Speciation via floral heterochrony and presumed mycorrhizal host switching of endemic butterfly orchids on the Azorean archipelago

Bateman, Richard M.; Rudall, Paula J.; Bidartondo, Martin I.; Cozzolino, Salvatore; Tranchida-Lombardo, Valentina; Carine, Mark A.; Moura, Mónica

doi:10.3732/ajb.1300430

Cited by 25 publications

(70 citation statements)

References 75 publications

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“…388 Population clustering showed a consistent pattern indicating two independent genetic clusters: P. bifolia 498 Bateman et al 2014), in a previous study (Esposito et al 2016), we showed that in our studied sympatric 499 populations, mycorrhizal fungi were most likely not directly involved in maintaining species boundaries.…”

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Platanthera bifolia and P. chlorantha are terrestrial and rewarding orchids with a wide Eurasian distribution. Although genetically closely related, they exhibit significant morphological, phenological and ecological differences that maintain reproductive isolation between the species. However, where both species co-occur, individuals with intermediate These results are corroborated also by floral scent analyses, which confirmed a strong similarity in floral scent composition between intermediate morphotypes and P. bifolia. Therefore, this study provided a much more detailed picture of the genetic structure of a sympatric zone between two closely allied species and supports the hypothesis that intermediate morphotypes in sympatry could reflect an adaptive evolution in response to local pollinator-mediated selection. (Nilsson 1983;1985). These two closely related species exhibit not only 67 morphological differences, but also distinct ecological preferences (P. chlorantha favouring dry, 68 calcareous grasslands, while P. bifolia will be typically found in fresh to wet meadows on acidic soil). 80 Recently, a study on some Western-European Platanthera populations composed almost exclusively of 81 intermediate looking individuals, based on morphology and molecular markers, concluded that such 82 individuals were not hybrids, but constitute an independent lineage, distinct from both widespread species 83 (Durka et al. 2017). 84The level of geitonogamy was observed to be higher in P. bifolia than in P. chlorantha because 85 the latter has a pollinarium-bending mechanism that prevents deposition of the pollinia directly after 86 removal (Maad & Nilsson 2004;Maad & Reinhammar 2004). This process may also affect the probability 87 of hybrid formation (Ishizaki et al. 2013). An allopatric P. bifolia population with a high degree (i.e. 88 almost 60%) of self-pollination was found by Brzosko (2003), although self-pollination in Platanthera 89 species is considered generally rare (Nilsson 1983;Maad 2002). 90In the genus Platanthera, floral scent plays a crucial role in guiding pollinators to the flowers 91 (Nilsson 1983;1985;Tollsten & Bergström 1993). A strong fragrance is emitted after dusk, when 92 pollinators (nocturnal moths) are most active (Nilsson 1983;1985;Tollsten & Bergström 1993; Hapeman 93 & Inoue 1997;Plepys et al. 2002a;2002b). Floral fragrances of Platanthera have been classified into 94 linaloolic, lilac, geraniolic and benzenoic chemotypes depending on the main class of compounds present 95 in the blend (Tollsten & Bergström 1993;Plepys et al. 2002a;2002b (Plepys et al. 2002a;2002b). Furthermore, a change in floral scent composition has been suggested 98 by Nilsson (1983;1985) to prevent effective cross-pollination between both species (Nilsson 1978; 99 Tollsten & Bergström 1993), by acting as a reproductive barrier via ethological mechanisms. Tollsten & 100 Bergström (1993) discovered that important inter-individual and inter-population variation in floral scent 101 exists, and may act as an adapta...

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“…High levels of phenotypic distinctiveness coupled with weak molecular resolution suggestive of recent speciation, has been described for other Azorean taxa, namely the endemic Platanthera orchids (Bateman et al 2014) and has been referred to as a 'genetic divergence lag' (Bateman et al 2012). The hypothesis that L. filii resulted from a later speciation event in one of the oldest islands of the central group followed by dispersal to the remaining islands of the group and the establishment as the dominant form in those islands was suggested by Dias et al (2014) when discussing the within-archipelago population genetic structure obtained for the Azorean Leontodon.…”

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A revision of the genus Leontodon (Asteraceae) in the Azores based on morphological and molecular evidence

et al. 2015

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Two endemic species of Leontodon are currently recognized in the Azores archipelago: Leontodon filii and L. rigens. However, there has been confusion regarding the application of these names and field observations and herbarium studies suggested three morphotypes in the islands. Here, we present a taxonomic revision of the Azorean endemic Leontodon species using morphological characters and new molecular data from the ITS region and from three chloroplast regions: trnQ, trnV and matK. Fifty-one quantitative and qualitative morphological characters were examined that revealed consistent differences between specimens from the western, central and eastern subarchipelagos (where, on the latter, Leontodon is restricted to São Miguel). Molecular analysis revealed two well defined monophyletic groups, one comprising accessions from São Miguel and the second comprising accessions from the western group, while central group accessions were in an unresolved polytomy. Both analyses also indicated the occurrence of hybridization with L. saxatilis, a widespread non-endemic species. Taken together, molecular and morphological data suggest the reinstatement of a third Azorean Leontodon taxon endemic to the western group. A key to the Leontodon of the Azores and descriptions of the endemic taxa are provided.

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“…Recent studies have hypothesized that associations to specific mycorrhizal fungi may act as an extrinsic post‐zygotic barrier by preventing the germination of hybrid seeds through the lack of a proper fungal partner (Jacquemyn, Brys, Cammue, Honnay, & Lievens, 2011; Scopece et al., 2008). Changes in mycorrhizal fungi have thus the potential to drive orchid speciation (Bateman et al., 2014; Otero & Flanagan, 2006; Waterman & Bidartondo, 2008), and there is evidence, although limited, that the sharing of similar fungi is prerequisite for successful establishment of hybrids in orchids (Schatz et al., 2010). …”

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Floral scent and species divergence in a pair of sexually deceptive orchids

Gervasi

Selosse

Sauve

et al. 2017

Ecology and Evolution

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Speciation is typically accompanied by the formation of isolation barriers between lineages. Commonly, reproductive barriers are separated into pre‐ and post‐zygotic mechanisms that can evolve with different speed. In this study, we measured the strength of different reproductive barriers in two closely related, sympatric orchids of the Ophrys insectifera group, namely Ophrys insectifera and Ophrys aymoninii to infer possible mechanisms of speciation. We quantified pre‐ and post‐pollination barriers through observation of pollen flow, by performing artificial inter‐ and intraspecific crosses and analyzing scent bouquets. Additionally, we investigated differences in mycorrhizal fungi as a potential extrinsic factor of post‐zygotic isolation. Our results show that floral isolation mediated by the attraction of different pollinators acts apparently as the sole reproductive barrier between the two orchid species, with later‐acting intrinsic barriers seemingly absent. Also, the two orchids share most of their fungal mycorrhizal partners in sympatry, suggesting little or no importance of mycorrhizal symbiosis in reproductive isolation. Key traits underlying floral isolation were two alkenes and wax ester, present predominantly in the floral scent of O. aymoninii. These compounds, when applied to flowers of O. insectifera, triggered attraction and a copulation attempt of the bee pollinator of O. aymoninii and thus led to the (partial) breakdown of floral isolation. Based on our results, we suggest that adaptation to different pollinators, mediated by floral scent, underlies species isolation in this plant group. Pollinator switches may be promoted by low pollination success of individuals in dense patches of plants, an assumption that we also confirmed in our study.

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Speciation via floral heterochrony and presumed mycorrhizal host switching of endemic butterfly orchids on the Azorean archipelago

Cited by 25 publications

References 75 publications

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A revision of the genus Leontodon (Asteraceae) in the Azores based on morphological and molecular evidence

Floral scent and species divergence in a pair of sexually deceptive orchids

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