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Floral miniaturisation and autogamy in boreal-arctic plants are epitomised by Iceland’s most frequent orchid, Platanthera hyperborea
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 freq...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
PeerJ Inc.
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4400879/ https://www.ncbi.nlm.nih.gov/pubmed/25893148 http://dx.doi.org/10.7717/peerj.894 |
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author | Bateman, Richard M. Sramkó, Gábor Rudall, Paula J. |
author_facet | Bateman, Richard M. Sramkó, Gábor Rudall, Paula J. |
author_sort | Bateman, Richard M. |
collection | PubMed |
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. |
format | Online Article Text |
id | pubmed-4400879 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | PeerJ Inc. |
record_format | MEDLINE/PubMed |
spelling | pubmed-44008792015-04-17 Floral miniaturisation and autogamy in boreal-arctic plants are epitomised by Iceland’s most frequent orchid, Platanthera hyperborea Bateman, Richard M. Sramkó, Gábor Rudall, Paula J. PeerJ Biodiversity 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. PeerJ Inc. 2015-04-14 /pmc/articles/PMC4400879/ /pubmed/25893148 http://dx.doi.org/10.7717/peerj.894 Text en © 2015 Bateman et al. http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited. |
spellingShingle | Biodiversity Bateman, Richard M. Sramkó, Gábor Rudall, Paula J. Floral miniaturisation and autogamy in boreal-arctic plants are epitomised by Iceland’s most frequent orchid, Platanthera hyperborea |
title | Floral miniaturisation and autogamy in boreal-arctic plants are epitomised by Iceland’s most frequent orchid, Platanthera hyperborea |
title_full | Floral miniaturisation and autogamy in boreal-arctic plants are epitomised by Iceland’s most frequent orchid, Platanthera hyperborea |
title_fullStr | Floral miniaturisation and autogamy in boreal-arctic plants are epitomised by Iceland’s most frequent orchid, Platanthera hyperborea |
title_full_unstemmed | Floral miniaturisation and autogamy in boreal-arctic plants are epitomised by Iceland’s most frequent orchid, Platanthera hyperborea |
title_short | Floral miniaturisation and autogamy in boreal-arctic plants are epitomised by Iceland’s most frequent orchid, Platanthera hyperborea |
title_sort | floral miniaturisation and autogamy in boreal-arctic plants are epitomised by iceland’s most frequent orchid, platanthera hyperborea |
topic | Biodiversity |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4400879/ https://www.ncbi.nlm.nih.gov/pubmed/25893148 http://dx.doi.org/10.7717/peerj.894 |
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