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Iterative allogamy-autogamy transitions drive actual and incipient speciation during the ongoing evolutionary radiation within the orchid genus Epipactis (Orchidaceae).

ABSTRACT: BACKGROUND AND AIMS:The terrestrial orchid genus Epipactis has become a model system for the study of speciation via transitions from allogamy to autogamy, but close phylogenetic relationships have proven difficult to resolve through Sanger sequencing. METHODS:We analysed with restriction site-associated sequencing (RAD-seq) 108 plants representing 29 named taxa that together span the genus, focusing on section Epipactis. Our filtered matrix of 12 543 single nucleotide polymorphisms was used to generate an unrooted network and a rooted, well-supported likelihood tree. We further inferred genetic structure through a co-ancestry heat map and admixture analysis, and estimated inbreeding coefficients per sample. KEY RESULTS:The 27 named taxa of the ingroup were resolved as 11 genuine, geographically widespread species: four dominantly allogamous and seven dominantly autogamous. A single comparatively allogamous species, E. helleborine, is the direct ancestor of most of the remaining species, though one of the derived autogams has generated one further autogamous species. An assessment of shared ancestry suggested only sporadic hybridization between the re-circumscribed species. Taxa with the greatest inclination towards autogamy show less, if any, admixture, whereas the gene pools of more allogamous species contain a mixture alleles found in the autogams. CONCLUSIONS:This clade is presently undergoing an evolutionary radiation driven by a wide spectrum of genotypic, phenotypic and environmental factors. Epipactis helleborine has also frequently generated many local variants showing inclinations toward autogamy (and occasionally cleistogamy), best viewed as incipient speciation from within the genetic background provided by E. helleborine, which thus becomes an example of a convincingly paraphyletic species. Autogams are often as widespread and ecologically successful as allogams.

SUBMITTER: Sramko G

PROVIDER: S-EPMC6798847 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Iterative allogamy-autogamy transitions drive actual and incipient speciation during the ongoing evolutionary radiation within the orchid genus Epipactis (Orchidaceae).

Sramkó Gábor G Paun Ovidiu O Brandrud Marie K MK Laczkó Levente L Molnár Attila A Bateman Richard M RM

Annals of botany 20191001 3

<h4>Background and aims</h4>The terrestrial orchid genus Epipactis has become a model system for the study of speciation via transitions from allogamy to autogamy, but close phylogenetic relationships have proven difficult to resolve through Sanger sequencing.<h4>Methods</h4>We analysed with restriction site-associated sequencing (RAD-seq) 108 plants representing 29 named taxa that together span the genus, focusing on section Epipactis. Our filtered matrix of 12 543 single nucleotide polymorphis ...[more]

PMID: 31231754

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Project description:Background and aimsThe geographical distribution of plant species is linked fundamentally not only to environmental variables, but also to key traits that affect the dispersal, establishment and evolutionary potential of a species. One of the key plant traits that can be expected to affect standing genetic variation, speed of adaptation and the capacity to colonize and establish in new habitats, and therefore niche breadth and range size, is the plant mating system. However, the precise role of the mating system in shaping range size and niche breadth of plant species remains unclear, and different studies have provided contrasting results. In this study, we tested the hypothesis that range size and niche breadth differed with mating system in the orchid genus Epipactis.MethodsWe modelled the ecological niches of 14 Epipactis species in Europe using occurrence records and environmental satellite data in Maxent. Niche breadth and niche overlap in both geographic and environmental space were calculated from the resulting habitat suitability maps using ENMTools, and geographic range was estimated using α-hull range definition. Habitat suitability, environmental variable contributions and niche metrics were compared among species with different mating systems.Key resultsWe did not detect significant differences in niche breadth, occurrence probability or geographical range between autogamous and allogamous Epipactis species, although autogamous species demonstrated notably low variation in niche parameters. We also found no significant differences in niche overlap between species with the same mating system or different mating systems. For all Epipactis species, occurrence was strongly associated with land cover, particularly broad-leafed and coniferous forests, and with limestone bedrock.ConclusionsThese results suggest that the mating system does not necessarily contribute to niche breadth and differentiation, and that other factors (e.g. mycorrhizal specificity) may be more important drivers of range size and niche breadth in Epipactis and orchids in general.

Project description:Background and Aims. This paper concludes our series of publications comparing island and mainland speciation in European butterfly-orchids, by studying the morphology, phylogenetics and reproductive biology of the controversial circum-arctic species Platanthera (Limnorchis) hyperborea-the most frequent of seven Icelandic orchids. We draw particular attention to its phylogenetic placement, remarkable reproductive biology and morphological convergence on other Platanthera lineages through floral miniaturisation. Methods. Five populations of P. hyperborea in southwest Iceland were measured for 33 morphological characters and subjected to detailed multivariate and univariate analyses, supported by light and scanning electron microscopy of selected flowers. Representative samples from six populations were sequenced for nrITS and placed in a taxonomically broader phylogenetic matrix derived from previous studies. Key Results . Section Limnorchis consists of three distinct ITS-delimited clades based on P. stricta, P. sparsifolia-limosa-aquilonis and P. dilatata-hyperborea. Within the latter group, supposed species boundaries overlap; instead, the data indicate a crude stepwise series of ribotypic transitions extending eastward from North America to Iceland. Morphometric data failed to identify any taxonomically meaningful partitions among Icelandic P. hyperborea populations, despite the presence of a distinct and apparently plesiomorphic ribotype at the most glacially influenced habitat sampled. Microscopic study of the flowers revealed several distinguishing features (some not previously reported), including resupinate lateral sepals, toothed bract margins, club-shaped papillae shared by both the interior of the labellar spur and the stigmatic surface, and an exceptionally adhesive stigma that is reliably covered in disaggregated pollen masses prior to anthesis; auricles are absent. Conclusions. Ribotypes suggest that Icelandic P. hyperborea represents the terminus of a migration route that may have begun in East Asia before passing through North America and presumably Greenland. The incohesive pollinia, rapidly desiccating anther locules, weakly developed rostellum, exceptionally adhesive stigma and the close juxtaposition of compact male and female reproductive organs together conspire to cause routine autogamy and frequent cleistogamy, despite the continued production of substantial nectar reservoirs in the spur and consequent ongoing attraction to the flowers of insects, including mosquitoes. When considered in combination with independently derived lineages of Platanthera on the Azorean and Hawaiian archipelagos also bearing small green flowers, our observations show allometric and paedomorphic reductions in flower size as the primary evolutionary driver, but also indicate strong developmental and functional constraints.

Dataset Information

Iterative allogamy-autogamy transitions drive actual and incipient speciation during the ongoing evolutionary radiation within the orchid genus Epipactis (Orchidaceae).

Publications

Iterative allogamy-autogamy transitions drive actual and incipient speciation during the ongoing evolutionary radiation within the orchid genus Epipactis (Orchidaceae).

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