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Orchids and their pollinators in the hybrid zone. A. Pseudocopulating males of Andrena nigroaenea (Kirby) (Hymenoptera, Andrenidae) in both the "abdominal" and the "cephalic" positions on the flower labella of Ophrys lupercalis Devillers-Terschuren & Devillers; B. Pseudocopulating male of A. nigroaenea in the "abdominal" position on a flower of O. lupercalis with pollinaria on its head; C. Pseudocopulating male of Colletes cunicularius (L.) (Hymenoptera, Colletidae) in the "cephalic" position on the flower labellum of O. arachnitiformis; D. Pseudocopulating male of C. cunicularius on the flower labellum of O. lupercalis with pollinaria on its head; E. Pseudocopulating male of A. nigroaenea in "cephalic" position on the flower labellum of O. arachnitiformis; F. A detail of a flower of the natural hybrid between O. arachnitiformis and O. lupercalis at the study site in southern France. All photographs by NJ Vereecken.
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Sexually deceptive orchids of the genus Ophrys attract their pollinators, male insects, on a highly specific basis through the emission of odour blends that mimic the female sex pheromone of the targeted species. In this study, we have investigated a contact site between Ophrys arachnitiformis and O. lupercalis, two sympatric orchid species that ar...
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Context 1
... observations of pollinator behaviour during pseudo- copulations with fresh, unpollinated flowers of the orchid taxa illustrate that the pollinators of each parent taxon systematically initiated copulation attempts on the orchid labellum in the expected position (i.e., "abdominal" on O. lupercalis and "cephalic" on O. arachnitiformis). However, we have observed that the insects' copulatory activity on the flowers regularly led to changes in their position on the labellum and occasionally to the subsequent uptake of pollinaria when in the alternative position ( Figure 1). The supplementary video material [Additional file 1: Video] shows a male C. cunicularius pseudocopulating on the labellum of O. lupercalis, the other parent species, and withdrawing pollinaria on both its head and its abdomen tip during a single visit on the flowers. ...Context 2
... from our bioassays provide evidence for cross- attraction among orchid taxa towards patrolling males of C. cunicularius and A. nigroaenea (Figures 1 and 2). Spe- cifically, we found that for each pollinator, floral odour extracts of the most commonly associated Ophrys taxa (e.g. ...Context 3
... in this study, we have been able to show that pre-pollination (ethological and mechanical) isolation barriers, which are generally thought to repre- sent strong isolation mechanisms in flowering plants, especially when they act in concert (e.g. [64]), could be more permeable than previously thought in the genus Ophrys (Figure 1 and [Additional file 1: Video]). ...Context 4
... reproductive isolation is usually maintained but does not prevent opportunities for gene flow between sympatric species, at least theoretically. Besides, the attractiveness of orchids to alternative pollinators observed in O. arachnitiformis and O. lupercalis ( Figures 1 and 2) might enhance the reproductive output of these orchids at a local scale, a mechanism that should be favoured by selection since orchids in general and decep- tive ones in particular are often pollinator-limited in their reproductive success [34,42,66,67]. ...Similar publications
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Citations
... These compounds are presumably more volatile than the long-chained hydrocarbons typically used by various Ophrys species as primary attractants for their Andrena or Colletes bee pollinators [12,38,49,50]. Indeed, despite the fact that equivalent series of long-chained n-alkenes were also detected in high amounts in the cuticle solvent extracts of the labellum of O. speculum, these compounds do not constitute the behaviourally active compounds in this species [48], unlike in Ophrys species pollinated by solitary bees from the genera Andrena and Colletes [26,27,49,50,102,103]. Most of these long-chained cuticular hydrocarbons have low vapour pressure at room temperature and are expected to be effective only upon contact or at close range, like some contact sex pheromones in insects [38,104]. ...
Pollination by sexual deception specifically attracts male insects, through the floral scent and particular morphological features of the flower that serve as visual and tactile stimuli. The unique bond between the Ophrys speculum orchid and the male Dasyscolia ciliata wasp primarily stems from a few distinctive semiochemicals that mimic the female wasp’s sex pheromone, although the floral scent comprises a variety of compounds. An osmophore producing highly volatile compounds has been documented in four close relatives of O. speculum and is now being also investigated in this species. Given the existing debates regarding the structure of the labellum and stigmatic cavity in O. speculum, this study details their micromorphology. Additionally, comparisons of O. speculum flowers and female D. ciliata wasps under stereomicroscopy and scanning electron microscopy are conducted to seek new evidence of visual and tactile mimicry. The findings confirm that (i) an osmophore is present at the apical margin of the labellum in O. speculum flowers; (ii) the labellum features a distinct basal field homologous to those found in other Ophrys species; and (iii) the basal labellum region closely mimics the female wasp’s thorax and wings. The implications of these novel floral features are discussed within an evolutionary context.
... The latter is possible because the hybrids have a variety of novel trait combinations through chromosome assortment and recombination, as well as some transgressive traits not seen in either of the parental species (Rieseberg et al., 1999). These various new traits and new trait combinations could be explored by other pollinators in the community (Vereecken et al., 2010). For the hybrids, being pollinated by a new pollinator could be advantageous, as the hybrids would avoid direct competition for pollination service with their progenitors. ...
Hybridization is common in flowering plants and is believed to be an important force driving adaptation and speciation. The flowers of hybrids often exhibit new trait combinations, which, theoretically, could attract new species of pollinators.
In this study, we found that the hybrids between a hummingbird‐pollinated species Mimulus cardinalis and a self‐pollinated species Mimulus parishii attract bumblebees (Bombus impatiens), a pollinator not attracted to either of the progenitor species.
This novel attraction is explained by new combinations of floral traits in hybrids, including, most importantly, petal color, in addition to nectar concentration and corolla size. To understand how petal color variation is perceived by bumblebees, we performed reflectance spectroscopy and multispectral imaging to model the flower appearance in bee vision. This analysis showed that color variation would impact the ease of detection. We also found that YUP, the genetic locus responsible for a large portion of floral color variation and previously shown to be important in bee interactions with other Mimulus species, also played an important role in this novel attraction.
These results together suggest that the attraction of new pollinators to hybrid plants could be an underexplored avenue for pollinator shift and speciation.
... Studies focusing on changes in scent related to hybridization are even scarcer (Rubini Pisano et al., 2019). However, these have revealed that scent in hybrids may present three different patterns relating to the parental types (Rezende et al., 2020;Rubini Pisano et al., 2019): (i) intermediate chemical profile (Campbell et al., 2016;Cortis et al., 2009;Zito et al., 2018), (ii) absence of compounds present in parental types (Bischoff et al., 2014) and (iii) a chemical profile with new, transgressive scent compounds in relation to the parentals (Chartier et al., 2016;Marques et al., 2016;Rubini Pisano et al., 2019;Vereecken et al., 2010). Likewise, characters regarding floral resources may also be affected by hybridization. ...
Hybrid systems represent ‘new ecological opportunities’, as the changes in their vegetative and reproductive traits may facilitate colonization of new niches. The Cactaceae species Xiquexique gounellei and Xiquexique tuberculatus present different habitat preferences in the Brazilian Caatinga, however, across their distributions, some populations occur sympatrically and some individuals showed vegetative characteristics intermediate between these two species, suggesting a hybrid zone. These individuals also clearly did not belong to either of the two species, leading us to suppose that they could be hybrids, named as X. × heptagonus. Taking into account this assumption, we used a series of protocols to compare the floral attributes and signals, and floral biology displayed by the putative hybrid with those of its parents. The results showed that the flowers of the hybrid are morphologically intermediate to those of their parents. The colour of the external elements of the perianth is transgressive, and the white colour of the internal perianth-segments is shared between the three taxa. Scent analyses showed that X. × heptagonus has a scent profile that is intermediate to those of its parents, with only a few compounds indicating a transgressive phenotype. Both taxa of Xiquexique received visits from nectarivorous bats (Glossophaginae and Lonchophyllinae) and from the hawkmoths Agrius cingulata and Erinnyis ello. Our results reinforce the existence of this hybrid in the genus Xiquexique being derived from the possible parent species present. We also revealed how the floral morphology and the visual and olfactory cues of X. × heptagonus were shaped by the hybridization.
... The qualitative and quantitative patterns of VOC expression in hybrids are heterogeneous (López-Caamal 2014). In some species, hybridization could lead to the production of new secondary metabolites that are not present in parental species, due to the obstruction of biosynthetic pathways (Vereecken et al. 2010;Kong et al. 2012). In other hybrid species, highly variable proportions of several compounds are present. ...
The chemistry of plants represents a taxonomic and phylogenetic value. Researchers have recently used volatile organic compounds (VOCs) for taxonomic studies. The present work analysed and determined, for the first time, the usefulness of floral volatile compounds in the taxonomy of two species of Rhamnus sect. Alaternus, as well as the hybrid between these taxa. The two species show significant quantitative and qualitative differences. The terpenes linalool, ocimene, caryophyllene, and green volatiles are exclusive to Rh. alaternus , while farnesene (terpene), methyl salicylate and methyl benzoate (benzoids) are obtained from Rh. ludovici-salvatoris . Both volatilomes were attractive to Hymenoptera pollinators; therefore, these pollinators could serve as the main hybridisation vector. In addition, Rh. alaternus shows greater chemical and genetic heterogeneity than Rh. ludovici-salvatoris . Hybrids between the two species, Rh. × bermejoi, are closer in chemical similarity to Rh. alaternus than Rh. ludovici-salvatoris .
... A previous study suggested that various bacterial taxa from a particular phylotype share similar phenotypic traits or life-history strategies, whereby they could adapt to a specific environment (Delgado-Baquerizo et al. 2018 ). Ho w e v er, extensiv e e vidence on the r oles of morphological tr aits pr efers to focus on the macr obiota (Donohue 1999, Ver eec ken et al. 2010, Chartier et al. 2021, lar gel y due to the lack of conservative and easy-to-observe morphological features of microorganisms. It restricts the efforts to disentangle biogeogr a phic patterns and mechanisms of community assembly to pr edict the r esponse of soil micr obiota to climate c hange (Wang et al. 2022 ). ...
The patterns of biogeographic distribution and assembly processes of microbiota are of vital importance for understanding ecological adaptation and functioning maintenance. However, the role of morphological characteristics in microbial assembly is still poorly ascertained. Here, by integrating high-throughput sequencing and robust extrapolation of traits, we investigated taxonomic and phylogenetic turnovers of various cyanobacterial morphotypes in biocrusts to evaluate the contributions of deterministic and stochastic processes across a large scale of drylands in northwestern China. The results showed that the non-heterocystous filamentous category dominated biocrusts in the arid ecosystem and exhibited strong tolerance against environmental fluctuations. Despite the significant distance-decay relationship of β-diversity detected in all categories, both species composition and phylogenetic turnover rates of coccoid cyanobacteria were higher than non-heterocystous filamentous and heterocystous morphotypes. Moreover, the assembly of cyanobacteria was driven by different ecological processes that the entire community and non-heterocystous filamentous morphotype were governed by deterministic processes, while stochasticity prevailed in heterocystous and coccoid cyanobacteria. Nonetheless, aridity can modulate the balance between determinism and stochasticity and prompt a shifting threshold among morphotypes. Our findings provide a unique perspective to understanding the critical role of microbial morphology in community assembly and facilitate the prediction of biodiversity loss under climate change.
... Vereecken et al. [127] studied populations in southern France where O. lupercalis forms hybrid swarms with O. arachnitiformis (synonymised by some authors with O. exaltata)a microspecies that belongs not only to a different mesospecies but also to a different macrospecies, Sphegodes (Figures 1 and 18). Since all authors agree that the two parents represent different bona fide species, it is not surprising that their pseudo-pheromone cocktails are distinct and supposedly attract two different genera of pollinating bees. ...
... Moreover, the authors also described anarchic pollinators that varied in both the position on the labellum in which they attempted to mate with the flowers and the position(s) on the insect where the pollinaria consequently became attached. Given this valuable evidence, we view the author's opinion that Ophrys' "reproductive barriers are more permeable than [previously] thought" ( [127], p. 5) as seriously understated. ...
... Supposed morphological distinctions and pollinator preferences are tested weakly if at all. Only in the case of the hybrid swarms between O. lupercalis and O. arachnitiforms was hybrid sterility observed, and this resulted from an apparently rare case of not pre-zygotic but rather post-zygotic sterility, due to this particular population of O. lupercalis being tetraploid and thus incompatible with the more typically diploid O. arachnitiformis [127]. ...
Simple Summary: Our frequently deployed approach to optimally circumscribing species requires large-scale field sampling within and between populations for large numbers of morphometric characters, followed by multivariate ordinations to objectively seek discontinuities (or, failing that, zones of limited overlap) among sets of populations considered to represent species. Corresponding boundaries are sought in DNA-based outputs, either phylogenies or preferably ordinations based on population genetic data. Herein, we analyse within a molecular phylogenetic framework detailed morphometric data for the charismatic bee orchids (Ophrys), seeking a 'mesospecies' species concept that might provide a compromise between the nine 'macrospecies' recognised primarily through DNA barcoding and the several hundred 'microspecies' recognised primarily through perceived pollinator specificity. Our analyses failed to find robust groupings that could be regarded as credible mesospecies, instead implying that each macrospecies constitutes a morphological continuum. This problematic result encouraged us to reappraise both our morphometric approach and the relative merits of the contrasting macrospecies and microspecies concepts, and to reiterate the key role played by genetics in species circumscription. Abstract: Despite (or perhaps because of) intensive multidisciplinary research, opinions on the optimal number of species recognised within the Eurasian orchid genus Ophrys range from nine to at least 400. The lower figure of nine macrospecies is based primarily on seeking small but reliable discontinuities in DNA 'barcode' regions, an approach subsequently reinforced and finessed via high-throughput sequencing studies. The upper figure of ca. 400 microspecies reflects the morphological authoritarianism of traditional taxonomy combined with belief in extreme pollinator specificity caused by reliance on pollination through pseudo-copulation, enacted by bees and wasps. Groupings of microspecies that are less inclusive than macrospecies are termed mesospecies. Herein, we present multivariate morphometric analyses based on 51 characters scored for 457 individual plants that together span the full morphological and molecular diversity within the genus Ophrys, encompassing 113 named microspecies that collectively represent all 29 mesospecies and all nine macrospecies. We critique our preferred morphometric approach of accumulating heterogeneous data and analysing them primarily using principal coordinates, noting that our conclusions would have been strengthened by even greater sampling and the inclusion of data describing pseudo-pheromone cocktails. Morphological variation within Ophrys proved to be exceptionally multidimensional, lacking strong directional trends. Multivariate clustering of plants according to prior taxonomy was typically weak, irrespective of whether it was assessed at the level of macrospecies, mesospecies or microspecies; considerable morphological overlap was evident even between subsets of the molecularly differentiable macrospecies. Characters supporting genuine taxonomic distinctions were often sufficiently subtle that they were masked by greater and more positively correlated variation that reflected strong contrasts in flower size, tepal colour or, less often, plant size. Individual macrospecies appear to represent morphological continua, within which taxonomic divisions are likely to prove arbitrary if based exclusively on morphological criteria and adequately sampled across their geographic range. It remains unclear how much of the mosaic of subtle character variation among the microspecies reflects genetic versus epigenetic or non-genetic influences and what proportion of any contrasts observed in gene frequencies can be attributed to the adaptive microevolution that is widely considered to dictate speciation in the genus. Moreover, supplementing Biology 2023, 12, 136. https://doi.org/10.3390/biology12010136 https://www.mdpi.com/journal/biology Biology 2023, 12, 136 2 of 52 weak morphological criteria with extrinsic criteria, typically by imposing constraints on geographic location and/or supposed pollinator preference, assumes rather than demonstrates the presence of even the weakest of species boundaries. Overall, it is clear that entities in Ophrys below the level of macrospecies have insufficiently structured variation, either phenotypic or genotypic, to be resolved into discrete, self-circumscribing ("natural") entities that can legitimately be equated with species as delimited within other less specialised plant genera. Our search for a non-arbitrary (meso)species concept competent to circumscribe an intermediate number of species has so far proven unsuccessful.
... This implies that S. arvensis is able to emit a stable scent bouquet to "pretend" that a floral reward is present potentially to maintain pollinator attraction. However, in other plant species the scent emission increases and composition of scent compounds change under water stress (Burkle & Runyon, 2016;Campbell et al., 2019;Glenny et al., 2018;Rering et al., 2020), leading to possible recognition mismatches between plant and pollinators, especially in highly specialized pollinator attractive systems (Vereecken et al., 2010). If pollinators are no longer able to find their host plants, this would lower visitation rate and pollination success and reduces the reproductive success of the plant. ...
Water deficit can alter floral traits with cascading effects on flower‐visitor interactions and plant fitness. Water stress induction can diminish productivity, directly resulting in lower flower production and consequently seed set. Changes in floral traits, such as floral scent or reward amount, may in turn alter pollinator visitations and behaviour and consequently can reduce pollination services resulting in lower reproduction output. However, the relative contribution of this indirect in comparison to the direct effects to changes in seed set are not fully understood.
We manipulated water availability using rain‐out shelters in a field experiment and measured effects on floral scent bouquet, morphology, phenology, flower‐visitor interactions, pollination and seed set. Plant individuals of Sinapis arvensis (Brassicaceae) were randomly assigned to one of three treatments: mean precipitation (=control), reduced mean precipitation or drought period treatment.
Our results show that decreasing water availability lowers the number of flowers and seed set. This indicates a direct link between water stress and seed set, as seed mass increases with increasing flower number. The indirect link of water stress via floral traits, pollinator visits and pollination has weaker effects on seed set. However, floral traits remain relatively stable under decreased water availability, whereas plant growth and flower abundance decrease, potentially in order to allow investment in more resources in fewer flowers to maintain pollination success. Thus, plants are able to compensate for water stress and can maintain floral trait expression, such as a stable scent emission and bouquet, to retain pollinator attraction.
These findings indicate that the direct link from water stress to seed set has a stronger impact on plants reproductive success than the indirect link through altered floral trait expression and pollinator visits in a generalist plant species.
Read the free Plain Language Summary for this article on the Journal blog.
... -Hypothèse 2 : Les individus hybrides devraient pouvoir être identifiés car ils présenteraient des valeurs intermédiaires au niveau de certains traits. Cependant, il a été prouvé que des hybrides entre Ophrys arachnitiformis et O. lupercalis pouvaient aussi émettre des composés olfactifs inédits, en tout cas non émis par les populations parentales (Vereecken et al., 2010). Conformément au modèle de zone de tension, on peut aussi supposer que la fitness des hybrides (à évaluer) sera inférieure à celle des individus des taxons parentaux. ...
La compréhension de l’évolution des populations et des espèces passe par l’étude des liens entre les génotypes, les phénotypes qu’ils déterminent et la fitness que ces derniers confèrent à un individu donné. Historiquement, l’écologie et l’évolution se sont principalement attelées à décrypter les liens entre variation phénotypique et fitness, souvent en considérant les bases génétiques de la variation phénotypique comme une « boîte noire » dont l’accès était hors d’atteinte. Au mieux, le génotype était considéré comme un marqueur pour expliquer les patrons de distribution géographique de la variation phénotypique et éventuellement pour retracer l’histoire des populations et des espèces. La biologie fonctionnelle s’est quant à elle plutôt focalisée sur l’étude des mécanismes par lesquels le génotype façonnait le phénotype. Or faire le lien entre phénotype et fitness dans un contexte réaliste peut nécessiter une étude de la performance de ces phénotypes (et des génotypes qui les déterminent) en populations naturelles. L’avènement des approches dites « -omiques » a, en partie, permis de lever les verrous technologiques qui ont longtemps freiné la mise en place d’une recherche résolument intégrative. Or, en dépit de cette révolution dans le domaine des sciences du vivant, trouver des modèles biologiques pertinents pour mettre en place ce type de recherche demeure un défi majeur. Dans certains cas, un modèle peut paraître tout à fait approprié pour travailler en populations naturelles mais ses caractéristiques intrinsèques limitent la possibilité d’accéder à l’intégralité de l’information génomique et/ou de son utilisation en conditions contrôlées. Dans d’autres cas, le modèle a tout du candidat idéal en conditions expérimentales mais présente des limites concernant la validation de la pertinence des phénotypes en populations naturelles. Le modèle biologique parfait n’existant tout simplement pas, je propose dans ce manuscrit à la fois un retour d’expérience personnel et une feuille de route à propos de pistes possibles pour entreprendre et mener une recherche intégrative et potentiellement fructueuse pour inférer ces liens entre génotypes, phénotypes et fitness et mieux appréhender les processus qui sous-tendent l’émergence et le maintien de la diversité biologique.
... In nature, both discrete and continuous traits are known to affect rates of hybridization, and thus SiPhyNetwork allows either type of phenotypic trait to affect the hybridization potential of different lineages. Likewise, in some systems, traits that are more similar may enhance the likelihood of hybridization (Dincȃ et al., 2013;Pereira et al., 2014), while in others, opposite trait values create novelty for hybrids to succeed (Vereecken et al., 2010). SiPhyNetwork permits the user to define how trait values interact to determine whether hybridization occurs. ...
Gene flow is increasingly recognized as an important macroevolutionary process. The many mechanisms that contribute to gene flow ( e . g ., introgression, hybridization, lateral gene transfer) uniquely affect the diversification of dynamics of species, making it important to be able to account for these idiosyncrasies when constructing phylogenetic models. Existing phylogenetic-network simulators for macroevolution are limited in the ways they model gene flow.
We present SiPhyNetwork, an R package for simulating phylogenetic networks under a birth-death-hybridization process.
Our package unifies the existing birth-death-hybridization models while also extending the toolkit for modeling gene flow. This tool can create patterns of reticulation such as hybridization, lateral gene transfer, and introgression.
Specifically, we model different reticulate events by allowing events to either add, remove, or keep constant the number of lineages. Additionally, we allow reticulation events to be trait-dependent, creating the ability to model the expanse of isolating mechanisms that prevent gene flow. This tool makes it possible for researchers to model many of the complex biological factors associated with gene flow in a phylogenetic context.
... Floral scent is one of the most important signals to attract pollinators, especially for some sexually and food deceptive orchids [150,151]. methylglutaryl-CoA synthase (HMGS) were found to be responsible for floral scent of C. goeringii [103,153]. In C. faberi, jasmonic acid carboxyl methyltransferase (JMT), an important gene in MeJA biosynthetic pathways was highly upregulated in blooming flowers [154]. ...
Orchidaceae is one of the largest, most diverse families in angiosperms with significant ecological and economical values. Orchids have long fascinated scientists by their complex life histories, exquisite floral morphology and pollination syndromes that exhibit exclusive specializations than any other plants on earth. These intrinsic factors together with human influences also make it a keystone group in biodiversity conservation. The advent of sequencing technologies and transgenic techniques represents a quantum leap in orchid research, enabling molecular approaches to be employed to resolve the historically interesting puzzles in orchid basic and applied biology. To date, 15 different orchid genomes covering four subfamilies (Apostasioideae, Vanilloideae, Epidendroideae and Orchidoideae) have been released. These genome projects have given rise to massive data that greatly empowers the studies pertaining to key innovations and evolutionary mechanisms for the breadth of orchid species. The extensive exploration of transcriptomics, comparative genomics, and recent advances in gene engineering have linked important traits of orchids with a multiplicity of gene families and their regulating networks, providing great potential for genetic enhancement and improvement. In this review, we summarize the progress and achievement in fundamental research and industrialized application of orchids with a particular focus on molecular tools, and make future prospects of orchid molecular breeding and post-genomic research, providing a comprehensive assemblage of start-of-art knowledge in orchid research and industrialization.
