Evolution of Crassulacean Acid Metabolism (CAM) as an escape from ecological niche conservatism in Malagasy<i>Bulbophyllum</i>(Orchidaceae)

Gamisch, Alexander; Winter, Klaus; Fischer, Gunter A.; Comes, Hans Peter

doi:10.1101/2021.01.09.426039

Cited by 5 publications

(19 citation statements)

References 92 publications

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“…50 extant species of this clade are variously distributed across the island’s main rainforest biomes (i.e. Central Highland, Eastern Lowland, Northwest Sambirano), indicating that niche evolution proceeded without phylogenetic constraints (Gamisch et al ., 2016, 2021). Markedly similar to this, our PCA of Procrustes‐fitted flower shape data for 38 Clade A species (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Phylogenetic data for Clade A species were derived from Gamisch et al . (2021), who report a time‐calibrated maximum clade credibility (MCC) tree for Malagasy Bulbophyllum as a whole (179 out of 210 spp. ), built on concatenated DNA sequence data from three nuclear regions (nrITS, PI, Xdh ) and five plastid gene regions ( atp I– atp H, ycf1 , mat K, trn D –trn E, psb A –trn H), and estimated under a relaxed (log‐normal) clock in Beast v.1.8.4 (Drummond et al ., 2012).…”

Section: Methodsmentioning

confidence: 99%

“…We colour coded the taxa according to their taxonomic section and phytogeographic zone/rainforest type (i.e. Central Highland, Eastern Lowland and/or Northwest Sambirano), using data from previous bioclimatic cluster and ecological niche model analyses (Gamisch et al ., 2016, 2021; see Table S1). Flower shape variation along each of the first two axes (PC1, PC2) was modelled by first identifying the species closest to the average shape of the Procrustes‐fitted samples (i.e.…”

Section: Methodsmentioning

confidence: 99%

“…The relative fit of the three models was assessed using the Generalized Information Criterion (GIC), and the model with the lowest score was considered the best one (function GIC ). To account for phylogenetic uncertainty, we performed these analyses over 100 trees sampled from the Bayesian posterior distribution of the complete Malagasy Bulbophyllum phylogeny (Gamisch et al ., 2021) and then pruned to match the 38‐species dataset of Clade A . Under the preferred model (OU; see Results), we estimated the ‘rate of adaptation’ parameter, α (ranging from zero to infinity), which is generally interpreted as the strength of selection, which reverts the trait values of species (within a clade) back towards a long‐term mean value ( μ ) or primary adaptive optimum ( sensu Hansen, 1997, 2014), if they stochastically evolve away from it (Mahler & Ingram, 2014; Blomberg et al ., 2020; Meireles et al ., 2020).…”

Section: Methodsmentioning

confidence: 99%

“…in total) since about the Mid‐to‐Late Miocene ( c . 12.7 Ma; Gamisch & Comes, 2019; Gamisch et al ., 2021). The c .…”

Section: Introductionmentioning

confidence: 99%

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Evidence for selectively constrained 3D flower shape evolution in a Late Miocene clade of Malagasy Bulbophyllum orchids

et al. 2021

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Summary Questions concerning the evolution of complex biological structures are central to the field of evolutionary biology. Yet, still little information is known about the modes and temporal dynamics of three‐dimensional (3D) flower shape evolution across the history of clades. Here, we combined high‐resolution X‐ray computed tomography with 3D geometric morphometrics and phylogenetic comparative methods to test models of whole‐flower shape evolution in the orchid family, using an early Late Miocene clade (c. 50 spp.) of Malagasy Bulbophyllum as model system. Based on landmark data of 38 species, our high‐dimensional model fitting decisively rejects a purely neutral mode of evolution, suggesting instead that flower shapes evolved towards a primary adaptive optimum. Only a small number of recently evolved species/lineages attained alternative shape optima, resulting in an increased rate of phenotypic evolution. Our findings provide evidence of constrained 3D flower shape evolution in a small‐sized clade of tropical orchids, resulting in low rates of phenotypic evolution and uncoupled trait–diversification rates. We hypothesise that this deep imprint of evolutionary constraint on highly complex floral structures might reflect long‐term (directional and/or stabilizing) selection exerted by the group’s main pollinators (flies).

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

“…in total) since about the Mid‐to‐Late Miocene ( c . 12.7 Ma; Gamisch & Comes, 2019; Gamisch et al ., 2021). The c .…”

Section: Introductionmentioning

confidence: 99%

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Evidence for selectively constrained 3D flower shape evolution in a Late Miocene clade of Malagasy Bulbophyllum orchids

et al. 2021

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C4 Equivalent Decarboxylation Competence in Tropical Orchids

et al. 2023

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Tropical xero-epiphytic orchids undergo a photosynthetic mechanism called ‘Crassulacean Acid Metabolism’, a modification of Calvin–Benson cycle. This anabolic process aids in the long-term retention of organically fixed CO2, imprinting them as active sequestrators and fixers of gaseous CO2. The malate decarboxylation competence of enzymes—phosphoenolpyruvate carboxykinase (PEPCK), Nicotinamide Adenine Dinucleotide malic enzyme (NAD-ME) and Nicotinamide Adenine Dinucleotide Phosphate malic enzyme (NADP-ME) in xero-epiphytic orchids that concentrate CO2 by employing RuBisCO to embark on a carboxylation route is defined in this paper. Physiological parameters like photosynthetic rates, and quantum yield, accompanied by histomorphometry were analysed. Our study indicated PEPCK as the dominant decarboxylating enzyme in tropical orchids. The efficiency of PEPCK was reinforced by two additional malic enzymes, which are dependent on cofactors, namely Nicotinamide Adenine Dinucleotide and Nicotinamide Adenine Dinucleotide Phosphate. These results indicated the need to appraise the potential of tropical orchids as strategic plant contenders for CO2 triggered greenhouse effect mitigator.

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Gains and losses of the epiphytic lifestyle in epidendroid orchids: review and new analyses with succulence traits

Collobert

Perez‐Lamarque

Dubuisson

et al. 2022

Preprint

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Background and Aims Epiphytism has evolved repeatedly in plants and has resulted in a considerable number of species with original characteristics. Succulent forms in particular are thought to have evolved as an adaptation to the epiphytic environment, because the water supply is generally erratic compared to soils'. However, succulent organs also exist in terrestrial plants, and the question of the concomitant evolution of epiphytism and succulence has received little attention, not even in the epidendroid orchids, which account for 68% of vascular epiphytes. Methods We reconstructed a new time-calibrated phylogenetic tree of Epidendroideae with 203 genera treated in Genera Orchidacearum, from which we reconstructed the evolution of epiphytism and other traits including stem and leaf succulence, while testing the correlated evolution between lifestyle and morphological traits. Furthermore, we reconstructed the ancestral geographic ranges to interpret major character changes during the Cenozoic. Key Results Epiphytism evolved at least 7.1 My ago in the neotropical Sobralieae, 11.5 My ago in the Arethuseae in Southeast Asia and Australia, and 39.0 My ago in the common ancestor of the Dendrobieae and Cymbidieae in the three previous areas, and was notably lost in the Malaxideae, Collabieae, Calypsoeae, Bletiinae, and Eulophiinae. Stem succulence is inferred to have evolved once, in a terrestrial ancestor 43.1 My ago, thus preceding the evolution of epiphytism by at least 4.1 My. If lost, stem succulence was almost systematically replaced by leaf succulence in epiphytic lineages. Conclusions Epiphytism probably evolved from terrestrial orchids already possessing succulent stems, which appeared during Eocene climatic cooling. Both epiphytic and secondary terrestrial Epidendroideae may have appeared in seasonally-dry forests. Thus, we believe that the emergence of stem succulence in early epidendroids was a key innovation in the evolution of orchids, facilitating the colonisation of epiphytic environments that led to the greatest diversification of orchids.

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Evolution of Crassulacean Acid Metabolism (CAM) as an escape from ecological niche conservatism in MalagasyBulbophyllum(Orchidaceae)

Cited by 5 publications

References 92 publications

Evidence for selectively constrained 3D flower shape evolution in a Late Miocene clade of Malagasy Bulbophyllum orchids

Evidence for selectively constrained 3D flower shape evolution in a Late Miocene clade of Malagasy Bulbophyllum orchids

C4 Equivalent Decarboxylation Competence in Tropical Orchids

Gains and losses of the epiphytic lifestyle in epidendroid orchids: review and new analyses with succulence traits

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