Miocene Horse Evolution and the Emergence of C4
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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.