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Floral miniaturisation and autogamy in boreal-arctic plants are epitomised by Iceland's most frequent orchid, Platanthera hyperborea.

Bateman RM, Sramkó G, Rudall PJ - PeerJ (2015)

Bottom Line: 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.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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Royal Botanic Gardens Kew , Richmond , United Kingdom.

ABSTRACT
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.

No MeSH data available.


Related in: MedlinePlus

Bivariate plot of taxon mean values for (A) labellum length versus spur length and (B) lateral sepal width versus lateral sepal length for Platanthera hyperborea plus seven putative species and two hybrid combinations in Platanthera section Platanthera.Error bars represent sample standard deviations. The dashed line shows the regression, whereas the dotted line indicates parity in values of the two variables.
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fig-11: Bivariate plot of taxon mean values for (A) labellum length versus spur length and (B) lateral sepal width versus lateral sepal length for Platanthera hyperborea plus seven putative species and two hybrid combinations in Platanthera section Platanthera.Error bars represent sample standard deviations. The dashed line shows the regression, whereas the dotted line indicates parity in values of the two variables.

Mentions: Mean values and standard deviations for metric characters of particular interest in all eight measured taxa were plotted together in pairwise combinations to yield scatter-diagrams that were subsequently subjected to regression. Ideally, type II regression would have been used. However, when R2 values are high (as here), reciprocal type I regressions (switching dependent and independent variables) reliably yields near-identical results. Examples of bivariate plots presented here are labellum length versus spur length (Fig. 11A), length versus width of lateral sepals (Fig. 11B), overall width versus length of gynostemium (Fig. 12A), and separation of the proximal ends of the pollinaria (i.e., the viscidia) versus separation of their distal apices (Fig. 12B). Each of these four plots provides substantial discrimination between most of the eight putative species of Platanthera. Although coefficients of variation are comparatively high (15–25%) for these eight metric parameters in most taxa, they are noticeably lower (<12%) for P. azorica and P. hyperborea. This difference can readily be explained for P. azorica, which effectively constitutes a single metapopulation (and thus represents a single gene pool occupying a comparatively narrow environmental spectrum), but it less clear why metric floral characters would be less variable in P. hyperborea.


Floral miniaturisation and autogamy in boreal-arctic plants are epitomised by Iceland's most frequent orchid, Platanthera hyperborea.

Bateman RM, Sramkó G, Rudall PJ - PeerJ (2015)

Bivariate plot of taxon mean values for (A) labellum length versus spur length and (B) lateral sepal width versus lateral sepal length for Platanthera hyperborea plus seven putative species and two hybrid combinations in Platanthera section Platanthera.Error bars represent sample standard deviations. The dashed line shows the regression, whereas the dotted line indicates parity in values of the two variables.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4400879&req=5

fig-11: Bivariate plot of taxon mean values for (A) labellum length versus spur length and (B) lateral sepal width versus lateral sepal length for Platanthera hyperborea plus seven putative species and two hybrid combinations in Platanthera section Platanthera.Error bars represent sample standard deviations. The dashed line shows the regression, whereas the dotted line indicates parity in values of the two variables.
Mentions: Mean values and standard deviations for metric characters of particular interest in all eight measured taxa were plotted together in pairwise combinations to yield scatter-diagrams that were subsequently subjected to regression. Ideally, type II regression would have been used. However, when R2 values are high (as here), reciprocal type I regressions (switching dependent and independent variables) reliably yields near-identical results. Examples of bivariate plots presented here are labellum length versus spur length (Fig. 11A), length versus width of lateral sepals (Fig. 11B), overall width versus length of gynostemium (Fig. 12A), and separation of the proximal ends of the pollinaria (i.e., the viscidia) versus separation of their distal apices (Fig. 12B). Each of these four plots provides substantial discrimination between most of the eight putative species of Platanthera. Although coefficients of variation are comparatively high (15–25%) for these eight metric parameters in most taxa, they are noticeably lower (<12%) for P. azorica and P. hyperborea. This difference can readily be explained for P. azorica, which effectively constitutes a single metapopulation (and thus represents a single gene pool occupying a comparatively narrow environmental spectrum), but it less clear why metric floral characters would be less variable in P. hyperborea.

Bottom Line: 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.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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Royal Botanic Gardens Kew , Richmond , United Kingdom.

ABSTRACT
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.

No MeSH data available.


Related in: MedlinePlus