Evolution of crassulacean acid metabolism (CAM) as an escape from ecological niche conservatism in MalagasyBulbophyllum(Orchidaceae)

Abstract

Despite growing evidence that niche shifts are more common in flowering plants than previously thought, little is known of whether such shifts are promoted by changes in photosynthetic pathways.Here we combine the most complete phylogeny for epiphytic Malagasy Bulbophyllum orchids (c. 210 spp.) with climatic niche and carbon isotope ratios to infer the group's spatialtemporal history, and the role of strongly expressed crassulacean acid metabolism (CAM) in facilitating niche shifts and diversification.We find that most extant species still retain niche (Central Highland) and photosynthesis (C 3 ) states as present in the single mid-Miocene (c. 12.70 million yr ago (Ma)) ancestor colonizing Madagascar. However, we also infer a major transition to CAM, linked to a late Miocene (c. 7.36 Ma) invasion of species from the sub-humid highland first into the island's humid eastern coastal, and then into the seasonally dry 'Northwest Sambirano' rainforests, yet without significant effect on diversification rates.These findings indicate that CAM in tropical epiphytes may be selectively advantageous even in high rainfall habitats, rather than presenting a mere adaptation to dry environments or epiphytism per se. Overall, our study qualifies CAM as an evolutionary 'gateway' trait that considerably widened the spatial-ecological amplitude of Madagascar's most species-rich orchid genus.

Diversification Slowdown in the Cirrhopetalum Alliance (Bulbophyllum, Orchidaceae): Insights From the Evolutionary Dynamics of Crassulacean Acid Metabolism

“…These changes have been linked to rapid radiations in many plant lineages in Asia ( Wen et al, 2014 ). It is also worth noting that past monsoon activity has been implicated in playing a crucial role in diversification of Malagasy Bulbophyllum ( Gamisch et al, 2021 ), as well as in the slowdown in diversification of Primulina (Gesneriaceae) in southern China ( Kong et al, 2017 ). The impact of other environmental and climatic factors (i.e., global temperature changes and reginal monsoons) should be thoroughly investigated in future studies.…”

“…From a phylogenetic perspective, the switch from C 3 to obligate CAM has been suggested to be relatively rare to moderate at the species level, as reflected by few speciation events: e.g., three times over 6–10 Myr in Asparagaceae subfam. Agavoideae ( Heyduk et al, 2016 ); three times over 7.36 Myr in Malagasy Bulbophyllum Gamisch et al (2021) ; four times over 11.5 Myr in Orchidaceae subtribe Eulophiinae ( Bone et al, 2015 ); 10 times over 7 Myr in Bromeliaceae subfam. Bromelioideae ( Silvestro et al, 2014 ); 20 times over 15 Myr in Euphorbia (Euphorbiaceae) ( Horn et al, 2014 ); 10 times among the Orchidaceae ( Silvera et al, 2009 ); and nine times over 11.8 Myr in the Cirrhopetalum alliance in the present study ( Table 4 , based on S1).…”

“…The Cirrhopetalum alliance is a well-supported clade of c. 210 species belonging to the diverse epiphytic genus Bulbophyllum ( Hu et al, 2020 ). A mixture of both CAM and C 3 photosynthetic pathways has been reported in Malagasy Bulbophyllum ( Gamisch et al, 2021 ). Here, we use a robust time-calibrated species-level molecular phylogeny of the Cirrhopetalum alliance ( Hu et al, 2020 ), together with data on historic CO 2 concentrations ( p CO 2 ) and photosynthetic pathways of all species sampled, to: (1) infer the diversification of the Cirrhopetalum alliance; (2) investigate the photosynthesis-dependent diversification integrated with p CO 2 , specifically focusing on CAM-associated speciation and extinction rates; and (3) re-assess the role of CAM as a possible key innovation in the diversification of epiphytic orchids.…”

“… Silvera et al (2009) suggested that CAM is a drought avoidance mechanism that stimulated the evolution of epiphytism and that epiphytism in turn promoted higher rates of speciation in a wider range of ecological niches. Newly generated data have nevertheless shown that the evolution of CAM and epiphytism in Orchidaceae are so closely associated that it is difficult to disentangle the individual effect of either ( Givnish et al, 2015 ), and Gamisch et al (2021) demonstrated that the transition from C 3 to CAM was not associated with significantly higher diversification rates in Malagasy Bulbophyllum (Orchidaceae subfam. Epidendroideae).…”

“…Epiphytic orchids with species-rich CAM lineages and C 3 sister clades represent a good model to investigate diversification dynamics ( Givnish et al, 2015 ; Gamisch et al, 2021 ). The Cirrhopetalum alliance is a well-supported clade of c. 210 species belonging to the diverse epiphytic genus Bulbophyllum ( Hu et al, 2020 ).…”