Reassessment of the previous evaluations: modern or primitive?
Previous studies have proposed several potentially taxonomically diagnostic dental characteristics of H. floresiensis. These are summarized and discussed below.
I2/C diastema is frequently observed in Au. afarensis but is rare in Au. africanus, Paranthropus, and Homo (White et al., 1981; Kimbel and Delezene, 2009). Brown et al. (2004) described that, in LB1, “(s)ize, spacing and angulation of the maxillary incisor alveoli, and absence of a mesial facet on the canines suggest that incisor I2 was much smaller than I1, and there may have been a diastema.” This inference is not supported by our CT scan, which shows close proximity between the I2 and C1 alveoli (Figure 5a).
Brown and Maeda (2009) reported that the mandibular canine size of LB1 and LB6/1 is ‘small’ like various other groups of post-1.7 Ma Homo, whereas those of earlier Homo and Australopithecus were either ‘variable,’ ‘medium,’ or ‘large’ (their Table 3). We here metrically reexamine this claim. Table 2 compares ‘relative canine size’ among various archaic Homo groups and a global sample of modern humans (H. sapiens). The ‘relative canine size’ is defined as dimensional proportion of C1 (LL diameter) relative to the premolar and molar lengths (additive MD diameters for P3 −M2 or P3 + M1 + M2). The available small fossil sample indicates that relative canine size tends to be smaller in H. habilis than in later Homo, contrary to the claim of Brown and Maeda (2009). The values for the two H. floresiensis individuals are within the upper range of the variation for H. habilis, and are also well within the variations exhibited by the later archaic and recent Homo groups. Therefore, relative canine size is of limited use to assess the taxonomic affinities of H. floresiensis.
Dimensional proportion of the mandibular canine and first premolar relative to the postcanine tooth row (%)a
||P3 + P4 + M1 + M2 (MD)
||P3 + M1 + M2 (MD)
||P3 + P4 + M1 + M2 (MD)
||P3 + M1 + M2 (MD)|
|H. habilis (East Africa, 2.0–1.6 Ma)|
| KNM-ER 1802
| KNM-ER 60000
| OH 7
| OH 13
| OH 16
|H. habilis (mean)
|Dmanisi Homo (Georgia, 1.75 Ma)|
|H. ergaster (East Africa, 1.5–1.0 Ma)|
| KNM-ER 992
| KNM-WT 15000
| OH 22
|Early Javanese H. erectus (Sangiran, >1.0 Ma)|
| Sangiran 22
|European terminal Early Pleistocene Homo (Gran Drina, 0.8 Ma)|
| ATD H1
| ATD 6-96
|African early Middle Pleistocene Homo (Tighenif and Baringo, 0.8–0.5 Ma)|
| Tighenif 1
| Tighenif 2
| Tighenif 3
| KNM-BK 8518
|Chinese Middle Pleistocene H. erectus (Zhoukoudian, 0.75 Ma)|
| Zhoukoudian B1
| Zhoukoudian G1
| Zhoukoudian K1
|Post-habilis archaic Homo (mean)
|H. sapiens (mean)
| (N: range)
a Measurements for the comparative fossil sample were taken by Y.K. based on high-quality casts produced from the original specimens by Y.K. or Gen Suwa except for KNM-ER 60000 (Leakey et al., 2012
), Dmanisi (Martinón-Torres et al., 2008
), KNM-WT 15000 (Brown and Walker, 1993
), Gran Drina (Bermúdez de Castro et al., 1999
; Carbonell et al., 2005
), Tighenif (Bermúdez de Castro et al., 2007
), and Zhoukoudian (Weidenreich, 1937
). The H. sapiens
is a global sample from Asia, Oceania, Europe, and Africa, and is based on high-quality casts prepared by Y.K.
The P4s of LB1 are bilaterally rotated parallel to the tooth row. This was cited as a unique trait (Brown et al., 2004) or indicative of some developmental abnormality (Hershkovitz et al., 2007) and/or affinity with local, living ‘pygmy’ groups of Flores (Jacob et al., 2006). However, tooth rotation is a relatively commonly observed dental anomaly both in modern (Jacob et al., 2006; Lukacs et al., 2006) and pre-modern (e.g. Early Pleistocene Homo from Dmanisi (Rightmire et al., 2006) and Konso (Suwa et al., 2007)) hominins as well as other mammals (Natsume et al., 2006), with suggested etiologies including some genetic mechanism and a lack of space for the normal tooth eruption (Baccetti, 1998; Natsume et al., 2006). Therefore this trait is not taxonomically diagnostic and does not necessarily indicate a severe growth abnormality.
The P3s of H. floresiensis are unique and were a focus of attention in previous studies (Brown et al., 2004; Brown and Maeda, 2009). A previous claim that (some of) these are deciduous first molars (Obendorf et al., 2008) has been effectively rejected by Brown (2012) based on crown and root morphology as well as the state of wear. Brown and Maeda (2009) suggested that its MD elongated, asymmetric crown shape represents a (very) primitive hominin condition, which changes to a more derived, molarized, bicuspid, and symmetrical P3 in later australopiths and early members of Homo. According to these authors, the P3 crown morphology of H. floresiensis is also similar to ~1.75 Ma Homo from Dmanisi (Martinón-Torres et al., 2008), but metrically distinguishable from H. erects (sensu lato) and H. sapiens (their Figure 12). Jacob et al. (2006) claimed that the “enlarged, block-like” P3 similar to the condition in LB1 are observed worldwide in H. sapiens, although no numerical data were provided to support their view.
In Figure 8, we compare our revised P3 crown diameters of H. floresiensis with those of a global H. sapiens sample as well as the Early Pleistocene Homo specimens from East Africa (H. habilis and H. ergaster), Caucasus (Dmanisi Homo), and Java (early Javanese H. erectus from the lower and upper stratigraphic levels of Sangiran). In this chart, the P3s from three H. floresiensis individuals are situated at the margin of the large cloud of H. sapiens due to the formers’ relatively larger MD diameters. MD elongated P3 crown configurations are frequently observed in H. habilis and Dmanisi Homo, and represent a primitive state for Homo (Wood and Uytterschaut, 1988; Tobias, 1991; Brown and Maeda, 2009). However, contrary to Brown and Maeda (2009), this crown shape is not restricted to H. habilis and Dmanisi Homo but is also seen in an East Africa specimen dated to 0.8–1.2 Ma (OH 22: Rightmire, 1980; Antón, 2003). Therefore, H. floresiensis exhibits a primitive, MD elongated P3 crown shape shared with H. habilis, but such crown morphology does exist, albeit in small numbers, in later Homo groups.
Scatter plot of P3 MD and BL crown diameters (mm). The fossil comparative specimens included are as follows: H. habilis sensu lato: Omo 29-43, Omo 75-14, KNM-ER 1802, KNM-ER 60000 (Leakey et al., 2012); OH 6, OH 7, OH 13, OH 16, OH 68 (Clarke, 2012); H. ergaster: KNM-ER 992, KNM-ER 1814, KNM-ER 1808, KNM-WT 15000; Dmanisi Homo: D211, D2735, D2600 (Martinón-Torres et al., 2008); Sangiran Lower: S 6a, S 9, S 22; Sangiran Upper: S 7-25. Measurements for the above fossil specimens were taken by Y.K. based on high-quality plaster casts produced from the original specimens by Y.K. or Gen Suwa, or from the literature. The H. sapiens is a global sample from Asia, Oceania, Europe, and Africa, and is based on high-quality plaster casts prepared by Y.K (n = 208).
P3 of H. floresiensis has a transverse crest that is oriented distolingually, and, at its end, has a small lingual cusp that is situated near the crown’s distolingual corner. A similar crest and cusp arrangement, which contributes to reduce the talonid, is found in D2735 from Dmanisi (Martinón-Torres et al., 2008) and a few post-habilis African Homo P3s (KNM-ER 992, KNM-WT 15000 (left), OH 22). Although a distally oriented transverse crest is a plesiomorphic hominin condition seen in great apes, Ardipithecus ramidus, and Australopithecus anamensis (Ward et al., 2001, 2013; Suwa et al., 2009; Delezene and Kimbel, 2011), the P3s of Au. afarensis and H. habilis have altered so that the transverse crest tends to form an acute angle with the mesial protoconid ridge and the lingual cusp is placed slightly mesial or opposite to the buccal cusp (Suwa, 1990; Suwa et al., 1996; Delezene and Kimbel, 2011). Thus, the distal location of lingual cusp in some post-habilis Homo as well as H. floresiensis P3s is a secondary acquisition of the primitive pattern that is derived compared to H. habilis. In support of this view, these Pleistocene Homo P3s also lack other plesiomorphic features present in early Pliocene hominins such as an obliquely elongated crown shape (strong mesiobuccal protrusion of the buccal face) and sharp occlusal crests (Suwa et al., 1996; Delezene and Kimbel, 2011). Although the transverse crests of the H. floresiensis P3s have lost their edges by wear, the unworn portions clearly show that these crests have thick bases.
The H. floresiensis P3s are, however, unique, showing the beveled, generally flat but wrinkled mesiolingual occlusal surface as described above. This feature is associated with a low, mesially restricted Mmr. It is different to the ‘open’ anterior fovea frequently seen in Australopithecus as well as archaic and modern Homo P3s, where a distinctly elevated Mmr is deeply incised by a furrow emanating from the pit-like anterior fovea, and is not associated with fine enamel wrinkling (e.g., Johanson et al., 1982; Tobias, 1991; Grine and Franzen, 1994). In Table 2, we compare MD dimensional proportions of P3 within the postcanine tooth row, i.e. P3/(P3 −M2) or P3/(P3 + M1 + M2). This comparison indicates that the relative P3 lengths tend to be smaller in H. sapiens, moderately large in the Early–Middle Pleistocene Homo particularly in post-habilis Homo taxa, and extremely large in H. floresiensis. The metric data reported by Wolpoff (1971) also show that P3/M1 size ratio is higher in H. erectus and Neanderthals than in H. sapiens.
To summarize, H. floresiensis P3 exhibits a primitive crown shape but is derived from H. habilis in cuspal arragement, and is unique in its relatively large size and the beveled and wrinkled mesiolingual crown.
Mandibular premolar root
Brown and Maeda (2009) emphasized that the bifurcated or Tomes’ mandibular premolar root forms seen in H. floresiensis are rare in H. sapiens (Shields, 2005). We agree that the roots of these (and anterior) teeth of H. floresiensis are robust and primitive, although we found that the P4 roots of LB1 and LB6/1 are not bifurcated but should be described as Tomes’ form with a mesiobuccal cleft (see above).
Brown and Maeda (2009) suggested that such ‘complex’ root forms are more frequently observed in Australopithecus and East African early Homo than in Sangiran H. erectus (their Table 3). This is incorrect. Observed frequencies of double-rooted mandibular premolars do not significantly differ between H. habilis (4/13 (P3) and 5/10 (P4)) (Suwa, 1990; Tobias, 1991; Wood, 1991; Leakey et al., 2012) and the older Sangiran H. erectus (3/6 (P3) and 4/6 (P4)) (Kaifu et al., 2005b). Single-rooted mandibular premolars do exist in H. habilis (e.g. KNM-ER 1483, 1501; OH37: Wood, 1991), and non-double-rooted P3s from Sangiran include Tomes’ root form (S 6a, S 22: Weidenreich, 1945; Kaifu et al., 2005a). Thus, the available limited information about mandibular premolar root form is not very useful to discuss the evolutionary origin of H. floresiensis. More detailed morphometric analyses are needed to investigate detailed evolutionary changes in root morphology of the Pleistocene Homo (e.g. Kupczik and Hublin, 2010; Emonet et al., 2012; Le Cabec et al., 2013).
Molar crown shape
Jacob et al. (2006) listed the following molar traits of LB1 as evidence to link this individual with a modern ‘pygmy population’ from Flores: (1) a tendency for the longitudinal fissure to shift away from the buccolingual axis on mandibular molars, (2) rhomboid outlines of upper molars reflecting hypocone reduction, and (3) squared lower molar outlines related to hypoconulid loss.
The meaning of the first point is not clear to us. In our observation, the longitudinal fissures of LB1 and LB6/1 are remarkable in that their distal segments are shifted extremely lingually. This trait is more frequently found in the Early Pleistocene Homo than in H. sapiens, although this observation needs to be verified metrically in future studies. We will numerically examine the second and third points elsewhere, but we here note that it is metacone, not hypocone, that shows marked reduction on the M1 and M2 of LB1. We confirmed that the mandibular molars of the two H. floresiensis individuals are four-cusped teeth with no hypoconulid. Four-cusped M1s and M2s have been unknown among H. erectus assemblages from Indonesia and China (Martinón-Torres et al., 2007). This morphology is also rare among the Middle–Late Pleistocene European archaic Homo (Martinón-Torres et al., 2012). However, Zanolli (2013) recently reported four four-cusped M2s that may have been derived from the terminal Early Pleistocene Bapang (Kabuh) Formation in the Sangiran Dome, Central Java (chronology based on Hyodo et al., 2011). Four-cusped M2s are relatively common in modern human populations (24%), but four-cusped M1s are rare (1%) (calculated from the data based on a large global modern human sample (n = 6790–8638) in Scott and Turner, 1997: Appendix A). Therefore, the condition in H. floresiensis (both of the existing two individuals have four-cusped M1 and M2) is not a typical observation even for H. sapiens. In consideration of a report that the loss of hypoconulid is correlated with the reduction in mandibular molar size in H. sapiens (Scott and Turner, 1997), it is possible that H. floresiensis independently lost the hypoconulid in association with the reduction of their mandibular molars.
Molar size sequence
During the course of the Homo evolution, the posterior molars experienced more marked size reduction than in the first molar, resulted in alteration of the molar size sequence within a dentition, from plesiomorphic ‘M1 < M2 ≥ M3’ to ‘M1 > M2 > M3’ (Wolpoff, 1971; Bermúdez de Castro and Nicolás, 1995; Kaifu et al., 2005b; Kaifu, 2006). The maxillary and mandibular molar size in H. floresiensis decreases posteriorly (M1 ≥ M2 > M3). This is a derived character seen in post-habilis grade Homo (Brown et al., 2004).
Mandibular dental arcade shape
Dental arcade shape, which became wider during hominin evolution, is a useful character for taxonomic purposes (Rosas and Bermudez de Castro, 1998; Kaifu et al., 2005b; Spoor et al., 2015; Villmoare et al., 2015). Brown and Maeda (2009) suggested that the narrow dental arcades seen in the LB1 and LB6/1 mandibles are shared with pre-1.7 Ma Homo and Australopithecus but not present or very uncommon in Asian H. erectus or later Homo. This view has been disproved by a later metric reinvestigation, which showed that their arcades are actually wider than seen in H. habilis or Dmanisi Homo, and are similar to early H. erectus from Java (Kaifu et al., 2011).