Floral Isolation Is the Main Reproductive Barrier Among Closely Related Sexually Deceptive Orchids

Xu, Shuqing; Schlüter, Philipp M.; Scopece, Giovanni; Breitkopf, Hendrik; Gross, Karin; Cozzolino, Salvatore; Schiestl, Florian P.

doi:10.1111/j.1558-5646.2011.01323.x

Cited by 117 publications

(202 citation statements)

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“…In Ophrys, speciation by pollinator shift has been hypothesized, and there is evidence both for pollinator-driven genetic differentiation and selection on floral hydrocarbon profiles (4,6,9,10). In particular, specific pollinators mediate strong floral isolation among the coflowering closely related species O. sphegodes and O. exaltata by effectively preventing gene flow, whereas other reproductive barriers are largely absent (11). These species differ mainly in the double-bond position of their major alkenes (9), implying that the genes underlying this alkene difference may be barrier genes (6).…”

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confidence: 99%

Stearoyl-acyl carrier protein desaturases are associated with floral isolation in sexually deceptive orchids

Schlüter

Gagliardini

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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153

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The orchids Ophrys sphegodes and O. exaltata are reproductively isolated from each other by the attraction of two different, highly specific pollinator species. For pollinator attraction, flowers chemically mimic the pollinators' sex pheromones, the key components of which are alkenes with different double-bond positions. This study identifies genes likely involved in alkene biosynthesis, encoding stearoyl-acyl carrier protein (ACP) desaturase (SAD) homologs. The expression of two isoforms, SAD1 and SAD2, is flower-specific and broadly parallels alkene production during flower development. SAD2 shows a significant association with alkene production, and in vitro assays show that O. sphegodes SAD2 has activity both as an 18:0-ACP Δ 9 and a 16:0-ACP Δ 4 desaturase. Downstream metabolism of the SAD2 reaction products would give rise to alkenes with double-bonds at position 9 or position 12, matching doublebond positions observed in alkenes in the odor bouquet of O. sphegodes. SAD1 and SAD2 show evidence of purifying selection before, and positive or relaxed purifying selection after gene duplication. By contributing to the production of species-specific alkene bouquets, SAD2 is suggested to contribute to differential pollinator attraction and reproductive isolation among these species. Taken together, these data are consistent with the hypothesis that SAD2 is a florally expressed barrier gene of large phenotypic effect and, possibly, a genic target of pollinator-mediated selection.acyl-acyl carrier protein desaturase | isolation genes | pollination | speciation R eproductive isolation is a central topic in the study of evolution, its origin and maintenance being critical for the process of speciation. This statement is especially true for ecological speciation, in which divergent selection pressures on key traits drive the establishment of reproductive isolation even in the absence of geographic barriers to gene flow (1). This process fits the genic view of speciation, in which only few loci of large effect may be responsible for species differentiation, whereas gene flow is possible throughout the rest of the genome (2, 3). In practice, the challenge in studying these processes is identifying the traits under divergent selection and their genetic basis (1). In plants with strong pollinator-mediated reproductive isolation (floral isolation), however, key floral traits are direct targets of selection (1, 4). By identifying the molecular mechanisms underlying these traits, genes directly involved in reproductive isolation (so-called "barrier" or "isolation" genes) or even speciation can be identified (3-5).Strong floral isolation and high pollinator specificity make sexually deceptive orchids an excellent system for identifying barrier genes (4, 6). Rewardless orchids of the genus Ophrys attract male insects by sexual mimicry, inducing mating attempts of pollinators with flowers, whereby pollen is transferred. The key component to this system is the chemical mimicry of the pollinator female's sex pheromone (7, 8), a ...

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confidence: 99%

Stearoyl-acyl carrier protein desaturases are associated with floral isolation in sexually deceptive orchids

Schlüter

Gagliardini

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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153

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“…In our study, floral isolation mediated by floral scent appears to be the only significant barrier to gene flow between two recently diverged orchid species. Although the predominant importance of ethological floral isolation in sexual mimics has also been shown in other species (Scopece et al., 2007; Sedeek et al., 2014; Whitehead & Peakall, 2014; Xu et al., 2011), our study adds information on the traits underlying floral isolation and shows a negative association between fruit set and plant density, a situation that may favor a pollinator switch. In addition, it considers mycorrhizal fungi as a factor for species isolation, which has rarely been done in orchids and never before in the genus Ophrys .…”

Section: Discussionmentioning

confidence: 69%

“…Relative ploidy level was analyzed using flow cytometry following Xu et al. (2011). Two pollinia were chopped and mashed together with approximately 25‐mm 2 leaf material of Phaseolus coccineus (2 n , 1C = 1.01 ± 0.4 pg) which served as internal standard (IS), with a sharp razor blade in 1‐mL ice‐cold Baranyi's solution (0.1 mol/L citric acid, 0.5% Triton X‐100).…”

Section: Methodsmentioning

confidence: 99%

Floral scent and species divergence in a pair of sexually deceptive orchids

Gervasi

Selosse

Sauve

et al. 2017

Ecology and Evolution

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Speciation is typically accompanied by the formation of isolation barriers between lineages. Commonly, reproductive barriers are separated into pre‐ and post‐zygotic mechanisms that can evolve with different speed. In this study, we measured the strength of different reproductive barriers in two closely related, sympatric orchids of the Ophrys insectifera group, namely Ophrys insectifera and Ophrys aymoninii to infer possible mechanisms of speciation. We quantified pre‐ and post‐pollination barriers through observation of pollen flow, by performing artificial inter‐ and intraspecific crosses and analyzing scent bouquets. Additionally, we investigated differences in mycorrhizal fungi as a potential extrinsic factor of post‐zygotic isolation. Our results show that floral isolation mediated by the attraction of different pollinators acts apparently as the sole reproductive barrier between the two orchid species, with later‐acting intrinsic barriers seemingly absent. Also, the two orchids share most of their fungal mycorrhizal partners in sympatry, suggesting little or no importance of mycorrhizal symbiosis in reproductive isolation. Key traits underlying floral isolation were two alkenes and wax ester, present predominantly in the floral scent of O. aymoninii. These compounds, when applied to flowers of O. insectifera, triggered attraction and a copulation attempt of the bee pollinator of O. aymoninii and thus led to the (partial) breakdown of floral isolation. Based on our results, we suggest that adaptation to different pollinators, mediated by floral scent, underlies species isolation in this plant group. Pollinator switches may be promoted by low pollination success of individuals in dense patches of plants, an assumption that we also confirmed in our study.

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“…Other potential pre-zygotic isolation mechanisms are also absent including differences in pollen position on the vector and flowering times. Hybrids are considered to be relatively common in Caladenia (Backhouse and Jeanes 1995) suggesting that postzygotic reproductive barriers to hybridisation in the genus are weak or absent, which is also characteristic of sexual deception in general (Peakall et al 1997, Stökl et al 2008, Vereecken et al 2010, Xu et al 2011, Whitehead and Peakall 2104. The distribution of C. villosissima overlaps extensively with that of C. parva in western Victoria, and the distributions of C. phaeoclavia and C. parva meet in southern Victoria and the Grampians, indicating there is a high likelihood of introgression between the three taxa.…”

Section: Discussionmentioning

confidence: 99%

“…Strong prezygotic pollinator-mediated reproductive isolation is considered to be characteristic of sexually deceptive orchids (Paulus and Gack 1990, Bower 1996, Xu et al 2011, Whitehead and Peakall 2014. The shared pollinator indicates pollinator-mediated reproductive isolation is absent between the three Caladenia species and that they may hybridise where their ranges meet or overlap.…”

Section: Discussionmentioning

confidence: 99%

Pollinator sharing by the sexually deceptive Green-comb Spider Orchids, Caladenia phaeoclavia, C. parva and C. villosissima (Orchidaceae: Caladeniinae): taxonomic considerations

Bower¹

2015

Telopea

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Sexually deceptive orchids are pollinated when male insects perform mating behaviours on the femalemimicking labellum. Such orchids are characterised by extreme pollinator specificity, having only one, or occasionally a few, closely related insect species as pollen vectors. Sharing of a sexually deceived pollinator species between two or more orchid species is rare among Australian orchids in the Drakaeinae and Caladeniinae pollinated by male Thynnid wasps. In this paper putative pollinator sharing within a complex of three morphologically similar species of Greencomb Spider Orchids, Caladenia parva G.W. Carr, C. phaeoclavia D.L. Jones and C. villosissima G.W. Carr, was investigated using pollinator baiting and choice testing in the field. The three orchid taxa are shown to share the same thynnid wasp pollen vector, Lophocheilus anilitatus (Smith) over the entire geographic range of the complex in New South Wales and Victoria. Pollinator baiting and choice testing at 42 locations revealed no evidence for the existence of cryptic pollinator species in L. anilitatus. The close morphological similarity of the three orchids, their sharing of the same pollinator and lack of evidence of a reproductive isolating mechanism, suggest they belong to the same biological species, C. parva. However, phylogenetic analysis is desirable to confirm the monophyly of the three morphospecies and the possible existence of polyploidy in C. villosissima merits investigation.

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Floral Isolation Is the Main Reproductive Barrier Among Closely Related Sexually Deceptive Orchids

Abstract: Floral isolation is an important

Cited by 117 publications

References 73 publications

Stearoyl-acyl carrier protein desaturases are associated with floral isolation in sexually deceptive orchids

Stearoyl-acyl carrier protein desaturases are associated with floral isolation in sexually deceptive orchids

Floral scent and species divergence in a pair of sexually deceptive orchids

Pollinator sharing by the sexually deceptive Green-comb Spider Orchids, Caladenia phaeoclavia, C. parva and C. villosissima (Orchidaceae: Caladeniinae): taxonomic considerations

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