Macroevolution

(This is a copy of an essay that I published in 2006. I made some minor revisions to remove outdated context.)

Overheard at breakfast on the final day of a recent scientific meeting: "Do you believe in macroevolution?" Came the rely: "Well, it depends on how you define it."
                                                                         Roger Lewin (1980)

There is no difference between micro- and macroevolution except that genes between species usually diverge, while genes within species usually combine. The same processes that cause within-species evolution are responsible for above-species evolution.
                                                                         John Wilkins

The minimalist definition of evolution is a change in the hereditary characteristics of a population over the course of many generations. This is a definition that helps us distinguish between changes that are not evolution and changes that meet the minimum criteria. The definition comes from the field of population genetics developed in the early part of the last century. The modern theory of evolution owes much to population genetics and our understanding of how genes work. But is that all there is to evolution?

The central question of the Chicago conference was whether the mechanisms underlying microevolution can be extrapolated to explain the phenomena of macroevolution. At the risk of doing violence to the positions of some of the people at the meeting, the answer can be given as a clear, No.
               Roger Lewin (1980)

No. There's also common descent—the idea that all life has evolved from primitive species over billions of years. Common descent is about the history of life. In this essay I'll describe the main features of how life evolved but keep in mind that this history is a unique event that is accidental, contingent, quirky, and unpredictable. I'll try and point out the most important controversies about common descent.

The complete modern theory of evolution encompasses much more than changes in the genetics of a population. It includes ideas about the causes of speciation, long-term trends, and mass extinctions. This is the domain of macroevolution—loosely defined as evolution above the species level. The kind of evolution that focuses on genes in a population is usually called microevolution.

As a biochemist and a molecular biologist, I tend to view evolution from a molecular perspective. My main interest is molecular evolution and the analysis of sequences of proteins and nucleic acids. One of the goals in writing this essay is to explain this aspect of evolution to the best of my limited ability. However, another important goal is to show how molecular evolution integrates into the bigger picture of evolution as described by all other evolutionary biologists, including paleontologists. When dealing with macroevolution this is very much a learning experience for me since I'm not an expert. Please bear with me while we explore these ideas.

It's difficult to define macroevolution because it's a field of study and not a process. Mark Ridley has one of the best definitions I've seen ...

Macroevolution means evolution on the grand scale, and it is mainly studied in the fossil record. It is contrasted with microevolution, the study of evolution over short time periods., such as that of a human lifetime or less. Microevolution therefore refers to changes in gene frequency within a population .... Macroevolutionary events are more likely to take millions, probably tens of millions of years. Macroevolution refers to things like the trends in horse evolution described by Simpson, and occurring over tens of millions of years, or the origin of major groups, or mass extinctions, or the Cambrian explosion described by Conway Morris. Speciation is the traditional dividing line between micro- and macroevolution.
                                                                         Mark Ridley (1997) p. 227

When we talk about macroevolution we're talking about studies of the history of life on Earth. This takes in all the events that affect the actual historical lineages leading up to today's species. Jeffrey S. Levinton makes this point in his description of the field of macroevolution and it's worth quoting what he says in his book Genetics, Paleontology, and Macroevolution.

Macroevolution must be a field that embraces the ecological theater, including the range of time scales of the ecologist, to the sweeping historical changes available only to paleontological study. It must include the peculiarities of history, which must have had singular effects on the directions that the composition of the world's biota took (e.g., the splitting of continents, the establishment of land and oceanic isthmuses). It must take the entire network of phylogenetic relationships and impose a framework of genetic relationships and appearances of character changes. Then the nature of evolutionary directions and the qualitative transformation of ancestor to descendant over major taxonomic distances must be explained.
                                                                     Jeffrey S. Levinton (2001) p.6

Levinton then goes on to draw a parallel between microevolution and macroevolution on the one hand, and physics and astronomy on the other. He points out that the structure and history of the known universe has to be consistent with modern physics, but that's not sufficient. He gives the big bang as an example of a cosmological hypothesis that doesn't derive directly from fundamental physics. I think this analogy is insightful. Astronomers study the life and death of stars and the interactions of galaxies. Some of them are interested in the formation of planetary systems, especially the unique origin of our own solar system. Explanations of these "macro" phenomena depend on the correctness of the underlying "micro" physics phenomena (e.g., gravity, relativity) but there's more to the field of astronomy than that.

Levinton continues ....

Does the evolutionary biologist differ very much from this scheme of inference? A set of organisms exists today in a partially measurable state of spatial, morphological, and chemical relationships. We have a set of physical and biological laws that might be used to construct predictions about the outcome of the evolutionary process. But, as we all know, we are not very successful, except at solving problems at small scales. We have plausible explanations for the reason why moths living in industrialized areas are rich in dark pigment, but we don't know whether or why life arose more than once or why some groups became extinct (e.g., the dinosaurs) whereas others managed to survive (e.g., horseshoe crabs). Either our laws are inadequate and we have not described the available evidence properly or no such laws can be devised to predict uniquely what should have happened in the history of life. For better or worse, macroevolutionary biology is as much historical as is astronomy, perhaps with looser laws and more diverse objectives....

Indeed, the most profound problem in the study of evolution is to understand how poorly repeatable historical events (e.g., the trapping of an endemic radiation in a lake that dries up) can be distinguished from lawlike repeatable processes. A law that states 'an endemic radiation will become extinct if its structural habitat disappears' has no force because it maps to the singularity of a historical event.
                                                                 Jeffrey S. Levinton (2001) p.6-7

In conclusion, then, macroevolutionary processes are underlain by microevolutionary phenomena and are compatible with microevolutionary theories, but macroevolutionary studies require the formulation of autonomous hypotheses and models (which must be tested using macroevolutionary evidence). In this (epistemologically) very important sense, macroevolution is decoupled from microevolution: macroevolution is an autonomous field of evolutionary study.
     Francisco J. Ayala (1983)

I think it's important to appreciate what macroevolutionary biologists are saying. Most of these scientists are paleontologists and they think of their area of study as an interdisciplinary field that combines geology and biology. According to them, there's an important difference between evolutionary theory and the real history of life. The actual history has to be consistent with modern evolutionary theory (it is) but the unique sequence of historical events doesn't follow directly from application of evolutionary theory. Biological mechanisms such as natural selection and random genetic drift are part of a much larger picture that includes moving continents, asteroid impacts, ice ages, contingency, etc. The field of macroevolution addresses these big picture issues.

Clearly, there are some evolutionary biologists who are only interested in macroevolution. They don't care about microevolution. This is perfectly understandable since they are usually looking at events that take place on a scale of millions of years. They want to understand why some species survive while others perish and why there are some long-term trends in the history of life. (Examples of such trends are the loss of toes during the evolution of horses, the development of elaborate flowers during the evolution of vascular plants, and the tendency of diverse species, such as the marsupial Tasmanian wolf and the common placental wolf, to converge on a similar body plan.)

Nobody denies that macroevolutionary processes involve the fundamental mechanisms of natural selection and random genetic drift, but these microevolutionary processes are not sufficient, by themselves, to explain the history of life. That's why, in the domain of macroevolution, we encounter theories about species sorting and tracking, species selection, and punctuated equilibria.

Micro- and macroevolution are thus different levels of analysis of the same phenomenon: evolution. Macroevolution cannot solely be reduced to microevolution because it encompasses so many other phenomena: adaptive radiation, for example, cannot be reduced only to natural selection, though natural selection helps bring it about.
     Eugenie C. Scott (2004)

As I mentioned earlier, most of macroevolutionary theory is intimately connected with the observed fossil record and, in this sense, it is much more historical than population genetics and evolution within a species. Macroevolution, as a field of study, is the turf of paleontologists and much of the debate about a higher level of evolution (above species and populations) is motivated by the desire of paleontologists to be accepted at the high table of evolutionary theory. It's worth recalling that during the last part of the twentieth century evolutionary theorizing was dominated by population geneticists. Their perspective was described by John Maynard Smith, "... the attitude of population geneticists to any paleontologist rash enough to offer a contribution to evolutionary theory has been to tell him to go away and find another fossil, and not to bother the grownups." (Maynard Smith, 1984)

The distinction between microevolution and macroevolution is often exaggerated, especially by the anti-science crowd. Creationists have gleefully exploited the distinction in order to legitimate their position in the light of clear and obvious examples of evolution that they can't ignore. They claim they can accept microevolution, but they reject macroevolution.

In the real world—the one inhabited by rational human beings—the difference between macroevolution and microevolution is basically a difference in emphasis and level. Some evolutionary biologists are interested in species, trends, and the big picture of evolution, while others are more interested in the mechanics of the underlying mechanisms.

Speciation is critical to conserving the results of both natural selection and genetic drift. Speciation is obviously central to the fate of genetic variation, and a major shaper of patterns of evolutionary change through evolutionary time. It is as if Darwinians—neo- and ulra- most certainly included—care only for the process generating change, and not about its ultimate fate in geological time.
     Niles Eldredge (1995)

The Creationists would have us believe there is some magical barrier separating selection and drift within a species from the evolution of new species and new characteristics. Not only is this imagined barrier invisible to most scientists but, in addition, there is abundant evidence that no such barrier exists. We have numerous examples that show how diverse species are connected by a long series of genetic changes. This is why many scientists claim that macroevoluton is just lots of microevolution over a long period of time.

But wait a minute. I just said that many scientists think of macroevolution as simply a scaled-up version of microevolution, but a few paragraphs ago I said there's more to the theory of evolution than just changes in the frequency of alleles within a population. Don't these statements conflict? Yes, they do ... and therein lies a problem.

When the principle tenets of the Modern Synthesis were being worked out in the 1940's, one of the fundamental conclusions was that macroevolution could be explained by changes in the frequency of alleles within a population due, mostly, to natural selection. This gave rise to the commonly accepted notion that macroevolution is just a lot of microevolution. Let's refer to this as the sufficiency of microevolution argument.

At the time of the synthesis, there were several other explanations that attempted to decouple macroevolution from microevolution. One of these was saltation, or the idea that macroevolution was driven by large-scale mutations (macromutations) leading to the formation of new species. This is the famous "hopeful monster" theory of Goldschmidt. Another decoupling hypothesis was called orthogenesis, or the idea that there is some intrinsic driving force that directs evolution along certain pathways. Some macroevolutionary trends, such as the increase in the size of horses, were thought to be the result of this intrinsic force.

Both of these ideas about macroevolutionary change (saltation and orthogensis) had support from a number of evolutionary biologists. Both were strongly opposed by the group of scientists that produced the Modern Synthesis. One of the key players was the paleontologist George Gaylord Simpson whose books Tempo and Mode in Evolution (1944) and The Major Features of Evolution (1953) attempted to combine paleontology and population genetics. "Tempo" is often praised by evolutionary biologists and many of our classic examples of evolution, such as the bushiness of the horse tree, come from that book. It's influence on paleontologists was profound because it upset the traditional view that macroevolution and the newfangled genetics had nothing in common.

Just as mutation and drift introduce a strong random component into the process of adaptation, mass extinctions introduce chance into the process of diversification. This is because mass extinctions are a sampling process analogous to genetic drift. Instead of sampling allele frequencies, mass extinctions samples species and lineages. ... The punchline? Chance plays a large role in the processes responsible for adaptation and diversity.
        Freeman and Herron (1998)

We see, in context, that the blurring of the distinction between macroevolution and microevolution was part of a counter-attack on the now discredited ideas of saltation and orthogenesis. As usual, when pressing the attack against objectionable ideas, there's a tendency to overrun the objective and inflict collateral damage. In this case, the attack on orthogenesis and the old version of saltation was justified since neither of these ideas offer viable alternatives to natural selection and drift as mechanisms of evolution. Unfortunately, Simpson's attack was so successful that a generation of scientists grew up thinking that macroevolution could be entirely explained by microevolutionary processes. That's why we still see this position being advocated today and that's why many biology textbooks promote the sufficiency of microevolution argument. Gould argues—successfully, in my opinion—that the sufficiency of microevolution became dogma during the hardening of the synthesis in the 1950-'s and 1960's. It was part of an emphasis on the individual as the only real unit of selection.

However, from the beginning of the Modern Synthesis there were other evolutionary biologists who wanted to decouple macroevolution and microevolution—not because they believed in the false doctrines of saltation and orthogenesis, but because they knew of higher level processes that went beyond microevolution. One of these was Ernst Mayr. In his essay "Does Microevolution Explain Macroevolution," Mayr says ...

Among all the claims made during the evolutionary synthesis, perhaps the one that found least acceptance was the assertion that all phenomena of macroevolution can be ‘reduced to,' that is, explained by, microevolutionary genetic processes. Not surprisingly, this claim was usually supported by geneticists but was widely rejected by the very biologists who dealt with macroevolution, the morphologists and paleontologists. Many of them insisted that there is more or less complete discontinuity between the processes at the two levels—that what happens at the species level is entirely different from what happens at the level of the higher categories. Now, 50 years later the controversy remains undecided.
                                                                         Ernst Mayr (1988) p.402

Mayr goes on to make several points about the difference between macroevolution and microevolution. In particular, he emphasizes that macroevolution is concerned with phenotypes and not genotypes, "In this respect, indeed, macroevolution as a field of study is completely decoupled from microevolution." (ibid p. 403). This statement reiterates an important point, namely that macroevolution is a "field of study" and, as such, its focus differs from that of other fields of study such as molecular evolution.

If you think of macroevolution as a field of study rather than a process, then it doesn't make much sense to say that macroevolution can be explained by the process of changing alleles within a population. This would be like saying the entire field of paleontology can be explained by microevolution. This is the point about the meaning of the term "macroevolution" that is so often missed by those who dismiss it as just a bunch of microevolution.

The orthodox believers in the hardened synthesis feel threatened by macroevolution since it implies a kind of evolution that goes beyond the natural selection of individuals within a population. The extreme version of this view is called adaptationism and the believers are called Ultra-Darwinians by their critics. This isn't the place to debate adaptationism: for now, let's just assume that the sufficiency of microevolution argument is related to the pluralist-adaptationist controversy and see how our concept of macroevolution as a field of study relates to the issue. Niles Eldredge describes it like this ...

The very term macroevolution is enough to make an ultra-Darwinian snarl. Macroevolution is counterpoised with microevolution—generation by generation selection- mediated change in gene frequencies within populations. The debate is over the question, Are conventional Darwinian microevolutionary processes sufficient to explain the entire history of life? To ultra-Darwinians, the very term macroevolution suggests that the answer is automatically no. To them, macroevolution implies the action of processes—even genetic processes—that are as yet unknown but must be imagined to yield a satisfactory explanation of the history of life.

But macroevolution need not carry such heavy conceptual baggage. In its most basic usage, it simply means evolution on a large-scale. In particular, to some biologists, it suggests the origin of major groups - such as the origin and radiation of mammals, or the derivation of whales and bats from terrestrial mammalian ancestors. Such sorts of events may or may not demand additional theory for their explanation. Traditional Darwinian explanation, of course, insists not.
                                                              Niles Eldredge (1995) p. 126-127

Eldredge sees macroevolution as a field of study that's mostly concerned with evolution on a large scale. Since he's a paleontologist, it's likely that, for him, macroevolution is the study of evolution based on the fossil record. Eldredge is quite comfortable with the idea that one of the underlying causes of evolution can be natural selection—this includes many changes seen over the course of millions of years. In other words, there is no conflict between microevolution and macroevolution in the sense that microevolution stops and is replaced by macroevolution above the level of species. But there is a conflict in the sense that Eldredge, and many other evolutionary biologists, do not buy the sufficiency of microevolution argument. They believe there are additional theories, and mechanisms, needed to explain macroevolution. Gould says it best ....

We do not advance some special theory for long times and large transitions, fundamentally opposed to the processes of microevolution. Rather, we maintain that nature is organized hierarchically and that no smooth continuum leads across levels. We may attain a unified theory of process, but the processes work differently at different levels and we cannot extrapolate from one level to encompass all events at the next. I believe, in fact, that ... speciation by splitting guarantees that macroevolution must be studied at its own level. ... [S]election among species—not an extrapolation of changes in gene frequencies within populations—may be the motor of macroevolutionary trends. If macroevolution is, as I believe, mainly a story of the differential success of certain kinds of species and, if most species change little in the phyletic mode during the course of their existence, then microevolutionary change within populations is not the stuff (by extrapolation) of major transformations.
                                                         Stephen Jay Gould (1980b) p. 170

Naturalists such as Ernst Mayr and paleontologists such as Gould and Eldredge have all argued convincingly that speciation is an important part of evolution. Since speciation is not a direct consequence of changes in the frequencies of alleles in a population, it follows that microevolution is not sufficient to explain all of evolution. Gould and Eldredge (and others) go even further to argue that there are processes such as species sorting that can only take place above the species level. This means there are evolutionary theories that only apply in the domain of macroevolution.

The idea that there's much more to evolution than genes and population genetics was a favorite theme of Stephen Jay Gould. He advocated a pluralist, hierarchical approach to evolution and his last book The Structure of Evolutionary Theory emphasized macroevolutionary theory—although he often avoided using this term. The Structure of Evolutionary Theory is a huge book that has become required reading for anyone interested in evolution. Remarkably, there's hardly anything in the book about population genetics, molecular evolution, and microevolution as popularly defined. What better way of illustrating that macroevolution must be taken seriously!

Macroevolutionary theory tries to identify patterns and trends that help us understand the big picture. In some cases, the macroevolution biologists have recognized generalities (theories & hypotheses) that only apply to higher level processes. Punctuated equilibria and species sorting are examples of such higher level phenomena. The possible repeatedness of mass extinctions might be another.

Remember that macroevolution should not be contrasted with microevolution because macroevolution deals with history. Microevolution and macroevolution are not competing explanations of the history of life any more than astronomy and physics compete for the correct explanation of the history of the known universe. Both types of explanation are required.

I think species sorting is the easiest higher level phenomena to describe. It illustrates a mechanism that is clearly distinct from changes in the frequencies of alleles within a population. In this sense, it will help explain why microevolution isn't a sufficient explanation for the evolution of life. Of course, one needs to emphasize that macroevolution must be consistent with microevolution.

I have championed contingency, and will continue to do so, because its large realm and legitimate claims have been so poorly attended by evolutionary scientists who cannot discern the beat of this different drummer while their brains and ears remain tuned to only the sounds of general theory.
        Stephen Jay Gould (2002)

If we could track a single lineage through time, say from a single-cell protist to Homo sapiens, then we would see a long series of mutations and fixations as each ancestral population evolved. It might look as though the entire history could be accounted for by microevolutionary processes. This is an illusion because the track of the single lineage ignores all of the branching and all of the other species that lived and died along the way. That track would not explain why Neanderthals became extinct and Cro-Magnon survived. It would not explain why modern humans arose in Africa. It would not tell us why placental mammals became more successful than the dinosaurs. It would not explain why humans don't have wings and can't breathe underwater. It doesn't tell us whether replaying the tape of life will automatically lead to humans. All of those things are part of the domain of macroevolution and microevolution isn't sufficient to help us understand them.

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