Molecular phylogenetic analyses reveal multiple long-distance dispersal events and extensive cryptic speciation in Nervilia (Orchidaceae), an isolated basal Epidendroid genus
IntroductionThe terrestrial orchid genus Nervilia is diagnosed by its hysteranthous pattern of emergence but is nested among leafless myco-heterotrophic lineages in the lower Epidendroideae. Comprising ca. 80 species distributed across Africa, Asia and Oceania, the genus remains poorly known and pla...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2025-02-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2024.1495487/full |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850025276718710784 |
|---|---|
| author | Stephan W. Gale Jihong Li Somran Suddee Paweena Traiperm Craig I. Peter Tomas Buruwate Benjamin J. Crain Melissa K. McCormick Dennis F. Whigham Arni Musthofa Khyanjeet Gogoi Katsura Ito Yukio Minamiya Tatsuya Fukuda Sven Landrein Tomohisa Yukawa |
| author_facet | Stephan W. Gale Jihong Li Somran Suddee Paweena Traiperm Craig I. Peter Tomas Buruwate Benjamin J. Crain Melissa K. McCormick Dennis F. Whigham Arni Musthofa Khyanjeet Gogoi Katsura Ito Yukio Minamiya Tatsuya Fukuda Sven Landrein Tomohisa Yukawa |
| author_sort | Stephan W. Gale |
| collection | DOAJ |
| description | IntroductionThe terrestrial orchid genus Nervilia is diagnosed by its hysteranthous pattern of emergence but is nested among leafless myco-heterotrophic lineages in the lower Epidendroideae. Comprising ca. 80 species distributed across Africa, Asia and Oceania, the genus remains poorly known and plagued by vague and overlapping species circumscriptions, especially within each of a series of taxonomically intractable species complexes. Prior small-scale, exploratory molecular phylogenetic analyses have revealed the existence of cryptic species, but little is otherwise understood of origin, the scale and timing of its biogeographic spread, or the palaeoclimatic factors that have shaped its ecology and given rise to contemporary patterns of occurrence.MethodsHere, we sample widely throughout the generic range, including 45 named taxa and multiple accessions referable to several widespread ‘macrospecies’, as well as material of equivocal identity and probable undescribed status, for the first time enabling an evaluation of taxonomic boundaries at both species and sectional level. Using nuclear (ITS) and plastid (matK, trnL-F) sequence data, we conduct phylogenetic (maximum parsimony and Bayesian inference) and ancestral area analysis to infer relationships and resolve probable origin and colonisation routes.ResultsThe genus is strongly supported as monophyletic, as are each of its three sections. However, the number of flowers in the inflorescence and other floral characters are poor indicators of sectional affinity. Dated ancestral area analysis supports an origin in Africa in the Early Oligocene, with spread eastwards to Asia occurring in the Late Miocene, plausibly via the Gomphotherium land bridge at a time when it supported woodland and savanna ecosystems.DiscussionTaxonomic radiation in Asia within the last 8 million years ties in with dramatic Himalayan-Tibetan Plateau uplift and associated intensification of the Asia monsoon. Multiple long-range migrations appear to have occurred thereafter, as the genus colonised Malesia and Oceania from the Pliocene onwards. The bulk of contemporary species diversity is relatively recent, potentially explaining the ubiquity of cryptic speciation, which leaves numerous species overlooked and unnamed. Widespread disjunct species pairs hint at high mobility across continents, extinction and a history of climate-induced vicariance. Persistent taxonomic challenges are highlighted. |
| format | Article |
| id | doaj-art-345166cce2da4b378c196bd508378ecb |
| institution | DOAJ |
| issn | 1664-462X |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj-art-345166cce2da4b378c196bd508378ecb2025-08-20T03:00:54ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-02-011510.3389/fpls.2024.14954871495487Molecular phylogenetic analyses reveal multiple long-distance dispersal events and extensive cryptic speciation in Nervilia (Orchidaceae), an isolated basal Epidendroid genusStephan W. Gale0Jihong Li1Somran Suddee2Paweena Traiperm3Craig I. Peter4Tomas Buruwate5Benjamin J. Crain6Melissa K. McCormick7Dennis F. Whigham8Arni Musthofa9Khyanjeet Gogoi10Katsura Ito11Yukio Minamiya12Tatsuya Fukuda13Sven Landrein14Tomohisa Yukawa15Flora Conservation Department, Kadoorie Farm and Botanic Garden, Hong Kong, Hong Kong SAR, ChinaFlora Conservation Department, Kadoorie Farm and Botanic Garden, Hong Kong, Hong Kong SAR, ChinaDepartment of National Parks, Forest Herbarium, Wildlife and Plant Conservation, Bangkok, ThailandDepartment of Plant Science, Faculty of Science, Mahidol University, Bangkok, ThailandDepartment of Botany, Rhodes University, Grahamstown, Makhanda, South AfricaMariri Environmental Centre L5 South Concession, Niassa Special Reserve, MozambiqueNorth American Orchid Conservation Center, Smithsonian Environmental Research Center, Edgewater, MD, United StatesNorth American Orchid Conservation Center, Smithsonian Environmental Research Center, Edgewater, MD, United StatesNorth American Orchid Conservation Center, Smithsonian Environmental Research Center, Edgewater, MD, United StatesIntegrated Research Laboratory, Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta, IndonesiaThe Orchid Society of Eastern Himalaya, Daisa Bordoloi Nagar, Tinsukia, Assam, IndiaFaculty of Agriculture and Marine Science, Kochi University, Monobeotsu, Nankoku, Kochi, Japan0Tochigi Prefectural Museum, Utsunomiya, Japan1Graduate School of Integrative Science and Engineering, Tokyo City University, Tokyo, JapanFlora Conservation Department, Kadoorie Farm and Botanic Garden, Hong Kong, Hong Kong SAR, China2Tsukuba Botanical Garden, National Museum of Nature and Science, Tsukuba, JapanIntroductionThe terrestrial orchid genus Nervilia is diagnosed by its hysteranthous pattern of emergence but is nested among leafless myco-heterotrophic lineages in the lower Epidendroideae. Comprising ca. 80 species distributed across Africa, Asia and Oceania, the genus remains poorly known and plagued by vague and overlapping species circumscriptions, especially within each of a series of taxonomically intractable species complexes. Prior small-scale, exploratory molecular phylogenetic analyses have revealed the existence of cryptic species, but little is otherwise understood of origin, the scale and timing of its biogeographic spread, or the palaeoclimatic factors that have shaped its ecology and given rise to contemporary patterns of occurrence.MethodsHere, we sample widely throughout the generic range, including 45 named taxa and multiple accessions referable to several widespread ‘macrospecies’, as well as material of equivocal identity and probable undescribed status, for the first time enabling an evaluation of taxonomic boundaries at both species and sectional level. Using nuclear (ITS) and plastid (matK, trnL-F) sequence data, we conduct phylogenetic (maximum parsimony and Bayesian inference) and ancestral area analysis to infer relationships and resolve probable origin and colonisation routes.ResultsThe genus is strongly supported as monophyletic, as are each of its three sections. However, the number of flowers in the inflorescence and other floral characters are poor indicators of sectional affinity. Dated ancestral area analysis supports an origin in Africa in the Early Oligocene, with spread eastwards to Asia occurring in the Late Miocene, plausibly via the Gomphotherium land bridge at a time when it supported woodland and savanna ecosystems.DiscussionTaxonomic radiation in Asia within the last 8 million years ties in with dramatic Himalayan-Tibetan Plateau uplift and associated intensification of the Asia monsoon. Multiple long-range migrations appear to have occurred thereafter, as the genus colonised Malesia and Oceania from the Pliocene onwards. The bulk of contemporary species diversity is relatively recent, potentially explaining the ubiquity of cryptic speciation, which leaves numerous species overlooked and unnamed. Widespread disjunct species pairs hint at high mobility across continents, extinction and a history of climate-induced vicariance. Persistent taxonomic challenges are highlighted.https://www.frontiersin.org/articles/10.3389/fpls.2024.1495487/fullAsia monsoondiversificationhysteranthylower Epidendroideaeout-of-Africaspecies complex |
| spellingShingle | Stephan W. Gale Jihong Li Somran Suddee Paweena Traiperm Craig I. Peter Tomas Buruwate Benjamin J. Crain Melissa K. McCormick Dennis F. Whigham Arni Musthofa Khyanjeet Gogoi Katsura Ito Yukio Minamiya Tatsuya Fukuda Sven Landrein Tomohisa Yukawa Molecular phylogenetic analyses reveal multiple long-distance dispersal events and extensive cryptic speciation in Nervilia (Orchidaceae), an isolated basal Epidendroid genus Frontiers in Plant Science Asia monsoon diversification hysteranthy lower Epidendroideae out-of-Africa species complex |
| title | Molecular phylogenetic analyses reveal multiple long-distance dispersal events and extensive cryptic speciation in Nervilia (Orchidaceae), an isolated basal Epidendroid genus |
| title_full | Molecular phylogenetic analyses reveal multiple long-distance dispersal events and extensive cryptic speciation in Nervilia (Orchidaceae), an isolated basal Epidendroid genus |
| title_fullStr | Molecular phylogenetic analyses reveal multiple long-distance dispersal events and extensive cryptic speciation in Nervilia (Orchidaceae), an isolated basal Epidendroid genus |
| title_full_unstemmed | Molecular phylogenetic analyses reveal multiple long-distance dispersal events and extensive cryptic speciation in Nervilia (Orchidaceae), an isolated basal Epidendroid genus |
| title_short | Molecular phylogenetic analyses reveal multiple long-distance dispersal events and extensive cryptic speciation in Nervilia (Orchidaceae), an isolated basal Epidendroid genus |
| title_sort | molecular phylogenetic analyses reveal multiple long distance dispersal events and extensive cryptic speciation in nervilia orchidaceae an isolated basal epidendroid genus |
| topic | Asia monsoon diversification hysteranthy lower Epidendroideae out-of-Africa species complex |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2024.1495487/full |
| work_keys_str_mv | AT stephanwgale molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT jihongli molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT somransuddee molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT paweenatraiperm molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT craigipeter molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT tomasburuwate molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT benjaminjcrain molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT melissakmccormick molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT dennisfwhigham molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT arnimusthofa molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT khyanjeetgogoi molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT katsuraito molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT yukiominamiya molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT tatsuyafukuda molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT svenlandrein molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus AT tomohisayukawa molecularphylogeneticanalysesrevealmultiplelongdistancedispersaleventsandextensivecrypticspeciationinnerviliaorchidaceaeanisolatedbasalepidendroidgenus |