skip to main content


Title: Atmospheric CO2 decline and the timing of CAM plant evolution
Abstract Background and Aims

CAM photosynthesis is hypothesized to have evolved in atmospheres of low CO2 concentration in recent geological time because of its ability to concentrate CO2 around Rubisco and boost water use efficiency relative to C3 photosynthesis. We assess this hypothesis by compiling estimates of when CAM clades arose using phylogenetic chronograms for 73 CAM clades. We further consider evidence of how atmospheric CO2 affects CAM relative to C3 photosynthesis.

Results

Where CAM origins can be inferred, strong CAM is estimated to have appeared in the past 30 million years in 46 of 48 examined clades, after atmospheric CO2 had declined from high (near 800 ppm) to lower (<450 ppm) values. In turn, 21 of 25 clades containing CAM species (but where CAM origins are less certain) also arose in the past 30 million years. In these clades, CAM is probably younger than the clade origin. We found evidence for repeated weak CAM evolution during the higher CO2 conditions before 30 million years ago, and possible strong CAM origins in the Crassulaceae during the Cretaceous period prior to atmospheric CO2 decline. Most CAM-specific clades arose in the past 15 million years, in a similar pattern observed for origins of C4 clades.

Conclusions

The evidence indicates strong CAM repeatedly evolved in reduced CO2 conditions of the past 30 million years. Weaker CAM can pre-date low CO2 and, in the Crassulaceae, strong CAM may also have arisen in water-limited microsites under relatively high CO2. Experimental evidence from extant CAM species demonstrates that elevated CO2 reduces the importance of nocturnal CO2 fixation by increasing the contribution of C3 photosynthesis to daily carbon gain. Thus, the advantage of strong CAM would be reduced in high CO2, such that its evolution appears less likely and restricted to more extreme environments than possible in low CO2.

 
more » « less
NSF-PAR ID:
10468246
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Annals of Botany
ISSN:
0305-7364
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Background

    A current argument in the CAM biology literature has focused on the nature of the CAM evolutionary trajectory: whether there is a smooth continuum of phenotypes between plants with C3 and CAM photosynthesis or whether there are discrete steps of phenotypic evolutionary change such as has been modelled for the evolution of C4 photosynthesis. A further implication is that a smooth continuum would increase the evolvability of CAM, whereas discrete changes would make the evolutionary transition from C3 to CAM more difficult.

    Scope

    In this essay, I attempt to reconcile these two viewpoints, because I think in many ways this is a false dichotomy that is constraining progress in understanding how both CAM and C4 evolved. In reality, the phenotypic space connecting C3 species and strong CAM/C4 species is both a continuum of variably expressed quantitative traits and yet also contains certain combinations of traits that we are able to identify as discrete, recognizable phenotypes. In this sense, the evolutionary mechanics of CAM origination are no different from those of C4 photosynthesis, nor from the evolution of any other complex trait assemblage.

    Conclusions

    To make progress, we must embrace the concept of discrete phenotypic phases of CAM evolution, because their delineation will force us to articulate what aspects of phenotypic variation we think are significant. There are some current phenotypic gaps that are limiting our ability to build a complete CAM evolutionary model: the first is how a rudimentary CAM biochemical cycle becomes established, and the second is how the ‘accessory’ CAM cycle in C3+CAM plants is recruited into a primary metabolism. The connections to the C3 phenotype we are looking for are potentially found in the behaviour of C3 plants when undergoing physiological stress – behaviour that, strangely enough, remains essentially unexplored in this context.

     
    more » « less
  2. Abstract

    Clusia is a remarkable genus of Neotropical woody plants as its members engage in either C3 photosynthesis or employ, to varying degrees, crassulacean acid metabolism (CAM) photosynthesis. Information about the evolutionary history of CAM in Clusia is scarce. Restriction site-associated sequencing of 64 species (20% of the genus) provided strong support for most of the previously recognized nine lineages. Ancestral reconstruction using maximum parsimony or maximum likelihood under a one-rate model suggested that CAM evolved at least four times independently from a most recent common ancestor (MRCA) with C3, whereas a maximum likelihood two-rate model suggested that CAM was already present in the MRCA followed by reversions to C3 in several lineages. Phylogenetic generalized least square analysis assessed variation in seven leaf anatomical traits and CAM activity measured as δ 13C. Results indicate that CAM is highly correlated with palisade mesophyll layer thickness and cell size. In addition, correlation between 19 bioclimatic variables and δ 13C was evaluated. It was found that CAM is positively correlated with habitats with a more severe dry season and greater precipitation seasonality. Since CAM is weakly and/or only periodically expressed in many Clusia spp., and thus not readily reflected in δ 13C, future analysis of phylogenetically-informed CAM expression in Clusia must include physiological measurements such as CO2 exchange and/or diel changes in leaf acidity for each species under investigation.

     
    more » « less
  3. Abstract

    Australian Calandrinia has radiated across the Australian continent during the last 30 Ma, and today inhabits most Australian ecosystems. Given its biogeographic range and reports of facultative Crassulacean acid metabolism (CAM) photosynthesis in multiple species, we hypothesized (1) that CAM would be widespread across Australian Calandrinia and that species, especially those that live in arid regions, would engage in strong CAM, and (2) that Australian Calandrinia would be an important lineage for informing on the CAM evolutionary trajectory. We cultivated 22 Australian Calandrinia species for a drought experiment. Using physiological measurements and δ13C values we characterized photosynthetic mode across these species, mapped the resulting character states onto a phylogeny, and characterized the climatic envelopes of species in their native ranges. Most species primarily utilize C3 photosynthesis, with CAM operating secondarily, often upregulated following drought. Several phylogenetically nested species are C3, indicating evolutionary losses of CAM. No strong CAM was detected in any of the species. Results highlight the limitations of δ13C surveys in detecting C3+CAM phenotypes, and the evolutionary lability of C3+CAM phenotypes. We propose a model of CAM evolution that allows for lability and reversibility among C3+CAM phenotypes and C3 and suggest that an annual life-cycle may preclude the evolution of strong CAM.

     
    more » « less
  4. INTRODUCTION Inherent in traditional views of ape origins is the idea that, like living apes, early large-bodied apes lived in tropical forests. In response to constraints related to locomoting in forest canopies, it has been proposed that early apes evolved their quintessential upright torsos and acrobatic climbing and suspensory abilities, enhancing their locomotor versatility, to distribute their weight among small supports and thus reach ripe fruit in the terminal branches. This feeding and locomotor transition from a quadruped with a horizontal torso is thought to have occurred in the Middle Miocene due to an increasingly seasonal climate and feeding competition from evolving monkeys. Although ecological and behavioral comparisons among living apes and monkeys provide evidence for versions of terminal branch forest frugivory hypotheses, corroboration from the early ape fossil record has been lacking, as have detailed reconstructions of the habitats where the first apes evolved. RATIONALE The Early Miocene fossil site of Moroto II in Uganda provides a unique opportunity to test the predictions of terminal branch forest frugivory hypotheses. Moroto II documents the oldest [21 million years ago (Ma)] well-established paleontological record of ape teeth and postcranial bones from a single locality and preserves paleoecological proxies to reconstruct the environment. The following lines of evidence from Moroto II were analyzed: (i) the functional anatomy of femora and a vertebra attributed to the ape Morotopithecus ; (ii) dental traits, including molar shape and isotopic profiles of Morotopithecus enamel; (iii) isotopic dietary paleoecology of associated fossil mammals; (iv) biogeochemical signals from paleosols (ancient soils) that reflect local relative proportions of C 3 (trees and shrubs) and C 4 (tropical grasses and sedges that can endure water stress) vegetation as well as rainfall; and (v) assemblages of phytoliths, microscopic plant-derived silica bodies that reflect past plant communities. RESULTS A short, strong femur biomechanically favorable to vertical climbing and a vertebra indicating a dorsostable lower back confirm that ape fossils from Moroto II shared locomotor traits with living apes. Both Morotopithecus and a smaller ape from the site have elongated molars with well-developed crests for shearing leaves. Carbon isotopic signatures of the enamel of these apes and of other fossil mammals indicate that some mammals consistently fed on water-stressed C 3  plants, and possibly also C 4  vegetation, in a woodland setting. Carbon isotope values of pedogenic carbonates, paleosol organic matter, and plant waxes all point to substantial C 4 grass biomass on the landscape. Analysis of paleosols also indicates subhumid, strongly seasonal rainfall, and phytolith assemblages include forms from both arid-adapted C 4 grasses and forest-indicator plants. CONCLUSION The ancient co-occurrence of dental specializations for leaf eating, rather than ripe fruit consumption, along with ape-like locomotor abilities counters the predictions of the terminal branch forest frugivory hypotheses. The combined paleoecological evidence situates Morotopithecus in a woodland with a broken canopy and substantial grass understory including C 4 species. These findings call for a new paradigm for the evolutionary origins of early apes. We propose that seasonal, wooded environments may have exerted previously unrecognized selective pressures in the evolution of arboreal apes. For example, some apes may have needed to access leaves in the higher canopy in times of low fruit availability and to be adept at ascending and descending from trees that lacked a continuous canopy. Hominoid habitat comparisons. Shown are reconstructions of a traditionally conceived hominoid habitat ( A ) and the 21 Ma Moroto II, Uganda, habitat ( B ). 
    more » « less
  5. Abstract

    The evolution of sexually selected traits is a major topic in evolutionary biology. However, large-scale evolutionary patterns in these traits remain understudied, especially those traits used in male–male competition (weapons sensu lato). Here, we analyze weapon evolution in chamaeleonid lizards, both within and between the sexes. Chameleons are an outstanding model system because of their morphological diversity (including 11 weapon types among ~220 species) and a large-scale time-calibrated phylogeny. We analyze these 11 traits among 165 species using phylogenetic methods, addressing many questions for the first time in any group. We find that all 11 weapons have each evolved multiple times and that weapon origins are generally more frequent than their losses. We find that almost all weapons have each persisted for >30 million years (and some for >65 million years). Across chameleon phylogeny, we identify both hotspots for weapon evolution (up to 10 types present per species) and coldspots (all weapons absent, many through loss). These hotspots are significantly associated with larger male body size, but are only weakly related to sexual-size dimorphism. We also find that weapon evolution is strongly correlated between males and females. Overall, these results provide a baseline for understanding large-scale patterns of weapon evolution within clades.

     
    more » « less