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Homoplasy: Foe and Friend?

‘‘Homoplasy’’ sounds as if itmust be a product of the‘‘Hennigian’’ revolution,

but was coined more than a hundredyears ago by the distinguished biolo-gist E. Ray Lankester, who used it forphenotypic similarities that are inde-pendently acquired. It is the categoryof phenotypic characters that sub-sumes analogies, reversals, and epige-netic similarities—called homoiolo-gies, as well as parallelism andconvergence. Parallelism is the samemorphology produced by the samegenerative processes, whereas conver-gence is the production of the samemorphology by different generativeprocesses. Homoplasy has much totell us about selection and adaptation,yet it weakens the link between phylog-eny and the phenotype. It threatensthe effectiveness and reliability of phy-logenetic systematics because the cla-distic method is predicated by thebelief that covarying characters aremore likely to be homologies thanhomoplasies. Homoplasy is the noisethat drowns out the phylogenetic sig-nal. A recent workshop on homoplasywas organized by Charles Lockwoodand John Fleagle and funded by theWenner Gren Foundation and the In-stitute of Human Origins, to try toreach a consensus about the causes,prevalence, and effects of homoplasywith respect to primate and humanevolution.

Charles Lockwood and Drew Ren-dall reminded the participants thathomoplasy can be a blessing as well asa bane. Lockwood used the example ofSouth American primates to explorethe role of homoplasy in rapidly diver-sifying subfamilies that go on to evolvelocomotor and dietary specializationsin parallel. He found extensive evi-dence of postcranial homoplasies inatelids; if only postcranial characterstates had been used to sort that group,the homoplastic noise would have over-

whelmed the phylogenetic signal. Ren-dall explained that behavioral ecologyis predicated on the notion that simi-lar behaviors are likely to occur inresponse to similar environmental con-ditions. Reversing the coin, behaviorcan be used in phylogenetic recon-struction, but in this case behaviorsthat are less sensitive to environmen-tal pressures, such as some matingbehaviors, are to be preferred.

Another group of papers dealt withattempts to identify and, if possible,localize, homoplasy. Todd Disotell re-minded us that molecular data are notfree of homoplasy and explained thatstrategies for dealing with homoplasyin these data must be chosen intelli-gently. Thus, while it may be logical insome analyses to exclude third basepositions because they are particularlyprone to homoplasy, in other analyses,especially those at a lower taxonomiclevel, the exclusion of these data maydeprive the analysis of signal ratherthan noise. Blythe Williams used ho-moplasy as a tool to investigate therelationship between morphology andthe evolution of dietary preferences inthe Omomyids, one of the two groupsof earliest true primates. However, theassociations she found, such as theone between incisor size and molarshearing, could not necessarily be gen-eralized to other primate groups.

Turning to human evolution, Ber-nard Wood noted that homoplasy hasonly been an issue in hominin evolu-tion since the acceptance that is morecomplex than a ladder-like successionof ancestor-descendant species. Onceit was acknowledged that the occur-rence of multiple synchronic species isthe rule rather than the exception inhominin evolution, researchers be-came interested in techniques to recon-struct the relationships between spe-cies, and were thus exposed to theproblem of character conflict.

Recent reviews of attempts to re-

cover hominin phylogeny using phylo-genetic analysis have shown just howfragile some of these cladistic hypoth-eses are, and have demonstrated thatParanthropus and later Homo are theonly craniodentally based homininclades in which we can have someconfidence. Mark Collard reported theresults of a comparative morphomet-ric investigation to determine whethermasticatory characters are more proneto homoplasy than are data from theother regions of the cranium, andshowed that there is no basis for theseclaims. He went on to show that ifmasticatory characters are given equalweight in cladistic analyses, thenHomo rudolfensis is at least as stronglylinked with the australopiths as withlater Homo. Henry McHenry reviewedthe frustratingly sparse informationavailable for the hominin postcranialskeleton and concluded that at thisstage it is not possible to make generalpredictions about whether the cra-nium or the postcranial skeleton ismore or less prone to homoplasy.Marta Lahr, who showed that even inthe later part of the hominin fossilrecord there were examples of homo-plastic similarities between popula-tions, speculated about possiblemechanisms for this in the face ofother evidence for gene flow betweenthe populations. David Begun lookedat homoplasy more broadly across pri-mates, and concluded that in the con-text of fossil groups homoplasies can-not be identified a priori; they can onlybe identified a posteriori.

Steve Leigh and Laurie Godfrey ex-plored, in different ways, the contribu-tion that scaling, ontogenetic and oth-erwise, can make to determiningwhether apparently similar morpholo-gies have the same developmental ba-sis. Leigh focussed on the papioninsbecause Papio and Mandrillus sharemuch of their cranial morphology, yetthey are apparently not sister taxa.

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Using the papionin molecular phylog-eny as a reference, he employed bivari-ate and multivariate allometric meth-ods to tease out whether ontogeneticallometries could correctly identifymolecular sister taxa. Although Man-drillus and Papio resemble each otherin adult morphology, allometric analy-ses demonstrate major distinctions be-tween them. Godfrey introduced amodeling tool she and Michael Suther-land have developed. The model iscapable of dealing with trait or agematrices and ontogenetic series cap-tured in Euclidean shape space, and itis designed to simulate the effects ofthe eight generally recognized ontoge-netic processes, namely progenesis,hypermorphosis, neoteny, accelera-tion, predisplacement, postdisplace-ment, and rate hypo- and hypermor-phosis. The model can also calculatethe probability that heterochronic pro-cesses are sufficient to explain thebiological differences.

Four of the contributions addressedstrategies for identifying or ameliorat-ing the effects of homoplasies by mix-tures of empirical investigations andexploration of the developmental ba-sis of the potentially homoplastic mor-phology. Jukka Jernvall made us awareof the huge potential for dental homo-plasy. He estimated that living primateupper molars manifest fewer than 10%of the possible permutations of cuspmorphology and reminded us that thehypocone has evolved at least seventimes in primate evolution. He set outa hypothesis for the sequence of activa-tion of the regulatory genes respon-sible for cusp formation in upper mo-lars. From this, he predicted thatcharacters based on ‘‘short,’’ late-developing cusps are likely to be rela-tively unreliable as phylogenetic sig-nals. Wolfgang Maier drew on hisunrivaled knowledge of tooth morphol-ogy and his fine collection of wholeand sectioned embryos for examplesof homoplasy that ranged from thecrista obliqua in maxillary molars tothe complexity of the ethmoidal turbi-nates. Daniel Lieberman presented theresults of a study designed to identify,a priori, character states that are morelikely to be homoplastic within the

hominin clade. Collaborating with Col-lard, he brought together informationabout phenotypically-plastic responsesto strain in bones, and the effective-ness of craniodental variables for re-covering well-established molecularphylogenies. He found that there wasno simple relationship between charac-ters subject to high levels of strain,homoiology, and phylogenetic valency.Indeed, these variables were more ef-fective at recovering phylogeny thanwere less phenotypically-plastic char-acters. Is this association due tochance, or can variables be both highlyepigenetic within a species and effec-tive proxies from genetic propinquityat higher taxonomic levels? DavidStrait reported the early stages of afinite element analysis study designedto establish just which parts of theface of Paranthropus are designed toresist high masticatory stresses. Themodel will be validated using actualstrain data recorded in macaques. Theface of Paranthropus will then be sub-stituted and its strain regime calcu-lated. Testing facial features in thisway should help establish whether theyare functionally-integrated, and there-fore ‘over-represented’, in phyloge-netic analyses of early hominins.

Two contributions, by Brian Halland Judith Masters, effectively drewtogether, in different ways, the theoreti-cal, developmental, and operationalthreads of the homoplasy problem.Hall reminded us that that homologyis not the neat, well-defined conceptthat many had hoped it would be.Many apparently homologous struc-tures have different developmentalmechanisms. Moreover, the samedevelopmental mechanisms can havedifferent phenotypic manifestations.Hall used examples that ranged fromthe relation between Pax-6 and eyedevelopment to the roles of SOG andchordin in dorso-ventral patterningin arthropods and vertebrates. Theclear message is that homoplasy andhomology are not dichotomous states,but are the extremes of a spectrum.Developmental biologists are as muchin need of sound molecular phylog-enies as are paleontologists. Mas-ters’ presentation was equally impres-

sive and wide-ranging. She drew onexamples from African galagos toshow that while some structures wererepeatedly subject to homoplasy,others were persistently resistant tochange. Her theme was that no matterwhether researchers were workingwith molecular, morphological, orbehavioral evidence, we should bemore discriminating about the typeof evidence used. In each of theserealms of evidence it is clear that whilesome systems are strongly canalizedothers can be much more easily per-turbed.

What, then, are the lessons to belearned by the foot-soldiers who, likethe writer, regard homoplasy as thesand that disrupts the well-oiled clad-istic machinery we use to recover phy-logeny? First, we have to accept thathomoplasy exists and is very common.It is not just the result of ‘‘bad science,’’such as poor character choice. Sec-ond, in the absence of an independent,sound, molecular phylogeny, we havelittle prospect of labeling any charac-ter as 100% homologous or 100% ho-moplastic. As they say in all goodmanagement courses, insistence on100% achievement is the enemy ofprogress. As paleontologists, we willhave to be content with circumstantialevidence about homoplasy. Third,there is apparently no region of theprimate or hominin cranium that isthe equivalent of a homoplasy ghetto.Homoplasy affects all parts of the skel-eton in many ways. Last, we mustrealize that ‘‘homoplasy is data.’’ Ho-moplasy may interfere with our at-tempts to recover one aspect of evolu-tion, phylogeny, but if we only knewhow to recover phylogeny, homoplasyhas the potential to tell us about thehistory of adaptation. Is that not aprize worth striving for?

Bernard WoodHenry R. Luce Professor of Human Origins

George Washington UniversityDepartment of Anthropology

2110 G St NW Washington DC 20052Tel: (202) 994-6077

Fax: (202) 994-6097bwood@gwu.edu

r 1999 Wiley-Liss, Inc.

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