Decoupled taxonomic radiation and ecological expansion of open-habitat grasses in the Cenozoic of North America

Abstract

Because of a dearth of Cenozoic grass fossils, the timing of the taxonomic diversification of modern subclades within the grass family (Poaceae) and the rise to ecological dominance of open-habitat grasses remain obscure. Here, I present data from 99 Eocene to Miocene phytolith assemblages from the North American continental interior (Colorado, Nebraska, Wyoming, and Montana͞Idaho), constituting the only high-resolution midCenozoic record of grasses. Analyses of these assemblages show that open-habitat grasses had undergone considerable taxonomic diversification by the earliest Oligocene (34 million years ago) but that they did not become ecologically dominant in North America until 7-11 million years later (Late Oligocene or Early Miocene). This pattern of decoupling suggests that environmental changes (e.g., climate changes), rather than taxonomic radiations within Poaceae, provided the key opportunity for open-habitat grasses to expand in North America.grasslands ͉ phytoliths ͉ Great Plains G rasses are today of immense importance, both ecologically, in the form of grass-dominated vegetation (e.g., steppes and savannas), and economically, as cereals and feed for domesticated animals. The evolution of grasses and grasslands played a fundamental role in the formation of modern ecosystems and has captured the attention of botanists, geologists, and paleontologists alike (1). Still, despite over a century of research, the evolutionary history of the grass clade is largely unknown. Pollen data from northern Gondwana may indicate a Late Cretaceous or Paleocene origin of Poaceae [70-55 Ma (million years ago) (2, 3)], and unequivocal graminoid reproductive structures from Early Eocene deposits reveal that crown-group grasses existed in North America from this time onward (4, 5). However, for most of the Cenozoic, the fossil record of grasses is extremely poor, providing little insight into taxonomic diversification patterns within the family (1). Abundant and diverse grass fossils (e.g., pollen, leaves, and reproductive structures) do not appear until the Middle to Late Miocene, pointing to a scenario of ongoing taxonomic diversification within Poaceae in tandem with a successive spread of grass-dominated vegetation during this time (1, 6). A roughly simultaneous taxonomic proliferation and rise to ecological dominance of the grass family long after its origin is thought to have been stimulated by changes in global and regional climates toward increased seasonal aridity during the Neogene (7-9).Other lines of evidence are partly or fully at odds with this scenario. Molecular phylogenetic dating within the grass family, which is complicated by the non-clock-like behavior of the genes used (5, 10), has led to the suggestion that the main taxonomic diversification of modern grass subclades [e.g., Pooideae and PACCAD (Panicoideae, Arundinoideae, Chloridoideae, Centothecoideae, Aristidoideae, and Danthonioideae)] occurred sometime between 25 and 15 Ma (10). However, other molecular clock estimates indicate that these grou...

Decoupling the spread of grasslands from the evolution of grazer-type herbivores in South America

“…The presence of members of the Pooideae and PACMAD clades at Gran Barranca from at least 38 Myr ago agrees with previous phytolith work in Patagonia 10,45 , adding to the body of evidence that open-habitat grasses diversified prior to the EOT 14,46,47 . Thus, the rise to ecological dominance of openhabitat grasses lagged taxonomic diversification by at least 20 million years in southern South America.…”

“…This decoupling ARTICLE parallels the North American record 14 , suggesting that it reflects an evolutionary/ecological phenomenon rather than incomplete fossil records; similar patterns have been recorded in C 4 grasses 14 and several other organisms, such as early flowering plants and certain insect groups 48,49 . If true, the lag implies that different factors influenced pooid and PACMAD diversification versus ecological expansion 14 . What environmental (or other) changes allowed open-habitat grasses to become more abundant albeit not ecologically dominant in the Miocene of Gran Barranca?…”

“…Phytoliths were classified according to Strömberg 7,14 , using literature and a reference collection of phytoliths from modern plants (1,000 samples from 4500 taxa of vascular plants) (Supplementary Table S5). Some of our morphotypes correspond to morphotypes in the system used in previous studies of the Cenozoic of Patagonia 10,45 , initially devised by Bertoldi de Pomar 55 and expanded by subsequent workers 10 .…”

“…Diagnostic phytoliths are in classes PALM, ZINGI, other FI, CH TOT, POOID-D, POOID-ND, PAN, CHLOR, PACMAD general, OTGH and AQ (Supplementary Tables S4 and S5), although note that AQ is not included in vegetation analysis (ref. 14). In addition, a set of tall bilobates and polylobates with faceted, slightly irregular tops were grouped under Danthonioideae?/Bambusoideae?…”

“…We analysed these assemblages following the methods of Strömberg 14 to make them directly comparable to phytolith records in North America and Eurasia 7,14 . Phytolith assemblage analysis provides information about vegetation type, specifically the relative abundances and types of grasses.…”