AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 81:381-397 (1990)

Phylogenetic Relationships Among the Notharctinae of North America HERBERT H. COVERT Department of Anthropology, Hellems Building, Uniuersity of Colorado, Boulder, Colorado 80309-0233

KEY WORDS

Eocene, Synapomorphies, Smilodectes

Study of over 1,000 specimens representing all notharctine ABSTRACT genera and species leads to the conclusion that current concepts about the relationships of genera within the Notharctinae are incorrect. The following describes the more probable relationships among these genera. 1)Smilodectes and Notharctus are more closely related to each other than either is to any known early Eocene notharctine. Synapomorphies linking these genera include relatively narrow upper and lower molars, a relatively low-crowned P,, and paraconid size reduction on MIPS. 2) Among known Wasatchian notharctines, a clade consisting of Copelemur tutus and Cop. praetutus shares several lower molar synapomorphies with the Notharctus-Smilodectes clade, and therefore appears to form the Wasatchian sister group of Bridgerian notharctines. Synapomorphies documenting this relationship include well-developed entoconid notches on P,-M,, an anteriorly placed paraconid on M P ,and a long premetacristid on M2. 3) Copelemur and Pelycodus are independently derived from early North American Cantius. Recent suggestions that the European adapine taxa Leptadapis priscus and Microadapis sciureus share special phylogenetic relationships with Smilodectes are rejected. The reduced (or lack of a) paraconid and morphology of the paracristid and other features identified as synapomorphies linking these adapines with Smilodectes are also characteristic of most other adapines as well (e.g., other species of Leptadapis, Adapis, Europolemur, and Anchomomys). Such traits developed independently in Smilodectes, which is clearly a notharctine on the basis of many synapomorphies and thus are not evidence of a close phylogenetic relationship between Smilodectes and L. priscus or M . sciureus. The Notharctinae is an extinct subfamily of Eocene lemur-like primates. Recent reviews of notharctines (Gingerich and Simons, 1977; Gingerich, 1979, 1986; Gingerich and Haskin, 1981; Szalay and Delson, 1979; Covert, 1985) recognize between 14 and 22 valid species in four or five genera (Cantius, Pelycodus, Copelemur, Notharctus, and Smilodectes) (Table 1). These primates are known from large samples collected in early and middle Eocene deposits of the western United States and small samples from early Eocene deposits of England and France. Excellent stratigraphic information is available for some of this material. The Notharctinae are typically grouped with

@ 1990 WILEY-LISS, INC.

the Adapinae in the family Adapidae of the Primate suborder Prosimii (e.g., Simons, 1972) or the Primate suborder Strepsirhini (e.g., Szalay and Delson, 1979). In this paper I examine three aspects of notharctine phylogeny: 1)a “rediscovery”of the phylogenetic relationships of middle Eocene notharctines, 2) a new hypothesis about the relationship of middle Eocene notharctines to early Eocene forms, and 3) the possibility that notharctines are known from middle Eocene European deposits. The ideas and analyses presented here are abReceived February 19,1987, accepted May 17,1989.

382

H.H. COVERT TABLE 1. List of notharctine genera

Genus

No.1

Geographic range

Time range

Cantius

5-9

Pelycodus Copelemur Notharctus Smilodectes

1 4-5 3-4 1-3

France, England, western North America Western North America Western North America Western North America Western North America

Length of early Eocene Early Eocene Early Eocene Middle Eocene Middle Eocene

’Number of species in genus. Range for species number reflccts that there is debate about the number of valid species for genus.

stracted from Covert (19851, a more detailed Pelycodus [Cantius] and Notharctus. Like and much lengthier review of the biology of the latter, this genus may have evolved from Pelycodus jarrovii [C.uenticolis].” My own the notharctines. detailed analysis of the notharctine sample PHYLOGENETIC RELATIONSHIPS AMONG has provided substantial evidence that these THE NOTHARCTINAE hypotheses about notharctine phylogeny are Recent reviews of the Notharctinae have incorrect. suggested that the middle Eocene genera MATERIALS AND METHODS Notharctus and Smilodectes arose indepenCollections of notharctine material were dently from one or two species of early Eocene Cantius (I follow Gingerich and examined a t the Yale Peabody Museum Haskin [1981]in placing the vast majority of (YPM), Harvard‘s Museum of Comparative Wasatchian notharctines in Cantius rather Zoology (MCZ), the American Museum of than Pelycodus). For example, Gazin Natural History (AMNH),United States National Museum of Natural History (USNM), (1958:92)stated: Duke University Primate Center (DPC),the University of Michigan’s Museum of PaleonWithin the Notharctidae there seems no doubt but that Nothurctus was derived from Pelycodus [Can- tology (UM), the United States Geological tius]. Smilodectes, however, though clearly a nothSurvey (Denver) (USGS),Amherst College’s arctid, exhibiting numerous resemblances to NothPratt Museum (AC), the Milwaukee Public urctus and Pelycodus [Cantius], may not certainly be derived from known Pelycodus [Cantiusl. . . . Museum (MPM),the University of WashingSmilodectes, for this reason, possibly did not evolve ton’s Burke Museum, and the British Mufrom Pelycodus [Cantius] of the Rocky Mountain reseum of Natural History (BMNH). Colleceon. tions of adapine material were examined at a Gingerich and Simons (1977275)offered a number of these institutions plus the Muslightly different hypothesis about the ante- seum National &Histoire Naturelle (Paris), the Naturhistorisches Museum (Basel) (Eh), cedents of the middle Eocene notharctines: and the University of Montpellier’s LaboraAs a final point we should consider the relation- toire de Paleontologie. A large number of measurements, includships of early Eocene Adapidae to their middle Eocene descendants. As text-fig. 10 and all other ing len h, width, and height, were made on evidence suggests, Notharctus is a direct descen- the not arctine and adapine teeth. Records dant of Pelycodus jarrouii [Cantius uenticolis]. . . . The origin of Smilodectes, however, is a more diffi- were also made of the specific morphology of cult and still unresolved problem. Smilodectes could each tooth (i.e., cusp and crest number, be derived from either Pelycodus frugiuorus [Can- shape, and location; and occurrence of styles tius frugiuorus], or from P. jarrouii [C. uenticolis]. and cingula) (Covert, 1985).In this analysis I This latter possibility seems more likely, but further detailed stratigraphic and morphological study first identify the polarity of characters of interest. Second, I identify sister group relawill be required to confirm this. tionships among notharctines, and, third, a These two hypotheses are illustrated in phylogeny for this group is pro osed. BeFigure 1. Szalay and Delson (1979) are in cause Cantius ralstoni is one o f t e earliest essential agreement with Gingerich and Si- occurring notharctines and because its cheek mons in their interpretation of the anteced- teeth are quite similar to those of the early ents of middle Eocene notharctines. They omom ‘ds Teilhardina and Anernorhysis, I stated the following about Smilodectes (p. regar its dental morpholo as primitive for 118): “the dental formula is the same as in the subfamily. Only denta characters are

f

R

d”

Y

383

NOTHARCTINE PHYLOGENY A.

Smilodectes

Notharctus

B.

Smilodectes

C.

Notharctus

C.

frugivorus

venticolis

E a r l y Eocene

C.

abditus

/ Fig. 1. Hypotheses about the relationship between early and middle Eocene notharctines. A Phylogenetic

relationships proposed by Gazin (1958). B: Phylogenetic relationships proposed by Gingerich and Simons (1977).

considered in this report. Cranial and skeletal material is not well known for the early Eocene notharctines and thus cannot be used to sort out relationships at present. Further, cranial and skeletal morphology of

the middle Eocene notharctines certainly does not preclude any of the conclusions reached in this report. Finally, I have followed the faunal zonations used by Gingerich and Simons (1977) for the early Eocene

384

H.H. COVERT

a reduced metacone and Nunnopithex-fold (sometimes absent). All of the upper molars are relatively broad (buccolingually), with M2 being extremely broad. At least four fairly consistent changes occurred in the dentition of Cuntius by the middle of the (‘lowerGraybull” (Can. mckennai): The teeth became slightly larger, small styles (especially the parastyle and mesostyle) appeared on the upper molars, the Nunnopithex-fold is often more strongly deRESULTS veloped on M 1and M2, and occasionally the Cuntius rulstoni and the history of the M, has a squared talonid heel with two genus Cantius hypoconulids. During the ‘(upperGraybull” Can. trigonoThe evolutionary history of the genus Cuntius has been considered in detail by a num- dus continued the size increase noted above ber of previous researchers, and basic agree- for this genus (although at a slow and varied ment exists on the pattern of dental changes rate). The styles on its upper molars are that occurred during its history (Osborn, often slightly stronger in development, and 1902; Matthew, 1915; Gregory, 1920, 1937; the Nunnopithex-fold is often stronger in Guthrie, 1967; Gingerich and Simons, 1977; development than the same features on Can. Szalay and Delson, 1979). These changes mckennai teeth. During the “Lysite” the Cuntius lineage include increase in overall size, increase in size and strength of stylar cusps on upper (Can. abditus) is still characterized by a molars, and relatively greater development slight, but not consistent, size increase; of pseudohypocones on upper molars. As slightly stronger styles on P4-M3; and a stated above, Can. rulstoni appears to repre- slightly stronger Nunnopithex-fold on M1-2 sent the primitive dental condition for the that now can be described as a pseudohypoNorth American notharctines (the newly de- cone (Fig. 3). Prior to this stage in the Cunscribed Can. torresi [Gingerich, 19861may be tius lineage the Nunnopithex-fold is often slightly more primitive, but this does not fairly well-developed but rarely shows the alter any of the following analysis). Its mo- lingual and buccal swelling that develops lars have crowns of moderate height and are into a pseudohypocone during the “Lysite.” covered with fairly smooth enamel. M, and Two species of Cuntius occur during the M2 each have a paraconid, protoconid, meta- “Lostcabinian.”Cun.venticolis is the larger of conid, hypoconid, entoconid, and weak hypo- the two and is extremely similar to Can. conulid (Fig. 2) (dental nomenclature is that abditus in all dental traits. Can. frugiuorus of Kay, 1977). These teeth are fairly broad, is a distinctly smaller species and has often with M2 being nearly square. The paraconid been argued to document the only size deis placed at the mesiolingual corner of M 1 crease recorded in the history of this genus. and is displaced distally and compressed In addition, Can. frugivorus often has an M3 against the metaconid on M2.Neither of with a rounded talonid heel bearing a single these teeth (as with P4 and M3) has a hint of hypoconulid, and the styles on its upper an entoconid notch (a notch located distal to teeth are not particularly well-developed. In the entoconid). M3 is a relatively long tooth fact, in size and morphology, Can. frugivorus with a trigonid similar to that ofM,. M, has a weak entoconid, a strong rounded talonid heel that usually has a single hypoconulid, and a cristid obliqua that runs from the hypoconid to the protoconid. M2 and particuFig. 2. A: Occlusal view of right lower molars of Can. larly M’ are nearly triangular in occlusal ralstoni (AMNH 16098-M,_,, DPC 1345 Ms). B: Ocoutline. These teeth have a paracone, meta- clusal view of left (reversed) upper molars of Can. ralcone, and protocone; a narrow stylar shelf stoni (UM 65209). Bar = 1.0 mrn. Fig. 3. A Occlusal view of right lower molars of Can. with little stylar development; a nearly com- abditus (DPC 1533) (bottom) and lingual view of same plete medial cingulum; a small paraconule (top, reversed). B: Occlusal view of right upper molars of and metaconule; and a fairly strong Nunno- Can. abditus (DPC 179@-M’-’, DPC 2983-M3). Bar = pithex-fold. M3 is similar to M1 and M2, with 1.0 mm.

and Gingerich (1979) for the middle Eocene. There is ongoing debate on what is the “most proper” faunal zonation series for the Eocene of North America. Schankler (1980) lists seven such zonation series that have been defined for the early Eocene of North America since 1941. Readers who prefer Schankler’s zonations (or one of the other series listed in his first figure) can make the appropriate translations using his article.

m

cv

m

c3

386

H.H. COVERT

is quite similar to Can. trigonodus in dental detail. Thus, an equally plausible explanation of its occurrence in the “L~stcabinian’~ is that it is the reappearance of the earlier occurring taxon (Can. trigonodus), which for some unknown reason was not present (or was extremely rare) in faunas that are now known from “Lysitian” deposits (see Beard, 1988, for elaboration of this argument). As a final comment on Cantius, it is worth nothing that this genus has received a good deal of attention because of the apparent gradual nature of its evolution (e.g., Simons and Gingerich, 1977; Gingerich, 1985).

Pelycodus jarrovii Pelycodus is the least derived of the other notharctine genera. It differs from Cantius in 1) lacking or having an extremely reduced paraconid on M ,2) lacking a hypoconulid on M, and M2,an83) lacing styles on its upper molars (similar only to Can. ralstoni) (Figs. 4,5). This third trait may simply be a retention of the primitive notharctine condition. For a more complete discussion of the dental mor hology of Pelycodus, see Gingerich and HasEin (1981) and Rose and Bown (1984). Copelemur pruetutus and Cop. tutus These two species ofCopelemur differ from Cantius in having 1) a distinct entoconid notch on P4-M3 (because P, often lacks an entoconid, its notch might better be called a posterolingual notch, 2) relatively narrow (or long) molars (Table 21, 3) the paraconid shifted anteriorly on M2 and M,, and 4) the premetacristid lengthened on M, and M, (Figs. 4,s). For additional information on the dental morphology, see Gingerich and Simons (1977) and Covert (1985). Cop. consortutus and Cop. feretutus Gingerich and Simons (1977) included these taxa with Cop. pruetutus and Cop. tutus in Copelemur because of the presence of distinct entoconid notches on their lower molars. They noted that these species differed from Cop. pruetutus in having relatively broader molars and paraconids that are relatively more distally located (primitive notharctine characters). While not noted by Gingerich and Simons, Cop. tutus resembles Cop.praetutus in these characters. Furthermore, the entoconid notches on the molars of Cop. consortutus and Cop. feretutus are simply not as well-developed as those on

the other members of this genus. In fact, a number of Cantius specimens from the latter portion of the early Eocene have entoconid notches similar in size and shape to those of Cop. consortutus and Cop. feretutus. Thus it is not always easy to distinguish between specimens of these taxa and individuals of Can. frugiuorus and small Can. abditus. Notharctus Species of Notharctus differ from those of Cantius in having 1) distinct entoconid notches on P4-M3, 2) much narrower (or longer) lower molars (Table 2), 3) a paraconid shifted anteriorly on M2 and M,, 4) the premetacristid lengthened on M, and M3, 5) reduced paraconids on M2and M, (Figs. 7,9), 6) relatively narrower (longer)upper molars (Table 3), 7) a postparacrista running distobucally from the paracone and remetacrista running mesiobucally from t e metacone, 8) rectangular M3 (Fig. 7),9)reduction in the relative height of P4(Table 4), and 10) a fused mandibular symphysis (Fig. 4). Snilodectes Smilodectes differs from Cantius in all the ways that Notharctus does except that it lacks a fused mandibular symphysis (Figs. 4, 8,9). In addition, it differs from Cantius in 1) lacking a paraconid on M2 and M, and 2) having a cristid obliqua on M, that runs mesiolingually from the hypoconid to the distal trigonid wall immediately posterior to the metaconid (Fig. 8). Notharctine relationships Given this distribution and polarity of morphological characters (Fig. 4), what can we say about the evolutionary relationships of these genera? Notharctus and Smilodectes appear to share a large number of derived character states. Moreover, in one of the additional characters in which Smilodectes is uniquely derived (i.e., lacking paraconids on M2-3), it actually shows an enhancement of the derived state of Notharctus (reduced paraconids on lower molars). This is by far the largest agreement of derived character states within the Notharctinae; therefore, it is concluded here that Notharctus and Smilodectes are sister groups (as previously suggested by Covert, 1984). Because the Cop. praetutus and Cop. tutus clade share more derived states (five or six) with Notharctus and Smilodectes than do other Wasatchian notharctines, it is concluded here that

K

NOTHARCTINE PHnOGENY

1. Reduced a n d distally, compressed paraconid o n M

387

2.

2. Loss of s t y l e s on M l - , .

3 . Loss of hypoconulid on M , . 2 . 4 . Entoconid n o t c h o n P4 - M,.

5. Relatively narrow lower m o l a r s . 6 . Relatively narrow upper m o l a r s .

7. Relatively low-crowned P,. 8. Relatively anteriorly l o c a t e d paraconid on M 2 . 3 . 9. Relatively l o n g prernetacristid on M2+ 10. R e l a t i v e l y small p a r a c o n i d on 1-3-

11. Loss of p a r a c o n i d on M 12. 'W'-shaped on M I - 2 .

2.3.

buccal shear cres t s

13. Rectangular M 3 . 14. Fused mandibular symphysis. 15. Mesiolingually d i r e c t e d c r i s t i d obliqua o n M,. 16. I n c r e a s e d molar size.

17. I n c r e a s e d size of styles o n

M

1-2.

Fig. 4. Distribution of dental traits among the Notharctinae. Blank squares indicate presence of primitive state and black squares indicate presence of derived state. A, Taxa have buccal shear crests on their upper first two molars that approach the condition seen in Notharctus and SmzZodectes for the preparacrista and

postmetacrista but not for the postparacrista and premetacrista; B, Morphology that I consider to be further derived over the condition shown by Notharctus (i.e., further reduction in anteriorly located paraconid); C, I am not certain of the expression of this feature for these taxa.

1

1 1

389

NOTHARCTINE PHnOGENY

these two Copelemur species are the sister group of the middle Eocene notharctines (as previously suggested by Covert, 1982,1984). Figure 10 illustrates the cladistic relationships within the Notharctinae, and Figure 11provides an evolutionary scenario for this group of early primates. As illustrated in Figure 11, a number of branching speciation events occurred during the North American history of the Notharctinae. It is likely that one lineage and possibly two diverged from Cantius during the “lower Graybull.” The first, (split 1 of Fig. 111,which led to the earliest Cop. praetutus (first appearance, “upper Graybull”), initially involved the development of an entoconid notch on P4-M,. After this change a second divergence may have taken place (split 3a), leading to Cop. feretutus. Subsequent changes that occurred in the lineage leading to Cop. praetutus included the narrowing of the lower molars and an anterior shift of the paraconid on M2-3 that also contributed to the lengthening of the premetacristid and the lingual opening of the trigonid basin. A second lineage possibly diverged from Cantius during the “lower Graybull” (split 2a), leading to P.jarrouii (first appearance, late “upper Graybull”). Changes in this lineage would have included a size increase in the dentition, a size increase of the Nannopithex-fold on M1-’ creating a pseudohypocone, the development of a squared talonid heel on M,, the loss or extreme reduction of the paraconid on M,, and the loss of the hypoconulid on M1-,. If this speciation event occurred later (split 2b), it would have included a significant size increase, the loss of the paraconid (or extreme reduction) on Ma, the loss of styles on the upper molars (a return to the primitive condition), and the loss of the hypoconulid on Ml-2. If split 3a (discussed above) did not occur then it is quite likely that split 3b did. This split would have included the development of an entoconid notch on a t least and possibly on

Fig. 5. A Occlusal view of left lower molars of P. jurrouzi (USGS6549). B: Occlusal view of right upper molars ofP.jurrouii (USGS6549). Bar = 1.0 mm. Fig. 6 . Occlusal view of right lower second and third molars of Cop. tutus (composite of AMNH 16205 and 16206)(bottom) and lingual view of same (top, reversed); cusp tips have been reconstructed. 1, Location of entoconid notch; 2, anterior placement of the paraconid. Bar = 1.0 mm.

TABLE 2. Lower molar shape indices ( W / L X 100)l Species

Cantius C. ralstoni C. mckennai C. trigonodus C. abditus C. frugiuorus C. uenticolis Pelycodus P. jarrouii Copelemur C. consortutus C. feretutus C. praetutus C. tutus Notharcutus N . tenebrosus N. pugnax N. robustior Smilodectes S. aracilis

n

M1 Mean

s

n

Mean

s

36 45 44 84 16 13

85.7 88.4 88.9 88.9 87.1 87.8

5.5 5.7 4.4 3.9 3.7 3.8

53 62 54 122 18 20

95.8 97.2 96.0 96.0 95.8 95.4

4.5 5.1 3.7 4.3 3.8 5.2

1

87.5

3

95.0

1.6

5

88.1

6.2

3 5

6.0 3.6

1 5

83.5 84.9

3.6

4

93.2 95.6 85.8 91.1

17 15 45

79.0 81.7 81.5

4.4

2.8 6.3

17 20 50

82.6 85.3 86.2

4.5 4.3 5.4

37

78.5

3.1

34

84.4

3.7

M2

1

3.2

In, sample size; s, standard deviation

P4. If this represents the actual history of Cop. feretutus and Cop. consortutus, it would be evidence that they should be placed in the genus Cantius (or a new genus); otherwise, Copelemur would be polyphyletic. Toward the end of the “Lysite” another speciation event (split 4) occurred within this radiation. Can. frugiuorus differs from its precursor in being smaller, in having reduced stylar development, and in often having an M3 with a rounded talonid heel. An alternative possibility, as noted above, is that this smaller “Lostcabinian” species is a reappearance of Can. trigonodus. It is evident from Figures 10 and 11that Cantius is considered a paraphyletic taxon here. While this may not be acceptable to some, I prefer it over the alternative of naming at least two new notharctine genera, both of which would be morphologically indistinguishable from Cantius. A lineage split from that of Cop. tutus, leading to the middle Eocene notharctines before the end of the “Lostcabinian” (split 5). Changes that occurred here include the enlargement of upper molar styles, enlargement of M1-2 pseudohypocones,narrowing of the upper and lower molars, a slight reduction in the paraconid size on the lower molars, and a tendency for M3to be more rectangular in outline. Shortly after split 5 occurred another branching event took place

3

1

m

3

a

00

391

NOTHARCTINE PHYLOGENY

in the notharctine radiation (split 6),leading to Smilodectes (the remainder of Bridger notharctines belong in Notharctus). An initial change that occurred in the lineage leading to Smilodectes was a shift in the orientation of the cristid obliqua on M, (it runs into the distal trigonid wall near the metaconid rather than to the protoconid as it does in other notharctines). The following changes also occurred in this lineage before Bridger B times: There was a decrease in size, the pseudohypocone is shifted distolinpally and is more strongly developed on M than on M1(the reverse of the situation in other notharctines), the M3 has become more complex (i.e., stronger styles, stronger metacone, and relatively larger in comparison to M2), and the talonid heel on M, has become squared with at least two hypoconulids. An initial change that occurred in the Notharctus lineage after Smilodectes branched from it is fusion of the mandibular symphysis. By the beginning of Bridger B a split (split 7) had occurred in the Notharctus lineage. A slight increase in size of the dentition, an increase in size of upper molar styles, and an increase in the size of the pseudohypocones on the first two upper molars had occurred in the lining leading to N. p u g m . In contrast, the N. tenebrosus line is characterized by a slight decrease in size of the dentition and of the pseudohypoconeson Finally, theN. pugnax-N. robustior lineage is characterized by a slight increase in size during Bridger C times. DISCUSSION

The detailed analysis of notharctine dental morphology outlined above provides strong evidence for an alternative hypothesis of relationships of the two middle Eocene genera to one another and to the early Eocene notharctine genera than that of Gazin (1958), Gingerich and Simons (19771, and Szalay and Delson (1979). As outlined above, Smilodectes and Notharctus are linked by the narrowness of both their upper and lower molars, the strength of styles on

Fig. 7. A Occlusal view of right lower molars of N . tenebrosus (MPM 6650) (bottom) and lingual view of the same (top, reversed). B: Occlusal view of right upper molars ofN. tenebrosus (USNM 21962). Bar = 1.0 mm. Fig. 8. A Occlusal view of right lower molars of S. grucilis (USNM 21992) (bottom) and lingual view of the same (top, reversed). B: Occlusal view of right upper molars ofS. grucilis (YPM 12904). Bar = 1.0 mm.

their upper molars, the reduction of the paraconids on their lower molars, and the rectangular shape of M3.This makes it quite unlikely that they were derived independently from Cantius, which lacks these characters. This conclusion is in part a rediscovery of a suggestion first made earlier in this century. In 1926 Troxell pointed out that the dentitions of Smilodectes and Notharctus were very similar and concluded that the former genus should be sunk into the latter. This was accepted by many researchers, including Robinson (19571, until Gazin (1958) provided the initial detailed discussion of Smilodectes cranial material. Further, middle Eocene notharctines share with Cop. praetutus and Cop. tutus entoconid notches

TABLE 3. Uooer molar shaoe indices IL/W X 1001' Suecies

Cantius C. ralstoni C. mckennai C. trigonodus C. abditus C. frugiuorus C. uenticolis Pelycodus P. jarrovii Copelemur C. consortutus C. feretutus C. tutus Notharcutus N. tenebrosus N. pugnax N. robustior Smilodectes S. eracilis

n

M' Mean

s

n

MZ Mean

s

21 14 25 10 7 5

71.1 70.0 70.3 70.7 68.0 76.0

3.9 5.7 4.3 5.1 2.6 2.7

41 14 31 12 7 5

61.1 62.2 65.5 64.6 65.0 68.1

3.7 2.5 3.4 2.8 4.3 1.7

2

73.8

2

71.5

1

72.2

1 1

63.2 63.2 66.7

1 12 7 16

81.1 81.1 78.1

4.2 4.3 4.1

9 10 20

74.9 76.2 76.6

3.7 6.1 4.6

12

79.2

4.3

14

77.6

3.2

' n , sample size; s, standard deviation

TABLE 4. Lower fourth premolar height index ( H / L X 100)' Species

n

Mean

S

Cantius ralstoni Cantius mckennai Cantius trigonodus Cantius abditus Cantius uenticolus Copelemur praetutus Copelemur tutus Notharctus tenebrosus Notharctus pugnax Notharctus robustior Smilodectes gracilis

21 23 5 38 9 1

103.4 106.9 105.1 102.0 96.5 105.1 93.8 86.4 82.9 82.5 83.9

10.2 8.5 10.5 7.9 6.1

1

13 13 17 14

In, sample size; s, standard deviation.

8.2 8.5 8.0 9.6

392

H.H. COVERT

Fig. 9. From top to bottom: lingual view of first and second lower molars of Can. abditus (USGS 1379), lingual view of lower molars ofN. tenebrosus (MPM 6650), and lingual view of lower molars of S. grucilis (USNM

21992). Note similarities between Notharctus and Smilodectes in premetacristid length (1)and morphology of entoconid notch (2).

on P4-M3, mesiolingually laced paraconids, long premetacristids, anc r lingually opened trigonids on Ms3. Thus, it is likely that middle Eocene notharctines are derived from the Cop. praetutus-Cop. tutus clade rather than directly from Cantius, which lacks these characters. One could question the identification of the mesiolingually

placed paraconids, long premetacristids, and lingually opened trigonids as three discrete synapomorphies of this group rather than a single feature; certainly the first two are directly related to one another. However, the metaconid and paraconid could be widely spaced and connected by relatively tall postparacristids and premetacristids such that

393

NOTHARCTINE PHnOGENY Cantius torresi

Cantius ralstoni, -rnckennai

Pelycodus

Cantius trigonodus, abditus. venticolis, frugivorus

/

\

Copelemur feretutus, consortutus

Copelemur praetutus

w,

Notharctus

Srnilodectes Fig. 10. Cladogram illustrating the hypothesized relationships among North American Notharctinae. Bro-

ken lines indicate possible alternative relationships (see text for discussion).

the trigonid would not be open lingually. The fact that the trigonid is constructed in much the same fashion on MZp3of Cop. praetutus, Cop. tutus, Notharctus, and Smilodectes (Smilodectes has, however, lost the paraconid on these teeth) is strong evidence that this is a synapomorphous condition. The phylogenetic placement of Cop. consortutus and Cop. feretutus is a more complex issue. It can be argued (as by Gingerich and Simons, 1977, for example) that these animals are linked to Cop. tutus and Cop. praetutus on the basis of the entoconid notch. Because

they resemble Cantius in the vast majority of other dental characters they would represent the most primitive members of Copelemur. Alternatively, it could be argued that they have developed an entoconid notch in parallel with Cop. tutus and Cop. praetutus and are more properly considered as species of Cantius, or even as specimens of previously recognized species of Cantius. Beard and Covert (manuscript in preparation) discuss in detail the exact phyletic position of Cop. feretutus and Cop. consortutus. What characters did previous researchers

394

H.H.COVERT

I

Bridger C

N. r o b u s t i o r

W

2 W

0

0

Bridger B

W

i Bridger A

W

z W

0

U. Gray B u l l

0

stutur

W l.Li

L. Gray Bull

Sand Coulee

--

I

C. r a l r t o n i a n z C. t o r r e r i 1--

I

C. eppsi i n d C. r a v a g e i

--

v

-~

Fig. 11. Evolutionary scenario for the Notharctinae (see text for discussion).

use to link Cantius to the middle Eocene notharctines? 1) Cant. venticolis occurs in deposits (Lost Cabin equivalents) immediately underlying those in which middle Eocene notharctines are collected (Bridgerian equivalents); 2) Lostcabinian Cantius has fairly large styles and pseudohypocones on their upper molars, resembling the morphology of middle Eocene notharctines; and 3 ) Can. ventzcolis is larger than preceding members of its genus and slightly smaller

than the earliest occurring Notharctus and thus is of “appropriate size”to be antecedent to Notharctus. The importance of some of these characters could be questioned, but their credibility is a moot point here because they are all also characteristic of Cop. tutus,’ ‘There is some question as to the exad age of the deposits in which specimens of C. tutw have been collected.While Gingerich and Simons (1977)assumed that they date from deposits of ‘Lostcabinian” age, Lucas et al. (1981)reported that these deposits are more likely to be of “Lysite”equivalence.

NOTHARCTINE PHYLOGENY

which, as noted above, also shares a number of other characters with the middle Eocene notharctines. Beard (1988) has also recently considered the phylogeny of North American notharctines and has come to conclusions that differ somewhat from those of this paper. Specifically, he suggests that Smilodectes is derived from Copelemur and Notharctus is derived from Cantius. I would argue, however, that the majority of traits that he uses to link Smilodectes with Copelemur are also characteristic of Notharctus (e.g., paraconid placement, paracristid morphology, M, hypoconulid morphology, and mesostyle size). Further, while interesting, Beard’s analysis does not consider some of similarities in shape and morphology between the cheek teeth ofSmilodectesand Notharctus noted in this research (e.g., height of P4 and narrowness of upper and lower molars). When these points are considered, I believe that the proposed phylogeny of the notharctines in this paper is more plausible than that of Beard. Finally, both the hypothesized phylogeny proposed here and that of Beard consider Cop. praetutus and Cop. tutus to be important taxa for understanding the evolution of middle Eocene notharctines. Because both are known from very small and incomplete samples more complete specimens of these taxa should yield important insights for this debate. EVALUATIONS OF RECENTLY PROPOSED RELATIONSHIPS OF NOTHARCTINES TO MIDDLE EOCENE EUROPEAN FORMS

From time to time various European species have been allocated to the Notharctinae. Recent examples include the allocations of Leptadapis priscus and Microadapis sciureus to the Notharctinae by Schwartz and Tattersall (1982a,b). In 1916 Stehlin described a new species, Adapispriscus (referred to here as L. priscus following Szalay and Delson, 1979), based on two s ecimens, a mandible (Eh 596) preserving eavily worn P,-M, and an unworn M, (Eh 758). Both specimens were collected a t one of the middle Eocene localities at Egerkingen, Switzerland. Recently Schwartz and Tattersall (1982b) proposed that the type specimen of L. priscus actually should be attributed to the genus Smilodectes as S. priscus. This suggestion is based on a suite of dental characters that Eh 596 supposedly shares with S.gracilis. They de-

R

395

scribed Smilodectes as being distinct from other North American Eocene primates on the basis of four characteristics (p. 297):

“(1)lacking distinct paraconids on M1-3, (2) having stout, inferiorly descending paracristids that open the trigonids on M1-3, (3) having quite medially directed cristids obliquae on M1-3, and (4)having distinct entoconid notches on M1-2.” They found the type of L. priscus to “mirror”Smilodectes in characters 1-3, and they identify a shallow entoconid notch on the M2 of Eh 596. In addition, they described the second referred specimen of L. priscus to be “quite distinct from the type ofpriscus and should be excluded from this species.” My own analysis of L. priscus and S. gracilis has led me to quite different conclusions. First, the type specimen of L. priscus is so heavily worn that it is difficult to see any of the anatomical characteristics that are said to characterize it. Whether this specimen had small paraconids on M, or M whether its paracristids were “stout” and ‘Lferiorly descended,” how far medially directed the cristid obliquae were on M1 and M2, and if either M, or M2 had a distinct entoconid notch are simply indeterminate. Moreover, Eh 758, the second L. priscus specimen, has no characters that distinguish it from the type (besides its unworn state!), and it does show Schwartz and Tattersall’s first three “characters” of Smilodectes but it lacks an entoconid notch. In any event, as outlined in previous discussion, Smilodectes is not distinguished from other North American notharctines in having entoconid notches on M, and M2 (this feature is also characteristic of Copelemur and Notharctus) or in having quite medially directed cristid obliquae on MI and M2 ( N . tenebrosus is very similar to Smilodectes in this respect). In addition, S. gracilis is distinct from L. priscus in having a distinct entoconid notch on M,. Finally, many adapines-Adapis parisiensis, L. magnus, Protoadapis curuicuspidens, and Anchomomysgaillardi, for example-lack or have only weakly developed paraconids on M, and M2, possess inferiorly directed paracristids on MI and M2, and have medially directed cristid obliquaes. Thus, in the coincidental ways in which L. priscus may resemble S . gracilis, it also closely resembles the prevalent adapine character states. Taken together, the traits cited, as well as the balance of other dental characteristics,

396

H.H. COVERT

offer no convincing evidence that L. priscus shares a special phylogenetic relationship with Smilodectes. L. priscus is clearly an adapine and is still best assigned toleptadapis pending the recovery of more complete material. Stehlin (1916)named and described a second small adapine, Adapis sciureus (here referred to as Microadapis sciureus following Szalay and Delson, 19791, also from the Swiss middle Eocene. Schwartz and Tattersall (1982a) alleged that the type of this species, Eh 750, a mandible with C-M,, is also allied to S.gracilis. As with their placement of L. priscus in Smilodectes, their reasoning for this conclusion is unsound. At least in this case, however, we are dealing with a well-preserved and little-worn specimen. They described this specimen as having the following characters (p. 181):“large and genuinely caniniform lower canine,” a “complete and uninterrupted hypocristid,” and an “arcuate cristid obliqua on MI that swings over to meet the metaconid.” They further described the following “specific resemblances to Smilodectes”: a ‘lowering of the molar paraconid shelves front to back, and in the absence of the paraconid itself,” and “the arcuate cristid obliquae of the M, of sciureus matches that of Smilodectes in failing to meet a posteriorly directed crest emanating from the protoconid.” They concluded: “that M. sciureus, far from being allied to Adapis and its close relatives, fails to show any of the synapomorphies of this group; instead, it bears close affinities with North American Eocene strepsirhines, in particular Smilodectes.”

an entoconid notch together with the lack of a paraconid on the lower molars of Microadapis would mean that this species has reevolved a continuous hypocristid, since an entoconid notch is developed in the lineage leading to Smilodectes before the paraconid is lost. Such a change is certainly possible, but is more parsimonious t o conclude that Microadapis is an adapine because, contrary to Schwartz and Tattersall’s claims, this taxon is much more similar in detail to other adapines than to notharctines as has long been believed. CONCLUSIONS

1. The middle Eocene notharctine genera Smilodectes and Notharctus are sister taxa; thus they are not derived independently from any early Eocene notharctine species. 2. The sister taxon to the Notharctus-smilodectes clade is the Cop. tutus-Cop. pruetutus clade, not a species of Cuntius. 3. L. priscus and M . sciureus do not share special phylogenetic affinities with S.gracilis and are best retained in the subfamily Adapinae. ACKNOWLEDGMENTS

I thank R.F. Kay, E.L. Simons, K. Glander, R. MacPhee, M. Cartmill, B.A. Carlson, and especially K.C. Beard, R. Wikander, and an anonymous reviewer for reading and commenting on various stages of this paper. I also thank the following persons and institutions for access to specimens in their collections: the American Museum of Natural History, Dr. R.H. Tedford; National Museum of Natural History, Dr. R. Emry; Yale Peabody This conclusion is not defensible for the Museum, Dr. J.H. Ostrom and M.A. Turner; following reasons. 1) The three characters Museum of Paleontology at the University of that provide “specific resemblances to Michigan, Dr. P.D. Gingerich; Milwaukee Smilodectes” (paraconid shelf morphology, Public Museum, D. Gabriel; Burke Museum absence of paraconid, and cristid obliqua at the University of Washington, Dr. J.M. morphology on M,) are also specific resem- Rensberger; Museum of Comparative Zoolblances to species of Adapis, Leptadapis, ogy at Harvard University, Dr. F.A. Jenkins Europolemur, and Anchomomys (adapines Jr. and C. Schaff; U.S. Geological Survey from the European Eocene). These charac- (Denver), Dr. T.M. Bown; The Johns Hopters indicate no close link of Microadapis to kins University Department of Cell Biology Srnilodectes. 2 ) Schwartz and Tattersall and Anatomy, Dr. K.D. Rose; Pratt Museum (1982a) properly note that Microadapis at Amherts College, Dr. M.C. Coombs; Duke lacks the entoconid notch on its lower molars Primate Center, Dr. E.L. Simons and P. and squared talonid heel on M3 that charac- Chatrath; Museum National d’Histoire Naterize Smilodectes. If the morphocline polar- turelle, Paris, Dr. D.E. Russell; British Muities of the notharctine dentition described seum of Natural History, Dr. P. Andrews; earlier in this paper are correct, the lack of Naturhistorisches Museum, Basel, Dr. B.

NOTHARCTINE PHYLOGENY

Engesser; and Laboratoire de Paleontologie, University of Montpellier, Dr. M. Godinot. LITERATURE CITED Beard KC (1988) New notharctine primate fossils from the early Eocene of New Mexico and southern Wyoming and the phylogeny of Notharctinae. Am. J . Phys. Anthropol. 75:439-470. Covert HH (1982) Dietary adaptations of Pelycodus and a comment about the phylogenetic position of Copelemur. Am. J . Phys. Anthropol. 57:177 (abstract). Covert HH (1984) Phylogenetic relationships within the Notharctinae. Am. J . Phys. Anthropol. 63:148 (abstract). Covert HH (1985) Adaptations and Evolutionary Relationships of the Eocene Primate Family Notharctidae. Ph.D. thesis, Duke University, Durham, NC. Gazin CL (1958) A review of the middle and upper Eocene primates of North America. Smithsonian Misc. Coll. 141:l-112. Gingerich PD (1979) Phylogeny of middle Eocene Adapidae (Mammalia, Primates) in North America: Smilodectes and Notharctus. J . Paleontol. 53:153-163. Gingerich PD (1985) Species in the fossil record: Concepts, trends, and transitions. Paleobiology 11:2741. Gingerich PD (1986) Early Eocene Cantius torresi-Oldest primate of modern aspect from North America. Nature 319:319-321. Gingerich PD, and Haskin RA (1981) Dentition of early Eocene Pelycodus jarrouii (Mammalia, Primates) and the generic attribution of species formerly referred to Pelycodus. Contrib. Mus. Paleontol. Univ. Mich. 25:327-337. Gingerich PD, and Simons EL (1977) Systematics, phylogeny, and evolution of early Eocene Adapidae (Mammalia, Primates) in North America. Contrib. Mus. Paleontol. Univ. Mich. 24:245-279. Gregory WK (1920)On the structure and relationships of Notharctus, an American Eocene Primate. Mem. Am. Mus. Nat. Hist. 3:49-243. Gregory WK (1937) Supra-specific variation in nature and in classification. Am. Nat. 71:268-276.

397

Guthrie DA (1967) The mammalian fauna of the Lysite member, Wind River Formation (lower Eocene) of Wyoming. Ann. Carnegie Mus. 43:47-113. Kay RF (1977) The evolution of molar occlusion in the Cercopithecidae and early catarrhines. Am. J . Phys. Anthropol. 46:327-352. Lucas SG, Schoch RM, Manning E, and Tsentas C (1981) The Eocene biostratigraphy of New Mexico. Geo. SOC. Am. Bull. 92:951-967. Matthew WD (1915) A revision of the lower Eocene Wasatch and Wind River faunas. Part nT: Entelonychia, Primates, Insectivora (part).Bull. Am. Mus. Nat. Hist. 34:429-483. Osborn HF (1902) American Eocene Primates, and the supposed rodent family Mixodectidae. Bull. Am. Nat. Hist. 16:169-214. Robinson P (1957) The species of Notharctus from the middle Eocene. Postilla 28:l-27. Rose KD, and Bown TM (1984) Early Eocene Pelycodus jarrouii (Primates: Adapidae) from Wyoming: Phylogenetic and biostratigraphic implications. J . Paleontol. 58:1532-1535. Schankler DM (1980) Faunal zonation of the Willwood Formation in the Central Bighorn Basin, Wyoming. In PD Gingerich (ed.): Early Cenozoic Paleontology and Stratigraphy of the Bighorn Basin, Wyoming. Ann Arbor: University of Michigan Museum of Paleontology, pp. 99-114. Schwartz JH, and Tattersall I (1982a) Relationships of Microadupis sciureus (Stehlin, 19161, and two new primate genera from the Eocene of Switzerland. Folia. Primatola. 39:178-186. Schwartz JH, and Tattersall I (1982b) A note on the status of “Adaphispriscus” Stehlin, 1916. Am. J . Primatol. 3:295-298. Simons EL (1972)Primate Evolution: An Introduction to Man’s place in Nature. New York: Macmillan, 322 pp. Stehlin, HG (1916) Die Saugetiere des schweizerichen Eocaens. Critischer Catalog der Materialien. Part 7, second half. Abhandlungen der schweizerischen p a laontologischen Gesellschaft 41: 1299-1552. Szalay FS, and Delson E (1979) Evolutionary History of the Primates. New York: Academic Press. 580 DD. Troxell EL (1926) Smilodectes and Notharctus. J. Sci. 11:423428.

‘Am.