Phylogeny and classification of birds: A study in molecular evolution

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we must ning a

struggle

as ecologists

run-

race between documentation and disappearance or, perhaps, documentation or disappearance. And so when Webb writes, in this volume, on ‘Beyond the forest’ or Engel on ‘Rainforest as metaphor’ or Ratcliffe on ‘Science and ethics’, the working rainforest ecologist will sympathize with the attempt to express the intangible that anyone of any sensitivity who has entered a rain forest has sensed. This does not mean that one must espouse some of the more extreme tenets of ‘deep ecology’ or return to some modified preRaphaelite pastoral ethic, or attempt to twist Judaeo-Christian exploitationist philosophy into a return to sustainability, although these responses, to varying degrees, have been the responses of some. It is sufficient to recognize, simply, that there is more to human experience than simple description of the parts. In no other ecosystem that I am aware of is the systems notion of the whole being more than the sum of the parts so obvious as it is in rain forests. The whole is an object that inspires reverence as well as scientific curiosity. Reverence may be humanistic or religious or animistic and each will use their own metaphors to verbalize feelings, as have the various contributors to Webb and Kikkawa’s book. This section of the book is to be read for its thought-provoking qualities, not to be agreed with or disagreed with, necessarily, but to remind ecologists that they must see beyond their databases, vital as these are, if they are to convince nonscientists of the global importance of their enterprise - and nowhere is this more pressing than in the case of rain forests. This book joins a growing number of others that help provide answers to the ‘why?’ questions that ecologists are required to answer more and more in venues as different as the common room, the lecture theatre and the courtroom. Some of these deal with ethical and philosophical issues7, others with the aesthetics, others the economicg, yet others the historicall and sociological”. These works take the biologically trained ecologist into unfamiliar territory but territory into which we are obliged to go. Webb and Kikkawa’s volume provides an accessible approach to many of these issues and as such it will prove to be an invaluable resource. R.L. Kitching Dept of Ecosystem Management, University of New England, Armidale, NSW 2351, Australia

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References 1 Francis, W.D. (1929) Australian Rainforest Trees, Australian Government Publishing Service 2 Kitching, R.L., ed. (1988) The Ecology of Australia’s Wet Tropics (Proceedings of the Ecological Society of Australia, Vol. 151, Surrey Beatty 3 Rainforest Conservation Society of Queensland (1986) Tropical Rainforests of North Queens/and, Australian Government Publishing Service 4 Mitchell, A.W. (1986) The Enchanted Canopy, Macmillan 5 Head, S. and Heinzman, R. (1990) Lessons of the Rainforest, Sierra Club 6 Caufield, C. (1984) In the Rainforest: Report from a Strange, Beautiful,

1991

imperiled World, University of Chicago Press 7 Norton, B.G. (1986) The Preservation of Species: the Value of Biological Diversity, Princeton University Press 8 Ritchie, R. (1989) Seeing the Rainforests in 19th Century Australia, Rainforest Publishing 9 Myers, N.A. (1983) Wealth of Wild Species: Storehouse for Human Welfare, Westview 10 Dargavel, J., Dixon, K. and Semple, N., eds (1988) Changing Tropical Fores% Historical Perspectives on Today’s Challenges in Asia, Australasia and Oceania, Centre for Resource and Environmental Studies, Canberra 11 Hull, D. (1990) Science as a Process, University of Chicago Press

AvianPhylogenyand Distribution Phylogeny and Classification of Birds: A Study in Molecular Evolution by Charles G. Sibley and Jon E. Ahlquist, Yale University Press, 1990. f60.00/$100.00 hbk (xxiii + 976 pages) LSBN 0 300 04085 7

Distribution and Taxonomy of Birds of the World by Charles G. Sibley and Monroe, Jr, Yale University 1990.f75.00/$125.00hbk(xxiv paged ISBN 0 300 0469 2

Burt L. Press, + 1117

Charles Sibley has been interested in classifying birds for many years. In 1955 he produced a synopsis of birds of the world, subtitled ‘A manual of systematic ornithology’, and his efforts have not stopped since. Sibley has worked towards that one meaningful classification, the phylogeny. In the early 1970s he was using protein structure as a taxonomic character, but a decade later he had started publishing the results of the herculean task that he and Jon Ahlquist had set themselves to classify the birds of the world using DNA-DNA hybridization techniques. Now we have two books of truly historical significance. The first book, coauthored with Ahlquist, contains details of the methods used and the results obtained. The second, coauthored with Monroe, brushes aside technical detail to provide a listing of birds of the world, a taxonomy for them and details of their distributions and lifestyles. The taxonomy, being based on Sibley and Ahlquist’s studies, may be unacceptable to some, but the species accounts will be a goldmine for ornithologists and comparative

biologists alike. In addition to notes on habitats for each species, distributions are quite carefully described, with all place names being referenced in a gazetteer, allowing them to be located in an appendix of maps that cover the world. Sibley and Ahlquist’s book has been long awaited. Indeed, many practising research scientists already use Sibley and colleagues’ classification of birds in preference to more eclectic alternatives. One reason is that a hierarchical classification using the DNA-DNA hybridization method is likely to produce a reasonable reflection of phylogenetic relationships. In contrast, the standard classifications produced by so-called evolutionary taxonomists, who use both phylogenetic relationships and morphological similarity, allow evolutionary convergence to influence the decisions that are made. Of course, it might be argued that DNADNA hybridization is not simply a measure of divergence but a compound measure, including evolutionary parallelism and evolutionary convergence in addition to evolutionary divergence. DNA-DNA hybridization can be acceptable, therefore, as a reflection of phylogenetic tree structure, insofar as parallel and convergent evolution are not important at the DNA level. As Sibley and Ahlquist and others have claimed before, it seems a reasonable conjecture that DNA divergence, when measured over such a large part of the genome, is far more prominent than either parallelism or convergence. Much of Sibley and Ahlquist’s book is given over to describing the logical and technical basis for their methods. Perhaps some of their critics will be silenced. Our own view is that these

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authors have done much more than make an important start. Sibley judges the enterprise in the preface: ‘Our data are not perfect . . . that we should have done many things better is undeniable, but hindsight is always crystal-clear. We urge critics to set up their own laboratories, collect the necessary specimens, and improve on our work . . . perfection is for the future’. Some of their data are provided in the form of melting curves that depict the relationships between the percentage of single-stranded DNA and temperature for various cross-species comparisons (heteroduplex hybrids) and single-species standards (homoduplex hybrids). A summary statistic is calculated, and dendrograms are produced using both average-link clustering and the Fitch-Margoliash method. There are many reasons why Sibley and Ahlquist’s dendrograms might not represent the true phylogenetic-tree topology. For example, their summary statistics may be unsuitable, extrapolations are sometimes made necessary by experimental conditions, the clustering procedures may be inappropriate, replicated data are few and DNA divergence rates may differ among lineages. Unfortunately, only some of the data are provided and then only in graphical form, so it would not be possible for those who prefer other statistics or tree-building algorithms to use them on the data. In part, the authors might be criticized as having taken on too broad an enterprise, resulting in shallow conclusions. However, we wonder how we might have proceeded in their place. A pleasing feature of Sibley and Ahlquist’s book is the historical review of avian classification, which covers all the important taxonomic developments from the system that Linnaeus proposed, in the mid-18th century, onwards. It becomes clear how patterns in osteological structure, moulting sequence and protein electrophoresis are distributed among the groups of species and how these lines of evidence square with the DNA-DNA hybridization data. This interesting section also explains the inclusion of some rather odd species among the melting curves. For example, although almost every taxonomy previously published places the Old and New World vultures together in a group with the other diurnal birds of prey, it is not an original suggestion that the very obvious similarity between them represents convergent evolution. Sibley and Ahlquist place the New World vultures in the same family as the storks, in a group which,

if we follow the calibration they give us, may have diverged from the other raptors some 80 million years ago. Sibley and Ahlquist have shown several very interesting relationships and have probably cleared up some old debates, such as whether the hoatzin, a strange South American bird not obviously similar to any other species, is a cuckoo or a galliform. Perhaps more importantly, they have answered questions about a good many of the passerine relationships. Now the affinities of various families, such as the crows and shrikes, seem clearer, and we have a better idea of where to place some genera, many of which have been variously redistributed among different families for over two centuries. For example, if we are to believe the results, the members of the genus Melampitta really are birds of paradise, the bird known as the blackcollared triller is not a triller at all but a thrush, and Donacobius is a true wren; the list is long and remains, of course, far from complete. There are still many species whose affinities are unclear. The taxonomy is developing by a process of successive approximation toward a correct representation of the phylogenetic history. In 1982, Sibley and Ahlquist considered that the sylviine warblers and the babblers were taxonomically inseparable, that they were ecological groups and that if, say, the Dartford warbler was found in Asia instead of Europe it would be a babbler and not a warbler. With better evidence, they have now separated these tribes again. But, whereas the sylviines in 1982 included most European warblers, they now have only one genus. The others have all been moved to a different subfamily on the basis of new comparisons. But Sibley and Ahlquist have still not compared the DNA of all the species involved. The classification presented in the new book may be the best yet at representing the phylogeny, but it is not perfect. There are many comparisons still to be made for which Sibley and his co-workers have simply not been able to obtain the relevant DNA or for which they have ;.ot had time. And repeating some r.irmparisons would, no doubt, produ’ ‘9 slightly different results. We *,b;ght expect, and indeed we are lea .a believe in the introduction to the book, that the DNA-DNA hybridization technique reveals the ‘branching pattern of the phylogeny because the net effect of genetic evolution is divergence’. However, the evidence is not always quite so certain. For example, some of the melting-curve diagrams for the

ratites show that when one of the two rheas (the South American representatives of the group) is used as the tracer DNA, the Australasian ratites cluster together, apparently having the most similar DNA. The ostrich, the only African bird in this group, is further away from the rhea. The graph constructed with the ostrich as the tracer again shows the AustraloPapuan species clustering together and again, of the three groups, the ostrich and the rhea are furthest apart. But other curves, using other species as tracers, show what appear to be differing results, and the three tree-building algorithms used by the authors give three different possible phylogenies. There is little difference in the age at first breeding in the ratites as a group (which is the only measure of generation time that Sibley and Ahlquist can sensibly consider). They plump for a ‘tree that has the ostrich and rheas as sister taxa. We think they are right - the Indian Ocean between Australia and the Africa-South America complex opened up and separated the cassowary-kiwi lineage from that of the other species in this group before the Atlantic separated the rhea clade from the ostrich. But the example serves to show that the hybridization data must be treated with caution. One point puzzles us. The authors claim that generation time rather than chronological time dictates rate of DNA divergence, and that their trees are therefore somewhat erroneous - species with long generation times will be on branches that are too short. Nothing other than a few anecdotes are provided to support this very important claim, while trees have not been adjusted accordingly. Perhaps it was too late to change the trees, but the properly documented evidence is crucial. What Sibley and Ahlquist have produced is, we think, a phylogeny that will form the basis for subsequent studies. That is no mean achievement and, if he was the type to do it, Sibley might reasonably rest on his laurels. Already, others have taken up the cudgels, some to batter, others to defend. We return to the quotation from Sibley and Ahlquist’s preface, which has reflected A.C. Wilson’s approach: his laboratory at Berkeley has been doing exactly what needs to be done, and that is to perform more accurate tests, using better methods and improved forms of analysis.

Paul H. Harvey Peter Cotgreave Dept of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK

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