Dimetrodon Is Not a Dinosaur: Using Tree Thinking to Understand the Ancient Relatives of Mammals and their Evolution
The line of descent that includes all living mammals extends back in time over 300 million years. Many of the ancient relatives of mammals that fall along this line are very different in appearance from living mammals and are frequently mistaken for reptiles such as dinosaurs. This misconception is reinforced by the fact that these animals are often referred to as “mammal-like reptiles,” a term reflecting outdated methods for classifying organisms. In reality, these ancient mammal-relatives, known as synapsids, are more closely related to living mammals than they are to any reptiles. Evolutionary trees, which depict patterns of descent from common ancestors among organisms, are very useful for understanding why this is the case and for reconstructing the evolutionary histories of many of the unique characters found in mammals. Here, I provide an introduction to evolutionary trees and their implications for understanding the relationships between mammals, synapsids, and reptiles. This is followed by a review of synapsid diversity and a discussion of how evolutionary trees can be used to investigate when in synapsid history different mammalian characteristics first appeared.
KeywordsEvolutionary tree Mammalia Mammal-like reptile Non-mammalian synapsid Permian Phylogeny Synapsida Tree thinking Triassic
Dimetrodon is a member of the large group of terrestrial vertebrates or tetrapods known as the Synapsida. Synapsids include all living mammals as well as a diverse range of extinct relatives extending back to the latter parts of the Carboniferous Period of Earth history, about 305 million years ago. They are justifiably well known as one of the great evolutionary sequences preserved in the fossil record, illustrating the evolution of mammals from an ancient, somewhat lizard-like ancestor. The nature of this transition has been reviewed by a number of authors at differing levels of complexity and detail (e.g., Hopson 1987, 1991, 1994, 2001; Hotton 1991; Rubidge and Sidor 2001; Kielan-Jaworowska et al. 2003; Martin 2004; Benton 2005; Kemp 2005; Prothero 2007), and my goal is not to simply repeat the material available in those works. Instead, I will discuss two perhaps more fundamental issues that I believe often lead to confusion about the synapsid fossil record and how it informs paleontologists about the evolution of mammals. In both cases, evolutionary trees, which show how different organisms are related to one another, are key for organizing information and gaining deeper understanding.
The first issue concerns the relationship between mammals and other, so-called non-mammalian synapsids, as well as the relationship between Synapsida as a whole and other groups of tetrapods. Popular treatments often are not clear on the fact that non-mammalian synapsids differ from reptiles and why this is the case. Imprecise and out-dated language which does not reflect current scientific thinking, such as “mammal-like reptile” or “reptile-to-mammal transition”, also frequently creeps into the discussion. When combined with the fact that many early synapsids, including Dimetrodon, superficially appear more reptilian than mammalian, these problems obscure the true nature of some synapsids and their evolutionary significance. Therefore, I will endeavor to clarify where synapsids like Dimetrodon fall on the great family tree of life, how we know they belong there, and why their position means that they are not reptiles or dinosaurs.
The second topic I will address is synapsid diversity and how it relates to the evolution of mammals. Because the synapsid fossil record provides such a detailed view of the evolution of mammals, synapsid diversity is often portrayed as an almost linear sequence, with each member of the sequence possessing a greater number of mammal-like features than the last. However, such linear sequences are rarely accurate (see MacFadden 1992 and Prothero 2007 for discussions of “classic” examples of linear evolution in horses and hominids that have been shown to be inaccurate), and this is true for synapsids. Synapsids existed for over 80 million years before the first mammals evolved, and during this time, non-mammalian synapsids evolved a fascinating array of shapes, sizes, and ways of life. These forms include large sabre-toothed carnivores, herbivores with turtle-like beaks, carnivores and herbivores with tall sails on their backs, specialized burrowers, small weasel-like carnivores, hippo-sized herbivores with thickened skulls that may have been used for head-butting, and even a carnivorous species that might have been venomous. This diversity is sometimes overlooked because much of it is peripheral to the evolution of mammals. At the same time, its existence can lead to questions and confusion. For example, if Dimetrodon is our relative, and it had a sail on its back, does that mean our direct ancestors did too? To answer this question, I will describe how evolutionary trees can be used to infer where in synapsid history particular mammalian characters evolved, as well as to recognize when a feature of interest represents an evolutionary innovation peculiar to a specific subgroup of synapsids, and therefore is not of direct relevance to the evolution of mammals.
Evolutionary Trees and Synapsids or Why Mammal-like Reptile is a Misnomer
The Basics of Evolutionary Trees
Dimetrodon and other non-mammalian synapsids often are referred to as mammal-like reptiles, and the evolution of mammals from an earlier synapsid ancestor is sometimes described as the reptile-to-mammal transition. These phrases are misleading because they imply that non-mammalian synapsids are somehow akin to living reptiles, such as lizards, crocodiles, or snakes, and that reptiles are ancestors of mammals. Both of these ideas are incorrect, and the easiest way to see why this is the case is to consult an evolutionary tree or phylogeny.
Evolutionary trees have existed as long as the science of evolutionary biology itself. Famously, the only figure in Darwin’s On the Origin of Species (1859) is an evolutionary tree. In the last four decades, the use of phylogenies as a framework for testing hypotheses and answering questions (so-called tree thinking) has revolutionized many areas of biology and paleontology, and it is now a central part of the biological sciences (O’Hara 1988, 1997; for a historical treatment of some of the debates surrounding the rise of tree thinking, see Hull 1988). Accompanying this revolution has been a fundamental shift in how scientists classify organisms, and this in turn has rendered terms such as mammal-like reptile obsolete.
An important question to ask at this point is how do we reconstruct the patterns of descent from common ancestors that are represented by an evolutionary tree? After all, we cannot see the relationships between different organisms directly. The answer is that scientists infer patterns of relationship based on the distribution of characters among a set of organisms of interest. Characters used in this process can take many forms, including skeletal features, aspects of soft tissue anatomy at both the microscopic and macroscopic levels, and DNA sequences. Typically, a large amount of character data will be collected, and then a phylogeny will be sought that best explains the evolution of the greatest number of characters given a specific optimality criterion, such as minimizing the number of hypothesized evolutionary changes or the best fit to an independently derived model of how DNA sequences change over time (technical information on how phylogenies are constructed can be found in Kitching et al. 1998; Felsenstein 2004, and Huelsenbeck and Ronquist 2005). Special attention is usually given to characters that all members of a particular group inherited from their most recent common ancestor because those characters are particularly useful for recognizing if newly discovered organisms are members of that group. So, in a sense, the characters organisms possess are something like tags indicating who their ancestors were, and scientists increase the likelihood that they have reconstructed an accurate evolutionary tree by finding the tree that best explains the evolution of the greatest number of characters.
Where Do Synapsids Fit?
Now, let us add some fossils to our evolutionary tree (Fig. 4b). A noteworthy change in the reptile portion of the tree that takes place when we do this is that living birds now share a common ancestor with non-avian saurishcian dinosaurs. This is because birds are descendants of a group of saurischian (“lizard-hipped”) dinosaurs called theropods, making them dinosaurs themselves and allowing us to draw a distinction between non-avian dinosaurs (i.e., all those dinosaurs that are not birds) and “avian dinosaurs,” birds themselves (an excellent review of the dinosaurian origin of birds can be found in Chiappe 2007). More important in the context of the current paper are the many groups of extinct synapsids and early mammals known from the fossil record that are added to the branch leading up to extant mammals. All of the groups on this branch below the node labeled “Mammalia” are non-mammalian synapsids. That is, they are descendants of the most recent common ancestor of all synapsids, but not the most recent common ancestor of all mammals.
In the past, non-mammalian synapsids were often colloquially referred to as mammal-like reptiles. They were “mammal-like” because paleontologists understood that they were related to mammals and provided insight into the latter group’s evolution, but they were “reptiles” because they lacked key characters that defined mammals, such as a single jaw bone or three middle ear bones. Examining the phylogeny in Fig. 4b shows why this terminology has been abandoned by scientists as tree thinking has become common and taxonomic groups have come to be defined by patterns of shared ancestry. Non-mammalian synapsids are descended from the most recent common ancestor of all synapsids, and not the most recent common ancestor of reptiles, making them by definition part of a line of descent that is separate from all reptiles. The fact that some of the earliest synapsids, such as Dimetrodon (which is a member of the synapsid subgroup called sphenacodontids in Fig. 4b), superficially resemble living reptiles in some respects does not overturn this underlying pattern of common ancestry.
Tree thinking also helps to clarify the nature of the evolution of mammals and many of their distinctive characters. Using outdated taxonomic concepts and terminology such as “mammal-like reptile” confuse the issue because they suggest that reptiles are ancestors of mammals. In turn, this can lead to questions such as, “if reptiles are ancestors of mammals, why are reptiles still alive today?” and “where are the missing links between reptiles and mammals?” Once again, the answers to these questions are obvious if we consult our evolutionary tree (Fig. 4b). Reptiles are not ancestors of mammals; they are part of a separate line of descent from a common ancestor, so their existence in the modern world is no more surprising than the fact that you and your cousin both exist today. There are no “missing links” between reptiles and mammals for exactly the same reason. Because reptiles and synapsids (including mammals) are two separate lines of descent, the link between the groups is the common ancestor they share (just as you and your cousin are linked by being descendants of your grandparents). The fossil record preserves a number of extinct species that inform us about the characteristics of the last common ancestor of reptiles and synapsids, as well as fossil species that are near the base of the reptile and synapsid lines of descent [see e.g., Ruta and Coates (2007) for a sense of the diversity of the species just before this split, and Benton (2005), Kemp (2005), and Prothero (2007) for information on the earliest synapsids and reptiles]. These fossils provide important insights about what characters early members of both groups inherited from their common ancestor, which characters are new features that are unique to one group or the other, and the evolutionary and ecological context in which new characters and species evolved. Scientists use these indirect methods to understand the ancestors of groups of organisms because it is all but impossible to say with certainty whether a particular fossil is definitely an ancestor. However, by studying where various organisms fall on phylogenies and what characteristics the organisms possess, we can get a good sense of what an ancestor was like even if we cannot identify it exactly.
How to Recognize a Synapsid
A final important issue to address in this section is the question of how scientists recognize which animals are part of the group Synapsida. In other words, what does it take to be a synapsid? Once again, tree thinking is critical to answering this question, as are the concepts of definition and diagnosis.
Now that we understand who synapsids are and where they fall on the tree of life relative to other groups such as reptiles, let us turn to the topic of synapsid diversity and its implications for the evolution of many of the distinctive characters of mammals.
Tree Thinking, Synapsid Diversity, and the Evolution of Mammalian Characters
Because of their close relationship to living mammals and the fact that they provide a record of the evolutionary history of many mammalian characters, much research on non-mammalian synapsids is couched in the framework of mammal origins (e.g., Sidor and Hopson 1998; Sidor 2001, 2003). Similarly, most popular accounts of synapsids make a point of describing the order in which different mammalian characters evolved and the evolutionary steps in the process. Such works are important because they present the parts of synapsid history that are most directly our own and shed light on what our very ancient ancestors were like. However, in the interest of brevity and simplicity, the full diversity of non-mammalian synapsids is rarely addressed. This is unfortunate because although most people realize that living mammals vary from aardvarks and bats to whales and zebras, they are usually unaware of the fascinating array of shapes, sizes, and ways of life that non-mammalian synapsids evolved millions of years before the first mammals appeared. On the occasions when they do encounter some of this diversity, such as during museum visits, their unfamiliarity can lead to confusion about how it pertains to mammal evolution. A complete review of synapsid diversity is beyond the scope of this paper, but a few examples will help to provide a sense of its breadth.
A Selection of Synapsids
Dimetrodon and Edaphosaurus (Figs. 1, 6b) are two of the best-known and most distinctive early synapsids. Both animals are characterized by large sails on their backs, which are formed by elongated portions of their vertebrae, and which may have evolved as a means for them to more precisely regulate their body temperatures (Bennett 1996). Fascinatingly, evolutionary trees of synapsids suggest that Edaphosaurus and Dimetrodon evolved their sails independently, an example of the process of convergent evolution, where similar selective forces acting on distantly related organisms can result in the evolution of similar structures. Edaphosaurus also is noteworthy because it is one of the oldest known terrestrial vertebrates that is specialized for feeding on plants (Sues and Reisz 1998; Reisz 2006). Dimetrodon and Edaphosaurus are best known from fossil localities in the American southwest, particularly Texas, that range in age between about 300 million and 270 million years in age (Reisz 1986).
Now that we have seen some of the diversity of non-mammalian synapsids, we can examine how paleontologists use evolutionary trees to organize this diversity and to investigate where in synapsid history different mammalian characters evolved.
Using Tree Thinking to Organize Synapsid Diversity and Track Mammalian Characters
Because evolutionary trees depict patterns of descent from common ancestors, they are an extremely useful way to relate the diverse shapes, sizes, and ways of life observed in a group of animals such as the synapsids to their evolutionary history. In turn, this allows us to accurately determine where in synapsid history particular features of interest evolved, as well as whether they were present in the ancestors of mammals or only in lines of descent that do not lead to mammals.
Recall that when scientists construct a phylogeny, they consider a large number of characters and search for the tree that best explains the evolution of as many of those characters as possible. The resulting trees group species together based on inferred patterns of descent from common ancestors. Usually, the species in particular groups resemble one another for the simple reason that they inherited many of their similarities from common ancestors. However, evolutionary trees often contain some surprises as well. For example, detailed phylogenetic research indicates that Edaphosaurus, which falls in the group called “edaphosaurids” in Fig. 4b, and Dimetrodon, which falls in the group called “sphenacodontids” in Fig. 4b, do not share a common ancestor that possessed a sail on its back, despite the fact that both Edaphosaurus and Dimetrodon have sails on their backs. By grouping organisms together based on patterns of descent inferred from a large number of characters and not just a few potentially superficial similarities or differences, phylogenies provide a framework for asking and answering deeper questions about diversity. For example, do all descendants of a common ancestor share a similar way of life, such as being terrestrial carnivores, or do some evolve to adapt in other ecologies, such as an aquatic herbivore? Is there a correlation between the number of species in a group and the diversity of shapes, sizes, and ecologies found in the group? Do some lines of descent from a common ancestor display higher rates of speciation than others? Do superficially similar animals, such as Dimetrodon and Edaphosaurus, share a recent common ancestor or did they evolve their similarities independently?
In addition to their utility in studies of diversity, phylogenies also can provide great insight into the evolutionary history of individual characters. By “mapping” a character of interest onto a phylogeny, we can not only see which species possess the character but also make inferences about where in the history of the group the character evolved and whether it is likely that the character evolved only once or multiple times [reviews of methods used for mapping the evolution of characters on evolutionary trees can be found in Brooks and McLennan (1991) and Garland et al. (2005)]. The evolution of a bony secondary palate in different groups of synapsids provides a useful example of how tree thinking can elucidate the history of a character.
The first step in mapping the character onto the tree is to note which of the animals listed at the tips of the branches possessed a bony secondary palate. The results of this step are shown in Fig. 12b. Now, we will need to reconstruct whether the common ancestors of different groups also possessed a secondary palate. There are a number of ways to do this, but for simplicity, we will use a method called parsimony, which seeks to minimize the number of evolutionary changes that are necessary to explain the distribution of the character on the tree. The results of this step reveal an interesting pattern: A bony secondary palate evolved multiple times in synapsids (Fig. 12b). The character first evolved in the common ancestor of advanced anomodonts like Delectosaurus and Cistecephalus. It evolved a second time in the common ancestor of advanced therocephalians such as Bauria and Ericiolacerta. Finally, a bony secondary palate evolved a third time early in cynodont history. We prefer this scenario to others because it requires the fewest evolutionary changes. For instance, if we hypothesized that a secondary palate evolved in the common ancestor of therocephalians and cynodonts, our tree implies that this feature would need to have been lost in several therocephalian subgroups, necessitating four evolutionary changes, as opposed to the three required by our preferred hypothesis. Moreover, the pattern indicates that mammals inherited their bony secondary palate from a cynodont ancestor, whereas the secondary palates of anomodonts and therocephalians represent separate evolutionary innovations that are restricted to those groups, and thus are not directly relevant to the specific history of mammals. Finally, if we consider animals such as Procynosuchus or Ictidosuchoides, we find that although they lack a complete secondary palate, their internal nostrils are partially covered over by an incomplete secondary palate. These forms and their position on the phylogeny are important because they help to document the evolutionary transition between synapsids lacking secondary palates and those with complete secondary palates.
This tree thinking approach can be applied to any character and is very useful for answering a variety of evolutionary questions. For instance, to return to the question of whether our ancestors had a sail like Dimetrodon, character mapping implies that the answer is no. Hypothesizing that the common ancestor of mammals and Dimetrodon possessed a sail requires two evolutionary changes: one change to the sailed condition and a second change to the non-sailed condition in a more recent ancestor of mammals. In contrast, hypothesizing that a sail evolved in the immediate ancestor of Dimetrodon and its closest relatives and not in the common ancestor of Dimetrodon and mammals requires only one evolutionary change (i.e., the evolution of a sail in Dimetrodon’s ancestor; no change to the non-sailed condition is needed). Character mapping also can inform us about the order in which different characters evolved. For example, the method indicates that the novel jaw muscle arrangement found in mammals (including the presence of a masseter muscle) evolved before two of the tiny middle ear bones, which were formerly part of the lower jaw, were fully incorporated into the hearing system (e.g., Kemp 2005).
The evolution of mammals from non-mammalian synapsid ancestors is a significant topic for anyone interested in biology or paleontology. Not only is the process recorded in great detail in the fossil record, giving us much insight into the order in which characters changed and the functional and ecological contexts in which those changes occurred, but it is also part of our history. Because non-mammalian synapsids are our relatives, learning about them helps to answer the question of “where did we come from?” as much as studying fossil hominids or family genealogies. However, confusion often persists because of outdated ways of thinking about the topic.
Tree thinking is an excellent solution to the problem because evolutionary trees provide an excellent framework for asking and answering evolutionary questions and are now a common tool used by biologists and paleontologists. For example, because evolutionary trees depict patterns of descent from common ancestors, they are very useful for understanding the relationship of non-mammalian synapsids to mammals (they are all descendants of a common ancestor), as well as how synapsids are related to reptiles (they are descendants of a common ancestor, but reptiles and synapsids are separate lines of descent). Similarly, phylogenies are very useful for organizing patterns of diversity in large groups, such as the Synapsida, and when combined with techniques such as character mapping, they can provide much insight into the evolution of different characters.
So, when you are next confronted by non-mammalian synapsids, whether on television, at a museum, or in a book on prehistoric life, take a moment to use your tree thinking skills. They will help you to remember why Dimetrodon is not a dinosaur, why our ancestors did not have a sail like that of Edaphosaurus, and how scientists reconstruct the evolutionary history of mammalian characters.
Thanks are due to Don Prothero for organizing this special issue of Evolution: Education and Outreach and for inviting me to contribute to it. I also thank curators, collections managers, and friends at the Bayerische Staatssammlung für Paläontologie und historische Geologie (BSP), the Bernard Price Institute for Palaeontological Research (BP), The Field Museum (FMNH), the Iziko South African Museum (SAM), the Museum of Comparative Zoology (MCZ), the Palaeontological Institute (PIN), the Rubidge Collection (RC), and the University of California Museum of Paleontology (UCMP) for their assistance with the visits on which I took the photos in Figs. 5, 6, 7, 8, 9, 10, and 11. Christian Kammerer graciously allowed me to use the photos in Figs. 7b, 10c, and 11b. Audrey Aronowsky and Scott Buhrman commented on drafts of the manuscript. Christian Sidor and two anonymous reviewers also provided helpful comments and suggestions.