and speciation may shed light on the mechanisms of angiosperm diversification. Here, we report the 5.2 Gb chromosome-scale genome sequence of Ophrys sphegodes. We find evidence for transposable element expansion that preceded the radiation of the O. sphegodes group, and for gene duplication having contributed to the evolution of chemical mimicry. We report a highly differentiated genomic candidate region for pollinator-mediated evolution on chromosome 2. The Ophrys genome will prove useful for investigations into the repeated evolution of sexual deception, pollinator adaptation and the genomic architectures that facilitate evolutionary radiations.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Pollination and genome of Ophrys sphegodes.
a Pseudocopulation of an Andrena nigroaenea male with an Ophrys sphegodes flower. Photo courtesy of Noa Schwabe. b Schematic representation of sexual deception. An Ophrys orchid mimics the pollinator’s female insect’s hairs, wings and pheromones to lure the male into pseudocopulation. Photos courtesy of Noa Schwabe. c The 18 assembled pseudochromosomes of O. sphegodes are labelled from 1 to 18. From outside to inside: chromosomes; gene density in light green; Gypsy retroelements in turquoise; Copia retroelements in blue; cytosine methylome in light red; between-species differentiation (global FST) along chromosomes in grey. d Recent LTR insertions vs. their age, showing that LTR expansion reached its maximum at around 1.3 to 0.8 Ma ago.
Fig. 2
Fig. 2. Evolutionary relationships among orchid genomes.
a Phylogenomic tree showing estimated divergence time and evolution of gene families for 21 plant species, colour indicating different plant groups (see inset). Divergence times are indicated by light blue bars at the internodes; their ranges indicate the 95% confidence intervals (CI) of the divergence time. Numbers at the branches indicate the number of expanded (blue) and contracted (red) gene families in the lineages. Bubbles at the tips indicate expanded (blue) and contracted (red) gene families per species (see Supplementary Table 11 and Supplementary Fig. 9 for CI intervals and number of expanded/contracted gene families). b Genome comparison between O. sphegodes and P. zijinensis. Chromosome comparison shows a high degree of collinearity and some chromosome rearrangements (see also Supplementary Fig. 10).
Fig. 3
Fig. 3. Summary of the putative hydrocarbon biosynthesis pathway in O. sphegodes.
a Schematic representation of the core pathway showing the biosynthesis of a (Z)−9-alkene from fatty acyl precursors, depicting core proteins in blue boxes. b Gene copy numbers in the Ophrys (Osph, blue boxes) and other orchid genomes (green boxes), abbreviated by first letter of the genus and the first two letters of the species (as in Supplementary Table 11). Gene copy numbers were estimated by tallying the orchid members of orthogroups containing functionally annotated hydrocarbon biosynthetic genes. Gene families expanded in Ophrys are shown with a red outline. c Heatmaps of RNA-seq gene expression (green to blue; grey, not expressed) for O. sphegodes gene copies, showing expression for unpollinated mature flower labella of O. sphegodes (SPH) and O. exaltata (EXA). Numbers in red indicate significantly differentially expressed genes (FDR < 0.05).
Fig. 4
Fig. 4. Phylogenetic analyses of three gene families showing gene duplications.
a SAD gene family tree. b FAD gene family tree. c FAR gene family tree. Colour shading for taxa as in Fig. 2a. O. sphegodes genes are shown in bold, branch thickness indicating bootstrap support. The first three or four letters of each gene sequence indicate species (as in Supplementary Table 11), where Osph indicates O. sphegodes; Pgu and Pzi indicate Platanthera guangdongensis and P. zijinensis, respectively. Black bars highlight clustered genes shown in subsequent Figure panels. d SAD2 gene cluster on chr 4, containing SAD1/2/8/7Ψ (gene details in Supplementary Table 7 and Supplementary Data 1). e Details of a cluster on chr 1 containing 3 FAD homologues. f Details of scaffold 578 with 6 FAR gene homologues. Gene models of interest are drawn in red.
Fig. 5
Fig. 5. GBS-based population genetic analysis between four sympatric Ophrys species.
a Genetic distance among the different species of the O. sphegodes s.l. group plotted along the genome, colours showing the most genetically dissimilar species for a given 1 Mb window (see Supplementary Fig. 17 for genetic similarity). b Genome-wide PCoA plot of pairwise distances between plant individuals revealed genetic separation between the four species. c Global FST among the 4 species was elevated in one region on chr 2 (327–346 Mb, shown as black bar). d PCoA of this region of chr 2 shows increased separation between O. sphegodes and O. exaltata. Colours show the most dissimilar species in panels a and c (grey: no data), and species identity in panels b and d, where O. sphegodes is shown in blue; O. exaltata, O. garganica and O. incubacea are shown in red, green and yellow, respectively.
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