Limits...
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

Flowers of an inflorescence of Platanthera hyperborea from Thingvellir.(A) Recently opened flowers showing that the pollen masses have already collapsed onto the stigma. (B) Flower at a later stage of anthesis with a mosquito glued to its stigma. Scale bar = 5 mm (A), 2.5 mm (B). Images: R Bateman.
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fig-3: Flowers of an inflorescence of Platanthera hyperborea from Thingvellir.(A) Recently opened flowers showing that the pollen masses have already collapsed onto the stigma. (B) Flower at a later stage of anthesis with a mosquito glued to its stigma. Scale bar = 5 mm (A), 2.5 mm (B). Images: R Bateman.

Mentions: RB and PR conducted a week-long field trip in the southwest quadrant of Iceland during the period 3rd–9th July 2014, ranging for approximately 140 km to the east and northeast of Reykjavik (Fig. 1). Our visit was a little later than ideal, flowering of the orchid having peaked an estimated ten days earlier (Table 1). Many populations of P. hyperborea were encountered. The six populations subjected to detailed study were chosen to represent wide ranges of geographic locations, habitat types and population sizes (Fig. 1, Table 1); they included the presumed locus classicus of the species at Thingvellir. Ten plants in each population were selected for detailed measurement where feasible (only six plants were found in measurable condition at Solheimajokull). One or two plants per population were also sampled for DNA analysis (a further DNA sample was collected at Geysir, near the study population at Stong), and at both the Selfoss and Thingvellir populations, multiple inflorescences were removed for microscopic study. In addition, representative individuals from several populations were imaged in situ (Figs. 2 and 3).


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)

Flowers of an inflorescence of Platanthera hyperborea from Thingvellir.(A) Recently opened flowers showing that the pollen masses have already collapsed onto the stigma. (B) Flower at a later stage of anthesis with a mosquito glued to its stigma. Scale bar = 5 mm (A), 2.5 mm (B). Images: R Bateman.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig-3: Flowers of an inflorescence of Platanthera hyperborea from Thingvellir.(A) Recently opened flowers showing that the pollen masses have already collapsed onto the stigma. (B) Flower at a later stage of anthesis with a mosquito glued to its stigma. Scale bar = 5 mm (A), 2.5 mm (B). Images: R Bateman.
Mentions: RB and PR conducted a week-long field trip in the southwest quadrant of Iceland during the period 3rd–9th July 2014, ranging for approximately 140 km to the east and northeast of Reykjavik (Fig. 1). Our visit was a little later than ideal, flowering of the orchid having peaked an estimated ten days earlier (Table 1). Many populations of P. hyperborea were encountered. The six populations subjected to detailed study were chosen to represent wide ranges of geographic locations, habitat types and population sizes (Fig. 1, Table 1); they included the presumed locus classicus of the species at Thingvellir. Ten plants in each population were selected for detailed measurement where feasible (only six plants were found in measurable condition at Solheimajokull). One or two plants per population were also sampled for DNA analysis (a further DNA sample was collected at Geysir, near the study population at Stong), and at both the Selfoss and Thingvellir populations, multiple inflorescences were removed for microscopic study. In addition, representative individuals from several populations were imaged in situ (Figs. 2 and 3).

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