Speciation and phylogenetic resolution

CORRESPONDENCE References

21 Van Schaik, C.P. and Dunbar, RIM. (1990) Behamour 115.

1 Kleiman, D.G.and Malcolm, J. (1981) in Parental Behauior in Mammals (Cubernick, D.J. and Klopfer, P.H., eds), pp. 347-387,

Plenum Press 2 Rood, J.P. (1974) Nature 248, 176 3 Whitten, P.L. (1987) in Primate Societies (Smuts, B.B., Cheney, D.L., Seyfarth, R.M.,Wrangham, R.W. and Struhsaker, T.T., eds), pp. 343-357, University of Chicago Press 4 Brown, R.E. (1993) Behuu. Processes 30, l-28 5 Moehlman, P.D. (1989) in Camioore Behaoiour, Ecology and Euolution (Cittleman, J.L., ed.), pp. 143-163, Chapman &Hall 6 Sussman, R.W. and Garber, P.A. (1987) Int. J. frimatol. 8, 73-92 7 Wright, P. (1990) fnt. J. Primatot. 11,89-102 Aspects of.Social Euolution 8 Packer, C. (1986) in Ecological (Rubenstein, D.I. and Wrangham, R.W., eds), pp. 429-451, Princeton University Press 9 Rood, J.P. (1986) in Ecological Aspects ofSocial Evolution (Rubenstein, D.I. and Wrangham, R.W., eds), pp. 131-152, Princeton University Press 10 Coldizen, A.W. (1987) in Primate Societies (Smuts, B.B., Cheney, D.L. Seyfarth, R.M.,Wrangham, R.W. and Struhsaker, T.T., eds), pp. 34-43, University of Chicago Press 11 Cantoni. D. and Vogel, P. (1989)Anim. Behau. 38,205-214 12 Haenel, N.J. (1986) in The Behauioural Biology ofKiller Whales (Kirkevold, B. and Lockard, J.S., eds), pp. 285-300, A.R. Liss 13 Lopez, J.C. and Lopez, D. (1985) J. Mammal. 66,181-183 14 Barlow, G.W. (1972) Euotution 26, 307-310 15 Francis, CM., Anthony, E.L.P.. Brunton. J.A. and Kunz, T.H. (1994) Nature 367,691-692 16 Hector, A.C.K.,Seyfarth. R.M. and Raleigh, M.J. (1989) Anim. Behau. 38,262-271

17 Xia, X. and Millar, J.S. (1988) Can. J. Zoot. 66, 1184-1187 18 Clutton-Brock, T.H. (1991) The Evolution offarentof Cure, Princeton University Press 19 Maynard Smith, J. (1977) Anim. Behau. 25, l-9 20 Wynne-Edwards. K.E. and Lisk, R.D. (1989) Physiol. Behau. 45, 465-469

Speciation and phylogenetic resolution In their recent TREE article on speciation patterns, Hoelzer and Melnickl suggest that polytomies in phylogenetic trees should be considered as viable hypotheses of descent relationships in the same manner as bifurcating topologies. Although we appreciate their suggestion that some evolutionary events resulting in speciation are timed so closely together that this might result in poorly resolved or unresolved cladograms, we are concerned by their claim that this pattern should be accepted as a hypothesis of descent relationships among the taxa being studied. Even more alarming is the lack of a hypothetico-deductive process in their examination of the effects of speciation on cladogenesis. The issues raised by Hoelzer and Melnick are valuable, but their conclusions require further comment. The first problem centers on the lack of resolution inherent in many systematic studies at what Hennig2 called the interface between tokogeny and phylogeny. Tokogenetic relationships are characterized by reticulation and occur below the level of cladogenesis. Davis and Nixon3 elaborated on this subject and developed a rigorous and logical method for determining when phylogenetic analysis of entities is

30-62 22 Kruuk, H. (1989) The Social Badger, Oxford University Press 23 Trivers, R.L. (1972) in Sexual Selection and the Descent of Man (Campbell, B., ed.), pp. 136-179, Aldine 24 Hector, A.C.K.,Seyfarth, R.M. and Raleigh, M.J. (1989)Anim. Behal;. 38,262-271 25 Wynne-Edwards, K.E. and Lisk. R.D. (1984) Anim. Behau. 32. 626-628 26 Goldizen, A.W. (1987) Behau. Ecol. Sociobiol. 20.99-109 27 Small, M.F. (1990) Am. J. Primatol. 20, 267-282 28 Emlen, S.T. (1991) in Behaoiourat Ecology (3rd edn) (Krebs. J.R. and

Davies, N.B., eds), pp. 301-337, Blackwell 29 Creel, S.R., Wildt, D.E. and Monfort, S.L. (1993) Am Nat.141, 816-825 Rothe, H., Darms, K., Koenig, A., Radespiel, U. and Juenemann. B. (1993) Int. J. frimatot. 14, 79-93 31 Mills, M.G.L.(1990) Katahari Hyaenas - Comparatiue Behauioural Ecology of Two Species, Unwin Hyman 32 Macdonald, D.W. (1993) The Vetuet Ctow: A Naturn/ History of the Carnivores, BBC Books 33 Terborgh, J. and Goldizen, A.W. (1985) Behuu. Ecol. Sociobiol. 16. 30

293-299 34 Paul, A.. Kuester. J. and Arnemann, J. (1992) Folio Primatol. 58, 93-98 35 36 37

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Packer, C. (1980) Anim. Behau. 28,512-520 Rasa, O.A.E.(1987) S Afr J Wildt. Res. 83. 587-590 Ferrari, S.F. (1992) Am. J. Primatot. 26, 109-l 1X Price, E.C. (1990) Anim. Behau. 40, 784-786 Soini, P. (1982) FoRa Primatol. 39, 1-21 Oftedal, O.T. and Gittleman, J.L. (1989) in Camiuore Behuuiour, Ecology and Euotution (Gittleman, J.L.. ed. ). pp. 355-378. Chapman & Hall Malcolm, J.R. and Marten, K. (1982) Behac. Ecol Sociohiof. 10,

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Creel, S.R. and Creel, N.M. (1991) Behnv. Ecol Sociobiol. 28,

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appropriate. Their ‘population aggregation analysis’ takes the attributes observed for individuals in populations and determines whether or not these attributes are characters or traits. Only characters are used in phylogenetic analysis to discover the hierarchical descent relationship of populations. The lack of resolution at the interface between tokogeny and phylogeny has been discussed by many authors (Refs 2-5) as the outcome of reticulation. We suggest that the lack of resolution, and hence the need to call a set of relationships between taxa a polytomy, results from improperly using traits to infer phylogenetic patterns. Another possible explanation for the generation of polytomous relationships among taxa in a phylogenetic analysis concerns the treatment of competing phylogenetic hypotheses. In general, many investigators have used the consensus approach to reconcile competing hypotheses. This method invariably results in conservative phylogenetic hypotheses but has less explanatory power compared to fully dichotomous hypotheses. Several systematists6-8 have pointed to the logical inconsistencies involved in the use of consensus both for equally parsimonious trees generated for a data set and for competing hypotheses among data sets. There are several methodological and philosophical questions, not addressed by Hoelzer and Melnickl, that could help resolve the problem of polytomies. The first concerns choosing among equally parsimonious cladograms generated from the same data set. Character

weighting based on the homoplasy inherent in the characters in a data matrix allows choice among equally parsimonious cladograms7,9,10. Given that character weighting is a necessary part of phylogenetic analysisll, acceptance of all of the equally parsimonious trees generated from a single data matrix as equally viable hypotheses, is not necessarily warranted. This approach also suggests that acceptance of polytomous relationships produced by consensus of these ‘parsimony’ trees is equally unwarranted and philosophically unsound. Concerning competing hypotheses among data sets, total evidence approachesI*. have the greatest explanatory power (but see discussion in Ref. 14) and should also be considered as a viable method of inferring hierarchical descent relationships. The total evidence approach directly addresses the statement made by Hoelzer and Melnick concerning human-chimp-gorilla relationships: ‘.. .there is now a consensus that the origins of these three species occurred over a very brief period. Consequently the issue cannot be solved by collecting additional data or by rigorous statistical analyses’. Wheeler15 has shown in a series of computer simulations that addition of characters to a data matrix results in increased phylogenetic resolution while addition of taxa to a data matrix results in increased cladogram accuracy. Several empirical studies have also borne out these expectations, suggesting that resolution and accuracy are increased by the addition of data.

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CORRESPONDENCE Our second major concern with the kind of logic employed by Hoelzer and Melnickl centers on the scientific method employed. In their approach, it appears that geological or climatic events, and their impact on the divergence of the taxa involved in the classification, are more important in estimating the phylogeny than the character-state evidence belonging to the taxa. We argue that the geological and climatic information should be incorporated into hypotheses concerning the taxa under study and that these hypotheses be tested using all available evidence. While we do not dispute that these processes might have an effect on the patterns observed in phylogenetic analysis, we are concerned with the ad hoc assumption that they do. We are most alarmed by the statement in Hoelzer and Melnick’s last paragraph: ‘...the polytomous branching topology should be accepted, even if the dichotomous branching order can be supported by statistical analysis’. Advocating the rejection of a null hypothesis in the face of evidence to the contrary is a dangerous proposition. Such rejection removes a hypothesis from the realm of science and places the scientific value of a study in question. Since the exact details of the past events of divergence discussed by Hoelzer and Melnickl are unknowable, reconstructing them enters the realm of science only when investigated under a framework of well-articulated and testable hypotheses.

Rob DeSalle Dept of Entomology, American Museum of Natural History, New York, NY 10024, USA Robin Absher Dept of Biology, Yale University, New Haven, CT 06511, USA George Amato Science Resource Center, Wildlife Conservation Society, Bronx Zoo, Bronx, NY 10460, USA References 1 Hoelzer, G. and Melnick, D. (1994) Trends Ecol. Evol. 9, 104-107 2 Hennig, W. (1966) Phylogenetic Systematics, University of Illinois Press 3 Davis, J.I. and Nixon, KC. (1992) Syst. Biol. 41, 421-435 4 Kluge, A.G. (1989) Cladistics 5, 291-294 5 Vrana, P. and Wheeler, W.C. (1992) Cladistics 8, 67-72 6 Miyamoto, M.M. (1985) Cladistics 1, 186-189 7 Carpenter, J. (1988) Cladistics 4, 291-296 8 Barret, M., Donoghue, M.J. and Sober, E. (1991) Syst. Zoo/. 40,486-493 9 Farris, J.S. (1969) Syst. Zoo/. 18, 374-385 10 Goloboff, P. (1991) Cladistics 7, 215-232 11 Farris, J.S. (1983) Cladistics 2, 7-36 12 Kluge, A. (1989) Syst. Zoo/. 38, 7-25 13 Ernisse, D. and Kluge, A. (1993) Mol. Biol. Evol. 10,1170-1195 14 Bull, J.J. et al. (1993) Syst. Biol. 42, 384-398 15 Wheeler, W. (1991) in Extinction and Phylogeny (Novacek, M. and Wheeler, Q., eds), pp. 205-215, Columbia University Press

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Hoelzer and Melnickl describe two conditions under which polytomies, rather than dichotomous branches, may be defensible in phylogenetic reconstruction. One, termed a hard polytomy, exists when an ancestral species gives rise to three or more descendant species simultaneously, and there is no dichotomous branching sequence to reconstruct. The other, designated a soft polytomy, is admissible when phylogenetic relationships are impossible to reconstruct because, although the descendant taxa arose through a series of dichotomous branching events, the events occurred over such a short period that little, if any, opportunity has existed for character state changes to occur. The dichotomous branching pattern cannot be reconstructed because of a lack of information on relationships. The condition for which Hoelzer and Melnick permit a soft polytomy is actually an example of a larger phenomenon. The inability to reconstruct a dichotomous history will arise any time an ancestral species gives rise sequentially to two or more species without changing between speciation events. Descendant species will not share derived character states solely with the ancestral species, and a polytomy is the only possible reconstruction. ‘Living fossils’ - species that persist for very long periods without observable change - provide extreme examples of what may be a fairly common occurrence. Species may exist for long periods with little or no change in morphology or behavior, while giving rise sequentially to descendant species through vicariant events that isolate populations. Rapid speciation is not necessary for soft polytomies. Hoelzer and Melnick noted that additional data sets may reveal synapomorphies necessary to represent the dichotomous history of the group. Even in apparently stable species, one would expect long intervals between speciation events to produce detectable synapomorphies in evolutionarily unconstrained characters as a result of neutral mutations and drift. Unfortunately, these data often are unavailable when constructing a phylogeny, and a soft polytomy is the most acceptable representation of branching events.

L.M. Page S.M. Phelps Illinois Natural History Survey, 607 E. Peabody Drive, Champaign, IL 61820, USA References 1 Hoelzer, G.A. and Melnick. D.J. (1994)

Trends

Ecol. Evol. 9, 104-107

Reply from GA. Hoelzer and D.J. Melnick We agree for the most part with the comments of Page and Phelps. They have expanded on some of the ideas presented in our original articlel. However, the comments of DeSalle et al. demand closer scrutiny. They argue in favor of accepting a bifurcating topology for a phylogenetic tree under

circumstances that we believe may not warrant such a conclusion. In our opinion, this practice invites Type-l error in the estimation of tree topology. DeSalle et al. ignore the logical possibility of polytomous origins (i.e. hard polytomies), despite the literature on this topic (e.g. Refs 2-4) and the potential examples documented in our articlel. Indeed, their suggestion that polytomies should not be considered as legitimate hypotheses of evolutionary descent rests on the assumption that hard polytomies do not occur in nature a position we feel is untenable. DeSalle et a/. go on to make two specific criticisms. First, they suggest ways they believe can accurately resolve polytomies. These include: (1) ignoring all polymorphic data (i.e. use only ‘characters’ rather than ‘traits’s), presumably including gene frequency data; (2) the use of total evidence; and (3) character weighting, which is also promoted as ‘a necessary part of phylogenetic analysis’. The insistence on character weighting is puzzling given the frequency of published phylogenies for which characters were unweighted, including recent papers by DeSalle (e.g. Refs 6,7). In general, while these methods (including successive weightings) may resolve some polytomies, they may create others and surely will not resolve all polytomous nodes all the time. Furthermore, any analysis that replaces a hard polytomy with a series of bifurcations is misleading. The second major criticism is that we ‘appear’ to suggest that geological or climatic events should play an important role in phylogeny reconstruction. This is a distortion of our position. We merely pointed out that particular geological and climatic histories could yield polytomous origins and we used examples from the literature where this seems to be the case. In none of these cases, nor in any of our own research, was geological history used as evidence for a particular tree topology. Finally, the main point of our paper seems to have been lost on DeSalle et a/. That is, when the distance between nodes of a bifurcating tree is so small that the nodes may represent alternative conditions in a polymorphic ancestor, then the bifurcating topology may be wrong. This topological error may be statistically supported, even though there is no way of determining whether it accurately reflects the branching order of speciation or the tokogenetic relationships among populations in a polymorphic ancestor. There is also no way of knowing whether or not these two topologies are congruent. Hence, the information generally available to investigators, regardless of quantityg,lO, is sometimes insufficient to determine the branching order of species in a bifurcating tree. We applaud the development of moresophisticated methods aimed at the accurate resolution of soft polytomies; however, we stand by the following recommendations: (1) polytomies should be considered as phylogenetic hypotheses until they are satisfactorily resolved, because hard polytomies are a natural possibility; and (2) nodes should be collapsed into polytomies when they are so close together that they may reflect an ancient polymorphism, even if the bifurcating topology can be supported with statistical methods, because the reticulated pattern of gene flow and subsequent differential sorting of genetic variants can obscure the true TREE uol. 9, no. 8 August

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