evolution of hipercanivory - the effect of specialization[1]

q 2004 The Paleontological Society. All rights reserved. 0094-8373/04/3001-0000/$1.00

Paleobiology, 30(1), 2004, pp. 108–128

Evolution of hypercarnivory: the effect of specialization onmorphological and taxonomic diversity

Jill A. Holliday and Scott J. Steppan

Abstract.—The effects of specialization on subsequent morphological evolution are poorly under-stood. Specialization has been implicated in both adaptive radiations that result from key inno-vations and evolutionary ‘‘dead ends,’’ where specialized characteristics appear to limit subse-quent evolutionary options. Despite much theoretical debate, however, empirical studies remaininfrequent. In this paper, we use sister-group comparisons to evaluate the effect of morphologicalspecialization to a particular ecological niche, hypercarnivory, on subsequent taxonomic and mor-phological diversity. Six sets of sister groups are identified in which one clade exhibits hypercar-nivorous characteristics and the sister clade does not. Comparison results are summed across thecategories ‘‘hypercarnivore’’ and ‘‘sister group.’’ We also evaluate whether increasing degrees ofspecialization are correlated with decreasing phenotypic variation. Results presented here indicatethat specialization to hypercarnivory has no effect on taxonomic diversity, but a strong effect onsubsequent morphological diversity related to the jaws and dentition, and that increasing special-ization does not correlate with morphological diversity except in the most specialized saber-toothed taxa, which exhibit higher variance than less specialized morphs, possibly due to selectionon other characteristics.

Jill A. Holliday and Scott J. Steppan. Department of Biological Science, Florida State University, Talla-hassee, Florida 32306-1100. E-mail: [email protected], E-mail: [email protected]

Accepted: 21 May 2003

Introduction

The effect of specialization on subsequenttaxonomic and morphological evolution isfundamentally important to the tempo andmode of evolution and the role of adaptationin macroevolution (e.g., Futuyma and Moreno1988; Janz et al. 2001). However, there is littleconsensus as to how specialization affects di-versity: does it act to increase or decrease ratesof cladogenesis? How does specialization af-fect probability of extinction? Does it con-strain further adaptation? Certainly, much at-tention has been given to the possibility thatparticular specializations may promote taxo-nomic diversification; that is, a morphologicalor behavioral specialization may act as a keyinnovation, leading to an increase in rates ofcladogenesis (Liem 1973; Mitter et al. 1988;Farrell et al. 1991; Hodges and Arnold 1995;de Queiroz 1999; Dodd et al. 1999), but em-pirical studies have produced contrasting re-sults. Some workers have found that speciali-zation increases taxonomic diversity (e.g.,Liem 1973; Mitter et al. 1988; Farrell et al. 1991;Hodges and Arnold 1995; de Queiroz 1998;Dodd et al. 1999), some report the opposite

pattern (e.g., Price and Carr 2000), and othersfind no effect at all (e.g., Wiegmann et al. 1993;de Queiroz 1999; Janz et al. 2001).

Despite numerous studies of the effect ofspecialization on taxonomic diversification,studies of its effects on subsequent morpho-logical diversity (disparity) are few. In a the-oretical context, many workers have suggest-ed that possession of certain morphologicalcharacter states may reduce the ability to at-tain certain other states (Lauder 1981; Smith etal. 1985; Emerson 1988; Futuyma and Moreno1988; Werdelin 1996; Donoghue and Ree 2000;Wagner and Schwenk 2000), implying that thesubsequent evolutionary trajectories of somespecialized taxa may be limited. At its ex-treme, therefore, specialization could act as adead end (Moran 1988; Janz et al. 2001), lim-iting morphological diversification and poten-tially reducing rates of cladogenesis or, alter-natively, increasing extinction rates as special-ized taxa reduce their ability to adapt tochanging conditions. However, few studieshave directly identified and tested effects ofspecialization on subsequent phenotypicchange (but see Liem 1973; Moran 1988; War-heit et al. 1999).

109EVOLUTION OF HYPERCARNIVORY

We determined the effect of dental and cra-nial specialization to a meat-only diet, hyper-carnivory, on subsequent morphological andtaxonomic diversity in mammalian carni-vores. We used an explicitly phylogenetic ap-proach and applied it to repeated convergenc-es on hypercarnivory, increasing our statisti-cal power by evaluating results from multiplesister groups. We specifically tested the hy-potheses that (1) hypercarnivores have lowertaxonomic and craniodental morphologicaldiversity than do their sister groups and (2)increasing specialization leads to lower mor-phological diversity. To test these hypotheses,we quantified and compared diversity be-tween hypercarnivore clades and their prim-itively nonhypercarnivorous sister groups.The advantage of using sister groups is thatboth groups (when their stem lineages are in-cluded) have by definition had equal time todiversify. We used both species counts and themethods of Slowinski and Guyer (1993) to as-sess taxonomic diversity. We compared mor-phological diversities (disparities) by compar-ing variances of factor scores obtained fromprincipal-components analysis (Foote 1992,1993; Wills et al. 1994) and by comparing thedifferences in average frequency of characterchange between categories (Sanderson 1993).Finally, we used discriminant function anal-ysis to assign ‘‘degrees of specialization’’ tohypercarnivores and compared the disparityvalues of different levels of specialization.

The Order Carnivora

The order Carnivora is composed of 11 ex-tant and two extinct families of meat-eatingmammals. The diagnostic character for Car-nivora is the carnassial pair, the fourth upperpremolar and first lower molar, which in thisgroup have been modified as shearing bladesfor effective slicing of meat. Although theshearing carnassials are a synapomorphy forthis group, members of Carnivora, hereaftercalled carnivorans, have diversified to occupya wide range of ecological niches, and includehighly carnivorous clades such as cats (Feli-dae) and weasels and martens (Mustelidae),generalists like the dogs and foxes (Canidae),insectivores like the mongoose (Herpestidae),omnivores like the bears (Ursidae) and rac-

coons (Procyonidae), and strict herbivoressuch as the giant panda. Variation in ecologyis strongly reflected in the dentition (Van Val-kenburgh 1989), so a more omnivorous/fru-givorous diet is accompanied by a relative in-crease in grinding surfaces whereas a morehighly carnivorous diet is reflected by a rela-tive decrease in grinding surfaces and an in-crease in shearing edges.

Because of the tight correlation betweendentition and ecology, dental characters canbe used effectively to infer aspects of the dietor ecological niche. Van Valkenburgh (1988,1989) showed that variables including relativeblade length, canine tooth shape, premolarsize and shape, and grinding area of the lowermolars distinguished between dietary typesin extant carnivores. She compared guildcompositions of carnivoran communities,concluding that each guild comprised abroadly similar set of morphotypes occupyinga limited number of ecological niches (VanValkenburgh 1988, 1989). There is thus a sub-stantial overlap in certain regions of mor-phospace (Crusafont-Pairo and Truyols-San-tonja 1956; Radinsky 1982; Van Valkenburgh1988, 1989) resulting from convergence of un-related taxa to similar ecomorphologicaltypes, including meat-specialists, bone-crack-ers/scavengers, omnivores, and generalists(Van Valkenburgh 1988; Werdelin 1996). Suchiterative evolution produces natural replicatesand is conducive for comparative study.

Of the recognized carnivoran ecomorphs,the niche of the meat specialist, or hypercar-nivore, is associated with a diet comprisingmore than 70% meat, in contrast to the gen-eralist (Van Valkenburgh 1988, 1989), whichmay eat 50–60% meat with vegetable matterand invertebrates making up the remainder ofthe diet. Ecological specialization to hypercar-nivory is associated morphologically withspecific changes in the skull and dentition thatinclude a relative lengthening of the shearingedges, composed of the trigon of the upperfourth premolar and the trigonid of the lowerfirst molar, and reduction or loss of the po-stcarnassial dentition, the second and thirdlower molars and first and second upper mo-lars, teeth used for chewing or grinding food(Van Valkenburgh 1989; Hunt 1998). The facial

110 JILL A. HOLLIDAY AND SCOTT J. STEPPAN

portion of the skull frequently shortens aswell, an alteration thought related to main-taining high bite force (Van Valkenburgh andRuff 1987; Radinsky 1981a,b; Biknevicius andVan Valkenburgh 1996). Although the absenceof dietary data for many fossil taxa suggeststhat the term ‘‘hypercarnivore-morph’’ maybe more appropriate, in this paper those taxawith morphological characteristics consistentwith a hypercarnivorous diet will be called‘‘hypercarnivores.’’ Figure 1A illustrates ageneralized carnivoran with a ‘‘typical’’ toothformula; individual cusps are labeled. Figure1B–D illustrates hypercarnivorous modifica-tions in order of increasing specialization.Certain extant and extinct members of suchdiverse lineages as mustelids (weasels andstoats), viverrids (civets and genets), canids(dogs and foxes), hyaenids (hyenas), amphi-cyonids (extinct bear-dogs), and ursids (bears)have all evolved phenotypes characteristic ofhypercarnivory (Van Valkenburgh 1991; Bik-nevicius and Van Valkenburgh 1996; Werdelin1996), although the most extreme cases ap-pear to be in the families Felidae (cats) andNimravidae (extinct, noncat saber-tooths).Taxa trending toward hypercarnivory are fre-quently referred to as ‘‘cat-like’’ (Martin 1989;Hunt 1996, 1998; Baskin 1998), a descriptorthat reflects the distinctive adaptations of fe-lids for this niche.

In a study of evolution of hypercarnivory inthe family Canidae, Van Valkenburgh (1991)commented on the low apparent variability inthe cranial and dental morphologies of felidsand nimravids relative to canids, and sug-gested that this was possibly due to the ex-treme specialization to hypercarnivory in theformer two groups. Lack of variation in felidcraniodental characteristics has been notedqualitatively by many authors (e.g., Radinsky1981a,b; Flynn et al. 1988), but few have at-tempted to quantify this phenomenon or to as-certain cause and effect. Quantitative evalua-tions of felid diversity have been generallylimited to within family or genus (e.g., Glassand Martin 1978; Werdelin 1983; Kieser andGroeneveld 1991; O’Regan 2002) or, if amongfamilies, have dealt primarily with relativepositioning of groups in morphospace (e.g.,Glass and Martin 1978; Radinsky 1981a,b,

1982; Werdelin 1983; Van Valkenburgh 1991)or body-size correlates (Van Valkenburgh1990; Gittleman and Purvis 1998; Gardezi andda Silva 1999).

There are, of course, various reasons whyany particular clade might not exhibit certainmorphologies, including lack of genetic vari-ation, functional constraint, stabilizing selec-tion, or competition (Smith et al. 1985; Brooksand McLennan 1991). Additional causes mayinclude intrinsically low rates of evolution ora recent rapid radiation (Schluter 2000), eitherof which might suggest a pattern of constraintbut actually reflect a lack of time. Anotherpossibility is sampling bias, where alternativemorphotypes may exist but occur in geo-graphic areas where sampling is rare or non-existent. Any study of the evolution of a char-acter therefore benefits from the inclusion ofas many different groups as possible that haveevolved the trait of interest. We evaluated sixseparate clades of hypercarnivorous taxa forwhich phylogenies are available in the litera-ture. By including a variety of groups, wewere able to mitigate the effects of phylogenyand thus evaluate the effects of the speciali-zation itself. Furthermore, because differenthypercarnivorous taxa exhibit varying degreesof specialization, we could also assess the ef-fects of increasing specialization on characterchange and morphological diversity.

Methods

Definition

Because identification of a hypercarnivo-rous taxon is partly a subjective decision,opinions may vary between workers. In abroad sense, the designation ‘‘hypercarni-vore’’ has been used to describe taxa that haveincreased the slicing component of the denti-tion relative to the grinding component (VanValkenburgh 1991). However, taxa that fit thisoverall categorization can be further subdi-vided according to relative robustness (wid-ening) of the premolars (Van Valkenburgh1991). In combination with the features ofelongated blade, reduced postcarnassial teeth,and a shortened face, normal-sized or nar-rowed premolars produces the ‘‘cat-like’’ phe-notype. In contrast, relative broadening of the


FIGURE 1. A, Generalist dentition. The talonid is basined, with the hypoconid and entoconid cusps roughly equalin size. Note that the m2 and m3 are unreduced. B, Dentition trending toward hypercarnivory. The shearing bladeis slightly elongate, and the hypoconid and entoconid are unequal in size (hypoconid is larger). The m2 and m3are somewhat reduced in size. C, Trenchant talonid. The shearing blade is elongate, and the hypoconid is enlargedand medial, whereas the entoconid is completely reduced. The m2 and m3 are reduced. D, Note the absence of atalonid, including loss of the hypoconid and entoconid. The shearing blade extends the entire length of the m1, them2 is reduced or absent, and the m3 is absent.

premolars appears to be an alternative trajec-tory that leads not to a truly cat-like conditionbut toward more hyena-like (bone-cracking)characteristics (Van Valkenburgh 1991). Al-though end-members of these groupings (e.g.,felids vs. hyaenines) are easily differentiated,gradations between groups can be subtle, ascan be the difference between a generalistwith hypercarnivorous tendencies and a hy-percarnivore (e.g., between some ancestorsand descendants). To reduce the necessity forarbitrary judgments, for this study we estab-lished a minimum definition of a hypercarni-vore in order to more objectively differentiatebetween cat-like, hyena-like, and transitional

forms. The following combination of charac-teristics was therefore considered minimallydiagnostic when evaluating putatively hyper-carnivorous taxa for inclusion in this study:trigonid not less than 70% of the length of them1, width of the fourth lower premolar notgreater than 60% of its length, entoconid andhypoconid unequal.

Given the above qualifications, it is impor-tant to note that hypercarnivorous clades inthis study were recognized on the basis of be-ing basally hypercarnivorous. Therefore, if thefirst two branches for a given clade were hy-percarnivorous, the entire group was consid-ered so, because hypercarnivory was estab-


lished as the ancestral condition. Any evolu-tion of the phenotype subsequent to that an-cestral condition was then considered part ofthe total diversity of that clade.

Taxa and Phylogenies

Hypercarnivorous taxa were initially iden-tified through literature searches for taxa de-scribed as hypercarnivorous or highly preda-ceous. Diet (where known) and dental for-mula were also taken into account. Besides allmembers of the families Felidae and Nimrav-idae, taxa described by various workers as hy-percarnivorous include the hyaenid generaChasmaporthetes, Hyaenictis, and Lycyaena (Wer-delin and Solounias 1991); members of theSimpsonian subfamily Mustelinae (now rec-ognized as paraphyletic), especially the genusMustela (Ewer 1973; King 1989); the viverridCryptoprocta ferox (Wozencraft 1984, 1989;Werdelin 1996); and hesperocyonine canids ofthe genera Enhydrocyon, Ectopocynus, and Par-enhydrocyon (Van Valkenburgh 1991; Wang1994). Additional taxa identified include the‘‘paleomustelids’’ Megalictis and Oligobunis(Baskin 1998), as well as certain borophaginecanids including Euoplocyon, Epicyon, Osteobo-rus, and Borophagus (Wang et al. 1999); the am-phicyonids Daphoenictis (Martin 1989), Tem-nocyon, and Mammocyon (Van Valkenburgh1991, 1999); and the ursids Hemicyon johnhen-ryi (Van Valkenburgh 1991), Cephalogale, andPhoberocyon (Van Valkenburgh 1999).

A literature search for species-level, char-acter-based phylogenies for these taxa andtheir sister groups produced mixed results. Insome cases, character-based phylogenies arenot available and these taxa were consequent-ly excluded from study (e.g., amphicyonids,ursids, and paleomustelids). In those caseswhere multiple phylogenies were available,we critically examined the possibilities andchose the better-supported tree based on cri-teria that included use of a data matrix, typeand amount of evidence (molecular vs. mor-phological, kind and number of morphologi-cal or molecular characters, appropriatenessof gene or genes used), and congruence withalternative phylogenies. Sister groups wereidentified from available higher-level analy-ses; however, in several cases (e.g., Mustela, Fe-

lidae), there is significant disagreement re-garding the appropriate sister taxon. When adefinitive sister group could not be deter-mined, analyses were repeated with severalalternative sister groups. Two groups thatcontain hypercarnivorous taxa, the borophag-ine canids and the ‘‘paleomustelids,’’ were notincluded in diversity comparisons but wereincluded in degree-of-specialization analyses.Borophagines, which trend strongly toward abone-crushing phenotype, did not meet ourworking definition of hypercarnivores andwere consequently excluded from sister-group comparisons. However, the distinctivebone-crushing modifications of the groupwere useful in determining relative position-ing in morphospace and in assigning degreesof specialization for other taxa being evaluat-ed. In addition, there is a substantial range ofvariation within the ‘‘bone-crushing’’ special-ization of borophagines, and although sam-pling was incomplete, the placement of spe-cific taxa such as the derived Euoplocyon wasof general interest. Paleomustelids did notmeet the criteria set out for phylogenies (noneavailable were based on a data matrix), but be-cause these taxa have been repeatedly de-scribed as very specialized to the hypercar-nivore niche (Baskin 1998), their position inmorphospace relative to other hypercarni-vores was of interest.

Six sets of sister groups did meet the criteriafor inclusion in this study, in that all met theminimum requirements for a hypercarnivoreand a species-level phylogeny was available.These sister-group sets are the clades Felidae/Hyaenidae, Mustela/Galictis-Ictonyx-Pteronu-ra-Lontra-Enhydra-Lutra-Amblonyx-Aonyx, Phil-otrox-Sunkahetanka-Enhydrocyon/Cynodesmus,Cryptoprocta/Eupleres-Fossa, Chasmaporthetes-Lycyaena-Hyaenictis/Palinhyaena-Ikelohyaena-Belbus-Leecyaena(Hyaena)-Parahyaena-Hyaena-Pliocrocuta-Pachycrocuta-Adcrocuta-Crocuta(hereafter designated Palinhyaena-Crocuta[Werdelin and Solounias 1991]), and Nimrav-idae/Aeluroidea. Phylogenies used are shownin Appendix A.

Sister Groups

Felidae/Hyaenidae. Relationships among thefeliform carnivore families—Felidae, Hyaeni-


dae, Viverridae, and Herpestidae—have beennotoriously difficult to ascertain. The hyper-carnivorous family Felidae is most commonlyrecognized as sister to the family Hyaenidae(Wozencraft 1989; Wyss and Flynn 1993; Bin-inda-Emonds et al. 1999), although otherworkers have found support for a sister-grouprelationship with the insectivore/omnivore/generalist group Viverridae (Hunt 1987; Huntand Tedford 1993) or all other feliforms (Flynnand Nedbal 1998). Use of Hyaenidae may beconsidered a relatively conservative compari-son, because Hyaenidae has less diversitythan either of the alternative sister groups(Flynn et al. 1988). However, it should be not-ed that a hypercarnivorous clade (Chasma-porthetes-Lycyaena-Hyaenictis) is nested withinthe hyaenids as well. Because of the lack ofconsensus regarding the appropriate sistertaxon, we performed two comparisons for Fe-lidae, one against Hyaenidae and one againstViverridae. Within Felidae, the relationshipsamong the various genera and species havelikewise been problematic. The phylogeny weused is a composite based on the phylogeniesof Mattern and McLennan (2000) for crown-group felids and of Neff (1982), Turner andAnton (1997), and Martin (1998a) for machai-rodontines. Consensus for the ancestry of fe-lids leads from Proailurus, which exhibits atrenchant talonid and two lower molars, toPseudaelurus, which has a much reduced tal-onid and a reduced m2, to the clade compris-ing Felinae 1 Machairodontinae, which haslost the m2 as well as the talonid and has de-voted the entire lower carnassial to slicing (seeGinsburg 1983; Hunt 1996, 1998; Martin1998b). The species-level phylogeny forHyaenidae is from Werdelin and Solounias(1991).

Chasmaporthetes-Lycyaena-Hyaenictis/Palin-hyaena-Crocuta. Within Hyaenidae, tenden-cies toward increased carnivory first appear ingeneralist forms such as Ictitherium, Thalassic-tis, Hyaenotherium, and Hyaenictitherium. Rec-ognizably hypercarnivorous taxa are presentin the clade composed of the genera Chasma-porthetes-Lycyaena-Hyaenictis. These taxa havebeen described as cursorial and somewhat‘‘cat-like’’ (Werdelin and Solounias 1991).Their sister clade paralleled the development

of certain of these hypercarnivorous charac-teristics in the evolution of a trenchant heeland loss of the m2 in some taxa (Werdelin andSolounias 1991, 1996), but members of the Pal-inhyaena-Crocuta clade trend strongly towardbone-cracking modifications (e.g., premolarwidth .60% of premolar length), and extanthyaenids in this group are known to occupy ascavenging/bone-cracking niche (Ewer 1973;Nowak 1999) in contrast to the apparentlyhighly predaceous tendencies of Chasmaporth-etes-Lycyaena-Hyaenictis. We follow Werdelinand Solounias (1991) in recognizing thesegroups as monophyletic with distinctly differ-ent ecologies, acknowledging that the taxa inthe Palinhyaena-Crocuta clade have becomespecialists in their own right.

Philotrox-Sunkahetanka-Enhydrocyon/Cyno-desmus. Within the hesperocyonine canids,the clade identified as hypercarnivorous com-prises the genera Enhydrocyon, Philotrox, andSunkahetanka. The four species of Enhydrocyonare clearly hypercarnivorous relative to earlierhesperocyonines—Enhydrocyon crassidens hasbeen described as the most derived hespero-cyonine for this niche. However, Philotrox andSunkahetanka also exhibit modifications char-acteristic of hypercarnivory, along with othercharacteristics consistent with bone-crushinghabits. In Wang’s (1994) cladogram, Sunkahe-tanka and Philotrox are successive outgroups toEnhydrocyon, thus establishing hypercarnivo-ry as the basal condition for this clade. Wetherefore included these taxa in a hypercar-nivorous clade and contrast them to a sistergroup composed of the two-species nonhy-percarnivorous genus Cynodesmus. Althoughthe immediate outgroup to this Philotrox-Sun-kahetanka-Enhydrocyon/Cynodesmus clade, Me-socyon, has also been described by some work-ers (Van Valkenburgh 1991; Wang 1994) as hy-percarnivorous, its tendencies are very slight,and it does not meet our criteria: Mesocyon re-tains a strongly basined talonid and well-de-veloped postcarnassial teeth (m2 and m3) andhas a relative blade length of less than 70%.

Cryptoprocta/Eupleres-Fossa. Cryptoprocta isa monotypic genus in the family Viverridae(Wozencraft 1984) whose phylogenetic affini-ties have been problematic. There is ongoingwork regarding the relationships of viverrids


(e.g., Veron and Catzeflis 1993; Veron 1995; Ve-ron and Heard 1999); however, these phylog-enies have limited taxon and character sam-pling and are not adequate for our purposes.The most robust phylogeny for viverrids pres-ently available, and that based on the widestsampling, is that of Wozencraft (1984), where-in the two taxa Eupleres goudotii and Fossa fos-sana are the sister group to Cryptoprocta ferox.

Mus t e l a / G a l i c t i s - I c t ony x - P t e ronu ra -Lontra-Enhydra-Lutra-Amblonyx-Aonyx. Mus-tela is a highly predaceous genus of small car-nivores in the family Mustelidae (Ewer 1973;King 1989). Despite a great deal of recent at-tention that has included both molecular andmorphological analyses (Bryant et al. 1993;Masuda and Yoshida 1994; Dragoo and Ho-neycutt 1997; Koepfli and Wayne 1998), intra-familial relationships remain contentious. Asa result, we used several alternative phyloge-nies (Bryant et al. 1993; Dragoo and Honeycutt1997; Koepfli and Wayne 2003) and evaluatedresults for each group in turn.

Nimravidae/Aeluroidea. In contrast to thelarge number of phylogenetic hypotheses pro-posed for extant Mustelidae, the extinct saber-toothed family, Nimravidae, is relatively im-poverished. Of the phylogenies available, onlythose of Bryant (1996) for Nimravinae and Ge-raads and Gulec (1997) for Barbourofelinaemeet the criteria for inclusion. We graftedthese nonoverlapping phylogenies together tocreate a single composite tree for use in ourstudy. The relationship of Nimravidae to oth-er carnivoran taxa is also not well established,and various workers place nimravids basal toall of Carnivora (Neff 1983) or to Canidae(Flynn et al. 1988), or sister to Felidae (Martin1980) and Feliformia (Baskin 1981). Bryant(1991) and Wyss and Flynn (1993) evaluatedthe various hypotheses and attempted to ob-tain a better resolution by incorporating ad-ditional evidence. Both concluded that thebest (if weakly) supported hypothesis is thatNimravidae is sister to the aeluroid carnivor-ans, an opinion followed here.

Taxonomic Diversity

Several methods are available for compari-son of taxonomic diversity and determinationof whether rates of cladogenesis have been af-

fected by a given trait. The simplest is a bi-nomial sign test (Sokal and Rohlf 1994), whichallows direct comparison of species diversitybetween sister groups. Species are countedand the group (hypercarnivorous vs. nonhy-percarnivorous) with more species receives aplus sign; the group with fewer species re-ceives a minus. The numbers of signs acrossall groups under study are then contrastedunder a null hypothesis of no significant dif-ference. A more complex alternative is that setforth by Slowinski and Guyer (1993). Theirmethod, which incorporates a model of ran-dom speciation and extinction, uses Fisher’scombined probability test (Sokal and Rohlf1994) to determine whether certain traits havecaused significantly higher diversity. This ap-proach has been applied in evaluations of spe-cies diversity for both plants (Hodges and Ar-nold 1995; Dodd et al. 1999; Smith 2001) andanimals (Gardezi and da Silva 1999).

We obtained species counts from the pri-mary literature (see Table 1 for references) forall six sister-group pairs under study and ap-plied both tests against the null hypothesisthat specialization to hypercarnivory had noeffect on the subsequent diversification of anaffected clade. The most common alternativehypothesis is that specialization to hypercar-nivory, as with many other kinds of resourcespecialization, should reduce subsequentcladogenesis. However, this may not be thecase. Using matrix representation to create su-pertrees for all extant carnivoran taxa, Binin-da-Emonds et al. (1999) tested for adaptive ra-diations under the methods of Nee et al.(1995). Contrary to the argument that special-ization should negatively affect cladogenesis,their results suggested that both Mustela andFelidae may have undergone more speciationevents than would be expected by chance(Bininda-Emonds et al. 1999), although, for Fe-lidae at least, this result may be an artifact ofa high rate of extinction in the sister group(Hyaenidae). Because the effects of speciali-zation on taxonomic diversity are uncertain,we performed one-tailed tests in the directionof decreased species diversity and then re-peated the tests in the direction of increasedspecies diversity.


TABLE 1. Taxonomic diversity. References for species counts are as follows: Hesperocyoninae: Wang (1994); Mus-telidae, Viverridae, and Herpestidae: Nowak (1999); Hyaenidae: Werdelin and Solounias (1991); Felidae: Nowak(1999), Berta and Galiano (1983), Martin (1998a), Ginsburg (1983), Turner and Anton (1997), Berta (1987), Hemmer(1978), Glass and Martin (1978), Werdelin (1985), Hunt (1996); Nimravidae: Bryant (1996), Geraads and Gulec(1997).

HypercarnivoreNo. ofspecies Sister group

No. ofspecies

Felidae 86 Hyaenidae 69Hyaenidae: Chasmaporthetes/Lycyaena/

Hyaenictis15 Hyaenidae: Crocuta/Palinhyaena 15

Nimravidae 24 Felidae/Hyaenidae/Viverridae/Herpestidae 228Canidae: Hesperocyoninae Enhydro-

cyon/Philotrox/Sunkahetanka6 Canidae: Hesperocyoninae Cynodesmus 2

Viverridae: Cryptoprocta 1 Viverridae: Eupleres/Fossa 2Mustelidae: Mustela 17 Mustelidae: Galictis/Ictonyx/Pteronura/Lontra/

Enhydra/Lutra/Amblonyx/Aonyx26

FIGURE 2. Representative cranial and dental measure-ments used in morphological analyses. JL, jaw length;TRL, tooth-row length; ZAW, zygomatic-arch width;lm1, length of M1; trigonid, trigonid length; HAR,height of ascending ramus; MAT, distance from condy-loid process to coronoid process; MFL, distance fromcondyle to front of masseteric fossa; COM1, distancefrom carnassial notch to condyle.

Morphological Diversity

Data Collection. Cranial and dental mate-rial in the collections of the American Muse-um of Natural History, the Field Museum, the

Florida Museum of Natural History, and theNatural History Museum, London, was mea-sured for our study. Appendix B lists speciesname, collection number, and museum foreach specimen. Measurements were taken tothe nearest 0.01 mm with digital calipers.Where only a single specimen was availablefor a species, measurements were repeatedtwo to three times, and the mean taken ofthose measurements. Where multiple speci-mens were available, two to four specimenswere measured, and those measurementswere used to obtain a mean for the species.Where information regarding sex was avail-able and species were known to be sexuallydimorphic (e.g., Mustela, some felids), onlymales were included in the data set.

Measurements. We measured 290 speci-mens for the following distances (Fig. 2): jawlength (JL), tooth-row length (TRL), zygomat-ic-arch width (ZAW), length of P4 (lP4), lengthof M1 (lM1), length of M2 (lM2), length of p3(lp3), width of p3 (wp3), length of p4 (lp4),width of p4 (wp4), length of m1 (lm1), widthof m1 (wm1), length of m2 (lm2), length of m3(lm3), trigonid length (m1 trigonid), height ofascending ramus (HAR), distance from con-dyloid process to coronoid process (MAT),distance from condyle to front of massetericfossa (MFL), and distance from carnassialnotch to condyle (COM1). The variables JL,TRL, ZAW, MAT, MFL, and COM1 are fromRadinsky (1981a,b). For hesperocyonine ca-nids, we used the published data of Wang(1994).


The following eight shape or proportionvariables were derived from the original mea-surements. These variables were used for bothdisparity analyses and character mappingand are based in part on those of Van Valken-burgh (1988, 1989): relative blade length (RBL,defined as trigonid/lm1), grinding surfacelength relative to tooth-row length (GSL/TRL,GSL defined as lp3 1 lp4 1 lm1 1 lm2 1 lm32 trigonid), shape of the m1 (m1 shape, wm1/lm1), shape of the p4 (p4 shape, wp4/lp4),shape of the p3 (p3 shape, wp3/lp3), ratio oflM1 to lP4 (M1/P4), m1 length relative totooth-row length (lm1/TRL), and grindingsurface length relative to m1 length (lm1/GSL). Of these, the variables RBL and p4shape have previously been shown to differ-entiate effectively between dietary types incarnivorans (Van Valkenburgh 1988, 1989).Van Valkenburgh (1988, 1989) also used anarea measure, TGA (total grinding area),which we have modified to a linear measure,GSL. Like TGA, GSL denotes the relativeamount of grinding surfaces in the tooth row.Relative blade length is generally used as anindicator of highly carnivorous taxa, becausehypercarnivores increase the size of the tri-gonid relative to the length of the entire m1.Shape of both the p3 and the p4 is indicativeof bone in the diet, because wider premolarsindicate a more durophagous dietary niche intaxa that have reduced the postcarnassial den-tition (Van Valkenburgh 1988, 1989; Werdelin1989; Werdelin and Solounias 1991). As men-tioned above, widening of the premolars inconjunction with elongation of the shearingblade can be considered an alternative trajec-tory for hypercarnivorous specialization. M1/P4 is a partial measure of the postcarnassialdentition and therefore an indicator of the rel-ative amount of postcarnassial surface area;m1 shape, estimated by dividing the width ofthe m1 by its length, is representative of anemphasis on slicing as the tooth narrows.GSL/TRL indicates the proportion of the teethin the jaw not devoted to slicing; GSL is stan-dardized by the upper tooth row because car-nivoran jaw lengths are independent of skulllength and neither is a reliable standard at alevel higher than family (Van Valkenburgh1990). lm1/GSL likewise indicates the propor-

tion of postcanine tooth surface area taken upby the lower carnassial. lm1/TRL is essential-ly a measure of the length of the face stan-dardized to body size (as indicated by m1length; Gingerich 1974; Van Valkenburgh1988; Werdelin and Solounias 1991): the facetends to shorten as taxa become more highlycarnivorous and the position of the carnassialsis altered to maintain high bite force (Radin-sky 1981a,b; Van Valkenburgh and Ruff 1987;Biknevicius and Van Valkenburgh 1996).

In addition to the above eight characters,the following 19 shape or proportion mea-sures were used for character mapping butnot multivariate analyses: P4 shape, blade/GSL, lp3/lm1, lp4/lm1, lm1/JL, MFL/JL,MAT/HAR, MFL/COM1, lm1/MAT, TRL/ZAW, ZAW/JL, lm1/ZAW, (lM1 1 lM2)/P4,MAM/HAR, and (discrete characters) shapeof the m1 talonid basin (Van Valkenburgh1988), position of carnassial (Van Valkenburgh1988), position of P4 protocone, shape of pro-tocone, and presence or absence of the m2.

Data Preparation: Missing Data. Many ofthese data come from fossil material, so someproportion will be missing in most groups (to-tal original missing cells ranged from 50% inhyaenids to 28% in Felidae). Because some ofour statistical methods require that all cellscontain values, however, we treated missingdata as follows: For disparity analyses involv-ing PCA, individual taxa with .50% missingdata were excluded from analysis. Missingdata in the remaining taxa were handled ei-ther by replacement with the group mean orby replacement using regression based on an-other highly correlated character. Replace-ment values for individual measurementswere calculated on the basis of family or ge-neric-level means and regression. Where cor-relation analysis did not indicate any goodcorrelate for a particular variable, missingdata for that measure were of necessity re-placed by the overall mean. Because resultsfrom separate analyses by the two methodsdid not differ substantially, we report onlythose based on replacement by regression. Foranalyses involving character mapping, taxawith missing values were excluded for thatcharacter.

Variance. Distributions of all variables


were evaluated prior to analyses, and trans-formations were performed as appropriate. Tocompare disparities between hypercarnivoresand their sister groups, we performed princi-pal components analysis (PCA) based on cor-relation matrices of the above-listed variablesand analyzed differences in variance for thecategories ‘‘hypercarnivore’’ and ‘‘sister’’ ineach of the six sets of sister taxa. To obtain dis-parity values, we calculated the total variancefor each member of each hypercarnivore–sis-ter group pair by determining the variance ofits factor scores (eigenvalues) for the first fiveeigenvectors. Five factors were generally suf-ficient to explain .90% of the variation in a setof data. Values thus obtained were then scaledby the amount of variance explained by eachvector, and scaled values summed to create asingle composite disparity score for eachmember of the set. Each of the six pairs of sis-ter groups was analyzed separately because ofa concern that strong loadings for particularvariables in some pairs of sister groups couldunduly influence the apparent variance in oth-er groups, masking taxon-specific variation(see also Warheit et al. 1999). However, cate-gorical disparity results did not change whenall data were analyzed in a single large set, al-though individual results for sister pairs didchange slightly. Variance was chosen as a rep-resentative disparity measure because it is rel-atively insensitive to sampling (Foote 1992,1997). Total values for each taxon set for eachcategory were then contrasted by WilcoxonRank Sums against a null model of no differ-ence.

Character Mapping. An alternative mea-sure of evolutionary rate, frequency of char-acter change, is calculated as the number of in-dependent derivations of any given characterstate divided by the number of branches on atree (Sanderson 1993). Up to 27 characterswere mapped onto phylogenetic trees forgroups under study, and frequency of changefor each character was determined for each sis-ter clade. Frequency of change was averagedover all characters for each member of the sis-ter-group pairs. Incomplete sampling (eithermissing taxa or missing characters) preventedinclusion of all 27 characters in some groups.In these situations, the average was calculated

from the characters available. Results by cat-egory (hypercarnivore, sister) were pooledand evaluated with Wilcoxon Rank Sums.

Degree of Specialization. As noted above,hypercarnivorous taxa can be subdividedgenerally into ‘‘cat-like’’ and ‘‘hyaena-like’’morphotypes on the basis of robustness of thepremolars. However, the stages of evolution ofa hypercarnivorous phenotype are not dis-crete but can better be viewed as grades on acontinuum. Thus, we combined all hypercar-nivorous taxa into a single data set and eval-uated the position of each specimen in a sin-gle, ‘‘hypercarnivore’’ morphospace. Initialdata exploration consisted of examination oftwo- and three-dimensional graphs of com-binations of original variables as well as plotsof PC factor scores for the combined data setbased on the eight variables listed in Figure 2.Distributions of all variables were examinedprior to analysis and transformations per-formed as necessary.

Because our intent was to assign each spec-imen to a specific degree of specializationwithin hypercarnivores overall, some sense ofrelative position in space of each specimenwas necessary. Thus, the following were des-ignated as ‘‘reference’’ taxa and assigned lev-els of specialization a priori: Proailurus (5 lev-el 3), Pseudaelurus (5 level 4), Felis (5 level 5),and Hyaena (5 level 7). These taxa have dis-tinct specializations (hyena 5 bone) or knowndegrees of development relative to each other(Proailurus → Pseudaelurus → Felis) (Radinsky1982; Ginsburg 1983; Hunt 1998), and wereused as identifiers to provide reference (posi-tional) information for the remaining taxa.This enabled us to determine the appropriatenumber of levels and to assign the remainingspecimens to levels on the basis of clusteringand spacing around these reference taxa. Hy-enas (level 7) were included as indicators oftaxa with bone-eating tendencies, thus allow-ing us to distinguish between cat-like and hy-ena-like morphs. However, this numeric des-ignation is only an identifier and is not meantto imply a position along a continuum ofchange; this level was not included in analysesof disparity based on degree of specialization.

After assigning each specimen to a level,taxon assignments and the original eight var-


TABLE 2. Disparity values obtained for each set of sister groups. Disparity was calculated as the sum of the scaledvariance of the first five factor scores obtained from PCA.

Hypercarnivore Disparity Sister group Disparity

Felidae 46.20 Hyaenidae 116.66Hyaenidae: Chasmaporthetes/Lycyaena/

Hyaenictis44.91 Hyaenidae: Crocuta/Palinhyaena 109.95

Nimravidae 90.65 Felidae/Hyaenidae/Viverridae/Herpestidae 79.01Canidae: Hesperocyoninae Enhydro-

cyon/Philotrox/Sunkahetanka84.53 Canidae: Hesperocyoninae Cynodesmus 180.56

Viverridae: Cryptoprocta ferox 21.47 Viverridae: Eupleres/Fossa 107.64Mustelidae: Mustela 36.87 Mustelidae: Galictis/Ictonyx/Pteronura/Lontra/

Enhydra/Lutra/Amblonyx/Aonyx117.60

iables were entered into a discriminant func-tion analysis (DFA). Unlike PCA, which is anobjective method used to identify that com-bination of variables that explain the maximalamount of variation along successive orthog-onal axes, DFA is used to find the combinationof variables that most clearly distinguishes be-tween previously defined categories (in thiscase, degrees of specialization), so that theprobability of misclassification when placingindividuals into categories is minimized (Dil-lon and Goldstein 1984). The accuracy andstability of the classifications is assessed by us-ing jack-knifing. Because levels were beingcompared with each other, it was importantthat they be as well-supported as possible. Asmall number of taxa could not be unequivo-cally assigned to a specific degree of special-ization, which made their a priori assignmentsfor DFA necessarily somewhat arbitrary. Be-cause the functions used by DFA to discrimi-nate between categories is based on the mem-bership in those categories, we performed suc-cessive iterations of DFA and made adjust-ments to taxon assignments until we couldobtain high accuracy upon resampling whilestill maintaining correspondence with the nat-ural divisions observed in PC plots. The finalpercentage of correct assignments was 98.6%for fit based on original assignments and 96%for cross-validated data.

Disparity Based on Degree of Specialization.Methods for determining disparity valuesbased on degree of specialization are identicalto those set out for comparison of sister-groupsets, but rather than comparing the variancesof the members of a pair of sister groups, weperformed a single PCA including all hyper-

carnivorous taxa and then determined scaledvariance for each level of degree of speciali-zation. Disparity values thus obtained wereplotted against degree of specialization to de-termine whether degree of specialization anddisparity were correlated.

Results

Taxonomic Diversity

Species counts for the six sets of hypercar-nivores are shown in Table 1. Neither a signtest nor the method of Slowinski and Guyer(1993) yielded a significant difference in tax-onomic diversity between hypercarnivoresand their sister groups. Most sister-group setswere roughly equivalent, with hypercarnivo-rous Felidae and hesperocyonine canids ex-hibiting slightly greater taxonomic diversityand Viverridae and Mustela slightly lower di-versity. Species counts for the hypercarnivo-rous Chasmaporthetes-Lycyaena-Hyaenictis andthe bone-cracking Palinhyaena-Crocuta wereequal. The only hypercarnivorous taxon thatshowed any notable difference in taxonomicdiversity relative to its sister group was Nim-ravidae, a group whose relatively basal posi-tion in the carnivoran phylogeny places it assister to all of Aeluroidea. Setting aeluroid di-versity equal to one (the opposite extreme forsister-group comparisons) did not alter theseresults.

Morphological Diversity

Variance. Hypercarnivores show signifi-cantly lower morphological diversity than dotheir sister groups (p , 0.01, Wilcoxon RankSums; Table 2, Fig. 3), and these results are ro-


FIGURE 3. Average disparity for six clades of hypercar-nivorous taxa and their respective sister groups. Dis-parity is the sum of the scaled variances of the first fivefactor scores obtained from PCA of the eight variablesrepresentative of skull and dental morphology illustrat-ed in Figure 2. Wilcoxon Rank Sums p , 0.01.

TABLE 3. Average frequency of change obtained for each set of sister groups, calculated as the number of inde-pendent derivations of a character state/number of nodes on the phylogeny.

Hypercarnivore

Averagefrequency of

change Sister group

Averagefrequency of

change

Felidae 0.1370 Hyaenidae 0.1841Hyaenidae: Chasmaporthetes/Lycaena/

Hyaenictis0.1206 Hyaenidae: Crocuta/Palinhyaena 0.1637

Nimravidae 0.2289 Felidae/Hyaenidae/Viverridae/Herpestidae

0.1838

Canidae: HesperocyoninaeEnhydrocyon/Philotrox/Sunkahetanka

0.0714 Canidae: Hesperocyoninae Cynodesmus 0.1786

Viverridae: Cryptoprocta ferox 0 Viverridae: Eupleres/Fossa 0.3182Mustelidae: Mustela 0.1607 Mustelidae: Galictis/Ictonyx/Pteronura/

Lontra/Enhydra Pteronura/Lontra/Enhydra/Lutra/Amblonyx/Aonyx

0.2195

bust to perturbations of the various data sets(e.g., different included variables, data trans-formations, inclusion or exclusion of question-able taxa, alternative sister groups). Method ofreplacement of missing values also had no ef-fect on the results of the analyses. Exclusion ofProteles cristatus, the highly derived aardwolf,from sister-group analyses for felids andhyaenids did not affect the significance of theresults overall, although it did result in rough-ly equivalent disparity values for felids andhyaenids. Comparisons of felids with an al-ternative sister clade (viverrids), also did notaffect our results: felids are relatively lower

and viverrids relatively higher in disparitywhen compared with each other. Exclusion ofboth felids and nimravids and their sistergroups from the pooled values also did not af-fect the results, which remained significant atp , 0.02. Nimravidae, the saber-toothed non-cat family, was the only group of the six thatshowed disparity equivalent to or higher thanthat of its sister taxon.

Frequency of Change. Average frequency ofchange was calculated for six sets of hyper-carnivore/sister pairs. We found that the twocategories, hypercarnivore versus sister, weresignificantly different for the two groups (p ,0.037, Wilcoxon Rank Sums). Of the six, all hy-percarnivore clades except Nimravidaeshowed lower frequency of change relative totheir sister group. Congruent with compari-sons of variance, the family Nimravidae ex-hibited a higher frequency of change relativeto its sister taxon; this value was the second-highest frequency of change of any clade eval-uated (Table 3, Fig. 4).

Degree of Specialization. Six categories ofspecialization were identified for hypercarni-vorous taxa, ranging from the somewhat spe-cialized hesperocyonine canid genera Philo-trox-Sunkahetanka-Enhydrocyon through highlyspecialized saber-toothed taxa. A two-dimen-sional plot based on the shape variables ofRBL and GSL to TRL indicates placement ofkey specimens and is coded by degree of spe-cialization (Fig. 5) rather than taxon. Althoughthe assignment of taxa to a particular degreeof specialization was, as much as possible,


FIGURE 4. Average frequency of change for six clades ofhypercarnivorous taxa and their respective sistergroups. Nimravids are the uppermost symbol in the leftcolumn. Wilcoxon Rank Sums p , 0.04.

FIGURE 5. Plot of proportional variables indicating po-sitioning of taxa in morphospace when coded by degreeof specialization. Relative blade length is calculated asthe length of the trigonid (shearing blade) relative to thelength of the entire m1 and reflects the amount of meatin the diet. GSL/TRL is a measure of tooth surfaces notdevoted to slicing relative to the length of the face. De-grees 1 and 2 represent taxa that are relatively less spe-cialized (e.g., mustelids and hesperocyonine canids).Degree 6 represents taxa that are relatively more spe-cialized and is composed exclusively of felid and nim-ravid saber-toothed taxa.

TABLE 4. Degree of specialization was assigned on the basis of evaluation of location in principal components spaceand a priori designations in combination with discriminant function analysis. A total of 109 individual specimenswere evaluated; the following list is condensed where genera or families did not vary.

Level 1 Level 2 Level 3 Level 4 Level 5 Level 6

Mustela putorius Mustela altaica Dinictis felina Pseudaelurus Felinae SmilodonEnhydrocyon

basilatusMustela felipei Lycyaena Nimravides

galianiNimravides

catacopisXenosmilus

hodsonaeEnhydrocyon

crassidensMustela frenata Proailurus Cryptoprocta

feroxParamachairodus Barbourofelis

Enhydrocyonpahinsintewakpa

Mustela kathiah Pogonodon Eusmilus

Philotrox condoni Mustela nigripes Dinictis cyclops Hoplophoneusoccidentalis

Sunkahetankageringiensis

Mustela nivalis Hoplophoneusoharrai

Mustela sibirica Hoplophoneusprimaevus

Mustela vison Nanosmiluskurteni

Nimravusbrachyops

Nimravusgomphodus

phylogeny free, taxa did tend to fall stronglyinto groupings consistent with phylogeny.Thus, hesperocyonine canids constituted allbut one member of level 1, whereas mustelidsmade up all members of level 2. Levels 3 and4 were more diverse and included saber-toothed taxa, viverrids, felids, and hyaenids,but level 5 was composed entirely of membersof Felidae (both Felinae and Machairodonti-nae), and level 6 was made up of saber-toothsfrom both Felidae and Nimravidae. Assign-

ments of particular species to degrees of spe-cialization are shown in Table 4.

Disparity by Degree of Specialization. Dis-parity values obtained by summing the vari-ance of the first three factor scores for each de-


FIGURE 6. Disparity for different degrees of speciali-zation to hypercarnivory, ranging from less (1) to more(6) specialized. Degree 1 is composed of hesperocyoninecanids and one mustelid. Degree 2 is exclusively mem-bers of Mustela. Degree 3 is composed of Proailurus,Cryptoprocta, hyaenids, and some felids and nimravids.Degree 4 includes Pseudaelurus and some felids and nim-ravids. Degree 5 is exclusively felines and some ma-chairodontines. Degree 6 is composed of machairodon-tine and nimravid sabertooths. Note the discontinuous-ly high variance of degree 6 relative to degrees 1–5.

gree of specialization show a distinct positivecorrelation between variance and increasingspecialization. However, this correlation be-comes nonsignificant as successive factorscores are added to the sum (Fig. 6). Level 6,composed exclusively of saber-toothed taxa, isnoteworthy in that disparity is higher thanthat seen in any of the other specialist groups,and this result does not change even when lev-el 6 is partitioned by nimravids or machairo-dontines (felid saber-tooths). Nimravids inlevel 6 score particularly high for disparityvalues, although their disparity remains com-paratively low relative to those of ‘‘generalist’’families also evaluated (Viverridae and Mus-telidae).

Discussion

Our results show that morphological spe-cialization to hypercarnivory strongly affectsmorphological but not taxonomic diversity.Discordance between levels of taxonomic andmorphological diversification has been ad-dressed previously by several workers (e.g.,Foote 1993; Roy and Foote 1997; Eble 2000)and, depending on the direction of the differ-ence, may be explained as a result of diffusionthrough morphospace, morphospace packing,or selective extinction. In this case, the lack ofan effect on species number is likely a result

of continued subdivision of the available re-sources, possibly by body size (see, e.g., Da-yan et al. 1989, 1990), even as the structure ofthe feeding apparatus is maintained. On alarger scale, however, it is surprising that sub-sequent evolution has not produced a greaterdiversity of form in the time since the spe-cialization appeared. The hypercarnivoreclades in this study are identified under a cri-terion of being basally hypercarnivorous; it iscertainly not a requirement for the clade as awhole. Their lower morphological diversity isalso not a result of lack of time: Pseudaelurusevolved at approximately 20 Ma, and modernfelids appeared at ca. 16 Ma (Radinsky 1982).In the same time period, the sister group,Hyaenidae, diversified greatly, producingforms as varied as insectivore/omnivores,generalists, bone-cracker/scavengers, and itsown version of the hypercarnivore (Werdelinand Solounias 1991, 1996). Interestingly, thepresence of hypercarnivores within the basal-ly non-hypercarnivorous hyaenid clade ap-pears to have had only a small effect on over-all morphological diversity within this group,although the alternative sister taxon, Viverri-dae, exhibits even higher disparity relative tofelids. The clade of hypercarnivorous hyaen-ids, Chasmaporthetes-Lycyaena-Hyaenictis, isknown from at least the late Miocene (Berta1998), but although taxonomically it diversi-fied equally with the Palinhyaena-Crocutaclade, all indications are that it deviated littlefrom the meat-specialist morphotype. In con-trast, although the Palinhyaena-Crocuta cladeevolved specialists in its own right (bone-crackers), the brown and striped hyenas arearguably somewhat omnivorous in knownhabits (Ewer 1973; Van Valkenburgh 1989; No-wak 1999), and certainly the specialization foringestion of bone does not appear to limitmorphological disparity in the variables in-cluded in our study. Disparity for the singlespecies of Cryptoprocta was calculated from sixspecimens, two of which are Pleistocene sub-species, but is still substantially lower thanthat of its sister clade Eupleres-Fossa: the lattertaxa are highly divergent in phenotype rela-tive to each other. In the case of Mustela, mem-bers of this genus occupy a highly predaceousniche that, with the exception of the extinct sea


mink, Mustela macrodon (Estes 1989), and Mus-tela vison, which eats fish, crabs, etc. (Ewer1973), appears to have been retained over thepast 10–15 Myr. Mustela’s putative sistergroups include the otters and various gener-alist taxa. The noncat saber-toothed family,Nimravidae, had approximately 30 Myr to dif-ferentiate and all remained hypercarnivorous,whereas the last group evaluated, hypercar-nivorous canids of the genera Philotrox, Sun-kahetanka, and Enhydrocyon, exhibit disparitylower than that observed between two mem-bers of the single sister genus Cynodesmus.

Results from variance comparisons are sup-ported by all comparisons of average frequen-cy of character change, an important findingbecause these approaches capture distinctlydifferent views of morphological change.Whereas disparity based on variance reflectsoccupied morphospace around a group mean,frequency of change has utility in assessingevolutionary flexibility or rates of change (see,e.g., McShea 2001), as represented by the num-ber of changes in a given character state rela-tive to the number of opportunities (branches)on the tree (Sanderson 1993). Note that, forour purposes, this measure was used explic-itly to evaluate the frequency of any statechange in any direction rather than a compar-ison of forward changes to reversals or stasis,a topic that will be addressed in a subsequentpaper. Thus, not only do hypercarnivoroustaxa occupy less morphospace overall than dotheir sister groups, they also appear to movefrom state to state less frequently within thatspace. This suggests that once taxa achieve thehypercarnivorous morphotype, they are effec-tively limited in their subsequent evolution.This consistent reduction in variability in fiveout of six clades evaluated strongly suggeststhe presence of a functional constraint, andthis pattern is made even more interesting be-cause of the sharp contrast with saber-toothednimravids, a group whose high values for dis-parity and frequency of change suggest thepossibility of an escape from such a con-straint. In a combined morphospace, wherenimravids consistently show high disparityrelative to other taxa, the variables with thelargest loadings on the first two principalcomponents axes are m1/TRL and shape m1

on axis 1, and GSL/TRL and RBL on axis 2.Thus, nimravids are more variable in preciselythose hypercarnivore characters of the great-est importance: relative size and shape of thecarnassial (axis 1) and the proportion of thetotal tooth row used for slicing (axis 2). How-ever, one of the more interesting results is thatthe two nimravid clades, Nimravinae and Bar-bourofelinae, do not exhibit the same patternsof variation in this combined principal com-ponents space. In the analysis describedabove, variance for barbourofelines was high-est on the first axis, whereas variance for nim-ravines was highest on the second. This dif-ference is intriguing, especially in light of sug-gestions that Nimravidae is paraphyletic (Neff1983; Morales et al. 2001; Morlo et al. 2003).

Recognizing that, in most groups, hyper-carnivory does strongly affect subsequentmorphological flexibility, the idea that increas-ing specialization within the hypercarnivo-rous niche should be accompanied by decreas-ing disparity has intuitive appeal. The lack ofcorrelation between the two is therefore anunexpected result, although it may be an ar-tifact of the method used to assign degree ofspecialization. As noted previously, therewere several taxa that did not fit clearly intoparticular categories. Such taxa were thus out-liers in any grouping, and consequently theyexerted relatively greater influence on dispar-ity of the group in which they were placed. Al-though this had little effect on the ability ofDFA to accurately classify taxa (at worst, 78–80% were still correctly reclassified), it didlead to low confidence in the fine-scale patternof disparity between degrees of specialization,even when the categorical functions (thegroups) themselves were well supported byresampling. One pattern did not change, how-ever: level six, composed entirely of highly de-rived saber-toothed taxa, exhibited discontin-uously high disparity levels regardless of howthe groups were partitioned. This finding isconsistent with the unexpectedly high valuesobserved for nimravids for measures of vari-ance and average frequency of change. Indeed,diversity in saber-tooths was commented onby Radinsky (1982), who noted the unexpect-ed positioning of Eusmilus within canid mor-phospace on the first axis in his own analysis.


If a hypothesis of functional constraint oncharacters related to the carnassial feeding ap-paratus can be accepted, then it follows thatstrong selection on some other characteristics,most obviously the canines, may have overrid-den this constraint in saber-toothed groups.

The results presented here suggest thatthere is a point as taxa evolve toward hyper-carnivory where morphological flexibility be-comes substantially curtailed relative to someearlier stage. In a framework of morphologicalchange along a continuum, however, it is alsoapparent that there must still be alternativetrajectories available to hypercarnivores atsome stage in their evolution. Hypercarnivo-rous taxa that enhance the bone-cracking orcrushing portion of their dentition (e.g., hye-nas of the Palinhyaena-Crocuta clade, boro-phagines) appear to retain some measure offlexibility, although bone-crackers were notevaluated in this data set and the lower num-ber of known occurrences make this aspectdifficult to assess. Taxa that enhance the ca-nines (saber-tooths) likewise appear to exhibitentirely different patterns of diversity relativeto other cat-like hypercarnivores, as though bybecoming saber-toothed they have escapedthe cat phenotype. It is worth noting, however,that no hypercarnivores appear able to easilyreverse to a more generalized condition—infact, for the phylogenies used in this study,there are no known instances of the ‘‘cat-like’’phenotype reversing to a generalist or omniv-orous/insectivorous condition or even mov-ing into a bone-cracker/scavenger niche.When degree of specialization to hypercarni-vory is mapped onto the phylogenies for thesegroups (results not shown), movement awayfrom a more specialized toward a less spe-cialized condition is also an extremely rare oc-currence (one mustelid, one nimravid), sug-gesting that there is a strong directionality tochange for this phenotype.

Dollo’s law, which addresses the idea of ir-reversibility in evolution, states that a struc-ture, once lost, cannot be regained. Felids havereceived a certain amount of attention in thisregard (e.g., Werdelin 1987; Russell et al. 1995)because of their extreme and, excepting lynx-es, persistent reduction in the dental formula.An alternative explanation for the lower dis-

parity observed for hypercarnivorous taxa,then, may be that it is merely a consequenceof simplification via loss and reduction ofcompound structures: structures that do notexist will not vary. Further, if lost structurescannot be regained, then the only possible di-rection of change will be toward continuedloss. However, this explanation alone is un-satisfactory: there is no reason why a taxonwith a reduced dental formula should be lessvariable in the structures that remain. Addi-tionally, not all of the taxa recognized as mor-phologically hypercarnivorous exhibit thevery extreme specializations of felids. Hyper-carnivory is recognized on the basis of a set ofproportions: relative lengthening of the car-nassial blade, relative shortening of the face,and relative reduction of the postcarnassialtooth row. Thus, although proportions of theskull and dentition may alter, the originalstructures may not be lost at all, and wouldthus remain available for selection to act uponin any given direction. To add to this, becausesister-group comparisons evaluate differencesbetween groups since a common ancestor,phenotypic change such as continued loss orreduction of structures over the course of thelineage will be recognized as variation withinthe taxon. Finally, and most importantly, thedata sets used herein to calculate disparity in-clude a number of non-dental variables. Be-cause the diversity is measured by the totalvariation in all included characters, the ob-served disparity values cannot be consideredmerely a result of simplification of the dentalformula. Rather, they are likely a result of bothloss of structures (leading to no variation) andof lack of variation in the remaining craniod-ental measures as well.

As mentioned, the most obvious explana-tion for lower morphological diversity in mul-tiple clades of hypercarnivores is functionalconstraint. A consideration of the known ecol-ogies and behaviors of the taxa involved, how-ever, suggests that this explanation may be anoversimplification. The taxa in this study varyin both size and degree of specialization; preytype (and hence killing method) ranges fromthe birds and lizards of small cats and mus-telids to the larger ungulates favored by bigcats. Given this potential diversity in killing


mode, it is difficult to imagine that the samefunctional forces are working at all levels ofthe size range, especially forces that are soconsistently strong that they retard or preventsubsequent modification. The evolutionarilystable systems proposed by Wagner andSchwenk (2000) seem more in line, in the senseof a complex of characters that becomes moreand more tightly integrated as selection acts toimprove functionality of the system as awhole. Wagner and Schwenk suggested thatthis is brought about by ‘‘internal selection’’on the relationships between characters, rath-er than selection directly on particular char-acteristics, and the patterns observed here cer-tainly appear to follow this premise.

If one views the feeding apparatus as atightly integrated functional complex fromwhich deviation is unlikely, new questionsarise: once taxa begin to trend toward hyper-carnivory, is subsequent phenotypic changebiased toward this niche? Is there a ‘‘point ofno return’’ after which reversal or modifica-tion is not possible? Clearly, escaping is dif-ficult, and in this case the taxa that do not ex-hibit lower disparity have apparently done soby evolving a very extreme alternative spe-cialization. Is it possible that taxa can onlymove from a less to a more specialized con-dition? Mapping of degree of specializationonto phylogenies appears to indicate just sucha progression, although more detailed studyis needed to determine the generality of thisphenomenon. More robust phylogenies formachairodontines and nimravids are sorelyneeded, as is a better understanding of inter-relationships between aeluroids as a whole,especially fossil taxa. Such phylogenies wouldbe of great benefit in ascertaining the mostlikely patterns of diversification in relation tothe carnivoran feeding complex and evolutionof hypercarnivorous specialization.

Acknowledgments

We thank J. Albright, J. Cooper, G. Erickson,J. Holliday, X. Wang, and G. Wagner forthoughtful discussion and input and B. Parkerfor statistical advice and unwavering enthu-siasm. We are grateful to K. Koepfli and R.Wayne for allowing use of their unpublishedmustelid phylogeny, and to L. Werdelin and

an anonymous reviewer for comments thatgreatly improved this manuscript. We alsothank C. Collins, the American Museum ofNatural History; R. Hulbert and C. McCaffery,Florida Museum of Natural History; B. Stan-ley, the Field Museum; and J. Hooker, the Nat-ural History Museum, London. This projectwas funded in part through grants receivedfrom Sigma Xi Grants-in-Aid-of-Research andthe American Museum of Natural HistoryCollections Study Grants.

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Appendix 1

Hypotheses of phylogenetic relationships for hypercarnivo-rous clades and their sister groups as used in this study. More-detailed, species-level phylogenies were used for frequency-of-change comparisons and are available from the authors uponrequest. A, Felidae/Hyaenidae. B, Philotrox-Sunkahetanka-Enhy-drocyon/Cynodesmus. C, Chasmaporthetes-Lycyaena-Hyaenictis/Palinhyaena-Crocuta. D, Mustela/Galictis-Ictonyx-Pteronura-Lon-tra-Enhydra-Lutra-Amblonyx-Aonyx. E, Cryptoprocta/Eupleres-Fossa. F, Nimravidae/Herpestidae-Viverridae-Felidae-Hyaeni-dae. Extinct taxa are represented by †.


Appendix 1. Continued.

Appendix 2

Specimens

Museum abbreviations are as follows: AMNH: American Mu-seum of Natural History; F:AM: Frick Collection, American Mu-seum of Natural History; FMNH: Field Museum of Natural His-tory; MCZ: Museum of Comparative Zoology, Harvard Univer-sity; NHM: The Natural History Museum, London; TMM: Texas

Memorial Museum; UF: University of Florida Museum of Nat-ural History. Specimens designated P, PM, UM, UT, or UC arecurrently housed at the Field Museum.

Felidae: Acinonyx: NHM 16573; Dinofelis paleonca: TMM31181-192, TMM 31181-193; Felis brachygnatha: NHM16537; Felisamnicola: UF 1933, UF 19351, UF 19352; Felis aurata: AMNH51998, AMNH 51994; Felis badia: FMNH 8378; Felis bengalensis:FMNH 62894; Felis chaus: FMNH 105559; Felis colo colo: AMNH


189394, AMNH 16695, FMNH 43291; Felis rexroadensis: UF25067, UF 58308; Felis serval: AMNH 34767, AMNH 205151; Felisviverrina: FMNH 105562; Homotherium serum: UF 22908, UF22909, UF 24992; Machairodus aphanistus: NHM 8975; Machairo-dus palanderi: F:AM 50476, F:AM 50478; Megantereon cultridens:AMNH 105446, NHM 49967A; Megantereon falconeri: NHM16350, NHM 16557; Megantereon hesperus: UF 22890; Metailurus:F:AM China L-604, F:AM 95294; Nimravides: AMNH 25206, UF24471, UF 24479, F:AM 61855, F:AM 104044; Nimravides catacop-is: AMNH 141216, AMNH 141217; Nimravides galiani: UF 24462;Panthera leo: UF 10643, UF 10645; Panthera onca: UF 14765, UF14766, UF 23685; Panthera pardus: AMNH 35522; Paramachairodusogygia: NHM 1574; Paramachairodus orientalis: NHM 8959; Proail-urus lemanansis: NHM 1646, NHM 9636, NHM 9640, AMNH105065, AMNH 101931, AMNH 107658; Pseudaelurus: AMNH18007, AMNH 27318, AMNH 27446, AMNH 27447, AMNH61938, AMNH 62129, AMNH 62190, AMNH 62192, F:AM61925, AMNH 27451-A, NHM 9633; Pseudaelurus intermedius:NHM 2375; Pseudaelurus marshi: F:AM 27453, F:AM 27457; Smi-lodon californicus: UF 167140, UF 167141; Smilodon floridanus: UF22704, UF 22705; Smilodon gracilis: UF 81700; Xenosmilus hodson-ae: UF 60000.

Nimravidae: Barbourofelis: P15811; Barbourofelis fricki: AMNH103202, AMNH 108193, F:AM 61982; Barbourofelis lovei: UF24447, UF 24429, UF 36858, UF 37052; Barbourofelis morrisi:AMNH 25201, F:AM 79999; Barbourofelis whitfordi: AMNHC38A–210, F:AM 69454, F:AM 69455; Dinictis: UF 155216, UF207947; Dinictis cyclops: AMNH 6937; Dinictis felina: AMNH38805, P12004, PM 21039; Eusmilus: F:AM 99259, F:AM 98189;Eusmilus cerebralis: AMNH 6941; Hoplophoneus: F:AM 69344, UC1754; Hoplophoneus occidentalis: AMNH 102394; Hoplophoneus pri-maevus latidens: UM 420, UM 701; Hoplophoneus oharrai: AMNH27798, AMNH 82911; Hoplophoneus oreodontis: AMNH 9764; Na-nosmilus kurteni: UF 207943; Nimravus: F:AM 62151; Nimravussectator: AMNH 12882; Nimravus brachyops: AMNH 6930; Nim-ravus gomphodus: AMNH 6935; Pogonodon: AMNH 1403, F:AM69369, AMNH 1398; Pogonodon platycopis: AMNH 6938; Sansa-nosmilus: AMNH 26608; Vampyrictis vipera: T 3335.

Hyaenidae: Acrocuta eximia: AMNH 26372, NHM 8971,M8968, M9041; Chasmaporthetes: AMNH 99788; Chasmaporthetesexilelus: AMNH 26369; Chasmaporthetes lunensis: AMNH 10261,AMNH 26955, F:AM China 94B–1046, F:AM China 96B 1054;Chasmaporthetes ossifragus: AMNH 108691, AMNH 95208; Cro-cuta: NHM 16565; Crocuta crocuta: AMNH 187771, FMNH98952, UF 5665; Hyaena bosei: NHM 1554, NHM 37133, NHM16578; Hyaena brunnea: FMNH 34584; Hyaena hyaena dubbah:FMNH 140216; Hyaenictitherium hyaenoides: F:AM China 14-L344, F:AM China 14-L35, F:AM China 26-B47; Ictitherium viv-errinum: F:AM China (G)-L100, NHM 8983, NHM 8987, NHM8988; Lycyaena chaeretis: NHM 8978, NHM 8979a; Lycyaena cru-safonti: AMNH 108175, AMNH 116120; Lycyaena dubia: F:AMChina 52-L495, F:AM China 56-L560; Palinhyaena reperta: F:AMChina 42-L338, F:AM China 51-L443; Pliocrocuta perrieri:

AMNH 27756, F:AM 107766, F:AM 107767, AMNH 27757; Pliov-iverrops: AMNH 99607; Proteles cristatus: FMNH 127833; Thal-assictis wongii: AMNH 20555, AMNH 20586; Tungurictis spocki:AMNH 26600, AMNH 26610.

Viverridae: Arctogalidia trivirgata stigmatica: FMNH 68709;Chrotogale owstoni: FMNH 41597; Cryptoprocta ferox: AMNH30035, FMNH 161707, FMNH 161793, FMNH 33950, FMNH5655; Cryptoprocta ferox spelaea: NHM 9949; Eupleres goudotii:FMNH 30492, AMNH 188211; Fossa fossa: AMNH 188209,AMNH 188210, FMNH 85196; Genetta genetta senegalesis: FMNH140213; Genetta maculata: FMNH 153697; Nandinia binotata:FMNH 25306; Prionodon linsang: FMNH 8371; Viverra zibetinapicta: FMNH 75883; Viverricula indica babistae: FMNH 75815,FMNH 75816.

Canidae: Hesperocyoninae: Cynodesmus thooides: AMNH129531; Ectopocynus antiquus: AMNH 63376; Ectopocynus simpli-cidens: F:AM 25426, F:AM 25431; Enhydrocyon basilatus: AMNH129549, F:AM 54072; Enhydrocyon crassidens: AMNH 12886,AMNH 27579, AMNH 59574; Enhydrocyon pahinsintewakpa:AMNH 129535; Hesperocyon gregarious: AMNH 9313; Mesocyoncoryphaeus: AMNH 6859; Mesocyon temnodon: F:AM 63367; Os-bornodon fricki: AMNH 27363; Osbornodon: AMNH 54325; Par-enhydrocyon: AMNH 81086; Parenhydrocyon josephi: F:AM 54115;Philotrox condoni: AMNH 32796, F:AM 63383; Prohesperocyon wil-soni: AMNH 12712; Sunkahetanka geringensis: AMNH 96714.

Canidae: Borophaginae: Aelurodon taxoides: F:AM 61781; Bor-ophagus diversidens: AMNH 67364; Borophagus secundus: AMNH61640; Epicyon haydeni: F:AM 61461; Epicyon saevus: F:AM 61432;Euoplocyon praedator: AMNH 18261; Euoplocyon: AMNH 25443,AMNH 27315; Paratomarctos euthos: F:AM 61101; Desmocyon tho-masii: AMNH 12874.

Mustelidae: Arctonyx collaris: AMNH 57373; Eira barbara:AMNH 128127, AMNH 29597, UF 3194; Enhydra lutra: UF 24196;Galictis cuja: AMNH 33281; Galictis vittata: UF 29310; Gulo gulo:AMNH 35054, FMNH 14026, AMNH 169501; Ictonyx: AMNH165812; Lutra canadensis: UF 24007; Martes americana: UF 13212;Martes cauvina: UF 5642; Martes foina: UF 29046, AMNH 70182;Martes pennanti: UF 23316; Mustela altaica: UF 26514; Mustela er-minea: UF 3982, UF 1417; Mustela felipei: AMNH 63839, FMNH86745; Mustela frenata: UF 26144, UF 4779; Mustela kathiah:FMNH 32502, AMNH 150090; Mustela nigripes: AMNH 22894;Mustela nivalis: UF 1418; Mustela putorius: UF 1425, UF 14422;Mustela sibirica: AMNH 114878, F:AM 104392; Mustela vison: UF4569, UF 4724, UF 8108; Mydaus javanensis: AMNH 102701; Poe-cilogale albinucha: AMNH 86491; Taxidea taxus: UF 384; Vormalaperegusna negans: AMNH 60103.

‘‘Paleo’’ mustelids: Brachysypsalis: AMNH 25295, AMNH25299, AMNH 27307, F:AM 25284, F:AM 25363, AMNH 27424;Megalictis: F:AM 25430; Megalictis ferox: P12283, P12154, P26051,UF 23928; Oligobunis crassivultus: AMNH 6903, PM 537; Oligo-bunis darbyi: P25609; Oligobunis floridanus: MCZ 4064; Plesictis cf.pygmaeus: NHM 27815; Plesiogulo marshalli: UF 19253; Promarteslepidus: P12155; Zodialestes: F:AM 27599, F:AM 27600; Zodialestesdaimonelixensis: P12032.

evolution of hipercanivory - the effect of specialization[1]

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