Some Light on the Mystery of Mysteries

Phylogeography: The History and Formationof Species By Avise, John. Cambridge MA: Harvard University Press (2000). 447 pp. $49.95In 1838, John W. F. Herschel, the son of the astronomer William Herschel and a photographic pioneer who actually invented the term photography, wrote a letter to Charles Babbage (the inventor of the computer). The letter was not about photography or computing machines, but about the nature of biological species. In the middle of it he said, “Of course I allude to that mystery of mysteries, the replacement of extinct species by others.”Charles Darwin wrote down Herschel's phrase in his notebooks with delight, and used it in the introduction to The Origin of Species. There he modestly said that he hoped to cast some light on the problem that Herschel had found so puzzling.Darwin's book certainly did cast a great deal of light on the process of evolution, but in spite of its title it did not cast very much on the origin of species itself. It left unanswered two very large questions. First, why are species such apparently discrete entities, in many cases so clearly separated from each other that it is easy for laypeople as well as taxonomists to classify them? Second, although his theory required that they must have arisen from different ancestral species in the past, what were the mechanisms by which they did so?We now know very much more than Darwin did about both of these questions. The problem of the morphological and behavioral separation between species has turned out to be far more difficult to answer than the problem of their origin; geneticists, ecologists, and behaviorists are still wrestling with it.The origin problem is rather more tractable. This new book is by John Avise of the University of Georgia, a pioneer in the use of sequence data to study the origins of species. The book is well written, and is a useful addition to the many books on the subject of evolutionary relatedness.We now know, as Darwin did not, that the sequences of genes obtained from present-day organisms contain a great deal of information about their past. The sequences can be obtained either from proteins or directly from DNA, and can be used to build trees of relatedness. These trees can in turn gives us a good idea of the genes' history. This remarkable insight, traceable to Walter Fitch and Emmanuel Margoliash (Science 155, 279, 1967), has revolutionized the science of taxonomy. It has also given rise to endless controversy.For example, for years there has been a bitter argument between two great schools of taxonomic thought. The first of these schools, the pheneticists, claim that in order to carry out the classification of organisms we dare not use anything other than measures of present-day phenotypic or genetic relatedness. Pheneticists point out that both the fossil record and geographic information are suspect sources of information. Fossils are a worry because we cannot be sure how the fossils that we have found in the rocks are related to the organisms that are alive today—they might easily have been on lineages that went extinct. Inference from geography is also a danger, because geography is always changing in unpredictable ways.But pheneticists can be fooled—convergent evolution can produce organisms or gene sequences that resemble each other, not because of recent common ancestry, but because they have converged on similar characteristics. Until recently, a group of Australian crow-like birds were classified with the crow family that is found in the rest of the world. But molecular studies have now shown that they are actually very distant from the crows and more related to the bower birds (C. Sibley et al., Auk 105, 409, 1988)!The second great school is made up of cladists, who claim that the order of the branches in the tree is centrally important, because it tells us far more about the sequence of evolutionary events than the mere degree of relatedness. Unfortunately, the branching order that can be inferred from sequences is often ambiguous, so it is frequently necessary to use information from geographical distributions and the fossil record to clarify the tree's structure. Cladists, by drawing on all the available information, take a far more holistic, evolutionary approach to the question of tree-building than do the pheneticists. At the same time, like the pheneticists, they run the risk that they can be led astray by misleading evidence.Avise does not discuss this controversy directly in his book. This is surprising, because the approach that he concentrates on is one that is helping to bridge the gap between these two schools of thought. The term “phylogeography,” which he and a number of his colleagues coined in 1987 (Annu. Rev. Ecol. Syst. 18, 489), is simply the application of gene data to questions of geographic distribution. This approach asks how much information can be gained from the gene sequences themselves, in order to wring as much evidence as possible out of them concerning their branching order. Pheneticists might quarrel with these methods, but if evidence for past events is really to be found in the sequences then it seems only fair that it should be used. This is particularly the case if the evidence agrees with what we can infer from fossils and geography.How much information is concealed in the gene sequences and overlooked if a simple measure of similarity is used? Sometimes, it turns out, there is quite a lot. For example, simply by comparing the sequences in a sample in all pairwise combinations, a great deal can often be revealed. As Henry Harpending and others have realized (Rogers and Harpending, Mol. Biol. Evol. 9, 552, 1992), the shape of this distribution can provide evidence for changes in population size over time.Tree patterns can also reveal considerable amounts of information. Avise has been one of the pioneers in the use of concordances of tree patterns between different genes and different populations. Are the tree patterns similar for different genes in the same species? If not, the data may be too noisy to be of much use. Does a single gene show the same pattern in two species? If it does, then the species are likely to have split very recently. Does a gene show the same pattern in two subpopulations of a species that are found in different geographical regions? If so, then these regions are likely to have been colonized recently.The book provides many examples of the use of phylogenetic concordance, particularly in the analysis of freshwater fish populations in the U. S. Southeast. These examples show that careful analysis of multilocus genetic polymorphisms can reveal a great deal about the history of their carriers.All is not plain sailing, however. The gene sequences can pack nasty surprises, some of which Avise discusses. One of these is the matter of the timescale of divergence. Mitochondrial sequences in many animal species can, because of their low levels of recombination, be traced back to an ancestral sequence from which all present-day sequences are descended. Coalescent theory, which follows a diversity of sequences back in time until the various sequences all coalesce into one, allows an approximate time to be calculated for this ancestral sequence. The most famous of these dates is the widely publicized coalescence time of about 200,000 years ago for the human species (R. Cann et al., Nature 325, 31, 1987). Unfortunately, the errors on this number are enormous and are not symmetrically distributed around the modal estimate. The distribution of possible coalescence times always has a great long tail that extends into the distant past. This is because, while the probability of a coalescence event is a constant per unit time, the number of coalescence events remaining drops dramatically as you move back in time. As a result of this uncertainty, for example, the question of when the human mitochondrial Eve lived, and which species she belonged to, is still very much an open one.The human mitochondrial tree has other problems that Avise only briefly examines. Mutational “hot spots” in the sequences can cause bases to flip back and forth repeatedly, losing phylogenetic information in the process. Correcting for this phenomenon can increase phylogenetic information (C. Wills, Evolution 50, 977, 1996), but even after this the tree is still untidy—mitochondrial sequences still do not sort out neatly along racial or geographic lines. It is likely that much of this remaining untidiness is the result of complex migration patterns throughout our history, perhaps confused even further by the occasional recombination event. In this case, the fossil and geographic evidence does not agree with that of the genes; it will be a long time before these conflicts are fully resolved and understood.Phylogeography is a useful term for the efforts to squeeze as much information out of gene sequences as possible, and Avise's book provides a good introduction to some of the problems that can be solved. I could only wish that the book had done a better job of placing these techniques in the broader context of taxonomic studies as a whole.