Reconstructing Behavior in the Fossil Record

In: Reconstructing Behavior in the Fossil Record. Eds: Plavcan, Kay, Jungers & Van Schaik 2002; Kulwer Academic/ Plenum Publishers, New York

Conclusions: Reconstructing Behavior in the Fossil Record

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MICHAEL PLAVCAN, RICHARD F. KAY, WILLIAM L. J UNGERS, and CAREL P. VAN SCHAlK

Introduction Paleontology is often seen as a descriptive science that d ocuments the morphological diversity of li fe in th e past. But description is jusLthe first step. An animal's morphology ca n offer information about locomotion, habitats, development, diet, social behavior, and other life-history parameters of species, allowing paleontologists LO understand the diversity of adaptations and behaviors of the past. This historical perspective can give a greater understanding of (he origins of adap tations and diversity of extant species. For example, Richmond and Strait (2000) rece ntly argued that [eall"'es of Lhe distal radius of AustraiojJitheClls ajarellsis-an obligate biped - deri ved from a knuckle-

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MI C HAE L PLAVC:\N • Departme nt o r Anatomy, New York College of Osteopathic ro.'ledicinc, Old Westbury, New York 11568; Present adch-ess: Dc parune nt or Anthropology, University of Arkansas, Fayeltc" iIIe, Arka nsas 7270 1. RI CHARD F. KAY • Departm e nt of l~iological Anthropology and Anatomy. Duke University Medi cal Ce lller, Durham, Nort h Carolina 27710. \VILLl Al'vt L. J UNGERS • De partm e nt of A.natomica l Sciences, H ealth Scie nces Center, State University of New York at Stony Bmok , StOIlY Brook, New York 11 79-18081. CAREL P. VAN SC I-lAJK • De pal-tm ent of Bi ologica l Anthropol of:,1' and AnatolllY. Duke Un i,'ersity . Box 90383. Dudmm , North Camli na 27708-0383.

Recotlslnu:lillg Behavior ill Ihr Primflll' Fossil Record, edited by Pla\'can el ill. Kluwcr Acadelllidl)le num rl.1blishers,

ew York. 2002.

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wa lking ances tor. Undersla ndin g th e primitive locomotor behav ior of the a ncestor of hOluinids helps li S to formulate models of the adap ti ve significance of bipeda li ty in ea rly horninids. Likelvise, slIch p aleontological clata can shed lig ht o n wheth e r or not trai ts shared in C0 l11111 0 n by a n exta nt taxo nomic group a re merely shared through common he riLa ge, or are mai ntained through stabilizing selection. For exampl e, Ross et a/ . (this volum e, Cha pter 1) point out that the alte red tooth co mbs or several extinct lemurs indica te tha t the too th co mb of living strepsirrhines is maintai ned by stabilizing selection, rather tha n be ing a phylogen etic constraint.

The Comparative Approach As shown by the pape rs presented here, there are a va rie ty o r ap proaches used to infe r be hav ior in extinct species. T hese range from simple informed specula tion to exu'apo lation fro m well-established form - function rela tionships. Reconstructin g beh avior in any foss il species must strike a bala nce be tween the enthusiastic inference of how a nimals lived in the past, and the ske pticism necessary to understand whe n we cross the bounda ry betwee n supported hypothesis and unsupported speculation. It seems that the skeptical part of the equa ti on is sometimes mi ss ing - while the re are many hypotheses put fon vard about the p ote ntial ada pta tions a ndliJe h istori es of extinct sp ecies. there are few studies tha l critique just h ow far we can go in making such inferences on th e basis of compa rative data. But ske p ticism is hea lthy in that il points to the weaknesses of our arguments and ge nerates new research and new ways o r looking at old data. For examp le. Smith (1 996) de monstrated clearly tha t extrapolation of beh aviors fro m empirica l statis tical relationships ca n be dece ptive if confidence intervals are ignored . Plavca n (2000, this volume) nOLes that e mpirical studies of the relationship be llvee n sexual dimorphism and mating systenls often do not support commonly held reconstructions of social behavior in exti nct species. H yla nde r and J o hnson (this volume) d emon stra te convincingly tha t ex perime ntal data can undermine commonl y held funct ional interpre tations of skele ta l m orp hology . Even so, reconsu"uctio ns of behavior in the fossil record have become much more rigorous in rece nt yea rs as investigators probe the weaknesses of pa rticular models, a nd seek ways to stren gthen comparative models used to infer behavior in extinct species. Ungar (this volume) de mo nstrates the great va riety of information that can be brought to bear on di etary inferen ces, largely as a result of years o f ca reful inves tigation. In this volume, God frey el at., Nunn a nd va n Scha ik, Rovosa and Vinyard , a nd Reed all discu ss innovative a nd relatively unexplored approaches to reconstructing be havior using comparative models. By necess ity , reconstructions o f the behavior of extinct sp ecies are limi ted to the evidence availa bl e in the foss il record . For the most part, th is constitutes osteologica l re ma ins, but other ty pes of evide nce a re some times available. For example, the e nvironmental context in which the foss il was fo und may offer

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insight into wha t th e species was, or was not, d oin g (Reed , this volume; l( ay el,

ai. , th is volume). T hus, a species th a t is consiste ntly round in savann a e nvironme nts probably was not a rboreal. Kay et al. (this volume) use this ty pe o f informati on to infer that Hm:nisella boliviensis was probably a t least partly te rrestria l- a surprising reco nstruction given that all living platyrrhines are almost e nti rely arboreaL Li kew ise, Reed (this volume) po in ts out that early hominicls seemed LO have lived not in savannas-as long assumed - but in ope n woodl and habitats. Thi s has profound impli cations lo r mode ls of earl y huma n evolution , forcing scholars to rethink the d iet, reso urce exploitation, a nd locomotion of earl y h ominids. T he strongest inference or be havior is deri ved from the foss il s themselves, and is usually based on an ada ptive or form - full ction an a logy to extant species. In Lhis volume, Unga r, Ross el al., and Kay et al. a ll point to one of the most \v idely-cited a nd best-kn own examples- the [act that well-d eveloped shea rin g crests on p rimate molar teeth indicate a folivorolls di et, because extant folivo rous primates show e nhanced sh earing on the molars, while nonfolivorous primates do not (Kay, 1975, 1978; Ungar , 1998). Ove r the last several d ecades, there has been a n ex plosion in understa nding the relation be hl.leen fo rm a nd function among ex tan t prima tes in all a natomical regions. T his kn owledge offers an e normous data base for reconstructin g be hav ior in the foss il record, and pote n tia lly allows the synthetic reconstruction or behaviors tha t extend beyond one-to-o ne corres ponde nces be twee n a particular fo rm and a particu lar fun ction (e. g., Godfrey et a.1 ., Jungers et at., and Kay et at. , this volume). It is still common practice to use individual exta nt sp ecies as ana logu es for the be h avior and ecology of simi la r extinct species (e.g., Simons and Ras mussen, 1996; Susma n, 1987; Tanner, 1987). This p ractice will a lways playa vital role in he lping to visualize and understand the bio logy of extinct species. For example, the image of Colopilheclls as rese mbling Sa,im.iri or Nliopithecus in social behavior is powerful (S imon s and Rasm ussen , 1996). But it is clear fro m all the papers in this volume tha t such analogies un to th e mselves do not constitute strong evide nce fo r the be havior of extinct species- there is simply too much va ria tion in the relmion between beh avior and mo rphology among extant species . .Th e behavior of extinct species is usuall y inferred on the basis of comparative an alyses th at seek to test hypotheses of ada ptatio n a nd fun ction in exta nt for ms. T he most widely ci ted me thod for using compara tive analys is to infer adapta tion and Function in ex tinct forms is tha t o f Ka)' and Cartmill ( 1977). 'T o brie fly summarize the ir approach , if a mong exta nt species a trait, T , can be shown to a lways be re lated to a functi on, F, and the lac k of tra it T is always associated with the lack of fun ction r, th e n if a fossil [axon has trai t T it is m ost parsi moni ous to assume that Function F was also present. T his view was put ro nvard in res ponse to the vie"" t.ha t adapta tions of any species Illllst be unde rsLOod in lhe con text of the ad aptations of its a ncestors, and that adapta tion is best und erstood as a [tInction of newly acquired charac ters whi ch indica te changes in form associa ted with changes in funCli on. For example ,

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Szalay and Delson (1979) argued that even though Roonyia possessed relatively large orbits by compa rison to exta nt diu rnal species, it was, nevertheless, probably diurna l because it inherited large orbits From a CO lllm on ancestor. Kay and Cartmill (1977) pointed out that this type of argument creates a n infinite regress. If one must understand the ad ap tatio ns of a species' ancestor in order to understa nd its ada ptations. then how is o ne [0 reconstruct the adaptations of the a ncestor? Presumably by referrin g to its ancestor, a nd so on a nd so on in a n infinite regress . While the argument of Kay and Ca rtmill is relatively straig htforward , recent advan ces in the definition and recognition of adaptations, and in comparative me thods e mployed to test adaptive hypotheses, de mand a reevaluation of the methods lIsed to reconstruct be havior in the fossil record (Ross et al., this volume). For example, Gould and Vrba (1982) pointed out that "adaptation" as a term is over-broad. They suggested that adaptation instead be restricted to traits that d evelop in specific response to selective p ressures. The term " exa p t3lion " was put forward for characters that are associated with some current function , but e ither d eveloped in response to some other selective pressure not associated with the curren t function , or developed as a consequence of some factor other than natural selection. This suggests that the presence of a charac ter in a n ex tinct species may have been associated with a different fun ction than that seen in its descende nt sp ecies. Furthermore, the point made by Gould a nd Lewontin (1979) that all structures do no t necessarily d evelop in res ponse to na tural selection sparked inte nse d ebates about the meaning of form/ function rela tions, adaptation, and the evolutionary mechanisms producing inte rspecific morphological dive rsity. At the very least the result has been the iden tification of a variety of mechanisms for altering form without reference to natural selection-the most famili ar of these being allometric effects. The implica tion is that one-to-one form - fu nction relations are not necessarily ad equate for inferring be havior in the fossil record, and an understanding of evolutionary mechanisms leading to particular forms becomes more important for inferring be havior ["om form . For example, La nde's (1980) model for correlated response between male a nd female characte rs has been used to explain the developme nt of elaborate facial projections and tusks in the fe males of several extinct suids, even though su ch structures probably served Little or no function in the fe males (Wright \ 993). In this sense, the classic form - function rela tion traditionally used to study adaptation becomes a subset of possible causes of the genera tion of morphological form . On th e other hand , Ross et al. and Kay et al. (this volume) point out that, for example, the existence of different definition s of adaptation d oes not necessaril y unde rmine the use of the Kay and Cartmill formula for inferring behavior. Curren t utility, as long as it is unive rsally present, ca n su ggest that stabilizing selection maintains feantres, valida ting th e inference of form/ fun ction relationships in fo ssils. Likewi se, Ross el al. point out tha t the "allomeul' as a criterion of subu'action" formulation comlllonl y llsed in compara tive studies misrepresents Gould's (1966) orig inal formulation, and

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ignores the fact tha t a llomeu"ic relationships may re Aeet ad ap tive cha nges in strUCUIres that are corre la ted ,vith size. The e nd result seems to be tha t car eful scrutiny of wha t is meant by ada ptation, and the biological basis of form/ fun ction rel ationships, lead s to more robust behavioral infere nces.

Phylogeny Most of th e co ntributions to this volume discuss the importance of phylogeny to reco nstructions of behavior in the fossil record . It is now well app recia ted that prima te morph ology represents a m osaic betwee n adapta tion and phylogenetic history. Different species do not res po nd ide ntically to similar selective pressures, and each species faces a unique set of adaptive pressure a nd historical constraints. For example, the re la tionship be tween molar shearing crest development and folivory varies a mong hominoids, platylThines, a nd cerco pithecoids (Kay and Un gar, 1996). The latter have higher shearing quo tients than the fonner two gr oups. Kay and Un gar (1996) also de mon strated a shift in the relationship betwee n [olivory and shearing crest d evelopm ent be t\veen Miocene and exta nt ho min oids, illustrating tha t form -function relationships can vary both among taxa a nd through time. Rece nt years have seen dramatic advances in the formulation of comparative analyses, es pecia lly with re gards to phylogenetic contro l, and many of these are free ly avail able on the web. For example, Kay et a.1. (this volume) use the CAlC (comparative a nalysis using independent contrasts) program of Pagel (1992), available on the Ox ford University web site, and based on Felsenstein's (1985) method of phylogene tic contras ts. T hese methods prov ide p owerful tests of ada ptive hypo theses controlling for the confounding effects of phylogen y. Meth ods based on " k.n own " phyloge n ies a nd di ve rge nce times have been cr itiqued on the basis that the phylogeny and dive rge nce times of many g roups is uncerta in . H owever, simulation sUlclies have de monstrated that even incorrect phylogenies provide better comparative results than sinlple a nalysis of sp ecies values (N unn , 1995; Purvis a nd Webste r, 1999). He nce, it is now widely conside red essential to employ some sor t of phylogene tic contro l in co mparative analys is, unl ess there is an ex plicitly justified reason for ignorin g phylogeny. Ross et al. (this volume) point out that recent years have \vitnessecl some scr utin y about th e ass umptions of phylogene tic an a lysis which is re levant to inferrin g behavior in fossils. The demonstration of phylogene tic correlations d oes not necessaril y prove phylogenetic constraiJl ts, just as a ny correlation c10es no t prove callsation. It has long been acknowled ged tha t the ma intenance of ch arac ters by stabilizing selection obvia tes the need for phylogenetic contl"Ol (Felsenstein, 1985; Pagel and H an 'ey, 1988), th ough the use of phylogenetic a nalysis will not produce a spurious result iJl such a case (Pagel, 1992). Neverthe less, as fa r as l-econstnlCting behavior in foss ils goes, aculally

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CONC LUSIONS, RECONSTRUCTING BEHAV IOR IN THE FOSSI L RECORD iden ti~l ing and quantifying phylogenetic cOlTelations may be more importa nt than simply controlling for potential phylogenetic bias in a comparative a nal ysis. Unfortunately, at this point there is no standard meth od to account for phylogenetic effects on behavioral reconstructions in a man ner analogous to allometric cOlTecti on for the effects of size. The primary concern of these meth od s is proper statistical control for nonindepende nce of d ata points in comparative analyses and elimination of the role of confounding factors in correlated evolution (Felsenstein, 1985; Kay et ,d., this volume ; Nunn, 1995; Pagel and Ha rvey, 1988; Purvis and Webster, 1999; Ross et at., this volume; Smith, 1996). The methods are not easi ly amenable to predicting unknown values in a tra it in a manne r analogous to estimating an unknown value from an empirically deri ved r egression equation. A commonly used technique [o r phy logenetic control often applied to the fossil record is to generate comparative relationships within restricted taxonomic gro ups. One widely known example of this is th e extrapolation of body size from tooth size rela tionships in different taxonomic groups of primates (Conroy, 1987). But this only goes so far, in that it cannot account for morphological shifts over time (as deJl10nstrated for molar shearing quotie nts by Kay and Ungar, 1996), and ca nnol accommodate species that are not clearly or uniquely related to a particular taxonomic group (for exampl e, if tooth size- body size relationships dine r between colobines and cercopithecines, to which group does one compare the common ancestor of the group?). Kay and Ungar's (1996) work suggests that evolutionary trends in the developillent of strucuu"es through time are pote ntially as meaningful as form/function relationships in living forms. Hence, extinct apes may have relatively little shearing by comparison to modern apes, but the developme nt of shearing that is relatively greater tha n Lhat seen in either contemporaries or older ta xa may be strongl y indicative of folivory. Application of such a model may be diffIcult, but potentially fruitful. Essentially, one would compare relative values of a trait among contemporary species, and assume that the total variation in behavi or seen among extant taxa waS similar in the extinct taxa. Such an assumption would itself rest on the assumption that changes in the character state over time reAect quantitative changes in the morpholog ical character, and no t qualitative changes in the basic relationship between form and function . Speculative as this may be, Kay and Ungar's example demonstrates that such an approach can offer powerful insight in to the pote ntial adaptive m eanin g of traits.

Standard Error from Comparative Analyses The previous discussion centered on the facL that most behavioral infe re nces in extinct species are based on eXLrapolation &"0111 a comparative analysis. Smith (1996) pointed out that standard e rrors in comparative relationships are

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MICHAEL PLAVCAN ETAL.

often insu ffi cie ntly apprecia ted by those infelTing life-history para me ters fr om morph ology, leadin g to sta tistica lly meaningless infe re nces. Smith 's logic is not lilnitecl to statistical ex trapolatio ns, though. Un less morphological variati on exactly corres ponds to a ny as pect of behavior, there is a lways e rror associa ted with a reco nsu'licLion (see a lso N un n and va n Scha ik, this volume; Plavcan , this volume). T here are two types of error that are associated with comparati ve analyses-s ta tistical error associated with measurin g and estimating form a nd function , and bi ological error refl ecting the lack of a precise re lation be twee n form a nd fll11c ti o n . The fo nner is fa miliar to most biologists. An y measure me nt of morphology or function is only a n estimate of th e true popula tion paralneter, a nd estima tes of the re la tion betwee n some form and function among sp ecies will consequentl y vary. H owever, there is also biologica l e rror in such relatio nships. As noted b), Jungers et ai. (this volume), estima tes of beha vior based on morph ology are likely to be highly conserva tive, because morphology does not capulre a ll of the Ilmctions and behaviors that are possible with a give n forl11 . Anilnals can easily modify their beh av ior in order to adapt to changes in a n environme nt. Ross et al. (this volume) point to Kinzey's (1978) hypothesis tha t some features are adapted not to common functions, but rathe r for the ex ploitation of " keystone" resources. Likewise, as noted by Ross et al., and H ylander and J ohnson, bony morphology can re present a compromise betwee n multiple functions. As discussed a bove, phylogeny can have a sign ificant impact on the exact design o f a feature. Consequently, the re is norma ll y a large va riation in the relationship be l1veen morphology a nd be havior ac ross species. Smi th 's message, while pointin g to logical p robl ems wi th extrap olating behavior from mo rphology, d oes not undermine behavio ra l inferences. Rather , understanding the underlying biological basis o f e lTor in the relationships should lead to more precise behav ioral inferences for extinct species. ]{nmving tha t there are taxonomic differe nces in form - function re la tionships of the de nti tion should improve dietar y reconstruction s, by limiting the comparative data to th ose anilnals that sePle as the most appropriate comparati ve mode l (Kay et al ., this volume) . Knowing tha t some re lationships are based on operational be havioral categorizations (see be lm\!) that are more or less biologically realistic can a llow one to place greater weight on certa in ty pes of evid ence, and can he lp resolve p ote ntial confl icts in behaviora l reconstn lction s.

Body Mass and Allometry 1n one form or a nothe r, the importance of body mass for reconstructing behavior in the foss il record appears in all chapte rs of this volu me. Body mass clearly plays a role in recon structing a lmost any kind of beh avior through th e

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ubiquitous inAuence of allOlnetl)' on most aspec ts of an animal's lllorphology, behavior, and life history. Many co mparative analyses control for th e al1ometric effects of body mass on morphology. Some studies control for allometric effects on behavior too (e.g. , Harvey et a.1., 1987) . Most allome tric control is straightfonvard-least-squares r egression is carried out on a comparative sample, u si ng the regressio n line a s a "criterio n of subtra ction. " Residuals ar e then used as the actua l clata. There is a large literature on problems associated with predicting variables from least-squares regressions (see Jungers et al ., 1995 for a disclission of the effects of different equations on size and shape). Body mass is clearly related to behavioral/ecolo gical variables in living species, and can play an important role in predicting the behavior of extinct species, especially when used in conjunction with ot her evidence. For example, " Kay's threshold" is a body size criterion for distinguishing between insectivo rOllS and fo livorolls diets of animals with well-developed molar shearing (Kay, 1975; Ungar, 1998, this vo lume). But, as pointed out by Nunn and van Schaik (this volume) and by others, relationships between body mass and behavioral/ ecological variables, while sta tistically significant, often are not strong enough to use body mass alone to predict behavior in th e fossil record. In this volume, Godfrey et al. and Jungers et a.1. both give explicit examples indicating how body mass can be a deceptive variable for reconstructing be havior. Smith (1996) has strongly critiqued the use of body mass in predicting behavioral/ecological traits in fossils on the basis of allometric equations. Apart from the large standard errors typical of relationships between behavioral data and body mass data, there is a problem in that comparative analyses of extant species evaluate th e relationship between body mass and behavioral/ecological variables, while analys es of fossils must extrapola te body mass from skel etal r emains. The extra ste p invo lved in extrapolating body m ass fr0111 the skeletal remains introduces substantial error into th e process (see also Fig. 1 in Nunn and van Schaik, this volum e) . Smith recommends that 1110re studies evaluate the direct relationship between behavioral/ecological vari ables and th e r em a ins that are actually preserved in th e fossil record. Unfortunately, this il11plies that those ·w ishing to infer anything about behavior from body mass in the fossil record wi ll need to empirically examine relations between skeletal variables a nd behaviors th at covary with body mass . Importantly, Ross et a.1. (this vo lume) note that the use of " allometry as a criteri o n of subtrac tion" ignores the fact that allometric r elationships themselves can provide meaningful inform a tion abollt size-related adaptation. An und erstanding of the underlying causes o f an allometric r elatio n ship can at best grea tly stren gthen confidence in behavioral or functional inferences, an d at worst inspire caution in such inferences. Plavca n (this volume) prese nts an example of how al101netric co rrection of data can actually r emove biological information critical to be havioral reconstruction. Occasionally, studies allometrically correct estimates of sexual dimorphism by r egr essing them against bo d y mass (e.g. , Ford, 1994; Mitani et

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ai., 1996). because it is well kn own th a t sexua l dimorphism tends to increase ,vith increas ing body size in primates. Tmporta nLl y, several studies suggest that boely mass has a causal influence on male mate compe tition, Stich that sexu al selection tends to be greater in large r species. This means that the correlatio n bel:\veen dimorphism and body size !night reflect only covariation between body size an d be havior. If true, size adjustment or diJllOrphism ca nnot be justified ror predicting behavior in the fossil record , because it inadve rtently rem oves th e va riation in dim orphism that is caused by beh avior.

Incomplete Extant Models lncomple teness of extant models is a difficult top ic to address. Species represe ntation alone may preclude the development of an adequate comparative model (Foley, 1999). For exampl e, compara tive a nalyses of sexual dimorphism in prima tes suggest tha t there is phylogenetic inertia in the pattern of dimorphism , lha t dimorphism is positively correlated 'with body mass, and the inte nsity of male-male competition, or th e operational sex ra tio, are positively correla ted with body mass. Vet CalofJilhecllS a nd AfJid:i'l