Dataset Information

Lack of strong selection pressures maintains wide variation in floral traits in a food-deceptive orchid.

ABSTRACT:

Background and aims

Angiosperms vary remarkably in traits such as colour, size and shape of flowers, yet such variation generally tends to be low within species. In deceptive orchids, however, large variation in floral traits has been described, not only between but also within populations. Nonetheless, the factors driving variation in floral traits in deceptive orchids remain largely unclear.

Methods

To identify determinants of variation in floral traits, we investigated patterns of fruit set and selection gradients in the food-deceptive orchid Orchis purpurea, which typically presents large within-population variation in the colour and size of the flowers. Using long-term data, fruit set was quantified in two populations over 16 consecutive years (2004-2019). Artificial hand pollination was performed to test the hypothesis that fruit set was pollinator-limited and that selfing led to decreased seed set and viability. Annual variation (2016-2019) in selection gradients was calculated for three colour traits (brightness, contrast and the number of spots on the labellum), flower size (spur length, labellum length and width) and plant size (number of flowers, plant height).

Key results

Fruit set was, on average, low (~12 %) and severely pollinator-limited. Opportunities for selection varied strongly across years, but we found only weak evidence for selection on floral traits. In contrast, there was strong and consistent positive selection on floral display. Selfing led to reduced production of viable seeds and hence severe inbreeding depression (δ = 0.38).

Conclusion

Overall, these results demonstrate that the large variation in flower colour and size that is regularly observed in natural O. purpurea populations is maintained by the consistent lack of strong selection pressures on these traits through time.

SUBMITTER: Jacquemyn H

PROVIDER: S-EPMC7424767 | biostudies-literature |

REPOSITORIES: biostudies-literature

ACCESS DATA

Similar Datasets

Project description:Background and aimsSelection exerted by pollinators on flowers is predicted to occur along two distinct axes. While pollinator attraction to flowers is governed by pollinator preferences, pollen transfer efficiency is mediated by the mechanical fit of pollinators to flower morphology. Although pollinator attraction in sexually deceptive orchids is typically underpinned by floral odour, morphological traits are expected to play a vital role in mechanical fit during floral contact with pollinators.MethodsHere we utilize a comprehensive and novel procedure to test for pollinator-mediated selection through mechanical fit with the flower labellum in the orchid Chiloglottis trapeziformis. This approach combines detailed pollinator observations related to plant reproductive fitness with complementary experimental manipulation and phenotypic selection analysis.Key resultsExperiments with virgin flowers revealed that pollen removal occurs only during vigorous pseudocopulation. This behaviour involves male wasps that grasp the insectiform callus structure on the labellum while probing the labellum tip in a forward orientation. Both orientation and duration of pseudocopulation were significant predictors of pollen removal, confirming a direct relationship between pollinator behaviour and plant fitness. Controlled floral manipulation that either shortened or elongated the distance between the callus and the labellum tip detected no change in pollinator attraction. The duration of pseudocopulation, however, was significantly reduced on flowers with shortened or elongated callus-tip distances, consistent with stabilizing selection. Phenotypic selection analysis confirmed this prediction in natural populations by uncovering evidence for stabilizing selection on the distance between the callus and the labellum tip.ConclusionsOur experimental manipulations and selection analysis in natural populations thus demonstrate stabilizing selection on the distance from the callus to the labellum tip, and illustrate the utility of employing multiple approaches to confirm selection exerted by pollinators on floral form.

Project description:Background and aimsThe events leading to speciation are best investigated in systems where speciation is ongoing or incomplete, such as incipient species. By examining reproductive barriers among incipient sister taxa and their congeners we can gain valuable insights into the relative timing and importance of the various barriers involved in the speciation process. The aim of this study was to identify the reproductive barriers among sexually deceptive orchid taxa in the genus Chiloglottis.MethodsThe study targeted four closely related taxa with varying degrees of geographic overlap. Chemical, morphological and genetic evidence was combined to explore the basis of reproductive isolation. Of primary interest was the degree of genetic differentiation among taxa at both nuclear and chloroplast DNA markers. To objectively test whether or not species boundaries are defined by the chemistry that controls pollinator specificity, genetic analysis was restricted to samples of known odour chemistry.Key resultsFloral odour chemical analysis was performed for 600+ flowers. The three sympatric taxa were defined by their specific chiloglottones, the semiochemicals responsible for pollinator attraction, and were found to be fully cross-compatible. Multivariate morphometric analysis could not reliably distinguish among the four taxa. Although varying from very low to moderate, significant levels of genetic differentiation were detected among all pairwise combinations of taxa at both nuclear and chloroplast loci. However, the levels of genetic differentiation were lower than expected for mature species. Critically, a lack of chloroplast DNA haplotype sharing among the morphologically indistinguishable and most closely related taxon pair confirmed that chemistry alone can define taxon boundaries.ConclusionsThe results confirmed that pollinator isolation, mediated by specific pollinator attraction, underpins strong reproductive isolation in these taxa. A combination of large effective population sizes, initial neutral mutations in the genes controlling floral scent, and a pool of available pollinators likely drives diversity in this system.

Project description:The Australian sexually deceptive orchid, Chiloglottis trapeziformis, employs a unique UV-B-dependent floral volatile, chiloglottone 1, for specific male wasp pollinator attraction. Chiloglottone 1 and related variants (2,5-dialkylcyclohexane-1,3-diones), represent a unique class of specialized metabolites presumed to be the product of cyclization between two fatty acid (FA) precursors. However, the genes involved in the biosynthesis of precursors, intermediates, and transcriptional regulation remains to be discovered. Chiloglottone 1 production occurs in the aggregation of calli (callus) on the labellum under continuous UV-B light. Therefore, deep sequencing, transcriptome assembly, and differential expression (DE) analysis were performed across different tissue types and UV-B treatments. Transcripts expressed in the callus and labellum (∼23,000 transcripts) were highly specialized and enriched for a diversity of known and novel metabolic pathways. DE analysis between chiloglottone-emitting callus versus the remainder of the labellum showed strong coordinated induction of entire FA biosynthesis and β-oxidation pathways including genes encoding Ketoacyl-ACP Synthase, Acyl-CoA Oxidase, and Multifunctional Protein. Phylogenetic analysis revealed potential gene duplicates with tissue-specific differential regulation including two Acyl-ACP Thioesterase B and a Ketoacyl-ACP Synthase genes. UV-B treatment induced the activation of UVR8-mediated signaling and large-scale transcriptome changes in both tissues, however, neither FA biosynthesis/β-oxidation nor other lipid metabolic pathways showed clear indications of concerted DE. Gene co-expression network analysis identified three callus-specific modules enriched with various lipid metabolism categories. These networks also highlight promising candidates involved in the cyclization of chiloglottone 1 intermediates (e.g., Bet v I and dimeric α,β barrel proteins) and orchestrating regulation of precursor pathways (e.g., AP2/ERF) given a strong co-regulation with FA biosynthesis/β-oxidation genes. Possible alternative biosynthetic routes for precursors (e.g., aldehyde dehydrogenases) were also indicated. Our comprehensive study constitutes the first step toward understanding the biosynthetic pathways involved in chiloglottone 1 production in Chiloglottis trapeziformis - supporting the roles of FA metabolism in planta, gene duplication as a potential source of new genes, and co-regulation of novel pathway genes in a tissue-specific manner. This study also provides a new and valuable resource for future discovery and comparative studies in plant specialized metabolism of other orchids and non-model plants.