C4 Photosynthesis Promoted Species Diversification during the Miocene Grassland Expansion

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.

The recent and rapid spread of Themeda triandra

“…Based on our dating analyses, the divergence between Themeda and its sister group occurred at 7.98 Ma (95% HPD 5.01-12.78), which is largely congruent with previous estimates (Estep et al 2014;Spriggs, Christin, and Edwards 2014). Within Themeda, the divergence of T. triandra from its sister group (T. arguens) occurred at 3.50 Ma (95% HPD 2.16-5.02 Ma) and the first divergence within T. triandra (crown node) at 1.48 Ma (95% HPD 0.79-3.45; Figure 2).…”

Climate change is projected to outpace rates of niche change in grasses

“…We used three time-calibrated molecular phylogenies to identify sister species and estimate rates of niche change. We used a phylogeny of 1230 grass species (Tree 2010 hereafter; [13]) and two phylogenies of 3595 grass species (Trees 2014 -1, 2014 -2; [2]). All trees were estimated from both chloroplast and nuclear sequences, but were calibrated differently.…”

“…The grasses (Poaceae) are a diverse (more than 11 000 species; [2]) and broadly important plant family. Natural grasslands cover approximately 25% of Earth's land area [3], and are habitats for many endemic plant and animal species (e.g.…”

Examining plant physiological responses to climate change through an evolutionary lens

“…In grasses, sedges, and eudicots, the origins of C 4 photosynthesis date to the Oligocene through the Miocene (Besnard et al, 2009;Christin et al, 2011;Spriggs et al, 2014). In bromeliads, orchids, and Euphorbia spp., origins of CAM photosynthesis date from the early Miocene to the late Pliocene (Horn et al, 2014;Silvestro et al, 2014;Bone et al, 2015).…”