An Indomalesian origin in the Miocene for the diphyletic New World jewel orchids (Goodyerinae, Orchidoideae): molecular dating and biogeographic analyses document non-monophyly of the Neotropical genera

Abstract

The jewel orchids (Goodyerinae), named after their often colourful leaves, have a pantropical distribution with a clear Asian centre of diversity. However, the Nearctic and Neotropical America together form a second centre of diversity, with one-third of known species of Goodyerinae. Previously, only a few American samples have been included in phylogenetic studies, and their putatively Asian origins and American divergence times were poorly known. To elucidate these topics, we inferred phylogenetic trees, performed molecular dating and reconstructed biogeographic history using nuclear ribosomal ITS and plastid matK sequences for 34 species of Goodyerinae from the New World and 76 previously published accessions of Cranichideae. Our well-supported phylogenetic topology suggests two independent dispersal events to the New World from the Indomalesian region during the Miocene. The first inferred dispersal of a Neotropical clade diverged c. 11 Mya from their most recent common ancestor (MRCA), comprising three highly supported subclades that do not match the limits of Aspidogyne, Kreodanthus and Microchilus as previously circumscribed. The second dispersal involved a largely Nearctic clade of Goodyera s.l. diverging c. 8.4 Mya from the MRCA and exhibiting a complex biogeographic history with subsequent dispersals between the Nearctic and Indomalesia. The occurrence of these species in gallery forests putatively prevented vicariance events imposed by the expansion of the Chacoan region as previously detected for epiphytic Orchidaceae. Eighty-nine nomenclatural combinations and three new names in Microchilus are proposed.

Molecular Phylogeny and Historical Biogeography of Goodyera R. Br. (Orchidaceae): A Case of the Vicariance Between East Asia and North America

“…Specifically, clade A included North American species ( G. striata and G. pubescens ) and they diverged at 10.88 Mya (95% HPD = 7.86–13.63 Mya) in comparison with c . 8.4 Mya of Smidt et al ( 2021 ) ( Figure 4 ). The diversification of Goodyera mainly occurred in 14 Mya, when the temperature began to decrease, which is similar to the result of Briggs ( 1995 ).…”

“…Erythrodes was affiliated to clade C with the characteristics of no-marking leaves and reflexed lateral sepals based on nuclear ITS, plastid trn L-F, and mat K genes (Hu et al, 2016 ). Chen et al ( 2019 ) and Smidt et al ( 2021 ) defined that clade C is the Microchilus subclade, in which diverse species exist including some Goodyera species. The results of Tu et al ( 2021 ) showed that Aspidogyne was a sister to the rest of clade C, followed by G. fumata , whereas Erythrodes and Goodyera formed a subclade based on plastid-coding genes' dataset.…”

“…Similarly, our study revealed that Aspidogyne longicornu was a sister to G. fumata and Erythrodes blumei was a sister to G. viridiflora and G. seikoomontana , respectively ( Figure 3 ). Smidt et al ( 2021 ) proposed the combinations of Microchilus s.l . including Aspidogyne, Microchilus , and Kreodanthus based on the results using ITS and mat K. However, the 79 CDS datasets revealed the placement of Aspidogyne within Goodyera clade.…”

“…We expect their most recent common ancestor (MRCA), which was distributed in a tropical or subtropical area and migrated to temperate Asia to survive against the rising temperature due to MCO. Smidt et al ( 2021 ) proposed the Neotropical clade including Aspidogyne in Goodyerinae diverged c . 11 Mya and derived from Indomalayan ancestors, but our study lacked the Neotropical species in Goodyerinae and focused on the genus Goodyera , so further research is needed.…”

“…Even though the Orchidaceae is the largest family among angiosperms, the results showed that only one lineage is in the orchid family. Currently, biogeographical analyses have been carried out on orchids (Guo et al, 2012 ; Givnish et al, 2016 ; Smidt et al, 2021 ), but the comprehension of the disjunctive pattern of orchids is still lacking compared to the other groups.…”