Abstract
Evolutionary slowdowns in diversification have been inferred in various plant and animal lineages. Investigation based on diversification models integrated with environmental factors and key characters could provide critical insights into this diversification trend. We evaluate diversification rates in the Cirrhopetalum alliance (Bulbophyllum, Orchidaceae subfam. Epidendroideae) using a time-calibrated phylogeny and assess the role of Crassulacean acid metabolism (CAM) as a hypothesised key innovation promoting the spectacular diversity of orchids, especially those with an epiphytic habit. An explosive early speciation in the Cirrhopetalum alliance is evident, with the origin of CAM providing a short-term advantage under the low atmospheric CO2 concentrations (pCO2) associated with cooling and aridification in the late Miocene. A subsequent slowdown of diversification in the Cirrhopetalum alliance is possibly explained by a failure to keep pace with pCO2 dynamics. We further demonstrate that extinction rates in strong CAM lineages are ten times higher than those of C3 lineages, with CAM not as evolutionarily labile as previously assumed. These results challenge the role of CAM as a “key innovation” in the diversification of epiphytic orchids.
Highlights
Understanding the dynamics of diversification over space and time and identifying the underlying biotic and abiotic causes of the patterns have been a major focus in evolutionary biology (Ricklefs, 2007)
Null models rejected, supporting the hypothesis of a slowdown in diversification DD models rejected, supporting the alternative diversity-independent model No significant rate shift detected; speciation decreased through time Speciation rate is dramatically decreased and extinction rate is constant Speciation is positively correlated to the drop of atmospheric pCO2 from the late Miocene to present Higher Crassulacean acid metabolism (CAM) associated speciation rate and 10-fold extinction rate to C3 Photosynthetic pathways explain most of the diversification heterogeneity actual sample size (n = 88)
The null distribution of γ values based on the simulated 1,000 trees against the empirical γ value based on Dataset 1 was compared using the Monte Carlo CR (MCCR) test statistic
Summary
Understanding the dynamics of diversification over space and time and identifying the underlying biotic and abiotic causes of the patterns have been a major focus in evolutionary biology (Ricklefs, 2007). The dynamics of speciation and extinction rates alone, or a combination of both, can lead to various distinctive diversification patterns (Donoghue and Sanderson, 2015; Louca and Pennell, 2020). Crassulacean acid metabolism (CAM) represents a striking example of ecological adaptation to CO2-constrained and water-limited environments (Michener and Lajtha, 2007). CAM photosynthesis is polyphyletic, having arisen independently from multiple C3 ancestors during the Miocene, possibly as a consequence of reduced atmospheric CO2 concentration (Raven and Spicer, 1996). This transition sometimes occurs in parallel with the colonisation of new ecological niches such as increasingly arid habitats, triggering adaptive speciation (Lüttge, 1996). It has been hypothesised that CAM might be a key evolutionary innovation, correlated with extraordinary species diversity in some vascular plant groups, such as Bromeliaceae (Silvestro et al, 2014), Cactaceae (Arakaki et al, 2011), Euphorbiaceae (Horn et al, 2014), and Orchidaceae (Silvera et al, 2009; Givnish et al, 2015)
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