Grass evolution and the fossil record

Introduction

The fossil record of grasses begins in the late Early Cretaceous (about 145 to 100.5 million years ago) and extends to the recent. It includes macrofossils (fossils that can be seen without a microscope), although most of the record consists of microfossils, such as pollen, phytoliths, and epidermal fragments. In the Cretaceous (about 145 to 66 million years ago) and Paleogene (about 66 to 23 million years ago), the record is sparse, although it does tell us two things: 1) grasses were present, even if they were not as dominant in some ecosystems as they are today, and 2) the major groups of grasses were diversifying as early as the Cretaceous. In the Neogene (about 23 to 2.6 million years ago), the fossil record of grasses explodes, reflecting changes in global climate that favored the expansion of open habitats. Data from grass fossils is supplemented by data from animal fossils and isotopes to give a picture of the evolution of grasslands through time.

Today, much of the world is covered by grasslands and/or tropical savannas (a type of habitat with scattered trees among grasses), including large parts of every continent except Antarctica and Europe (which still has grasslands in the southeast).

Cretaceous (145 to 66 million years ago)

Grasses evolved into a landscape ruled by dinosaurs, conifers, cycads, and flowering plants. Fossilized pollen grains reveal that angiosperms (seed-bearing plants that have flowers) diverged from gymnosperms (seed-bearing plants that do not have flowers) by at least the Early Cretaceous, which began 145 million years ago. The earliest credible angiosperm macrofossils, like Archaefructus liaoningensis and Montsechia vidalii, date to the Early Cretaceous (as old as about 130 to 125 million years ago). Angiosperms continued to diversify throughout the Cretaceous period, co-evolving with the insects that pollinated them. By the end of the Cretaceous, they had begun to dominate the landscape.

Grasses (the Grass Family or Poaceae) descend from a single common ancestor. The first grasses are thought to have evolved in the Early Cretaceous, based on fossil evidence. At that time, the Earth's southern continents—South America, Antarctica, Africa, Australia, and the Indian subcontinent—were joined together in a supercontinent called Gondwana; the northern continents—North America, Europe, and Asia (minus India)—were grouped into a supercontinent called Laurasia.

The oldest grass fossils date to the late Early Cretaceous and are about 113 to 101 million years old. These fossils are fragments of grass-like epidermis and phytoliths that were found on the teeth of a hadrosaur (duck-billed dinosaur) from China. These early fragments are thought to represent basally diverging grasses, and could even represent completely extinct groups of early grasses.

The oldest known grass macrofossils come from Late Cretaceous Burmese amber and are estimated to be about 110 to 94 million years old. These fossils include an unnamed grass spikelet infected with an ergot-like fungus and fossils assigned to the genus Programinis, including a spikelet (Programinis burmitis) and a leaf fragment (Programinis laminatus). Grass-like silica bodies (phytoliths) have been found in the leaf fragment, cementing its identity as a grass. As with the grass fossils from China, these fossils may represent completely extinct grasses.

The ancestor of all living grasses is thought to have lived on Gondwana, and by the Late Cretaceous (100.5 to 66 million years ago) much of the grass fossil record is from Gondwanan continents. Grass phytoliths found in the coprolites (fossilized dung) of sauropod dinosaurs (long-necked dinosaurs) dating from the very end of the Cretaceous (72 to 66 million years ago) have been found in India. Some of the phytoliths came from grasses in the BOP and PACMAD clades (the two largest groups of grasses), indicating that grasses had already partially diversified by the end of the Cretaceous. 

Possible grass pollen (pollen assigned to the genus Monoporites) has been found in Africa, India, and South America near the end of the Cretaceous, indicating that grasses were present on several continents by that time.

Paleogene (66 to 23 million years ago)

During the Paleocene (66 to 55 million years ago) to Eocene (about 55 to 34 million years ago) epochs, Earth's continents were getting closer to their present positions, although land bridges in the North Atlantic and North Pacific connected Eurasia and North America, and land bridges across the Southern Ocean connected Antarctica to both Australia and South America. (Note that these "land bridges" may have been interrupted by water, but the land masses were close enough that plants could disperse among them more easily than they can today.) Thus, plants were still able to expand their ranges across these adjoining continents. The Earth's global temperature was very warm in the late Paleocene to early Eocene, and cold-sensitive plants and animals could be found at high latitudes because the Earth's poles were much warmer than they are today.

Following their peak in the early Eocene, global temperatures cooled into the beginning of the Oligocene epoch (34 to 23 million years ago). Grasslands began to develop as early as the Eocene in North America, with open grasslands starting to replace forests beginning in the late Oligocene (about 26 million years ago). Evidence suggests that this change was driven by drying of the climate in North America, particularly during the winter season. The shift to grasslands took place later in Africa and Australia.

Grass pollen records are sparse during the Paleocene, occurring in South America, Africa, and India. Eocene pollen records indicate that grasses were widely distributed, found in North America, South America, Africa, Australia, Europe, and the eastern part of Asia. Phytolith records come mostly from the Americas and Turkey, and indicate that bamboos, pooids (cool-season grasses), and PACMADs were present.

Grass macrofossils from the Eocene to Oligocene are relatively rare. Compression fossils of grass spikelets containing pollen are known from the lower Eocene Wilcox Formation in Tennessee, U.S.A. Another report from North America is from the late Eocene Florissant flora of Colorado, U.S.A.; this report is of fruits assigned to the species Stipa florissantii. Stipa is a modern genus, and it is unclear if the Florissant grass really belongs within it. Additional scattered reports are known from the western U.S. and likely require further investigation.

In Europe, the spikelet Eograminis balticus has been found in Baltic amber (a European deposit), which probably dates to the Eocene. Eograminis is similar to moor grass (Molinia) in subfamily Arundinoideae of the PACMAD clade; modern members of this subfamily include the common reed (Phragmites australis) and the giant reed (Arundo donax). Other possible grass fossils found in Baltic amber are now considered doubtful.

In South America, a macrofossil of Chusquea, a type of bamboo that occurs today from Mexico to South America and in the Caribbean, has since been identified as a conifer branch with leaves. 

Neogene (23 to 2.6 million years ago)

Spread of grasslands

The fossil record of grasses is much richer in the Neogene (23 million years ago to 2.6 million years ago), reflecting changes in global climate, particularly global cooling and the drying of continental interiors. Events like the initiation of the Antarctic Circumpolar Current near the Eocene-Oligocene boundary, the uplift of the Himalayas in the Neogene, and the closure of the Isthmus of Panama about 3.5 million years ago contributed to global cooling. In South America, the uplift of the Andes mountain range played an important regional role, casting a rain shadow to the east.

Grasses thrived in these new drier and cooler habitats, dominating areas that were now too dry to sustain forests. Open, grass-dominated habitats began to appear, and grassland biomes became widespread in the late Neogene. During the later part of the Neogene, there was also a shift to increasing prevalence of C4 grasses in grasslands, as evidenced by stable carbon isotope data, mostly from paleosols and ungulate tooth enamel. C4 grasses thrive in drier and hotter climates than cool-season (C3) grasses.

The first evidence of C4-dominated grasslands is from Kenya and Uganda in eastern Africa, at about 21 to 16 million years ago. The inference that C4 grasses were present comes from phytoliths, stable carbon isotope analyses, and other types of data. Most global evidence for widespread dominance of C4 grasslands is less than 10 million years old. 

There are various hypotheses explaining the shift from the predominance of C3 to C4 grasses in the Neogene. One hypothesis is that the relatively frequent fires associated with grasses (and, specifically, C4 grasses) acted as a positive feedback mechanism, thereby further increasing C4 grass abundance. Grassland-fire feedbacks are generally seen as a major stimulator of C4 grass-dominated ecosystems and function to maintain and even spread grasslands today.

A decline in atmospheric carbon dioxide (CO₂) occurred around the same time as this vegetation shift. While scientists previously believed that this decline was caused by an increase in C4 photosynthesis that drew down the amount of carbon dioxide in the Earth's atmosphere, they now more commonly think that the drop in atmospheric carbon dioxide caused a shift to more C4 photosynthesis. C4 photosynthesis shuttles carbon dioxide into specialized bundle sheath cells in the leaf, which reduces photorespiration, the wasteful use of an oxygen molecule rather than a carbon dioxide molecule during the photosynthetic process. C4 plants are therefore more efficient at using of carbon dioxide during photosynthesis than C3 plants, and lower concentrations of atmospheric carbon dioxide may have favored plants with C4 photosynthesis.

During the Pliocene (5.3 to 2.6 million years ago), the climate became increasingly cold and arid, facilitating the expansion of grasslands in low-latitude areas. The Pliocene saw further increases in the expansion of C4-dominated vegetation on almost all continents. 

Neogene grass fossil record

The Neogene fossil record of grasses is significantly richer than the Cretaceous to Paleogene records in the abundance of reports. Fossil evidence of grasses comes from from every continent, including Antarctica. While pollen and phytolith records remain important, multiple macrofossil records are also documented from western North America (more specifically, the United States west of the Mississippi river), Europe, and eastern Africa, with a few additional records from South America, western Africa, eastern North America, and even northern Canada. Many Neogene records are simply assigned to the Grass Family (Poaceae), although some can be assigned to large subgroups (such as PACMADs), subfamilies, or even genera of grasses.

An interesting Miocene (23 to 5.3 million years ago) record comes from the Dominican Republic amber Lagerstattë (fossil deposit with exceptional preservation). It is a grass spikelet (Pharus primuncinatus) assigned to Pharus, a living genus of grasses sometimes called stalkgrasses that are found today in the subtropical to tropical Americas. The fossil spikelet has hook-like hairs and was preserved in the same piece of amber as a few strands of mammal hair, providing plausible evidence of epizoochory (dispersal of a seed or fruit on the outside of an animal's body, for example by gripping a mammal's hair). A spikelet of an extinct bamboo (Alarista succina) comes from the same deposit.

The earliest origins of C4 photosynthesis are estimated to date back to the Oligocene based on molecular dating techiques. Stable isotope analysis of fossil grass pollen also supports the appearance by C4 grasses by the Oligocene. The earliest evidence for C4 grass-dominated habitats is from the early Miocene of Africa (discussed above).

The earliest known C4 grass macrofossils, however, are from the late Miocene. One comes from the Miocene Dove Spring Formation, California, U.S.A., and is about 12.5 to 8 million years old; the other comes from the Miocene Ogallala Formation of Kansas, U.S.A., and is about 7 to 5 million years old. These fossil grasses have anatomical (cellular) preservation that shows the characteristic Kranz anatomy of C4 grass leaves. Kranz, meaning wreath, refers to the concentric arrangement of the mesophyll cells around the vascular bundles in C4 grasses when they are viewed in cross section.

Pleistocene to recent grasslands (2.6 million years ago to present)

During the Pleistocene, polar ice caps formed in the Northern Hemisphere and spread southward multiple times, alternately covering and exposing the northern parts of North America and well as some parts of northern Eurasia. As today, an ice sheet also covered Antarctica. Alpine glaciers were more extensive than they are today. Large parts of the globe were covered by grasslands, including tropical grassland savanna and steppes. 

A unique feature of the Pleistocene is the mammoth-steppe or steppe-tundra biome, which was, at the time of the last glacial maximum (about 26,000 to 19,000 years ago), the world’s most extensive biome. The mammoth-steppe was a grass-dominated ecosystem. Various lines of evidence, including macrofossils, phytoliths, and stable isotopes, show an abundance of graminoids (grasses and grass-like plants) in this biome. Additionally, grass DNA preserved in permafrost has provided evidence of specific species growing in high northern latitudes during the Pleistocene.

As the Earth warmed, the glaciers receded following the last glacial maximum, and land that was formerly covered by ice was exposed. Eventually, grasslands and savannas assumed their present distributions. Near the end of the Pleistocene to the early Holocene, around 10,000 years ago or even earlier, humans began to cultivate and domesticate grasses. In the modern world, many grasslands have been severely disturbed or completely replaced by fields of cultivated plants, livestock grazing, and development.