Miocene horse evolution and the emergence of C 4. grasses in the North American Great Plains
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1 Miocene horse evolution and the emergence of C 4 grasses in the North American Great Plains Adrienne Stroup EAR 629: Topics in Paleobiology 14 December 2012
2 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
3 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 lowcrowned 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 CO 2 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 C 3 plants dependent on greater amounts of CO 2, struggled to survive on their dwindling food source (Janis et al., 2000; Janis, 2008). By the early Miocene ( 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
4 vegetation, acting as a catalyst to promote the diversity and production of C 4 grasses (Wolfe, 1985; Janis, 1993; Wing 1998). During the late Miocene (7 Ma) a great shift in abundance from C 3 to C 4 vegetation occurred in North America, often called the C 3 /C 4 transition. C 3 and C 4 refer to two types of photosynthetic pathways in which a plant converts CO 2 into either three or four-carbon chain acids, respectively (Sage, 2004). C 3, 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 C 4, or Hatch-Slack cycle, is used by about 10% of modern terrestrial plants, including tropical and temperate grasses (MacFadden and Cerling, 1994; Sage, 2004). C 4 vegetation evolved in semiarid to arid climates, and are more adapted to drier environments that would be too harsh for C 3 plants. The evolution of the C 4 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 CO 2 levels. This adaptation resulted in plants that use water more efficiently than C 3 plants. In C 4 plants, the stomata only open during the day, allowing for a quick intake of CO 2 into the plant s cells, therefore less water is lost (Sage, 2004). These new C 4 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
5 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 19 th 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 wellpreserved 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 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).
6 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
7 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
8 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
9 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 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 mm long, and were less curved than in Pliohippus. This large monodactyl was common in the late Miocene ( 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,
10 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 C 3 /C 4
11 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 C 3 /C 4 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
12 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 C 4 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 C 3 and C 4 plants photosynthesize differently, they also combine stable carbon isotopes, like δ 13 C and δ 12 C, in different amounts. Studies performed on equid teeth have shown that δ 13 C values can be extracted from pulverized enamel, indicating whether the animal consumed C 3 or C 4 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 (CaPO 4 ), 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 δ 13 C values (MacFadden and Cerling, 1994). A positive shift in δ 13 C values from 12-15% in the enamel correlate with isotope levels in soil carbonate samples and prove that horses were grazing on C 4 grasses in the late Miocene (MacFadden, 1994; Wing, 1998; Janis et al., 2000).
13 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
14 America, but like other aspects of equid evolution, it is not that simple. The C 3 /C 4 transition happened after hypsodont dentition was dominant in horses. Though this adaptation occurred before the rise of abrasive C 4 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.
15 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.
16 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
17 Figure 3. Phylogeny of the Equidae family. Shaded areas indicate browsing taxa, where stippled areas indicate grazing taxa (MacFadden, 1992)
18 References Damuth, J.D., Fortelius, M., Andrews, P., Badgley, C., Hadley, E.A., Hixon, S., Janis, C., Madden, R.H., Reed, K., Smith F.A., Theodor, J., Van Dam, J.A., Van Valkenburgh, B, Werdelin, L., 2002, Reconstructing mean annual precipitation based on mammalian dental morphology and local species richness: Journal of Vertebrate Paleontology, v. 22 (suppl) no. 48A Evander, R.L., 1989, Phylogeny of the family Equidae, in Prothero, D.R., and Schoch, R.M., ed., The evolution of perissodactyls: New York, Clarendon Press (and Oxford University Press), p Janis, C.M., 1989, A climatic explanation for patterns of evolutionary diversity in ungulate mammals: Palaeontology, v. 32, no. 3, p Janis, C.M., 1993, Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events: Annual Review of Ecology and Systematics, v. 24. p Janis, C.M., Scott, K.M., and Jacobs, L.L. ed., 1998, Evolution of Tertiary mammals of North America, Volume 1: terrestrial carnivores, ungulates, and ungulatelike mammals: Cambridge, Cambridge University Press. Janis, C.M., Damuth, J., and Theodor, J.M., 2000, Miocene ungulates and terrestrial primary productivity: Where have all the browsers gone?: Proceedings of the National Academy of Sciences of the United States of America, v. 97, no. 14, p Janis, C.M., Damuth, J., and Theodor, J.M., 2004, The species richness of Miocene
19 browsers, and implications for habitat type and primary productivity in the North American grassland biome: Palaeogeography, Palaeoclimatology, Palaeoecology, v.207, p Janis, C.M., 2007, Artiodactyl Paleoecology and Evolutionary Trends, in Prothero, D.R. and Foss, S.E. ed., The evolution of artiodactyls: Baltimore, The John Hopkins University Press, p Janis, C.M., 2008, An evolutionary history of browsing and grazing ungulates, in Gordon, I.J. and Prins, H.H.T. ed., The ecology of browsing and grazing: Springer-Verlag Berlin Hiedelberg, p Kemp, T.S., 2005, The origin and evolution of mammals: Oxford, Oxford University Press. MacFadden, B.J., 1992, Fossil horses: systematics, paleobiology, and evolution of the family Equidae: Cambridge, Cambridge University Press. MacFadden, B.J., and Cerling, T.E., 1994, Fossil horses, carbon isotopes and global change: Trends in Ecology and Evolution, v. 9, no. 12, p MacFadden, B.J., 1998, Equidae, in Janis, C.M., Scott, K.M., and Jacobs, L.L. ed., Evolution of Tertiary mammals of North America, Volume 1: terrestrial carnivores, ungulates, and ungulatelike mammals: Cambridge, Cambridge University Press, p MacFadden, B.J., Solounias, N., and Cerling, T.E., 1999, Ancient diets, ecology and extinction of 5 million-year-old horses from Florida: Science, v. 283, p Prothero, D.R., 1998, The chronological, climatic, and paleogeographical background to
20 North American mammalian evolution, in Janis, C.M., Scott, K.M., and Jacobs, L.L. ed., Evolution of Tertiary mammals of North America, Volume 1: terrestrial carnivores, ungulates, and ungulatelike mammals: Cambridge, Cambridge University Press, p Raup, D.M., 1972, Taxonomic diversity during the Phanerozoic: Science, v. 177, p Sage, R.F., 2004, The evolution of C 4 photosynthesis: New Phytologist, v. 161, p Savage, R.J.G., and Long, M.R., 1986, Mammal evolution: an illustrated guide: New York, New York, Facts on File Publications. Solounias, N., Semprebon, G., 2002, Advances in the reconstruction of ungulate ecomorphology with application to early fossil equids: American Museum Novitates, v. 3366, p Thomasson, J.R., Nelson, M.E., and Zakrzewski, R.J., 1988, A fossil grass (Graminae: Chloridoidae) from the Miocene with Kranz anatomy: Science, v. 233, p Wing, S.L., 1998, Tertiary vegetation of North America as a context for mammalian evolution, in Janis, C.M., Scott, K.M., and Jacobs, L.L. ed., Evolution of Tertiary mammals of North America, Volume 1: terrestrial carnivores, ungulates, and ungulatelike mammals: Cambridge, Cambridge University Press, p Wolfe, J.A., 1985, Distribution of major vegetation types during the Tertiary: Geophysical Monograph, v. 32, p
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