C4 photosynthesis promoted species diversification during the Miocene grassland expansion.

Elizabeth L Spriggs,Pascal-Antoine Christin,Erika J Edwards,Robin Allaby

doi:10.1371/journal.pone.0097722

Elizabeth L Spriggs, Pascal-Antoine Christin + Show 2 more

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https://doi.org/10.1371/journal.pone.0097722

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Journal: PloS one	Publication Date: May 16, 2014
Citations: 108	License type: CC BY 4.0

Affiliation: Brown University, Providence College

Abstract

Identifying how organismal attributes and environmental change affect lineage diversification is essential to our understanding of biodiversity. With the largest phylogeny yet compiled for grasses, we present an example of a key physiological innovation that promoted high diversification rates. C4 photosynthesis, a complex suite of traits that improves photosynthetic efficiency under conditions of drought, high temperatures, and low atmospheric CO2, has evolved repeatedly in one lineage of grasses and was consistently associated with elevated diversification rates. In most cases there was a significant lag time between the origin of the pathway and subsequent radiations, suggesting that the ‘C4 effect’ is complex and derives from the interplay of the C4 syndrome with other factors. We also identified comparable radiations occurring during the same time period in C3 Pooid grasses, a diverse, cold-adapted grassland lineage that has never evolved C4 photosynthesis. The mid to late Miocene was an especially important period of both C3 and C4 grass diversification, coincident with the global development of extensive, open biomes in both warm and cool climates. As is likely true for most “key innovations”, the C4 effect is context dependent and only relevant within a particular organismal background and when particular ecological opportunities became available.

Highlights

IntroductionThe grasses (Poaceae) are a remarkable clade, in terms of both species richness and ecological breadth
Within flowering plants, the grasses (Poaceae) are a remarkable clade, in terms of both species richness and ecological breadth
All of the BiSSE tests on the BEAST maximum credibility tree strongly rejected the model of equal diversification rates for C3 and C4 taxa

Summary

Introduction

The grasses (Poaceae) are a remarkable clade, in terms of both species richness and ecological breadth. Grasses living in tropical and subtropical grassland or savanna systems almost exclusively utilize the C4 photosynthetic pathway [1,2,3] This trait is a complex modification over the ancestral C3 pathway that confers an advantage in open, hot, and dry conditions by concentrating CO2 inside plant cells and preventing high levels of photorespiration [4]. All of the 22–24 C4 origins occur within the PACMAD clade, while the sized BEP is entirely C3 [5,6,7,8,9,10] This clustering of all C4 origins in one of the two major grass lineages may be partly due to increased evolutionary accessibility to the C4 trait in this clade, based on a shared set of leaf anatomical attributes [11]

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