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.
At their most basic, evolutionary trees are diagrams that depict how recently three or more organisms shared a common ancestor (a useful introduction to phylogenies and tree thinking can be found in Gregory 2008). For example, in the simple phylogeny depicted in Fig. 2, we can see that humans and cats share a common ancestor because the branches of the tree leading up to them connect at their base (node 5). We also can see that crocodiles and turtles share a common ancestor because their branches connect at their base (node 4). Note, however, that the connection point (or node) between the branches leading up to turtles and crocodiles on the one hand, and cats and humans on the other, lies farther down the tree, at node 3. This implies that cats, humans, turtles, and crocodiles all share a common ancestor (node 3), but that this ancestor is older than the common ancestor of turtles and crocodiles (node 4) or the common ancestor of cats and humans (node 5). In other words, the phylogeny tells us that cats and humans share a more recent common ancestor with each other than either does with crocodiles or turtles, and that because of this more recent common ancestor, cats and humans are more closely related to each other than either is to turtles or crocodiles. Using the same logic, we can see that cats, humans, turtles, and crocodiles all share a more recent common ancestor (node 3) with each other than any does with salamanders and that salamanders, crocodiles, turtles, humans, and cats share a more recent common ancestor (node 2) with each other than any does with lungfish. Note that in all of this discussion, the relationships of particular organisms are always referred to relative to at least one other organism. This is because phylogenetic relationships are always relative. In other words, if we have only two organisms or groups, we can only state that they share a common ancestor, but we cannot state whether that common ancestor is recent or distant. Once we add in at least one more organism or group, however, we have a reference point that allows us to state that two of the organisms share a more recent common ancestor with each other (i.e., they are more closely related to each other) than either does with the third.
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.
The spread of tree thinking has had a profound effect on taxonomy and systematics, the sciences concerned with describing and naming species, and the placing of those species into larger named groups of organisms. Specifically, scientists now almost always try to recognize and name groups of species that are based only on patterns of common ancestry discovered through the construction of phylogenies, whereas older methods frequently conflated patterns of ancestry, the presence or absence of supposed “key” characters, and qualitative notions of how advanced different species were [the PhyloCode (Cantino and de Queiroz 2007), a proposed new set of rules for constructing names for organisms, represents one of the most fully developed results of this shift]. For example, Kielan-Jaworowska et al. (2003) recently defined mammals as “[the group] defined by the shared common ancestor of Sinoconodon, morganucodontans, Monotremata, Marupialia, and Placentalia, plus any extinct taxa shown to be nested with this [group]...” (p.2), a definition based on patterns of shared ancestry that are shown in a phylogeny (Fig. 3). In contrast, older definitions such as that of Simpson (1960) focused on the possession of particular characters, such as a single jaw bone or the presence of three middle ear bones, with less concern for whether the animals grouped together under such a definition included all descendants of a recent common ancestor. This methodological change is particularly important in the case of non-mammalian synapsids. Under older classification schemes, these animals were grouped with the reptiles because they lacked supposedly key mammalian characters, despite the fact that they are more closely related to mammals than to any reptiles. This is why non-mammalian synapsids often appear in older works describing the morphology, origins, and relationships of reptiles (e.g., Romer 1956; Carroll 1969a, b, 1970).
Where Do Synapsids Fit?
If we consider a phylogeny of living tetrapods and their close relatives (Fig. 4a), we can see that tetrapods are comprised of at least three and possibly four main groups, depending on whether caecilians, worm-like tetrapods found in the tropics, are more closely related to frogs and salamanders, as traditionally thought, or if they share a more recent common ancestor with mammals and reptiles (e.g., compare the trees of Ruta and Coates 2007 to that of Anderson et al. 2008). This uncertainty notwithstanding, the tree makes clear the relationships of living synapsids and reptiles: The three living synapsid groups, montreme mammals (platypus and echidnas), marsupial mammals (kangaroos, koalas, possums, and their relatives), and placental mammals (dogs, bats, whales, horses, humans, and their relatives) all are more closely related to each other than they are to any reptiles (i.e., they share a more recent common ancestor with each other than any living reptiles). In other words, reptiles and synapsids (represented among living animals by mammals) represent two distinct lines of descent from a common ancestor, and neither group is directly ancestral to the other. To claim that reptiles are ancestral to mammals would be similar to claiming that your cousin is ancestral to you. Both you and your cousin share common ancestors, your grandparents, but separate lines of descent lead from them to you and your cousin, one passing through your aunt or uncle, the other passing through your father or mother.
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.
The definition of a named group of organisms describes the limits of membership of that group. With the rise of tree thinking, the definitions of groups have come to focus on patterns of descent from common ancestors, as we saw with the definition of Kielan-Jaworowska et al. (2003) of mammals quoted above. A similar definition for Synapsida could take the form of “all animals more closely related to Homo sapiens than Terrapene carolina (the eastern box turtle).” However, although this definition tells us who is a synapsid (any animal that is more closely related to H. sapiens than to the reptile T. carolina), it does not tell us how to recognize synapsids if we find them as fossils or in the living biota. This is where the concept of diagnosis comes into play: A diagnosis is a list of characters we can see on a specimen that provide insight into the nature of its ancestry (additional information on the distinction of definition and diagnosis in the context of mammal evolution can be found in Rowe 1988; de Queiroz 1994, and Padian and Angielczyk 2007). Typically scientists develop diagnoses for groups by comparing the distribution of characters among different organisms to the relative placement of those organisms on an evolutionary tree. Through this process, they can determine which characters occur in only descendants of a particular common ancestor and thus can be used to identify such descendants. A good example of a diagnostic character that can be used to identify almost any synapsid is the presence of the so-called synapsid temporal opening, an opening on the side of the skull in the vicinity of where the jaw musculature attaches, which can be found (with slight modifications) in synapsids as distinctive as Dimetrodon and living mammals, including humans (Fig. 5). Useful diagnostic characters for living mammals include hair and the presence of mammary glands that allow female mammals to secrete milk to nourish their offspring.
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.