Comparative dental morphology of Propotto and Plesiopithecus

Propotto leakeyi was originally described by Simpson as a lorisiform strepsirrhine that might be related to the extant lorisid Perodicticus (commonly known as the potto)21. The hypodigm available to Simpson included the holotype (KNM-SO 508, his specimen “R”; KNM = National Museums of Kenya), a right mandible with P 3 -M 2 and alveoli for P 2 and M 3 as well as a small portion of the root of an enlarged anterior tooth (Figs. 1g and 2b); KNM-RU 1879 (specimen “S”), a left mandible with a very shallow P 2 alveolus, an erupting P 3 , fully erupted dP 4 and M 1 , alveoli for M 2 and an erupting M 3 (see M 1 and M 3 in Fig. 1c, d, respectively; this specimen also exhibits a laterally compressed and forward-facing alveolus for an anterior tooth); and KNM-RU 2084 (specimen “T”), a right mandible with M 2–3 that is most likely from Songhor but labeled as being from Rusinga (Fig. 1i). KNM-RU 1879 has “Songhor” written on the specimen despite the fact that the label suggests it might be from Rusinga; we consider it probable that the specimen is, in fact, from Songhor. If all of these specimens are indeed from Songhor, they would originate in the Chamtwara and the “Kapurtay Conglomerates” of Butler24, which Pickford25 put in his “Set I” fauna, and dated at 18.5–20 Ma. This estimate is mainly based on K-Ar dates of Bishop et al.26 published in 1969, so additional work is needed to provide more precise age constraints for these localities using contemporary methodologies. Digital models of all the fossil specimens figured here are available on MorphoSource (Table 1).

Fig. 1 Comparison of lower molar morphology of latest Eocene Plesiopithecus teras and early Miocene Propotto leakeyi and mandibular morphology and lower dentition of Plesiopithecus teras. a M 1–3 of DPC 11636, left mandible of Plesiopithecus teras (reversed for comparison, latest Eocene, Quarry L-41, Fayum Depression, Egypt); b M 1–3 of CGM 42291, holotype right mandible of Plesiopithecus teras; c Left M 1 of KNM-RU 1879, mandible of Propotto leakeyi (reversed for comparison; Simpson’s specimen “S”; note that this specimen is probably from Songhor despite the Rusinga accession number); d Left M 3 of KNM-RU 1879, mandible of Propotto leakeyi, reversed for comparison; e KNM-CA 1832, isolated right M 1 of Propotto leakeyi (early Miocene, Chamtwara, Kenya); f KNM-CA 2195, isolated right M 2 of Propotto leakeyi (early Miocene, Chamtwara, Kenya); g M 1 of KNM-SO 508, holotype right mandible of Propotto leakeyi (early Miocene, Songhor, Kenya; Simpson’s specimen “R”); h M 2 of KNM-SO 508, holotype right mandible of Propotto leakeyi; i M 2–3 of KNM-RU 2084, right mandible of Propotto leakeyi (possibly from Songhor despite the Rusinga accession number; Simpson’s specimen “T”); j DPC 13607, left mandible of Plesiopithecus teras, with an alveolus that we interpret as being for a small canine, and tooth crowns that we interpret as I 1 or I 2 and P 2 -M 2 . Digital models were created using CT scans made available by the Duke Lemur Center Division of Fossil Primates and the National Museums of Kenya, which were downloaded from www.morphosource.org and made available for reuse under a CC BY-NC license. Map of Africa is adapted from Google Earth Full size image

Fig. 2 Comparison of lower molar morphology of Daubentonia, Plesiopithecus, and Propotto, and volume rendering of the enlarged anterior teeth of Plesiopithecus and Propotto. a Left M 1–3 of AMNH M-41334, extant Daubentonia madagascariensis, with individual surfaces reoriented slightly to facilitate comparison (teeth are from right side in AMNH M-41334 but are reversed for comparison); b left P 3 -M 2 of Propotto leakeyi (holotype mandible KNM-SO 508, teeth are from right side but are reversed and reoriented slightly to facilitate comparison); c left mandible with I 1 or I 2 and canine-M 3 of Plesiopithecus (DPC 11636). Scale in left panel is for a–c (2 mm). d–f Volume renderings of the enlarged anterior tooth (probable I 1 or I 2 , rendered orange-yellow) in d KNM-KO 101, left mandible with partial root of I 1 or I 2 and crowns of P 3 -M 2 , Propotto leakeyi (early Miocene, Koru, Kenya); e KNM-RU 3690, right mandibular fragment with root and partial crown of I 1 or I 2 and crowns of P 3–4 , cf. Propotto leakeyi (early Miocene, Rusinga Island, Kenya); note that in this specimen the root of I 1 or I 2 extends under the roots of M 1 ; f DPC 11636, left mandibular corpus with complete crowns of I 1 or I 2 and canine-M 3 , Plesiopithecus teras. Digital models were created using CT scans made available by the Duke Lemur Center Division of Fossil Primates and the National Museums of Kenya, which were downloaded from www.morphosource.org and made available for reuse under a CC BY-NC license Full size image

Table 1 DOI addresses for digital surface models of figured fossil specimens Full size table

Simpson21 noted the “highly peculiar cheek teeth” (p. 51) of Propotto and the fact that its mandible deepened anteriorly, but nevertheless considered this taxon to be similar enough to the extant lorises Perodicticus and Nycticebus to recognize Propotto as an aberrant lorisid. Walker22 re-examined the hypodigm of Propotto and pointed out that the single-rooted P 2 was probably small (though no crown is preserved), and not enlarged and caniniform as in lorisiforms. Further, he interpreted the alveolus of Propotto’s enlarged anterior lower tooth as being for a caniniform canine, and contrasted that with the canine morphology that would be expected in lorisiforms, which incorporate the canine into a toothcomb. Finally, he noted that the mandibular corpus was also unlike those of lorisiforms in deepening anteriorly and having a deep masseteric fossa. Walker concluded that Propotto was a pteropodid fruit bat and not a primate, a conclusion that was accepted by Simpson in correspondence exchanged before the 1969 publication of Walker’s work (Supplementary Fig. 1).

In 1984, Butler24 described a few additional Propotto specimens from the early Miocene sites of Koru, Chamtwara, and Rusinga Island in western Kenya25. The specimens from Rusinga localities located in the Hiwegi Formation would be considerably younger, dated to ~17.9 Ma27. Butler discussed the resemblance of Propotto’s cheek teeth to those of primates such as Cheirogaleus, Perodicticus, and Pithecia, and also with the Neotropical phyllostomid bat Artibeus. He further noted that the enlarged anterior lower tooth of Propotto (which he also interpreted as a canine) is relatively larger than the lower canines of extant pteropodids, having a root that extends posteriorly to at least P 3 . Despite these observations, Butler ultimately supported the idea that Propotto represented a side-branch of the chiropteran family Pteropodidae, erecting a new subfamily, Propottininae, for the genus.

For the last half-century, discussion of Propotto’s significance as a possible primate has been deterred by the authoritative consensus reached by Simpson, Walker, and Butler that Propotto is a bat. However, it is now clear that the features that Walker cited in his criticism of Simpson’s identification of Propotto as a lorisid are all characteristic of the undoubted strepsirrhine primate Plesiopithecus and so do not necessarily exclude Propotto from Strepsirrhini (Fig. 1j). The laterally compressed and presumably highly procumbent lower anterior tooth of Propotto (Fig. 2d, e; unknown to both Simpson and Walker because this feature is only preserved in specimens described by Butler in 1984) does not occur in fruit bats, or for that matter any known living or extinct chiropteran. This feature is, however, present in Plesiopithecus (Figs. 1j and 2d–f) and Daubentonia.

Despite being very low-crowned, the lower molars of Propotto are fundamentally strepsirrhine in structure, and are very similar to those of Plesiopithecus (Fig. 1a–i). Differences from Plesiopithecus include extension of the oblique cristids to meet the protoconid apices, reduction or elimination of hypoflexids, reduction of metaconids, and presence of a cingulid around the lingual margin of the metaconids. The P 3–4 of Propotto and Plesiopithecus are very similar in having mesially shifted protoconids from which two dominant crests run distobuccally and distolingually to enclose well-developed talonids (Fig. 2b, c). An automated geometric morphometric analysis of lower molar morphology in strepsirrhines, pteropodids, Propotto, and various living and extinct euarchontans demonstrates that the shape of Propotto’s M 2 is most similar to that of strepsirrhines (and particularly those of cheirogaleids, Daubentonia and Plesiopithecus; Fig. 3). The molar morphology of this set of taxa occupies a morphospace that is distinct from sampled pteropodids. Strepsirrhine lower molars also have low principal component (PC) 1 values that separate them from all non-euarchontans, non-primates, tarsiers, and almost all sampled Paleogene primates. The only fossils that group with modern strepsirrhines on PC1 are Adapis, Propotto, and Plesiopithecus. On PC2, strepsirrhines are divided into a cluster of lemurids, indriids, lorisiforms, and Adapis with high values, and another including cheirogaleids (Microcebus, Cheirogaleus, Mirza, Phaner), Daubentonia, Plesiopithecus, and Propotto with low values. The pteropodid fruit bats Pteropus and Rousettus are well-separated from Propotto in having much higher PC1-2 scores, although they do overlap with the second group of strepsirrhines. Although we only plot PC1 (20% of variance) and PC2 (14% of variance) in Fig. 3, the most important clustering patterns are maintained on PC3 and PC4, as well (Supplementary Data 1–3).

Fig. 3 First two principal components (PC) resulting from principal component analysis of 1100 pseudolandmarks on a broad taxonomic sample of second lower molar teeth. Each point represents the tooth of one individual. Convex hulls and different colors indicate distinct extant taxonomic groups. Gray hulls with different marker symbols represent different fossil taxa. This sample includes teeth of extant non-primate treeshrews (Ptl: Ptilocercus, Tp: Tupaia sp.), cynocephalid dermopterans (Cn), and pteropodid fruit bats (Ptp). It also includes fossil non-primates and possible stem primates including Leptacodon sp. (Lp), various plesiadapiforms (Pls), and Altanius (Alt). It includes a number of extant primates including strepsirrhine lemurids (Lm), indriids (Id), cheirogaleids (ch), lorisids (Ld), and galagids (Gg), as well as Daubentonia madagascariensis. The extant haplorhine Tarsius is also included (Ts). Fossil haplorhines include Eosimias (Es) and Phenacopithecus (Ph). Early fossil prosimians include Donrussellia sp. (Dr), Cantius torresi (Ct), and Teilhardina sp. (Th). See Supplementary Data 1 for a list of all specimens included. See Supplementary Data 2 and 3 for principal component scores of additional components (e.g., 3–4), which also support the groupings of PC1–2 Full size image

In addition, digital reconstruction of the damaged upper molars of Plesiopithecus (Fig. 4a) reveals similarities with two upper molars from Chamtwara that were previously identified as “Lorisidae indet.” by Harrison23 (Fig. 4b). Manipulation of digital surfaces of these upper molars allowed us to confirm that they occlude perfectly with Propotto lower molars from Chamtwara (Fig. 1e, f), and they are accordingly identified here as the first known upper teeth of Propotto. The morphology of these upper molars also resembles that of the possible stem lorisiform Karanisia from the earliest late Eocene of Egypt (Fig. 4d)10, the stem strepsirrhine Djebelemur from the early or middle Eocene of Tunisia28, and, intriguingly, the enigmatic late Eocene primate Nosmips from Egypt, which has been placed with Plesiopithecus in some phylogenetic analyses20. Among extant primates, Propotto’s upper molars (particularly M1) are most similar to those of the dwarf lemur Cheirogaleus. Similarities to Djebelemur, Karanisia, Nosmips, and Plesiopithecus include the broad lingual and more restricted buccal cingula, absence of a metaconule, and a concave distal margin of M2. Although some of these features may be primitive within Strepsirrhini, this character suite is nevertheless clearly characteristic of early strepsirrhines, and is not found in any living or extinct chiropteran. The upper molars of Propotto differ from those of known Paleogene strepsirrhines in being very low-crowned (matching the pattern seen in the lower molars), and in exhibiting a massive lingual cingulum, flattened lingual surfaces of the buccal cusps, and a reduced protocone.

Fig. 4 Upper molars of early African strepsirrhines and extant Daubentonia from Madagascar. a Left M1 (on right) and M2 (on left) of DPC 12393, partial cranium of Plesiopithecus teras (latest Eocene, Quarry L-41, Fayum Depression, Egypt); reversed for comparison, the M1 is badly damaged and has been digitally reconstructed by segmenting out multiple fragments and repositioning them, while the M2 is lacking much of the buccal margin; b isolated right M1 [KNM-CA 1796, on right] and M2 [KNM-CA 1797, on left] of Propotto leakeyi (early Miocene, Chamtwara, western Kenya); c right M1 (on right) and M2 (on left) of AMNH M-41334, adult Daubentonia madagascariensis individual from Madagascar, locality unknown; d right M1 [on right, DPC 21639C] and M2 [on left, DPC 21636E] of Karanisia clarki (earliest late Eocene, Quarry BQ-2, Fayum Depression, Egypt); e oblique mesial view of DPC 21639C, right M1 of earliest late Eocene Karanisia clarki, showing the tall primary cusps, low parastyle, low lingual cingulum, and paraconule typical of early strepsirrhines; f oblique mesial view of KNM-CA 1796, right M1 of Propotto leakeyi, showing the low primary cusps, relatively tall parastyle, tall lingual cingulum, and absence of paraconule that is characteristic of this species. Scale is equal to 1 mm. Digital models were created using CT scans made available by the Duke Lemur Center Division of Fossil Primates and the National Museums of Kenya, which were downloaded from www.morphosource.org and made available for reuse under a CC BY-NC license Full size image

The anterior dentition of Plesiopithecus

The holotype of Plesiopithecus teras (CGM 42291; CGM = Egyptian Geological Museum) preserves a single enlarged and procumbent tooth mesial to P 2 -M 3 . A different mandibular specimen, DPC 11636 (DPC = Duke Lemur Center Division of Fossil Primates), was figured and discussed by Simons and Rasmussen13 (their Fig. 3) and preserves a small tooth (which the authors interpreted as a P 1 ) between the enlarged anterior tooth and the P 2 . They did note, however, that the tooth “might also be the lateral canine derived from a toothcomb” (p. 9949). At some point after the description of this specimen in 1994, the crown of the tooth was broken and glued back onto the root, although rotated into an incorrect orientation. We have reconstructed the tooth using digital models and provide additional views of the specimen for the first time (Figs. 2c and 5). The tooth differs markedly in morphology and orientation from the adjacent P 2 , and has several features that are more consistent with it being a vestigial canine. The evolution of Daubentonia’s rodent-like incisor morphology from a toothcombed ancestor would likely involve topographically shifting the canine out of the toothcomb to accommodate an enlarged incisor. Indeed, in Plesiopithecus, this canine is strongly procumbent relative to its root, has a flattened surface (corresponding to the mesial face of a typical toothcomb canine, but more appropriately described as topographically lingual in DPC 11636) demarcated by a distinct ridge from the surface best exposed in occlusal view (lingual in a typical toothcomb canine, better described as topographically distal in Plesiopithecus), which has a gently curving and apically convex buccal margin. Morphological evidence supporting identification of this tooth as a lower canine rather than as a first premolar is supplemented by the dental formulae of all known living and extinct crown strepsirrhines, which unequivocally indicates that the loss of the upper and lower first premolar occurred along that clade’s stem lineage, and therefore before the appearance of both the strepsirrhine crown group and the split between the chiromyiform and lemuriform lineages. Indeed, no African strepsirrhine, living or extinct, is known to retain a P 1 . In light of this, it is more parsimonious to interpret this tooth of Plesiopithecus as a reduced lower canine, requiring the enlarged anterior tooth of Plesiopithecus to be an incisor, and therefore more likely homologous with the anterior tooth of Daubentonia. This enlarged anterior tooth also shows some thinning of the lingual enamel (relative to that on the buccal surface), though not to the extent seen in Daubentonia. The Plesiopithecus mandible DPC 13607 has also been digitally reconstructed, revealing a tiny canine alvelous anterior to the P 2 (Fig. 1j); therefore the holotype is unlike the two other known specimens in lacking a canine.

Fig. 5 Comparative morphology of the lower dentition in crown strepsirrhines in phylogenetic context. From top to bottom, Galago senegalensis (MCZ 34381), Eulemur fulvus rufus (MCZ 16356), Microcebus (MCZ 45125), composite mandible of Plesiopithecus teras (DPC 11636; right side mirror-imaged), and Daubentonia madagascariensis (composite mandible using the corpus and incisor of AMNH M-185643 and the M 1–3 of AMNH M-41334). Digital models were created using CT scans made available by the Museum of Comparative Zoology and Harvard University, the American Museum of Natural History, and the Duke Lemur Center Division of Fossil Primates, which were downloaded from www.morphosource.org and made available for reuse under a CC BY-NC license Full size image

Phylogenetic placement of Propotto and Plesiopithecus

Phylogenetic analysis (see Methods) of our combined molecular and morphological data matrix using the Bayesian tip-dating method with fossilized-birth-death parameterization recovered Propotto as exclusively related to Daubentonia, and Plesiopithecus as the sister taxon to this Daubentonia-Propotto clade (Fig. 6). Standard Bayesian (“non-clock”) analysis recovered an exclusive Propotto-Plesiopithecus clade that is sister to Daubentonia. In both analyses, Propotto and Plesiopithecus are strongly supported as crown lemurs (posterior probability = 0.9) and are situated as stem chiromyiforms. Importantly, this result emerged despite controlling for two scoring biases that could have provided additional support for a Daubentonia-Plesiopithecus-Propotto clade. First, though there are sound reasons to consider Propotto’s enlarged anterior lower tooth to be homologous with that of Plesiopithecus, Propotto was conservatively not scored for either canine or incisor characters (i.e., only premolar and molar characters were scored). Second, Plesiopithecus’ enlarged anterior upper teeth were scored as canines and not incisors, although they could conceivably be enlarged incisors homologous with those of Daubentonia. To further avoid bias, we did not create any new characters or character states to capture novel observations of derived dental features shared by Daubentonia and Propotto to the exclusion of Plesiopithecus (see discussion below).

Fig. 6 Phylogenetic relationships and biogeography of living and extinct strepsirrhines. Time-scaled tree derived from Bayesian tip-dating analysis of the combined molecular and morphological dataset. Terminal branches are color coded according to continental biogeography, and internal branches are color coded according to Bayesian ancestral biogeographic analysis. Numerical values to the right of nodes represent clade support (posterior probabilities) and circled numbers at each strepsirrhine node represent the posterior probability of each biogeographic reconstruction. Complete time-scaled phylogenetic trees and biogeographic reconstructions are available at the Dryad Digital Repository associated with this study (https://doi.org/10.5061/dryad.gb182) Full size image

Bayesian stepping-stone estimation of marginal likelihoods for alternative placements of Plesiopithecus and Propotto, using the morphology matrix and constraining these two taxa to fall in different positions within the optimal time-scaled tree derived from the tip-dating analysis of molecular and morphological data, reveals that there is “strong” evidence (based on a Bayes factor of 15.64) for favoring a (Plesiopithecus (Daubentonia, Propotto)) topology over the (Daubentonia (Plesiopithecus, Propotto)) topology derived from the non-clock analysis. Other alternative constraints, such as situating Plesiopithecus and Propotto as advanced stem strepsirrhines or as stem lemurs, were decisively rejected by stepping-stone analyses (based on Bayes factors of 572.49 and 651.97, respectively). Bayesian reconstruction of ancestral morphological character states on the optimal clock topology identified 15 character state changes along the chiromyiform stem leading to the (Plesiopithecus (Daubentonia, Propotto)) clade, and 18 character state changes along the lineage leading to the Daubentonia-Propotto clade. The monophyly of Eocene-Recent chiromyiforms is supported by character changes relating to the modification of the anterior dentition to include only a single enlarged and procumbent incisor, as well as numerous details of premolar and molar crest and cusp development/placement, and increased depth of the mandibular corpus (see supporting data files held in the Dryad Digital Repository associated with this study (https://doi.org/10.5061/dryad.gb182)).

Biogeographic history of lemurs

Bayesian reconstruction of strepsirrhine biogeographic history strongly supports (posterior probability = 1) African origins for both Chiromyiformes and Lemuriformes, implying independent dispersals across the Mozambique Channel. Our analyses place the last common ancestor of Daubentonia and Propotto on the African continent at 27.9 Ma (near the early-late Oligocene boundary), suggesting that the dispersal to Madagascar that ultimately gave rise to Daubentonia likely occurred some time after the early Oligocene. The continental divergence of the chiromyiform and lemuriform lineages is estimated at 41.1 Ma (late middle Eocene) and the island origin of crown lemuriforms is estimated at 19.9 Ma (early Miocene).