Cenozoic climate change shaped the evolutionary ecophysiology of the Cupressaceae conifers - PubMed (original) (raw)

Cenozoic climate change shaped the evolutionary ecophysiology of the Cupressaceae conifers

Jarmila Pittermann et al. Proc Natl Acad Sci U S A. 2012.

Abstract

The Cupressaceae clade has the broadest diversity in habitat and morphology of any conifer family. This clade is characterized by highly divergent physiological strategies, with deciduous swamp-adapted genera-like Taxodium at one extreme, and evergreen desert genera-like Cupressus at the other. The size disparity within the Cupressaceae is equally impressive, with members ranging from 5-m-tall juniper shrubs to 100-m-tall redwood trees. Phylogenetic studies demonstrate that despite this variation, these taxa all share a single common ancestor; by extension, they also share a common ancestral habitat. Here, we use a common-garden approach to compare xylem and leaf-level physiology in this family. We then apply comparative phylogenetic methods to infer how Cenozoic climatic change shaped the morphological and physiological differences between modern-day members of the Cupressaceae. Our data show that drought-resistant crown clades (the Cupressoid and Callitroid clades) most likely evolved from drought-intolerant Mesozoic ancestors, and that this pattern is consistent with proposed shifts in post-Eocene paleoclimates. We also provide evidence that within the Cupressaceae, the evolution of drought-resistant xylem is coupled to increased carbon investment in xylem tissue, reduced xylem transport efficiency, and at the leaf level, reduced photosynthetic capacity. Phylogenetically based analyses suggest that the ancestors of the Cupressaceae were dependent upon moist habitats, and that drought-resistant physiology developed along with increasing habitat aridity from the Oligocene onward. We conclude that the modern biogeography of the Cupressaceae conifers was shaped in large part by their capacity to adapt to drought.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

The evolutionary trajectory of cavitation resistance (_P_50) in the Cupressaceae over deep time. Branch colors indicate ancestral reconstruction of _P_50 values. Clades are identified according to Gadek et al. (13) and the Cenozoic climate data are replotted from Zachos et al. (4). Node bars represent 95% credible intervals at each node. Tip expansions approximate the number of species found in each of the major clades per Farjon (12) (Cupressus n = 16, Juniperus n = 52, Callitris n = 15) and the proportion of species found in arid habitats (see text). Branch tips without expansions indicate monotypic genera. The node numbers correspond to the contrasts data in Fig. 3. Sketches provide examples of polymorphic foliage in the Cupressaceae with appressed, imbricate leaves found in more arid-adapted taxa. The height ranges of adult trees are presented alongside genus names (12).

Fig. 2.

Fig. 2.

The relationship between cavitation resistance and wood density (A), tracheid double-wall thickness:lumen diameter (B), hydraulic conduit diameter (C), and xylem-specific conductivity (D) in the Cupressaceae (means ± SD). T. baccata and S. verticillata were not included in the analysis. Asterisks indicate Cupressaceae taxa endemic to habitats in the southern hemisphere.

Fig. 3.

Fig. 3.

The relationship between leaf- and xylem-level traits in the Cupressaceae. Leaf stomatal conductance is positively correlated with stem water supply, _K_s (A; means ± SD). Reduced photosynthesis rates arise from the inverse relationship between _P_50 and _K_s, and by extension, g (C; see text for details). Asterisks indicate Cupressaceae taxa endemic to habitats in the southern hemisphere. PIC analyses (B and D) demonstrate the correlated evolution of leaf and xylem traits. Each independent contrast corresponds to trait divergence at a specific node; node numbers shown here (labeled “N”) correspond to nodes, or phylogenetic divergence events, in Fig. 1.

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