The possibility of a link between the rate (or amount) of evolution and speciation has interested biologists for over 50 years (Simpson 1944; Mayr 1954). In contrast to a gradualistic view of evolutionary change, the existence of a link might suggest some special role for speciation per se as a contributor to the modification part of Darwin’s descent with modification. It would also form part of the expected signature of punctuational evolution.
A few years ago, we realized it would be possible to detect whether short or punctuational episodes of evolution had occurred in the genes used to infer phylogenetic trees (Webster et al. 2003). For each species represented in a phylogenetic tree, we can measure two values. The first is the total amount of evolution that has occurred between the base or root of the tree and the modern species alive today. The base of the tree represents the common ancestor of all the modern or extant species. We call the amount of evolution that has occurred along each of the paths leading to the modern species, the total path length, and we calculate it as the sum of all the individual branches along the lineage. Bearing in mind that the branches record the amount of genetic change between successive species, the total path length records the amount of genetic change that separates the common ancestral species from its descendants. The second value we record is the number of nodes or historical splitting events along each path through the tree. Some lineages, such as many birds or monkeys living today, have gone through many speciation events since their respective common ancestors. By comparison, it would be interesting if, for example, species we think of today as “living fossils” have had few speciation events since the time of their last ancestor millions of years ago.
Figure 2 shows how the two values that we measure can be obtained from a phylogenetic tree. If evolution proceeds gradually and independently of speciation events, there would be no association or correlation between the number of nodes (historical speciation events) and path length (see Fig. 3a,c). That is, if the process of speciation plays no role itself in causing change, then we do not expect that modern species at the end of paths through the tree with more speciation events will have diverged more from their common ancestor at the base of the tree. If, on the other hand, speciation events are associated with an increase in the rate of evolution, we expect paths with more nodes along them to be longer; where there has been more speciation, more total genetic evolution will have accumulated (see Fig. 3b,c).
Our research group has applied this methodology to a large number of phylogenetic trees to search for evidence of punctuational evolution (Webster et al. 2003; Pagel et al. 2006). In one study, we collected information on the amount of gene-sequence evolution from 122 different sets of species. From these datasets, we constructed phylogenetic trees and examined them for a correlation between the number of speciation events and the amount of molecular evolution. The trees included in our study describe the evolution of organisms as diverse as beetles, mushrooms, rodents and roses. We found that, in 35% of trees we studied, there was evidence for bursts of evolution in genes associated with events of speciation—the signature of punctuational evolution. Figure 4 shows a real phylogeny of a group of endemic Hawaiian plants that displays the distinctive pattern of punctuational evolution. We were also able to examine whether punctuational effects were more common in some kinds of organisms than others. We found that punctuational changes were more common in plants (57%) and fungi (71%) than in animals (21%).
An objection that might be raised about our findings is that rather than indicating an effect of speciation on rates of evolution, the reverse could be true. That is, maybe it is the case that lineages within our phylogenies that have, for whatever set of reasons, higher rates of evolution speciate more often. This would give the pattern of more speciation being associated with more evolution but would say nothing about punctuational change. We cannot strictly rule out this objection but, as we have discussed elsewhere (Pagel et al. 2006), we think it unlikely. Evolutionary biologists have, for decades, sought evidence for traits associated with increased rates of evolution. For example, we might suspect that animals with shorter generation times will evolve more quickly because they reproduce many times for every time that an animal with a longer lifespan does. Very few examples of such traits have been discovered, and in our case we would not expect such traits to differ among the species within a given phylogenetic tree. This is because our trees describe groups of closely related species that tend to be very similar in such background characteristics as generation time or body size and measures of metabolism. For these reasons, we think our analyses point to speciation being the cause of the changes we measure.
Using our phylogenetic method for studying punctuated evolution, it is also possible to calculate how much of the total amount of evolution can be attributed to the bursts associated with speciation events. Each branch of a phylogeny is the product of two processes; some proportion of the evolution is punctuational and some is gradual. We were able to show that on average 22% of the evolution is attributable to the punctuational burst, with the remainder accumulated gradually. Despite there being significant differences in the likelihood of punctuational evolution occurring among plants, fungi and animals, we found no difference in the size of the effect.
Our studies, therefore, suggest that rapid bursts of evolution associated with speciation events represent an important, previously underappreciated contributor to evolutionary divergence. Interestingly, we find no genetic counterpart to the phenomenon of evolutionary stasis, the other part of Eldredge and Gould’s punctuated equilibrium theory. That is, if around 22% of the total evolution arises in bursts, somewhere around 78% is accumulating by gradual means. This may not be surprising because we have studied genes, whereas Gould and Eldredge studied morphology. It is well known that some kinds of genetic evolution can occur without causing a change to the species’ morphology. Evolutionary biologists call these changes neutral to signify that they do not produce measurable changes to the organism. By comparison, nonneutral or what are sometimes called coding changes are changes to genes that lead to measurable changes to organisms.
Our measures of genetic evolution include both of these kinds of change. There is good reason to expect that there will be gradual changes to the coding parts of genes during the long periods of time between speciation events. The coding parts of genes often evolve slowly, so we might expect these changes to be relatively small in number and consequently so might be their influence on the outward form of the organism. By comparison, neutral changes occur in the background all of the time, at a higher rate and independently of whether a species is changing its outward appearance or phenotype. There is reason to expect that these changes will be greater in number than the coding changes. Therefore, the periods of stasis in morphological traits that Eldredge and Gould and others have observed may correspond to periods of predominantly neutral changes in the genes we have studied.
In this sense, the 22% figure associated with speciation is, we believe, large. This is because we think the punctuational episodes are relatively short periods in the lifetime of a species and yet as much as 22% of the total genetic change is occurring in them. It may be possible, in the future, to untangle the evolutionary genetic changes that cause a change to the phenotype and those that do not and study these individually for their contribution to punctuational evolution. At the same time, as it stands, it is important to be clear that our results do not provide either evidence for or against stasis at the morphological level.