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

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.

In situmorphometric survey elucidates the evolutionary systematics of the EurasianHimantoglossumclade (Orchidaceae: Orchidinae)

“…We are not aware of any reports of pseudocopulatory behaviour shown by insects visiting Himantoglossum , and fruit-set figures rarely exceed the 80% threshold that constitutes the lower limit typical of autogamous orchids (e.g., Bateman, Sramkó & Rudall, 2015). In fact, fruit-set averages 34.3 ± 20.9% in H. hircinum , 28.7 ± 16.1% in the closely related H. adriaticum , and 39.6 ± 16.8% in the earlier flowering H. robertianum (figures derived by us from 21 individual studies summarised in Appendix 2 of Claessens & Kleynen, 2011).…”

Severe outbreeding and inbreeding depression maintain mating system differentiation inEpipactis(Orchidaceae)

“…Five species of the genus Epipactis showing pronounced differences in mating system were selected for the experiments: two putatively autogamous species ( E. muelleri and E. neglecta ) and three putatively allogamous species ( E. atrorubens , E. helleborine and E. palustris ) (Van der Cingel, ; Claessens & Kleynen, ; Jacquemyn & Brys, ). The three allogamous species belong to different phylogenetic clades within the genus Epipactis (Hollingsworth et al ., ; Tranchida‐Lombardo et al ., ; Bateman et al ., ), and the two autogamous species also show significant genetic differentiation and are expected to have independent origins (Squirrell et al ., ; Hollingsworth et al ., ; Tranchida‐Lombardo et al ., ; Bateman et al ., ). The autogamous E. muelleri and E. neglecta mostly grow in closed and dark deciduous forest sites (Delforge, ), whereas the allogamous species generally prefer somewhat more open habitats.…”

“…This wide variation has largely been attributed to specific adaptations to pollinators, most likely to increase cross‐pollination and to avoid the deleterious effects of selfing (Darwin, ; Tremblay et al ., ). Nonetheless, facultative and obligate autonomous self‐pollination has been repeatedly observed within the orchid family (Hagerup, ; Catling, , ; Van der Cingel, , ; Duffy et al ., ; Bateman et al ., ). These observations agree to some extent with the general theory for mating system evolution, which predicts that species will evolve to either complete selfing or complete outcrossing, depending on the balance between automatic selection favouring self‐fertilization and costs resulting from inbreeding depression (ID) (Lande & Schemske, ; Charlesworth & Charlesworth, ; Goodwillie et al ., ).…”

“…Although most species in this genus are nectar rewarding (Claessens & Kleynen, 2011), there are notable differences in mating system, with a large number of allogamous species relying on pollinators for successful fruit and seed set and a series of species that are predominantly autogamous and are no longer dependent on pollinators for fruit set (Van der Cingel, 1995;Claessens & Kleynen, 2011). Morphological (Richards, 1982) and molecular studies (Squirrell et al, 2002;Hollingsworth et al, 2006;Bateman et al, 2015) have shown that autogamy has iterative, but recent origins from allogamous ancestor populations or species in Epipactis. The shift towards selfing is frequently associated with small distribution areas, low plant densities and limited pollinator availability, all of which may have created gamete limitation and therefore enhanced rapid evolution towards selfing (Van der Cingel, 1995;Squirrell et al, 2002;Tranchida-Lombardo et al, 2011).…”

An integrative anatomical, morphological, micromorphological and molecular approach to Turkish epidendroid and orchidoid species (Orchidaceae)

“…and Platanthera Rich. (Bateman et al 2015(Bateman et al , 2017. However, studies on the histological, anatomical and micromorphological structures of temperate orchids are rare.…”