114 Update TRENDS in Ecology and Evolution Vol.22 No.3

Letters Of clades and clans: terms for phylogenetic relationships in unrooted trees

Mark Wilkinson1, James O. McInerney2, Robert P. Hirt3, Peter G. Foster1 and T. Martin Embley3

1 Department of Zoology, The Natural History Museum, London, SW7 5BD, UK 2 Department of Biology, National University of Ireland, Maynooth, Co. Kildare, Ireland 3 Division of Biology, The Devonshire Building, University of Newcastle upon Tyne, Newcastle upon Tyne, NE1 7RU, UK

During the late 1980s, the molecular biology community of misinterpretation. The unrooted relationships to be became aware that the words ‘homology’ and ‘similarity’ described are precisely those that could be converted into were being used in much of the scientific literature as though the analogous rooted relationship by rooting the tree. they were synonyms. This situation was clarified [1] and We propose the term ‘clan’ (from the Gaelic for family) as their current usage is usually appropriate. Recently, we the unrooted analogue of monophyletic group or clade. have felt a similar need for standard and indeed, new, There are two complementary clans for every nontrivial terminology for describing relationships in unrooted phylo- split or bipartition in an unrooted tree. Were the tree to be genetic trees in our teaching of molecular evolution. Distinct rooted, at least one of the two clans defined by a given split terms could help teachers to explain, and students to under- would necessarily be monophyletic. A trivial split in an stand, the fundamental concept of phylogenetic relation- unrooted tree [i.e. between one of the leaves (terminal taxa, ships and the important differences between unrooted and OTUs) and all the others] yields a single clan. rooted trees. Rooted trees have an explicit ancestral node We suggest using ‘adjacent group’ as the unrooted that is known, whereas unrooted trees have no such node. analogue of sister group. Clans or leaves are adjacent Unrooted trees are common in molecular phylogenetics. groups if there is some rooting of the tree in which they However, much of the terminology used to describe are sister groups. In a fully bifurcating rooted tree, a clade relationships in trees was developed for rooted trees. or leaf has a unique sister group; by constrast, in an The use of terms and phrases such as ‘clade’, ‘monophyletic unrooted tree, each has up to three adjacent groups group’, ‘more closely related to’ and ‘sister taxa’ to describe (Figure 1), underlining the potential for selective misap- relationships in unrooted trees is problematic, but not plication of rooted tree terminology. Exceptionally, for uncommon [2–7]. clans that include all but one leaf (corresponding to a To say that some genes or taxa are more closely related trivial split), that single leaf is the only adjacent group to each other than they are to others is to say that they of those clans. To convey the unrooted analogue of the have a common ancestor that is not an ancestor of any of rooted ‘some taxa are more closely related to each other the others (i.e. that they share a more recent common than to some other taxa’, we recommend ‘some taxa are ancestry) [8]. Similarly, to say that a group is monophy- split from some other taxa’. letic, or that it is a clade, is to say that all of its members are more closely related to each other than any of them are to any non-member. To say that two groups are sister taxa is to say that they are each others closest relatives [9,10]. Thus, all of these concepts can be specified only by rooted phylogenetic trees. It is clear that unrooted trees do convey information about phylogenetic relationships. For example, they tell us that some sets of taxa cannot be either monophyletic or sister taxa under any possible rooting. They tell us that some groups could be clades or could be sister taxa given one or more rootings of the tree. Given the increase in the number of unrooted trees being published, we suggest that it would be useful to have terms that provide us with unrooted counterparts of ‘clade’, ‘more closely related’ and ‘sister groups’. Distinct terms would help prevent misapplication of rooted tree terminology to unrooted trees and would avoid the concomitant danger Figure 1. An unrooted tree with the ‘clan’ including E, F and G encircled. E, F and G are ‘split from’ A, B, C and D and vice versa. Arrows indicate the seven possible rootings under which the encircled clan is also a clade. Its three adjacent groups Corresponding author: Wilkinson, M. ([email protected]). are A and B (roots 3, 4 and 5), C and D (roots 2, 6 or 7) and A, B, C and D (root 1); if Available online 18 January 2007. the encircled clan is a clade, one of the adjacent groups must be its sister taxon. www.sciencedirect.com Update TRENDS in Ecology and Evolution Vol.22 No.3 115

Our prime concern is that the use of the terminology of Gnetales’ closest relatives are conifers. Proc. Natl. Acad. Sci. U. S. A. rooted trees to describe relationships in unrooted trees 97, 4092–4097 4 Brochier, C. et al. (2004) Archaeal phylogeny based on proteins of the implies an assumption that the root is in a part of the tree transcription and translation machineries: tackling the Methanopyrus that would make the use of the rooted terms correct. kandleri paradox. Genome Biol. 5, R17 Injudicious use of rooted terms could lead to incompatible 5 Cnor, B. et al. (2003) Maximum likelihood on four taxa phylogenetic assumptions regarding the position of the root. In many trees: analytic solutions. In RECOMB’03 (Vingron, M. et al., eds), p. unrooted trees, the root might not be known exactly, but 7683, ACM Press 6 Hall, B.G. (2004) Phylogenetic Trees Made Easy, Sinauer Associates assuming that it occurs in some part of the tree might be 7 Xia, X. (1998) The rate heterogeneity of nonsynonymous substitutions quite reasonable and, therefore, justify judicious use of the in mammalian mitochondrial genes. Mol. Biol. Evol. 15, 336– rooted term. Such assumptions are better stated than 344 implied. 8 Wilkinson, M. (1994) Common cladistic information and its consensus representation: reduced adams and reduced cladistic consensus trees and profiles. Syst. Biol. 43, 343–368 References 9 Kitching, I. et al. (1998) Cladistics: The Theory and Practice of 1 Reeck, G.R. et al. (1987) ‘Homology’ in proteins and nucleic acids: a Parsimony Analysis, Oxford University Press terminology muddle and a way out of it. Cell 50, 667 10 Page, R.D.M. and Holmes, E.C. (1998) Molecular Evolution: A 2 Ben Ali, A. et al. (2001) Phylogenetic relationships among algae based on Phylogenetic Approach, Blackwell Science complete large-subunit rRNA sequences. Int. J. Syst. Evol. Microbiol. 51, 737–749 3 Bowe, L.M. et al. (2000) Phylogeny of seed plants based on all three 0169-5347/$ – see front matter ß 2006 Elsevier Ltd. All rights reserved. genomic compartments: extant gymnosperms are monophyletic and doi:10.1016/j.tree.2007.01.002

Book Review On Lilliputians and Brobdingnagians Why Size Matters: From Bacteria to Blue Whales by John Tyler Bonner, Princeton University Press, 2006. US$16.95/£9.95 hbk (176 pages) ISBN 0 691 12850 2

Andre J. Riveros

Center for Insect Science and ARL, Division of Neurobiology, University of Arizona, Tucson, AZ, 85721-0077, USA

Size is one of the most conspicuous our universe. But for Bonner, size is much more than just properties of anything occurring in the a static physical property in those macro and micro living or inanimate world. We see around worlds. In fact, the fundamental argument of his book us small and large living and non-living gives size a central role as a ‘dynamic’ property (a mover entities; our universe is enormous and in evolution and not just a by-product of it) that is size even characterizes our immaterial strongly tied to fundamental features of living systems, images of gods and thoughts. We obvi- such as shape, structure and function. He develops his ously assign those differences in size by argument through five rules that are supported by cor- comparison, according with the perception relates of size: strength, surface, abundance, complexity of our own size. But, are those differences and rates of living processes. in size relevant in the natural world? Does size really The first three rules are strongly connected to physical matter? These questions are far from trivial and are shared laws or constraints. Strength and surface relate to the fact by scientific disciplines as diverse as ecology, evolutionary that certain magnitudes characterizing an object vary with biology, neurobiology and developmental biology, among different powers as size varies. Surface and strength others. increase with a square power of the linear dimension, In Why Size Matters, John Tyler Bonner categorically similar to the surface area of a sphere. By contrast, weight argues that size is a fundamental factor in evolution; in and volume increase with a cubic power, similar to the his own words: ‘No living entity can evolve or develop volume and the weight of the sphere just mentioned. How- without taking size into consideration’. Bonner starts ever, abundance is linked to a more obvious physical law: with a nice historic view of the human perception of bigger entities occupy more space, which makes the relation- size, from the development of Galileo’s telescope to ship between size and abundance the only rule exhibiting a observe distant celestial bodies to van Leeuwenhoek’s negative correlation. This is exemplified in living forms, for microscope to discover the micro world. Today, such tools which being bigger also means greater resource require- have their modern descendants that range from the ments and, consequently, lower population densities. Hubbell telescope to the electron microscope, which give The other two rules, complexity and rate of living us a new understanding of the micro and macro levels in processes, have been of special interest in previous works [1,2] by Bonner and a considerable portion of this book is

Corresponding author: Riveros, A.J. ([email protected]). devoted to them. On the one hand, changes in size go along Available online 2 January 2007. with increases or decreases in complexity, which, in Bon- www.sciencedirect.com