Euprimate origins: the eyes have it

News and Views

Euprimate origins: the eyes have it

Matthew J. Ravosaa,b*, Denitsa G. Savakovaa

aDepartment of Cell and Molecular Biology, Northwestern University Feinberg School of Medicine, 303 East Chicago Avenue,Chicago, IL 60611-3008, USA

bDepartment of Zoology, Division of Mammals, Field Museum of Natural History, Chicago, IL, USA

Received 3 October 2003; accepted 11 December 2003

Keywords: Skull form; Activity cycle; Nocturnal visual predation; Orbital convergence; Diet; Allometry/scaling; Ontogeny;Phylogeny; Euprimates; Plesiadapiformes; Mammals

Introduction

The remarkable discovery of a well-preservedPaleocene plesiadapiform (Carpolestes) with aunique constellation of skeletal features has re-kindled debate regarding the patterning of adap-tive and morphological transformations during theorigin of archaic (Plesiadapiformes) and modern(Euprimates) primates (Bloch and Boyer, 2002,2003; Sargis, 2002; Kirk et al., 2003). In positingthat a series of manual and pedal characters sharedbetween Carpolestes and basal euprimates arehomologous and derived (rather than simply acase of functional convergence), Bloch and Boyer(2002, 2003) argue persuasively that graspingappendages and terminal-branch feeding precededthe evolution of increased levels of orbital conver-gence and binocular visual acuity characteristic ofthe earliest euprimates. With Carpolestes recon-structed as frugivorous (and having low levelsof orbital convergence), grasping extremities incarpolestids and the ancestors of euprimates are

inferred to be adaptations for terminal-branchforaging on fruits, flowers, and buds (Bloch andBoyer, 2002, 2003; Sargis, 2002). Accordingly, thephylogenetic independence of grasping andforward-facing orbits is incompatible with thelong-influential nocturnal visual predation hypoth-esis (NVPH) of euprimate origins (Cartmill, 1972,1974, 1992; Kay and Cartmill, 1974, 1977; Kirket al., 2003). Instead, grasping capabilities in basaleuprimates are interpreted as exaptations for noc-turnal visual predation, supporting an alternativescenario regarding the sequence of acquisition andfunction of euprimate postcranial synapomorphies(Rasmussen, 1990; Sussman, 1991). Bloch andBoyer’s (Bloch and Boyer, 2002, 2003) study alsosuggests that grasping adaptations occurredprior to the emphasis on leaping behaviors as acomponent of the locomotor repertoire in basaleuprimates (Szalay, 1973, 1981; Szalay et al., 1987;Dagosto, 1988).

This characterization of early primate phy-logeny highlights a long-running controversyregarding the craniodental adaptations and behav-ior of basal euprimates, specifically the functionalsignificance of an important euprimate synapo-morphy: forward-facing or convergent orbits(Fig. 1). Whereas advocates of the NVPH

* Corresponding author. Tel.: +1-312-503-0492;fax: +1-312-503-7912

E-mail address: [email protected](M.J. Ravosa).

Journal of Human Evolution 46 (2004) 357–364

0047-2484/04/$ - see front matter � 2004 Elsevier Ltd. All rights reserved.doi:10.1016/j.jhevol.2003.12.002

emphasize that felid-like nocturnal visual preda-tion is critical for unraveling the adaptive signifi-cance of increased levels of orbital convergenceand binocular acuity during euprimate origins(Cartmill, 1972, 1974, 1992; Kay and Cartmill,1974, 1977; Allman, 1977, 1982; Kirk et al., 2003),critics of this view counter that more appropriatefunctional analogs for the evolution of theeuprimate visual system and circumorbital regionare to be found among nocturnal arborealfrugivores such as pteropodids and didelphimorphmarsupials (Sussman and Raven, 1978; Pettigrewet al., 1989; Rasmussen, 1990; Sussman, 1991;Crompton, 1995). While the principal sourceof disagreement centers on the extant clade(s)selected to elucidate the functional underpinningsof orbital character states, this unresolved debateis further abetted by the lack of a broad-basedempirical analysis of factors posited to influencevariation in orbital orientation. This is especiallysurprising given that elevated levels of orbitalconvergence are also purportedly linked to thepresence of relatively smaller orbital diameters(Cartmill, 1980), such that convergence increaseswith skull size due to the negative allometry of

eye/orbit size (Kay and Cartmill, 1977; Martin,1990) (Fig. 1). Here, we address these outstandingissues by integrating comparative and ontogeneticinformation regarding functional, allometric, andsystematic variation in orbital convergence amongdiverse clades of living and fossil mammals.

Materials and methods

To assess the relationship between increasedorbital convergence and visual strategy as well asphylogenetic and size-related patterns of adultorbital proportions in primate and non-primatemammals, a series of comparative analyses wereperformed using species means of adult skullmeasures and representing each family by nearlyall of its genera. Since the presence of intra-familialvariation in activity cycle or diet is vital for dis-tinguishing between competing explanations forforward-facing orbits (Ewer, 1973; Nowak, 1999;Zeveloff, 2002), phylogenetically restricted com-parisons were performed among seven didelphi-morph marsupials (n=68),1 11 procyonids (n=88),five tupaiids (n=21), and 28 herpestids (n=183). Toexamine relative and absolute levels of orbitalconvergence in basal euprimates of the Eocene,four omomyids (n=8, nocturnal predators) andfour adapids (n=12, diurnal foragers) were com-pared to functional analogs and sister taxa(Simons, 1962; Ewer, 1973; Richard, 1985; Martin,1990, 1993; Fleagle, 1999; Nowak, 1999; Zeveloff,2002): 11 extant primate nocturnal predators(n=48),2 31 felids (n=208, nocturnal predators),64 pteropodids (n=277, nocturnal foragers), 28herpestids (n=183, mostly diurnal predators), adermopteran (n=6, nocturnal foragers), fivetupaiids (n=21, mostly diurnal predators), and two

1 To eliminate the possibility that the enlarged masticatoryapparatus of folivorous didelphimorphs would differentiallyinfluence the orientation of the lower orbital margin, and thusvariation in orbital convergence across this clade (Cartmill,1972), no such marsupials are included herein.

2 Orbital convergence data for four cheirogaleids and twotarsiids are from Ross (1995). Species means for three galagidsand two lorisids are based on data collected either by theauthors or Ross (1995). Linear dimensions of the skull for all 11nocturnal faunivores were taken by the authors.

Fig. 1. Superior view of a primate skull (adapted from Cartmill,1972). Orbital convergence describes the extent to which theorbital margins face forward. Orbits directed more anteriorlyare convergent (A) while those directed more laterally aredivergent (B). High levels of orbital convergence are posited tofacilitate binocular stereoscopic acuity and increased depthperception at close range. All other things being equal (i.e.,similar snout, interorbital, and zygomatic arch proportions),the presence of a relatively large eye/orbit (B exceeds A)displaces the lateral orbital margin more posteriorly along thezygomatic arch, thus decreasing the amount of convergence.

M.J. Ravosa, D.G. Savakova / Journal of Human Evolution 46 (2004) 357–364358

plesiadapiforms (n=2, diurnal foragers). A benefitof this last, higher-level comparison over previouswork (Ravosa et al., 2000) is the inclusion ofperhaps the most appropriate analogs based onbody size, activity cycle, and feeding behavior forthe earliest primates of modern aspect: living pri-mate nocturnal predators (Simons, 1962; Richard,1985; Martin, 1990, 1993; Fleagle, 1999).

The scaling of orbital proportions was furtherinvestigated for the postnatal ontogeny of sixstrepsirrhine primates: Propithecus verreauxi (11adults and 24 juveniles), Eulemur fulvus (10 adultsand 27 juveniles), Hapalemur griseus (11 adults and20 juveniles), Otolemur crassicaudatus (11 adultsand 21 juveniles), Nycticebus coucang (12 adultsand 31 juveniles), and Perodicticus potto (12adults and 34 juveniles). These data allow one tocontrol for activity cycle as well as the influence ofphylogenetic variation in circumorbital form onallometric patterns of orbit orientation. These taxawere also selected because they represent bothextant strepsirrhine infraorders and most extantsuperfamilies, equal the interspecific range of vari-ation in convergence values, and closely approxi-mate the skull morphology of basal euprimates. Inall species, at least five adults of each sex wereexamined.

The angle of orbital convergence was measuredto 0.5 degrees using a dihedral goniometer(Cartmill, 1972, 1974, 1980; Ross, 1995; Ravosaet al., 2000). Orbital diameter (height and width)

and two linear measures of skull size (palate lengthand nasion-inion chord) were collected with digitalcalipers accurate to 0.1 mm. The nasion-inionchord allows for direct comparisons with priorresearch (Cartmill, 1972, 1974; Ross, 1995; Ravosaet al., 2000). An advantage of palate length isthat it facilitates the examination of specimens,typically fossils, in which the posterior aspect ofthe cranial vault, and thus inion, is damaged ormissing.

To test for the allometry of orbital orientation,correlations between convergence and skull sizewere calculated in each clade (species means) andgrowth series (individual specimens); results aresimilar regardless of whether palate length or thenasion-inion chord is used to represent skull size(Table 1 and Table 2). Least-squares (LS) regres-sions of orbital diameter were calculated to aid inthe interpretation of allometric changes in orbitalconvergence. As convergence increases with sizein the euprimate/felid sample (r=0.754 vs. palatelength, P<0.001) as well as across the sampleof pteropodids, herpestids, plesiadapiforms,tupaiids, and dermopterans (r=0.613 vs. palatelength, P<0.001), values for these two groupswere compared with an analysis of covariance(ANCOVA) of LS regression lines. Size-controlledcomparisons of convergence levels were evaluatedwith non-parametric ANOVAs (Mann–Whitney Utest). Comparisons of convergence LS residualswere assessed using the Mann–Whitney U test or

Table 1Bivariate correlations and regressions for mammalian interspecific series

Family (n) Orbital convergence (r) vs. Ln (orbital diameter) vs.ln (palate length)

Palate lengtha Nasion-iniona LS slope ra

Pteropodidae (64 taxa, 277 adults) 0.588*** 0.644*** 0.689 0.949***Tupaiidae (5 taxa, 21 adults)b,c 0.684** 0.770** 0.608 0.914**Procyonidae (11 taxa, 88 adults)b,d 0.500** 0.560** 0.496 0.835***Herpestidae (28 taxa, 183 adults)b,e 0.422** 0.415** 0.742 0.911***Felidae (31 taxa, 208 adults) 0.240* 0.257* 0.666 0.975***

aSignificance levels: ***=P<0.01; **=P<0.05; *=P%0.15.bLS analyses performed on the “one activity cycle” sample used to calculate orbital convergence r’s.cWith convergence r’s figured for one activity cycle (n=4 diurnal taxa), r=0.979 and 0.989 (P<0.01).dWith convergence r’s figured for one activity cycle (n=8 nocturnal taxa), r=0.748 and 0.838 (P<0.01).eWith convergence r’s figured for one activity cycle (n=27 diurnal taxa), r=0.567 and 0.556 (P<0.01).

M.J. Ravosa, D.G. Savakova / Journal of Human Evolution 46 (2004) 357–364 359

95% confidence limits about the LS line. Allanalyses were performed with SYSTAT 7.0 andcombined with visual inspections of the datascatter.

Results and discussion

Three sets of comparisons bear on the unre-solved questions regarding the functional signifi-cance of forward-facing orbits. First, nocturnalarboreal frugivores such as pteropodids exhibitrelatively low levels of orbital convergence, similarto that in tupaiids, dermopterans, herpestids, andplesiadapiforms (Fig. 2). Apart from representingthe plesiomorphic condition for euprimate sistertaxa and presumably all eutherians, more diver-gent orbits characterize mammals with widely dis-parate activity cycles, including diurnal predatorsas well as nocturnal and diurnal foragers. Incontrast, Eocene euprimates are similar to noctur-nal primate and felid analogs in uniquely possess-ing proportionally larger (Kay and Cartmill, 1977;Martin, 1990) and relatively convergent orbits(Fig. 2; significantly higher Y-intercept [39.748 vs.28.353] such that the euprimate/felid LS regressionline is transposed above that for the remainingtaxa, ANCOVA P<0.001). Further comparisonsbetween similarly sized nocturnal omomyids andextant primate nocturnal faunivores indicate nosignificant group differences in levels of orbitalconvergence (Mann–Whitney U test amongspecies means of 12–26 mm for palate length,

P=0.240). Therefore, the derived presence of rela-tively large eyes and forward-facing orbits in thefirst modern primates suggests that consequentincreases in stereoscopic acuity and image clarityat close range were functionally linked to noctur-nal stalking and capturing of mobile prey(Cartmill, 1972, 1974, 1992; Allman, 1977, 1982).

More phylogenetically restricted comparisonsfurther demonstrate the lack of an associationbetween nocturnal frugivory and pronouncedorbital convergence. In procyonids the nocturnal,more frugivorous kinkajou (Potos) possesses anamount of orbital convergence equivalent to itsnocturnal sister taxa (Fig. 3a). Interestingly, it andother nocturnal predators display relatively higheramounts of convergence than diurnal predators(Mann–Whitney U test of residuals from the pro-cyonid LS line, P=0.001). This suggests that thesmall vertebrate and insect component of thekinkajou diet, a proclivity shared with other noc-turnal procyonids, underlies variation in orbitalform within and between nocturnal and diurnalspecies in this clade. Likewise, the nocturnalfaunivore Ptilocercus exhibits a relatively greateramount of convergence than its diurnal tupaiidsister taxa (Fig. 3b; studentized residual of 5.974from the tupaiid LS line). In didelphimorphs ofsimilar size, four nocturnal faunivores of thegenera Philander, Chironectes, and Metachirus(mean=53.5(, range=50.4–57.8() all possesssignificantly more convergent orbits than threenocturnal arboreal frugivores of the genusCaluromys (mean=42.4(, range=42.0–43.0()

Table 2Bivariate correlations and regressions for strepsirrhine ontogenetic series

Species (n)a Orbital convergence (r) vs. Ln (orbital diameter)vs. ln (palate length)

Palate lengthb Nasion-inionb LS slope rb

Propithecus verreauxi (11A and 24J) 0.692** 0.726** 0.750 0.921**Eulemur fulvus (10A and 27J) 0.711** 0.683** 0.599 0.982**Hapalemur griseus (11A and 20J) 0.416* 0.441* 0.580 0.838**Otolemur crassicaudatus (11A and 21J) 0.653** 0.721** 0.732 0.914**Nycticebus coucang (12A and 31J) 0.832** 0.785** 0.769 0.972**Perodicticus potto (12A and 34J) 0.677** 0.756** 0.776 0.884**

aA=adults; J=juveniles or non-adults.bSignificance levels: **=P<0.001; *=P%0.05.


(Mann–Whitney U test among species means of30–38 mm for the nasion-inion chord, P=0.034).Compared to other primarily diurnal herpestids,the diminutive nocturnal faunivore Dologale alsoevinces a relatively elevated degree of convergence(Fig. 2; studentized residual of 3.057 from theherpestid LS line). These independent analysesconsistently demonstrate that forward-facingorbits in living and fossil mammals are related toan adaptive strategy of nocturnal visual predation.

One can nonetheless identify apparent supportfor the relationship between elevated orbital con-vergence and frugivory. In nocturnal pteropodids,larger-bodied species are more frugivorous andevince greater convergence than smaller, more

insectivorous sister taxa (Table 1). This patternalso characterizes orbital and dietary variationbetween adapids and the smaller-bodied omo-myids (Fig. 2). However, there are several reasonswhy these correlations are spurious and due to theindependent scaling of dietary preference and orbitorientation. Controlling for activity cycle andgiven the preponderance of faunivory, orbital con-vergence nevertheless increases with skull size indiurnal herpestids, nocturnal procyonids, diurnaltupaiids, and felids (Table 1; Figs. 2 and 3).Postnatal development in three lorisiformes andthree lemuriformes, taxa arguably most similar tobasal euprimates in skull form, is likewise uni-formly characterized by size-related increases in

Fig. 2. Orbital convergence versus skull size in extant primate nocturnal predators, Eocene basal euprimates, primate sister taxa, andother putative analogs (adult species means). Omomyids (and adapids) are similar to felids and primate nocturnal faunivores inpossessing relatively higher levels of orbital convergence than plesiadapiforms, tupaiids, dermopterans, pteropodids, and herpestids. Incontrast to diurnal herpestids, the diminutive nocturnal faunivore Dologale (arrow) also displays a relatively greater degree ofconvergence. These and other (Fig. 3 and text) comparisons suggest that the derived presence of forward-facing orbits and stereoscopicacuity in the earliest modern primates were adaptations for nocturnal visual predation. Lastly, the presence of elevated orbitalconvergence in diurnal adapids is likely due to phyletic increases in body size from a smaller basal euprimate with omomyidlikeconvergence levels (see text, Table 1 and Table 2).


orbital convergence (Table 2). Allometric changesin orbital convergence among these primates con-tinue long after the early postnatal shift to weaning(inferred from the eruption of the first permanentmolar [Smith et al., 1994]) and relatively invariantadult feeding and chewing behaviors (see Watts,

1985 and review in Ravosa and Hogue, 2003).Such comparisons, especially the ontogenetic evi-dence, offer strong empirical support for the argu-ment that the allometric patterning of convergenceis simply a structural consequence of the negativescaling of orbital diameter both during ontogenyand across a size series of close relatives (Cartmill,1980; see Table 1 and Table 2).

Conclusion

To contribute novel insights into our under-standing of major adaptive transformations inskeletal form during euprimate origins, we charac-terized the complex and unappreciated suite ofecological and structural influences on variation inorbital convergence among primate and non-primate mammals. One important finding is that,in order to evaluate the adaptive significance of agiven level of orbital convergence, it is vital tocontrol for the scaling of orbit size (as well as, ofcourse, phylogeny). Indeed, selection for higherlevels of convergence at small body sizes has toovercome the tendency for smaller sister taxa todevelop more divergent orbits due to the presenceof relatively large eyes. Such countervailing factorsare presumably further pronounced if a givenmorphological transformation is coupled witha shift in activity cycle, i.e., the evolution of arelatively large-eyed nocturnal descendant from asmaller-eyed diurnal ancestor.

There are several implications of our study forcompeting scenarios of euprimate origins. Con-trary to prior assertions (Sussman and Raven,1978; Pettigrew et al., 1989; Rasmussen, 1990;Sussman, 1991; Crompton, 1995), phylogeneticallyand allometrically controlled analyses highlight theunmistakable imprints of nocturnality and visualpredation on the evolution of the skull and sensorysystem in the first primates of modern aspect(Cartmill, 1972, 1974, 1992; Kay and Cartmill,1974, 1977; Allman, 1977, 1982; Kirk et al., 2003).Since the first euprimates were unlikely to havebeen larger than the 100 g Carpolestes (Martin,1990, 1993; Fleagle, 1999; Bloch and Boyer, 2002;Sargis, 2002), allometry cannot be invoked toexplain the derived presence of relatively higher

A

NASION-INION CHORD (mm)

CO

NV

ER

GE

NC

E (

°)

Nocturnal

Diurnal

B

NASION-INION CHORD (mm)

CO

NV

ER

GE

NC

E (

°)

Nocturnal

Diurnal

Fig. 3. Orbital convergence versus skull size in procyonids (A)and tupaiids (B) (adult species means). In the former group (A)the nocturnal, more frugivorous kinkajou (Potos; arrow) exhib-its only an average amount of orbital convergence versus othernocturnal sister taxa. This is the opposite of claims thatelevated convergence and stereoscopic acuity are associatedwith nocturnal frugivory. In support of the NVPH, procyonid(A) and tupaiid (B) nocturnal faunivores (solid circles) displayrelatively greater levels of convergence than diurnal predators(open circles). Similar to other mammals, orbital convergenceincreases allometrically in these two clades (Table 1 and Table2). Such comparisons underscore the importance of controllingfor size in assessing the functional and phylogenetic significanceof forward-facing orbits.


levels of orbital convergence in this clade (as wouldbe the case if a descendant were larger in body sizethan its ancestor). Thus, while the evidence ofCarpolestes supports earlier studies regarding themore mosaic sequence of acquisition of euprimatesynapomorphies (Rasmussen, 1990; Sussman,1991), accompanying ecomorphological modelspositing the importance of nocturnal arboreal fru-givory as a basis for elevated orbital convergenceare unfounded. Conversely, although the NVPH’sexplanation for the functional significance ofincreased visual acuity is well supported, becausecertain grasping features arguably predate the ori-gin of Euprimates (Bloch and Boyer, 2002, 2003;Sargis, 2002), the shift to predatory and leapingbehaviors in this clade occurred in an ancestoralready frequenting a terminal-branch milieu(Szalay, 1973, 1981; Szalay et al., 1987; Dagosto,1988) and with little modification in body size.This is at odds with the NVPH’s adaptive scenariofor the coevolution of a wider range of euprimatecranial and postcranial synapomorphies from anancestor with minimal grasping capabilities(Cartmill, 1972, 1974, 1992; Kay and Cartmill,1974, 1977; Kirk et al., 2003). Interestingly, andsimilar to recent evidence regarding the pattern ofanthropoid origins (cf. Fleagle, 1999), new fossildiscoveries from earlier stages of primate historysuggest a more stepwise evolution of the firsteuprimate specializations.

Acknowledgements

The following kindly offered access to speci-mens: W. Stanley, L. Heaney, B. Patterson (FieldMuseum of Natural History); C. Beard (CarnegieMuseum of Natural History); R. MacPhee(American Museum of Natural History); C.Smeenk, D. Reider (Rijksmuseum van NatuurlijkeHistorie); R. Angermann (Humboldt UniversitatMuseum fuer Naturkunde); R. Thorington, L.Gordon, R. Emry, R. Purdy (National Museum ofNatural History); D. Gebo (Northern IllinoisUniversity); M. Tranier, D. Robineau, J. Cuisin,F. Renoult, M. Godinot, B. Senut, C. Berge(Museum National d’Histoire Naturelle); P.Jenkins (British Museum of Natural History);

B. Latimer, L. Jellema (Cleveland Museum ofNatural History); M. Rutzmoser (HarvardMuseum of Comparative Zoology); and R. Kay,C. Vinyard (Duke University Medical Center). M.Cartmill is thanked for the loan of a dihedralgoniometer. M. Dagosto, M. Hamrick, A. Hogue,W. Hylander, W. Kimbel, E. Kowalski, V. Noble,B. Shea, M. Silcox, S. Stack, Y. Wu, and threeanonymous reviewers generously provided com-ments and/or help. This study further benefitedfrom discussions at the 2001 First-Ever Inter-national Conference on Primate Origins andAdaptations. This research was supported by theLeakey Foundation, NSF (BCS-9709587 andBCS-0129349), Wenner-Gren Foundation forAnthropological Research, and NorthwesternUniversity.

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Euprimate origins: the eyes have it