Evolutionary Transitions in the Fossil Record of Terrestrial Hoofed Mammals
© Springer Science+Business Media, LLC 2009
Received: 9 September 2008
Accepted: 30 March 2009
Published: 16 April 2009
In the past few decades, many new discoveries have provided numerous transitional fossils that show the evolution of hoofed mammals from their primitive ancestors. We can now document the origin of the odd-toed perissodactyls, their early evolution when horses, brontotheres, rhinoceroses, and tapirs can barely be distinguished, and the subsequent evolution and radiation of these groups into distinctive lineages with many different species and interesting evolutionary transformations through time. Similarly, we can document the evolution of the even-toed artiodactyls from their earliest roots and their great radiation into pigs, peccaries, hippos, camels, and ruminants. We can trace the complex family histories in the camels and giraffes, whose earliest ancestors did not have humps or long necks and looked nothing like the modern descendants. Even the Proboscidea and Sirenia show many transitional fossils linking them to ancient ancestors that look nothing like modern elephants or manatees. All these facts show that creationist attacks on the fossil record of horses and other hoofed mammals are completely erroneous and deceptive. Their critiques of the evidence of hoofed mammal evolution are based entirely on reading trade books and quoting them out of context, not on any firsthand knowledge or training in paleontology or looking at the actual fossils.
The hoofed mammals, or ungulates, are the third-largest group of placental mammals alive today (after rodents and bats). Nearly all large-bodied herbivorous mammals, living and extinct, are ungulates. These include not only familiar groups such as the odd-toed perissodactyls (horses, rhinos, and tapirs) and even-toed artiodactyls (pigs, peccaries, hippos, camels, deer, giraffes, pronghorns, cattle, sheep, and antelopes) but also their extinct relatives. Depending upon which phylogeny is accepted, many paleontologists also consider elephants, sirenians, and hyraxes to be ungulates as well (see Novacek 1986, 1992; Novacek and Wyss 1986; Novacek et al. 1988; Prothero et al. 1988; Prothero 1993; Prothero and Schoch 2002; Gheerbrant et al. 2005). Nearly all of these groups have an excellent fossil record since the early Eocene because they are relatively large-bodied with robust bones so they fossilize easily, and they were widespread among the Holarctic continents. Consequently, they provide a number of outstanding examples of evolution in the fossil record and are the focus of many creationist distortions and falsehoods about fossils as well.
Phylogenetically speaking, whales are also ungulates, since the molecular, paleontological, and morphological evidence has now converged on the idea that they are closest to the hippo-anthracothere branch of the artiodactyls (see Prothero and Foss 2007). Indeed, the earliest whales did have small hooves, although as whales reduced and lost their hind limbs and modified their forelimbs into flippers, their hooves were lost. The example of whale evolution is such an outstanding case of macroevolution, however, and has made so much recent progress with amazing new specimens that we have set it aside as a separate article (Thewissen, this volume).
In this article, I will focus only on the best-documented examples of terrestrial hoofed mammals. These have proven to be historically important, ever since Huxley, Gaudry, and Kowalewsky first documented the fossil record of the evolution of the horse in Europe in the late 1860s and early 1870s and then were upstaged by O.C. Marsh’s incredible series of North American fossil horses in 1876 (MacFadden 1992). Fossil horses have since become one of the exemplars of evolution as displayed in the fossil record, endlessly repeated and recycled in textbooks and museum displays (but often with outdated or incorrect information). However, there are amazing evolutionary sequences known for tapirs, rhinos, brontotheres, camels, giraffes, and many other groups that receive much less notice. Here I will discuss just a few of these to allow the reader to see the incredible diversity of evidence for evolution that the fossil record provides. For more details, see Prothero (1994), Prothero and Schoch (2002), Chapter 14 in Prothero (2007), or the technical chapters in Prothero and Schoch (1989) and Prothero and Foss (2007).
The perissodactyls, or the odd-toed hoofed mammals, are not very diverse today. There are currently only four living species of tapirs, five species of rhinos, and a handful of species of horses, asses, and zebras. Most of these are endangered in the wild, and several have gone extinct in the last century. However, perrissodactyls were much more diverse in the Eocene and Oligocene, with a number of families and other lineages that are now extinct (e.g., brontotheres, palaeotheres, chalicotheres, lophiodonts, other tapiroids, hyracodonts, amynodonts) and even a higher diversity of extinct genera and species of horses, rhinos, and tapirs than are living today (Prothero and Schoch 1989, 2002). Each of these groups is easily fossilized and found in nearly all the Holarctic continents since the early Eocene, so they tend to have an excellent fossil record. Even though horse evolution has received the lion’s share of the publicity, the record of rhinos, tapirs, and brontotheres is also excellent, and each deserves more frequent mention as exemplars of evolution to replace the overused examples of horse evolution.
The most striking thing about perissodactyl evolution is that we can see the very earliest stages of their diversification preserved in the fossil record. For many years, paleontologists have focused on the archaic hoofed mammal (“condylarth”) group known as phenacodonts as the sister taxon of perissodactyls (Radinsky 1966, 1969; Thewissen and Domning 1992). These creatures were widespread around the Holarctic region of Eurasia and North America in the Paleocene and early Eocene and do indeed share many characters in common with perissodactyls. Phenacodonts, in turn, provide a link between perissodactyls and the most primitive clades of ungulates (Prothero et al. 1988). Moving even closer to true perissodactyls, we have the late Paleocene Chinese fossil known as Radinskya, which is a close sister group to almost all the earliest perissodactyls (McKenna et al. 1989). Known from a partial skull and a few other fragments, its teeth are more primitive than any bona fide perissodactyl, yet it shows some derived characters that make it a good sister taxon to that order. However, it is so primitive in most of its characters that McKenna et al. (1989) were unsure about its taxonomic assignment.
One would think an improving record of horse evolution should impress creationists with all the new data. Instead, they quote old ideas out of context to deny that horse evolution occurred at all, or use outdated quotations about the replacement of the simplistic linear model with the complex bushy model to deny the reality of horse evolution (Gish 1995: 189–197; Wells 2000:195–207). Others like Sarfati (2002: 132–133) claim that all these fossil horses are within the range of variation of modern horses. Clearly, he has never actually looked at the fossils, since primitive horses like Protorohippus do not even remotely resemble the smallest modern ponies of the genus Equus. Every single comment on horse evolution from the creationists’ literature betrays their complete lack of any firsthand knowledge of horse anatomy or fossils and shows that they cannot tell one bone from another. Instead, they criticize scientists for changing our ideas about horse evolution as we learned more from more and better fossils. Maybe this makes sense in their mindset of unchanging truths, but in the real world (and in science), more data are better, and change is good when the data demand it!
Rhinos Without Horns, Tapirs Without Snouts
The largest group of ungulates (living and fossil) is the order Artiodactyla. With over 190 living species and at least ten times as many fossil species, they are the most diverse and abundant large herbivores on the planet. They include pigs, peccaries, hippos, camels, deer, pronghorns, giraffes, sheep, goats, cattle, and antelopes. In addition, there are many more extinct families that are familiar only to paleontologists, including the primitive diacodexeids, the pig-like entelodonts, the ubiquitous oreodonts, the bizarrely horned protoceratids and dromomerycines, and many others. Nearly all domesticated animals that we eat (cattle, pigs, sheep, goats) or get milk from (cattle, goats) or use for leather or wool (cattle, sheep) are artiodactyls. As such, they are much more familiar to us, even though a lot remains to be learned about their evolution.
Artiodactyls are defined not just by their “cloven hooves” (even number of toes, two or four), but also by the symmetry of their feet. They have a paraxonic foot, with the axis of symmetry running between digits III and IV (middle finger and the ring finger, or third toe/fourth toe). Even more striking is the universal hallmark of all artiodactyls, the “double-pulley” astragalus in their ankles, which allows them to have very flexible fore and aft motions of their foot (but prevents lateral rotation). Artiodactyls have many other distinctive characteristics in their skulls and skeletons, especially in the unique crescent-shaped crests (selenodonty) that many groups independently evolved in their cheek teeth.
The origin and early evolution of artiodactyls is just now becoming better known as new discoveries are made (Prothero and Foss 2007). The sister taxon of artiodactyls is still controversial (Prothero et al. 1988; Theodor et al. 2005; Rose 2006; Prothero and Foss 2007). Various candidates have been proposed, ranging from archaic ungulates like the huge predatory mesonychids to the coatimundi-like arctocyonid ungulates such as Chriacus. In any case, the evidence suggests that artiodactyls are one of the first groups to branch off from the rest of the hoofed mammals. By the early Eocene, very primitive artiodactyls known as diacodexeids or dichobunids were widespread across Eurasia and North America. To the casual viewer, these creatures (about the size of a small dog) would look like a small musk deer or even rabbit-like, since they had long slender hind limbs for leaping. However, a closer look at the teeth and ankles and feet shows that they have all the hallmarks of artiodactyls, especially in the double-pulley astragalus and paraxonic foot.
By the middle Eocene, these diacodexeids had been replaced by a huge radiation of archaic artiodactyl groups in North America and Asia (Gazin 1955; Stucky 1998; chapters in Prothero and Foss 2007), nearly all of which are now extinct. Each of these groups is only slightly more advanced than their primitive sister groups, yet there are already trends toward the low-crowned grinding teeth (bunodonty) in the lineages that led to pigs, peccaries, and hippos (numerous genera from the middle–late Eocene of China and Thailand—Harris and Liu 2007). There were still others that were specialized in the direction of ruminants (Archaeomeryx from the middle Eocene of Mongolia—Metais and Vislobokova 2007) and camels (middle Eocene North American forms such as oromerycids and the camel Poebrodon). Europe had its own unique endemic radiation of seven artiodactyl families that evolved in isolation when Europe was a flooded archipelago (Erfurt and Metais 2007). There are so many of these excellent examples of evolution within these families that an entire book (e.g., Prothero and Foss 2007) is required to cover the topic. For the purposes of this essay, however, we will examine two that are particularly striking: the camels and the giraffes.
Camels Without Humps
Elephants and Their Kin
Both molecular and paleontological evidence agree that artiodactyls and perissodactyls are a natural group of ungulates. However, when it comes to a third major hoofed mammal clade, the tethytheres (elephants, sirenians, and their kin), there is a conflict between molecular evidence which places them in the Afrotheria (Springer et al. 2004; Murphy et al. 2001) and the morphological and paleontological evidence that unites them with ungulates (Novacek 1986, 1992; Novacek and Wyss 1986; Novacek et al. 1988; Prothero et al. 1988; Prothero 1993; Gheerbrant et al. 2005). We will not discuss this issue further here, because numerous laboratories and paleontologists are working to resolve the conflict. Many of primitive tethytheres had hooves, so we will treat them as hoofed mammals in an ecological sense, even if it is not clear that they are part of the Ungulata.
Elephants Without Trunks
One could not ask for a better example of a transitional fossil! It closely parallels the intermediate pattern of locomotion seen in walking whales such as Ambulocetus (Thewissen, this volume). When creationists have addressed this discovery at all (on their websites; none of their books mention it yet), they show their complete ignorance of the basics of anatomy and paleontology. Their argument boils down to “if it has four legs and feet, it can’t be a sirenian,” even though the details of the teeth, skull, and even the ribs share the specializations unique to the entire order Sirenia. In short, they do not understand the basic notion of homology and analogy. They automatically define “sirenian” so it cannot have legs and feet, just as they deny that Ambulocetus is a whale that walked (even though its skull and teeth and many aspects of the skeleton are typical of archaeocete whales). This kind of mental straitjacket and getting out of a dilemma by defining it away might make them feel better, but it is no excuse for knowing their anatomy or fossils or getting the facts straight.
In short, the fossil record of hoofed mammals is full of transitional fossils and even longer transitional sequences that demonstrate the origins of nearly all the living ungulates and tethytheres from ancestors that looked almost completely unlike their descendants. We now have the fossils that show where the perissodactyls came from (phenacodonts, Radinskya) and that document the radiation of the earliest horses, tapirs, rhinos, and brontotheres when they were almost indistinguishable to the untrained eye (Fig. 1). We have the fossils that demonstrate the evolution of the horse family, the rhinoceroses, the tapirs, and the brontotheres, along with other examples not covered in this article. Their phylogenies are now much more bushy and branching, but otherwise, the general trends are the same that were observed over a century ago. Creationists attempt to discredit these examples by saying that our switch from an orthogenetic linear model of the 1920s to the modern bushy branching pattern somehow denies that this fossil evidence does show change through time, but this only reveals the creationists’ lack of training in anatomy and paleontology. Likewise, we now have the fossils to document the early stages of the radiation of the artiodactyls and especially the bushy branching history of camels and giraffes, both of which lacked humps or long necks in their respective early histories. Finally, the fossil record of transitions within the Proboscidea is excellent, from pig- or tapir-like beasts like Moeritherium that creationists would never place in the “elephant kind” to a variety of mastodonts leading up to modern elephants. One of the best transitional fossils of all is Pezosiren portelli, a perfect intermediate form that shows how the aquatic manatees evolved from walking ancestors.
All of these examples are largely ignored by creationists, or when they do mention them, they use completely outdated arguments, quotes out of context, or simple lies and distortions that demonstrate the fact that creationists have no training in anatomy or paleontology and cannot tell one bone from another. In the most extreme cases, the creationists resort to semantic gyrations that define the problem away, so that if a fossil has terrestrial legs and feet, it cannot be a sirenian or a whale, even if every other aspect of the anatomy clearly indicates its phylogenetic affinities. Arguments such as this reveal the dogmatism and complete intellectual and scientific bankruptcy of creationists. If they really cared to find out whether there were transitional forms in the fossil record, they would stop quoting out of context from children’s books or outdated secondary sources and obtain the proper anatomical and paleontological training to study the fossils themselves. Since they do not even bother to do this, their arguments are worthless.
I thank Niles Eldredge for suggesting this volume and helping edit the proceedings and two anonymous reviewers for helpful comments on this article.
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