Leaf evolution in Southern Hemisphere conifers tracks the angiosperm ecological radiation

Abstract

The angiosperm radiation has been linked to sharp declines in gymnosperm diversity and the virtual elimination of conifers from the tropics. The conifer family Podocarpaceae stands as an exception with highest species diversity in wet equatorial forests. It has been hypothesized that efficient light harvesting by the highly flattened leaves of several podocarp genera facilitates persistence with canopy-forming angiosperms, and the angiosperm ecological radiation may have preferentially favoured the diversification of these lineages. To test these ideas, we develop a molecular phylogeny for Podocarpaceae using Bayesianrelaxed clock methods incorporating fossil time constraints. We find several independent origins of flattened foliage types, and that these lineages have diversified predominantly through the Cenozoic and therefore among canopy-forming angiosperms. The onset of sustained foliage flattening podocarp diversification is coincident with a declining diversification rate of scale/needle-leaved lineages and also with ecological and climatic transformations linked to angiosperm foliar evolution. We demonstrate that climatic range evolution is contingent on the underlying state for leaf morphology. Taken together, our findings imply that as angiosperms came to dominate most terrestrial ecosystems, competitive interactions at the foliar level have profoundly shaped podocarp geography and as a consequence, rates of lineage diversification.

Hemisphere-scale differences in conifer evolutionary dynamics

“…Our estimated divergence ages generally agree with results from published studies focusing on Podocarpaceae (15) and Pinaceae (23; in the conservative version of their calibrations), although they are considerably younger than a recently published study of Cupressaceae (24). The discrepancy in age estimates most likely results from differences in the implementation of prior age distributions, because both studies used a similar set of fossils as minimum age constraints.…”

“…This phylogeny is based on a molecular dataset including two nuclear genes (18S and a phytochrome gene, PHYP) and two chloroplast genes (matK and rbcL). A maximum-likelihood (ML) tree topology, which agrees well with previously published phylogenetic studies of conifers (e.g., [12][13][14][15][16], was used as a constraint topology for inferring the dated phylogeny. Divergence times were estimated using a Bayesian implementation of an uncorrelated lognormal relaxed clock model with fossil calibration points used as minimum age constraints (Materials and Methods).…”

Distribution of living Cupressaceae reflects the breakup of Pangea

“…Previous studies of gymnosperm radiations mostly have inferred Oligocene-age crown groups (14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26), and a recent meta-analysis found a median crown age for gymnosperm genera of 32 Ma, younger than that found for angiosperm genera (25). Our dating of those genera with more than one species in the Cupressaceae similarly suggests relatively recent diversifications (Fig.…”

Cenozoic climate change shaped the evolutionary ecophysiology of the Cupressaceae conifers

“…As might be expected, the subsequent distribution of plants and animals changed dramatically (5-7), leading to the development of entirely new biomes, such as grasslands (8) and cactus-dominated deserts (9). Other groups of plants became restricted to habitats that reflected the previous tropical conditions of their ranges (10,11). However, it is rare to find groups that reflect adaptation to both the Cretaceous-Early Paleogene greenhouse and the cooler, drier post-Eocene world.…”

“…In the southern hemisphere for example, members of the Podocarpaceae were subject to selective pressures arising from increasing aridity as well as greater ecological competition from angiosperms (10,11,39). Several of the drought-intolerant Podocarp lineages disappeared during the mid-to-late Cenozoic, and others found refugia in mesic tropical forests by evolving flattened leaves that allowed them to compete with angiosperms for light (10,11,39). Although the Podocarpaceae retreated, we speculate that Callitroid lineages may have succeeded in colonizing available arid habitats.…”