796 BOOK REVIEWS

Molecules and Morphology in Evolution: Conflict or Compromise?

Edited by Cohn Patterson (1987). Cambridge: Cambridge University Press. x + 229 pp. ISBN O-521-32271-5 (hbk), o-521-33860-3 (paper).

Compromise, of course. “I am not arguing,” wrote Simpson, “that any one kind ofevidence on evolution-genetic, molecular, phenotypic, or other-is superior but, on the contrary,

that no one kind s&ices in itself’ (Simpson, 1964, p. 1537). But just try to convince a molecular biologist!

Colin Patterson has edited a timely and interesting volume, one that I admire, and several contributions to which are truly insightful. A few general comments before tackling the papers,individually. First, readers of the book may be warned to wear sunglasses, lest their eyes be seared by the incandescence of Willi Hennig. Second, the city of Berkeley, California seems under-represented among the contributors (well, non-represented, to be more accurate) given the disproportionate contributions of that city to the subject of the book. Third, the wedding between the bones and the genes is a shotgun wedding, and Patterson does an excellent job (with very few exceptions) in keeping both sides of the family under rhetorical restraint. And fourth, is a primitive character plesiomorphic or plesiomorphous?

The first paper is an overview by Cohn Patterson, which sets forth the principles of phylogenetic analysis clearly. If evolution consists primarily of character transformation in a series ofconstantly bifurcating populations, and to a first approximation it may well, then there’s little to argue with. I would only add that in my opinion one good distance outweighs five bad characters.

Patterson accepts a protein clock on the basis ofabout 80 amino acid differences between shark alpha hemoglobin (on the one hand) and carp, salamander, chicken, mouse, and human (on the other). He misses a critical point, however, namely that the number of differences underestimates the number of substitutions. The data are consistent with wild fluctuations in rate, given two assumptions: first, that the molecule can only tolerate change at roughly 80 positions without sacrificing the integrity of the protein; and second, multiple substitutions at the same site after the molecule has “maxed out” at 80 are

undetectable. Nevertheless, Patterson’s discussion of homology in the context of the genome is terribly

important, and should be absorbed by all students interested in molecular evolution. If more geneticists read and appreciated this paper, there would be a lot less to argue about.

Andrews, though rejecting the protein clock accepted by Patterson, provides a clear analysis of the phylogenetic relationships of the Hominoidea, the best paper on the subject I have seen. I feel, however, that he takes the general transition/transversion bias in DNA evolution a little too much to heart, to the point of only reluctantly conceding that transitions are even informational. It probably shouldn’t be that much of a factor in taxa so closely related.

Further, Andrews cites two shared derived amino acid substitutions linking human and chimp that require comment. In the beta globin cluster, gene correction occurs between the gamma-A and the gamma-G gene in the Hominoidea: the two genes evolve in concert. In all the relevant taxa the two adjacent genes have the same codon sequence at position 104, except Gorilla, where gamma-G codes for Lys (as in Homo and Pan), and gamma-A has Arg (as in Pongo). It can thus either be an Arg to Lys change in the ancestor of Homo and Pan,

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followed by a parallel mutation in gamma-A of the gorilla, or an Arg to Lys change in an ancestor of Homo, Pan, and Gorilla, followed by a back-mutation in gamma-G of Gorilla. There is simply no way of telling. The other amino acid substitution linking Homo and Pan is alpha-globin 23, which looks better, but is actually fairly weak also. Humans and chimps have Glu, gorillas and orangs have Asp; but the two amino acids have similar properties and flip back and forth over the course of evolutionary time. The only gibbon sequence is a tentative partial sequence (Boyer et al., 1972), and as Andrews notes, many cercopithecines

have Glu (Kleinschmidt and Sgouros, 1987). Andrews blithely predicts that “in the long term it is undoubtedly [DNA] sequencing

that will provide the answers” (p. 31). But vis-&is Homo-Pan-Gorilla I don’t see that to the present it’s done anything other than confuse us more; and I’d be willing to bet a sixpack against Andrews’ optimism. The problem, I think, is the null hypothesis used in such studies; the null hypothesis is not that there are no synapomorphies linking two taxa, but that there are more homoplasies than synapomorphies. The implication of a failure to reject this null hypothesis is the likelihood that one could sequence forever, but if the phylogenetic signal-to-noise ratio doesn’t improve dramatically, the trichotomy will never

be resolved that way. McKenna performs a phylogenetic analysis at the protein level, by eyeballing the amino

acid substitutions in alpha-lens crystallin. His is a very successful integration of molecular data into a “case-study” of phylogeny. While his method may not be sufficiently high-tech for some, it drives home an important point about the advantages of gestalt analyses over electronic-the disadvantage is having to make sure you counted correctly.

Bishop & Friday successfully challenge the assumption of parsimony in protein phylogeny, by showing that a handful of amino acid substitutions actually link birds to mammals rather than to crocodiles. I am reminded of a comment by Lewontin: “Nature does not always operate by the simplest mechanism, and the principle of parsimony is only a methodological convention, not a fundamental revelation of the structure of the universe” (Lewontin, 1966, p. 339).

But then Goodman, Miyamoto and Czelusniak clasp William of Ockham to their collective bosom, and generate fully dichotomous parsimony trees. What might be useful in this type of analysis is an estimate of the level of non-parsimony acceptable-say 2% (?). Then, if a tree requires 1000 steps to be constructed, any branches saving fewer than 20 steps should be considered unresolved. For, in the absence of information on the topology of all trees requiring 1000-1020 events, the most parsimonious tree is the equivalent of an uncontrolled experiment, for we have nothing to compare it with. I see no reason to present as resolved any nodes which may not in fact be resolved by the given analysis: if this volume demonstrates anything, it’s that the general level of confusion is high enough already.

In Woese’s paper a little bit of molecular machismo emerges. Since the analytical grounds for his conclusions concerning the phylogenetic relations of bacteria are not made clear in the review, 1 can’t address those. However, his churlish remarks toward traditional modes of evolutionary studies, particularly in relation to rates and modes of change, seem to overlay a fundamental lack of familiarity with them. He says, for example, “‘it is important to note . that I use the term [macroevolution] as used by Simpson, i.e., to denote unexpected drastic and bizarre changes in phenotype, that occur relatively rapidly, etc.” (p. 179). The work he cites, however, uses the term in question to refer to “the rise of taxonomic groups that are at or near the minimum level of genetic discontinuity (species and genera)” (Simpson, 1944, p. 98).

798 BOOK REVIEWS

Woese’s opinion is that “[tlhe concept of the molecular clock is perhaps the most

important addition to evolutionary doctrine since the time of Darwin” (p. 181). Well,

certainly since the time of Kimura, I’d concede. And he summarizes: “Genotypic change

tends to be ‘clock-like’ and measures evolution’s tempo. Phenotypic change is its mode”

(p. 181). Perhaps his comment that “What we know today about the tempo-mode problem

is little more than what we knew 50 years ago” would be more apt in the first person

singular.

Fitch & Atchley perform the most interesting analysis, though ultimately inconclusive.

Using strains of laboratory mice whose genealogies are historically documented, they

asked whether genetic or phenotypic data can generate a concordant tree. Genetic data;

they find, do; morphological data don’t. Their phenotypic analysis, however, consists of a

phenetic study of 14 measurements of the mandible. It is interesting that the genetic data

yield the accurate phylogeny, but not really surprising that a limited phenetic

morphological analysis wouldn’t. That’s why people do phylogenetic analyses instead.

Nevertheless, a broader study of this nature would be very interesting.

Sibley & Ahlquist have a paper on birds, but in the absence of available documentation

the work merits no comment. They are, interestingly, the lone defenders in this volume of

the phenetic approach (though used without comment by Woese and Fitch & Atchley),

and their rationalization for it bears quoting:

If we are ever to reconstruct phylogeny, it must be done with methods that do not rely on the human eye as the instrument of comparison. It is self-deluding to assume that what we see is all we need to know to reconstruct phylogenies. Such a procedure is subjective and qualitative, and results only in an opinion-and this is a definition ofArt, not of Science. For a method to qualify as scientific, it must be objective and quantitative (p. 118, emphasis in original).

Enough to bring tears to Francis Bacon’s eyes. Actually, an “artist” with some pretty good

opinions was William King Gregory, who wrote way back in 1910 that:

Phylogeny is essentially an inductive subject, a reasoning by analogy, which is the shifting sand whereon hypotheses and theories are built. In general, the student must (1) concede nothing more than he is forced to, (2) strive to separate probability from plausibility, (3) test his hypotheses by the principle of negation, and (4) avoid explaining the little known through the less known. Above all (5) he must strive to keep in touch with all data bearing on the subject, (6) make constant reviews to see that no pertinent fact has been omitted and (7) test again and again his basal assumptions (Gregory, 1910, p. 106).

In all, Patterson’s book bears out this assessment. The question is not which set of data is

better, but rather which of the many facts we have at our disposal are telling us history, and

which are lying to us about it?

JON MARKS

Departments of Anthropology and Biology, Box 2114, Yale Station,

Yale University,

New Haven, CT 06520, U.S.A.

References

Bayer, S. H., Noyes, A. N., Timmons, C. F. & Young, R. A. (1972) Primate hemoglobins: polymorphisms and evolutionary patterns. J, hum. Ed 1, 515-543.

Gregory, W. K. (1910) The orders of mammals. Bull. Am. Mu. nut. Hist. 27, l-524.