Miocene horse evolution and the emergence of C4

grasses in the North American Great Plains

Adrienne Stroup

EAR 629: Topics in Paleobiology

14 December 2012

Environmental fluctuations in the Tertiary, especially the Miocene epoch, brought

about huge evolutionary changes in North American terrestrial animals. Herbivorous,

hooved mammals, called ungulates, were particularly affected. Odd-toed perissodactyls

and even-toed artiodactyls are the two most abundant orders within the grand order

Ungulata. As the landscape shifted from a mosaic of savanna-like grasslands and forests,

to a predominately open seasonal prairie biome, many changes within and between

artiodactyls and perissodactyls can be seen in the fossil record. With incomparable

completeness, one of the best examples of evolutionary change and adaptation is

illustrated in the perissodactyl family Equidae, to which modern horses belong.

During the late Eocene, a climate shift in the Northern latitudes toward cooler

temperatures and increased seasonality resulted in the extinction of many archaic

mammalian families, and the rise of many modern ones. During this epoch,

perissodactyls hit maximum diversity, but started to decline by the late middle Eocene

(45 Ma). By the end of the Oligocene (23 Ma) only four of the fourteen families

remained, which included horses, tapirs, rhinoceroses, and the now extinct titanotheres

(Janis, 2007). Grasses also started to appear in North America at this time (Wolfe, 1985;

Janis, 1993).

As the climate became more seasonal, the vegetation adapted by becoming more

deciduous, resulting in leaves with less fiber, and therefore more protein (Wing 1998;

Janis et al., 2000). This higher quality vegetation favored artiodactyls, allowing them to

rise to dominance and diversify, thus out-competing perissodactyls. Though this was

roughly a synchronous event, it was not a simple one to one replacement ratio.

Physiological differences in digestion may have aided in this progression. Based on

extant ungulates, artiodactyls are predominately foregut ruminants and perissodactyls are

hindgut fermenters. Ruminants have chambered stomachs that do no utilize fermentation

to digest foodstuffs. In addition, artiodactyls have bunodont cheek teeth, which are low-

crowned with rounded cusps ideal for processing a mixed, non-fibrous diet that would not

require fermentation (Janis, 1989; Janis, et al., 2000). Artiodactyls require vegetation

that is high quality, but due to their slow digestive process, they do not require a large

quantity at any given time. In contrast, perissodactyls can digest larger quantities of

vegetation in less time, allowing them to thrive on lower quality food, as long as there is

an abundance to consume. In this case, plant quality refers to the amount of protein it

contains (Janis et al., 2000).

In addition to seasonality, plummeting levels of atmospheric CO2 were recorded

shortly after the Paleocene Eocene Thermal Maximum at 51 Ma. Between then and 46

Ma these levels fluctuated from 4000 ppm to only 500 ppm. This may have contributed

to the subsequent rise in artiodactyls, as early Tertiary perissodactyls, which thrived on

C3 plants dependent on greater amounts of CO2, struggled to survive on their dwindling

food source (Janis et al., 2000; Janis, 2008).

By the early Miocene (23-16.5 Ma) the climate became warmer and drier than

during the Eocene, with temperatures peaking at 17 Ma, based on stable oxygen isotope

values; however, after a few periods of warming and cooling during the middle Miocene,

temperatures steadily started to drop by 8 Ma (Prothero, 1998). Incidentally, grass

species became more widespread, but general mammalian faunal diversity was on the

decline. The cooler temperature and increased aridity trend continued through the end of

the Miocene when Arctic cold fronts began to affect the productivity of North American

vegetation, acting as a catalyst to promote the diversity and production of C4 grasses

(Wolfe, 1985; Janis, 1993; Wing 1998).

During the late Miocene (7 Ma) a great shift in abundance from C3 to C4

vegetation occurred in North America, often called the “C3/C4 transition.” C3 and C4

refer to two types of photosynthetic pathways in which a plant converts CO2 into either

three or four-carbon chain acids, respectively (Sage, 2004). C3, or the Calvin cycle, is the

most common and successful mode of photosynthesis, with 85% of all modern terrestrial

plants using this type, including trees and shrubs. The C4, or Hatch-Slack cycle, is used

by about 10% of modern terrestrial plants, including tropical and temperate grasses

(MacFadden and Cerling, 1994; Sage, 2004). C4 vegetation evolved in semiarid to arid

climates, and are more adapted to drier environments that would be too harsh for C3

plants. The evolution of the C4 photosynthetic pathway is likely to be an adaptive

response to high rates of photorespiration and carbon deficiency, caused by

environmental factors such as high temperatures, drought, and low CO2 levels. This

adaptation resulted in plants that use water more efficiently than C3 plants. In C4 plants,

the stomata only open during the day, allowing for a quick intake of CO2 into the plant’s

cells, therefore less water is lost (Sage, 2004). These new C4 grasses appeared during the

late Miocene, and continued to be successful into the Plio-Pleistocene (Thomasson et al.,

1988; Janis, 1993; Kemp, 2005). The cold winters of the Plio-Pleistocene favored these

heartier, more seasonal grasses, and the warm savanna grasslands prevalent for most of

the Tertiary gave rise to the modern-day prairie (Janis, 2007). Though overall diversity

of perissodactyls dropped during this time of environmental change, equids successfully

adapted and reached their maximum diversity in the mid-to-late Miocene (Janis et al.,

1989).

The evolutionary history of the horse spans about 55 million years, and has long

been celebrated by 19th century paleontologists as a prime example of evolutionary

gradualism, or orthogenesis; however, more recent studies have proven that it is not that

straightforward (Savage and Long, 1986). It is now understood that the Equidae

phylogeny is actually representative of punctuated equilibrium. This rich and well-

preserved fossil lineage depicts a complex, branching family tree representing long

periods of morphological stability, interrupted with periods of quick evolutionary change

by the middle Miocene, around 16-11 Ma (Evander, 1989; MacFadden, 1992). Within

two to three million years, horses had reached their maximum diversity in North

America, increasing from five to thirteen genera. When viewing the Cenozoic overall, as

many as 35 genera belonged to the Equidae family, which originated in North America

and then radiated out to South America, Europe, Asia and Africa (MacFadden, 1998).

Figure 1 shows many of the equid genera that originated in North America over the

course of the Cenozoic, and provides a rough look at the great success of these animals in

terms of diversity, over a long period of time. The open vertical rectangles represent the

time range for each genus, as recorded in the Paleobiology Database, and the orange

squares indicate specific fossil collections cited in the database. Solid horizontal lines

indicate first and last appearance in the fossil record. At some fossil localities, as many

as twelve sympatric species have been recovered; however, by the end of the Miocene,

diversity declined and today only ten extant species in the genus Equus remain out of

more than thirty unique genera (MacFadden and Cerling, 1994; MacFadden 1998).

Early ungulates were primarily rooters and browsers, foraging in the forested

North American landscape of the early Tertiary (Savage and Long, 1986). One example

is Hyracotherium, also known as Eohippus, which originated in the Eocene. It is the

most primitive known ancestor of horses and all perissodactyls, and was a small cat-sized

mammal with the body mass of only 5-10 kg (MacFadden, 1992; Janis, 2007). Its first

and second upper molars (M1/M2) reached lengths of only 6 to 10 mm, which would be

considered brachydont, or low-crowned (MacFadden, 1998). Unlike later horses,

Hyracotherium had well-developed molars with high cusps, perfect for crushing food like

nuts, seeds and leafy vegetation, as opposed to grinding food back and forth with broad,

flat molars. Based on these data Hyracotherium is considered to be a browser. There is

some debate whether this ungulate actually belongs to the order of Perissodactyla or if it

is actually another type of ungulate called a condylarth. It is no wonder that MacFadden

refers to this genus as an “evolutionary mosaic of phenacodontid condylarth and

perissodactyl character states, as well as more derived states that define it as a member of

the Equidae” (MacFadden, 1992, p. 248). Unique among the Equidae family, this tiny

mammal had four toes on its hind limbs and three on its front limbs (MacFadden, 1992).

From its humble beginnings in the Eocene, horses grew in size and abundance

through the Oligocene, reaching their peak in diversity in the Miocene. Figure 2 shows

sampling coverage for Tertiary rock outcrops, which have been recorded in the

Paleobiology Database. Maps A-D present maps for the Eocene, Oligocene, Miocene and

Pliocene, respectively. Each colored marker represents a collection sample, of which

there are 244 in the Eocene, 79 in the Oligocene, 910 in the Miocene, and 92 in the

Pliocene. This figure gives an idea of how abundant horses were in the Miocene, but

might simply represent over sampled Miocene outcrops. Six representative genera

originating during that time include: Hypohippus, Megahippus, Parahippus,

Merychippus, Pliohippus, and Dinohippus. The first three are browsing forms and the

last three are grazing forms, as inferred by the ontogenetic variation, or crown height, of

their teeth, as well as other morphological changes. These taxa highlight such

morphological attributes and transitional forms within the Equidae family during the

Miocene in North America.

Hypohippus was the largest forest-dwelling horse of the Miocene, possibly

weighing around 600 kg, which is comparable to modern horses. It had brachydont

cheek teeth with upper molars (M1/M2) that measured at 27.5 mm long, and thus it was

likely a browser (Savage and Long, 1986; MacFadden, 1998). Megahippus was another

relatively large browsing horse that also had low-crowned cheek teeth for its size. Its

upper molars were approximately 25 to 27 mm in length. Though in many ways this

horse was primitive, it developed a few morphological attributes that were highly

specialized for browsing, like its distinctive cup-shaped symphysial region with

outwardly angled incisors ideal for nipping off leafy vegetation (MacFadden, 1998).

Typical amongst browsers, these two genera were tridactyl (three-toed) horses.

Another early Miocene tridactyl horse, Parahippus, was an intermediate form of

Merychippus (Savage and Long, 1986). Mesodont, or medium-crowned, cheek teeth

with approximate lengths of 16 mm help define this genus. The first appearance of

hypsodont teeth and reduced lateral side-toes are evident in this transitional genus as well

(MacFadden, 1998). Hypsodonty refers to the high-crowned cheek teeth, which include

the molars and premolars and extend into the sockets below the gum line. The teeth are

also characterized by their complex lophs (ridges) and the presence of cementum around

the roots (MacFadden, 1998).

Merychippus is often considered to be the first grazing horse of the middle

Miocene, which can be determined by its hypsodont dentition, but it may have been a

mixed feeder, eating both grasses and leafy vegetation (Janis et al., 2004). An

approximate length for Merychippus’ upper molars is between 16 and 21 mm. Its

comparatively longer limbs, as well as the reduced size of the ulna and fibula and their

fusion to the radius and fibula, respectively, are also characteristics of this equid (Savage

and Long, 1986; MacFadden, 1992). During a time when the North American landscape

was changing, and vast expanses of grasslands were becoming more prevalent, this

adaptation allowed these horses to out run predators more easily and affectively without

the risk of twisting an ankle or wrist joint. This is something that was not as necessary

for small, forest-dwelling browsers like the most primitive Hyracotherium, who needed

more flexible joints to navigate the uneven terrain of the forest floor (MacFadden, 1998;

Savage and Long, 1986). The three-toed Merychippus was a successful genus, from

which all later horse lineages have evolved, both extinct and extant (Savage and Long,

1986). Comparable to modern African ungulate communities, where a particular species

will be dominant over others in terms of species richness, Merychippus isonesus was a

dominant species in many Miocene locations throughout the North American Great

Plains (Solunias and Semprebon, 2002; Janis et al., 2004).

Though originally considered to be the first true one-toed horse and the precursor

to Equus, Pliohippus is now better understood as a transitional form. Some early

populations are tridactyl with the lateral metapodials greatly reduced, while later

populations are monodactyl horses. Differences in Pliohippus’ skull further differentiate

it from Equus, with the presence of deep depressions called fossae between the eye

socket and the nasal passage. These depressions are absent from modern horse skulls,

and are generally rare in extant mammals (Evander, 1989). Furthermore, the length of its

curved molars ranges between 22-27 mm, and therefore it was a hypsodont, grazing

equid. The curved dentition allowed for the longer teeth to fit in the skull. It should also

be noted that modern horses do not have curved molars as seen in Pliohippus

(MacFadden, 1992, 1998). Finally, Dinohippus gave rise to the extant and only

remaining horse genus, Equus. This genus had hypsodont cheek teeth that were between

26-27 mm long, and were less curved than in Pliohippus. This large monodactyl was

common in the late Miocene (11.6-5.3 Ma) and is a closer relation to the modern horse

based on morphological facial and dental features (MacFadden, 1998).

Though browsing horses, Hypohippus and Megahippus were larger in body mass

than Parahippus, which may account for the longer molar length in these two brachydont

mammals. They also represent the two of the final forms in a dead-end subfamily of

equids known as Anchithereiinae, of which Parahippus is also a part (see Figure 3).

Another subfamily, the Equinae, exists within the Equidae family. This subfamily is

broken down into smaller clades, Equini and Hipparionini. Equini horses are mostly

monodactyls, like Pliohippus and Dinohippus, whereas Merychippus belongs to the

Hipparionini clade. Hipparion horses were tridactyls with reduced lateral side-toes, had

characteristically complex enamel patterns on their hypsodont teeth, and were rather

abundant in the Miocene (Savage and Long, 1986). When observing Parahippus,

Merychippus, Pliohippus and Dinohippus, there is a steady increase in crown height over

time from one genus to the next (MacFadden, 1992, 1998).

Perissodactyls are also known by another name, Mesaxonia, and are defined by

the axis of symmetry running through their odd-toed feet, where the middle or third digit

is their weight-bearing toe. Most perissodactyls have three toes, but modern horses have

evolved into monodactyls. Horses have lost the need for their side hooves, the second

and fourth digits, since one hoof is an extremely successful adaptation for outrunning

predators on the hard ground of the open grassland (Savage and Long, 1986). An

interesting side note, the second and fourth digits can be seen on embryonic horses, as a

remnant of their distant three-toed relatives, but are obviously not visible on full-grown

adults (Evander, 1989).

From Hyracotherium to Equus, the development of hypsodont dentition resulted

in dramatic cranial changes, with the increased length of the preorbital facial region and a

deeper jaw to accommodate larger masseter muscles for processing tougher, more

abrasive silica-rich grasses (MacFadden, 1998; Janis, 2007, 2008). Changes in cranial

proportion were not gradual, and the most drastic lengthening of the preorbital region

occurred in the early Miocene (23-16 Ma), particularly in Parahippus, which is quite

apparent in comparison to the Oligocene horse, Miohippus, and the middle Miocene

Merychippus. In addition to an extended facial structure, equid skulls underwent many

other morphological changes as well during this time (MacFadden, 1992). Along with

these adaptations, hypsodont teeth with more complex lophs indicate a change in equid

diet. Throughout the literature, equid tooth morphology has been a classic indicator of the

changing paleoecology of the Miocene; however, hypsodonty occurred before the C3/C4

transition, around 18 Ma (MacFadden, 1992). What can explain this discontinuity in the

classical understanding of horses adapting to grasslands?

New research focused on fossil herbivore tooth enamel, has proven that teeth are

not just taxonomic identifiers, but may provide new insight on plant productivity and the

relationship between horses and the C3/C4 transition, which cannot be easily inferred

through floral macrofossils alone (Wing, 1998; Janis et al., 2000). A recent area of

research focuses on the microscopic wear on ungulate tooth enamel. Different types of

vegetation will create distinct scratches on a tooth’s chewing surface, thus better

indicating the animal’s diet, particularly its last meal (MacFadden, 1998; Solounias and

Semprebon, 2002). Enamel microwear analysis can help paleobiologists learn what plant

species existed in a given region like the Great Plains, when floral macrofossil evidence

is absent, and better understand the role these species played in their ecosystem.

Observed wear patterns include scratches, cross hatching, pits and gouges.

Patterns in Tertiary horses were compared with patterns of extant browsing and grazing

ungulates, and the results have both confirmed and contradicted previously accepted

knowledge. Analysis determined that Hyracotherium was indeed a browser because of

its similar wear patterns compared to modern seed and fruit eating browsers.

Surprisingly, the hypsodont Dinohippus was also determined to be a browser. New

research suggests that crown height may not be as closely related to diet as previously

thought. It is now believed that hypsodont dentition in ancient ungulates may indicate a

paleoecological change, though not necessarily one directly related to plants. When

observing modern ungulates, research has shown an inverse correlation between higher

crowned teeth and low precipitation levels, in that hypsodont ungulates are more

common in arid climates (Damuth et al., 2002; Janis, 2008). Fossil evidence suggests

hypsodonty emerged roughly around the same time as the highest recorded peaked in

temperature at 17 Ma, thus supporting the overall drying trend that occurred during the

Miocene. It should be noted that hypsodont ungulates are adapted, but not limited, to

grazing alone, and microwear analysis is particularly helpful in distinguishing the grazers

from the mixed feeders (Janis, 2008). Lastly, this adaptation would continue to be

advantageous later in the Miocene when horses fed on silica-rich C4 grasses (MacFadden

et al., 1999; Solounias and Semprebon, 2002). Enamel microwear analysis is not the only

type of dental research that may demonstrate the relationship between horses and grass.

Not only do C3 and C4 plants photosynthesize differently, they also combine

stable carbon isotopes, like δ13C and δ12C, in different amounts. Studies performed on

equid teeth have shown that δ13C values can be extracted from pulverized enamel,

indicating whether the animal consumed C3 or C4 vegetation. Compared to fossilized

bone, which contains more organic compounds like collagen, enamel is a much better

source from which isotope values can be drawn, since the values are not depleted through

diagenesis. The chemical makeup of enamel, which is basically calcium phosphate

(CaPO4), insures enough stable carbon will replace the phosphates during fossilization,

resulting in about 1% of the overall mass. Carbonate gas is extracted from the enamel

sample, and finally mass spectrometers are employed to record the δ13C values

(MacFadden and Cerling, 1994). A positive shift in δ13C values from 12-15% in the

enamel correlate with isotope levels in soil carbonate samples and prove that horses were

grazing on C4 grasses in the late Miocene (MacFadden, 1994; Wing, 1998; Janis et al.,

2000).

The literature on horse evolution is exceedingly rich due to the veritable

completeness of their fossil record, but inevitable gaps in the record create a sampling

bias, which must always be taken into account when interpreting data. An absolutely

accurate representation of the diversity and abundance of ancient life is impossible to

attain. Terrestrial vertebrate fossils are considerably rarer than marine invertebrates, due

to many factors. David M. Raup describes these factors as “filters” that affect a fossil’s

preservation (1972). These filters range from biological constraints on an organism (e.g.

soft bodied worms are less likely to be preserved than hard bodied clams) to geologic

processes (e.g. fossils may be destroyed in the metamorphic process of transforming

fossiliferous limestone to marble) among others. Because of the abundant evidence

collected, especially in terms of transitional forms, it appears that these filters have not

greatly affected the equid fossil record. The superb preservation and profusion of equid

fossils give researchers an excellent foundation for understanding not only this family of

mammals but also provides insight into the paleoecology of the Tertiary in general.

Many aspects of the evolution of horses are more complex than originally

thought. While advances in the field of paleobiology, such as enamel microwear and

stable carbon isotope analyses, have proven this, society has long favored the straight-line

phylogeny and simplistic view of equid adaptations from smaller to larger, three toes to

one toe, and low-crowned teeth to high-crowned teeth. MacFadden explains this

phenomena, writing that “Even today orthogenesis goes hand in hand with simplification

because together they provide such an elegant interpretation of the almost impossibly

complex evolution of the Equidae” (1992, p. 47). Hypsodonty was an evolutionary

adaptation in horses originally thought to be a direct result of the rise of grasses in North

America, but like other aspects of equid evolution, it is not that simple. The C3/C4

transition happened after hypsodont dentition was dominant in horses. Though this

adaptation occurred before the rise of abrasive C4 grasses, hypsodonty would still have

been favorable in these ungulates, which surpassed the dwindling perissodactyls to

become one of the most dominate and diverse families of the Miocene epoch.

Appendix - Figures

Figure 1. Analysis of taxonomic ranges of North American equid genera plotted against the Cenozoic North American Land Mammal Ages. The data were downloaded on 30 November, 2012 from the Paleobiology Database, using the Strauss and Sadler (1989) Confidence Interval Method.

Figure 2. - The sampling occurrences of the family Equidae in the United States throughout the Tertiary. The data were downloaded from the Paleobiology Database on 8 December, 2012, using the group name ‘mammals’ and the following parameters: time intervals = Paleocene, Eocene, Oligocene, Miocene Pliocene, country = United States, taxon = Equidae

Figure 3. Phylogeny of the Equidae family. Shaded areas indicate browsing taxa, where stippled areas indicate grazing taxa (MacFadden, 1992)

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