Ardipithecus challenge explication: the canine-premolar complex

Writing about the Sarmiento-White exchange (Sarmiento 2010; White et al., 2010) a couple of weeks ago, I mentioned that I had three areas of comment. The molecular clock argument was the first, the pelvis the second. My trip to Europe got in the way of finishing up these notes, but after the molecular clock and the pelvis, I’ve come to the third area – the canine-promolar complex.

Here is Sarmiento’s exposition:

Fourteen of the 26 characters in table 1 in (1) common to Ardipithecus and Australopithecus are in the canine/premolar complex. However, reliance on the canine/premolar complex to diagnose hominids (in the classic sense) has misdiagnosed Miocene fossil apes (i.e., Oreopithecus and Ramapithecus) as early human ancestors (12, 13). Character polarity for this complex is not clear-cut, with many early hominoids, especially females, often showing a humanlike condition. The canine/premolar complex shows such a marked grade of character lability (e.g., conspecific males and females show the diagnostic character differences) that reversals in polarity could have occurred repeatedly over the evolutionary periods necessary for these fossil genera to differentiate (12). Approximation to the humanlike canine/premolar complex, therefore, does not indicate that Ardipithecus is a hominid or ancestral to Australopithecus any more than it indicates that Oreopithecus and the orangutan-like females of Sivapithecus, both of which also share a humanlike premolar/canine complex, are hominids or represent a descendant-ancestor continuum.

Sarmiento here accepts that the C/P3 complex of Ardipithecus “approximates” the hominin condition. I would not go so far as this. I faced a big difficulty in understanding the description of the dentition by Suwa and colleagues (2009). As I pointed out last fall, they did not report standard measurements. Those have been hidden from everyone. Moreover, most of the metric comparisons presented graphically in the paper and its supplement are non-standard ratios.

Such comparisons have many disadvantages. Many lack any clear biological meaning (for example, why take the ratio of lower P3 height to M1 length?). Why use the maximum diameter of the P3 without any reference to the angle of the tooth relative to the mesiodistal axis?

A few things are clear from the description and photos of upper canines and lower third premolars in figure S14 of Suwa et al. (2009). Many of the Ardipithecus upper canines are worn on the tip, and some of them are worn extensively. None of them have “honing” wear, which means wear that enhances the cutting function of their distal edges. The upper canines of Ardipithecus are like male bonobos in their crown diameter and intermediate between male and female bonobos in their labial height. There are some similarly large canines in Australopithecus afarensis, although the average in that species is significantly lower in crown diameter.

Australopithecus afarensis has a range of P3 forms. Some are more apelike, asymmetrical crowns dominated by a single buccal cusp and angled relative to the mesiodistal axis. Others are more humanlike, with two more or less equal cusps and perpendicular to the mesiodistal axis. In Au. afarensis, the more apelike The Ardipithecus range of variation apparently never included any like these latter, humanlike P3s from Au. afarensis. The P3s of Ardipithecus also had substantially greater crown heights than typical of Australopithecus. The Ardipithecus P3 is hominin-like in only two senses: It is smaller than the chimpanzee equivalent, and never has a facet for honing wear on the upper canine. This may be why Suwa and colleagues (2009) and White and colleagues (2010) referred to the “C/P3 complex” instead of simply the P3. It may also explain why the research paper by Suwa and colleagues (2009) did not illustrate any comparative statistics of the P3. The fact is that the P3 of Ardipithecus is by itself apelike.

White and colleagues respond to Sarmiento’s points as follows:

The greatly expanded Ar. ramidus dental sample now further obviates Sarmientos assertions by establishing a metrically and morphologically refined Ar. kadabba-Ar. ramidus-Au. anamensis-Au. afarensis morphocline (57). It now seems clear that not all recovered Ar. ramidus canines can be female (7). Feminization of the male Ardipithecus C/P3 complex is robustly documented [detailed in the supporting online material in (7)]...

Wait a minute! “Robustly documented?!” There are no measurements!

...and is incompatible with Sarmientos argument that Ar. ramidus represents the stem taxon for both African apes and humans (1). If that were the case, a hominid-like C/P3 complex with lack of honing would need to have evolved in Ar. ramidus, only to have independently reverted to the honing complexes in each African ape clade.

White and colleagues here link two assertions. First, they assert that the C/P3 complex in Ardipithecus is actually like later hominins. On that assertion, the facts listed above are the pertinent ones. There are dental similarities, many of which are also shared with one or more lineages of Miocene apes. As Sarmiento claims, these similarities are arguably “shallow” – mostly they reflect the fact that Ardipithecus has smaller canines than chimpanzees.

Second, White and colleagues assert that the canine morphology of chimpanzees and gorillas is unlikely to represent an evolutionary reversal. This second assertion is taken up later in the comment:

The character distributions we noted in the pelvis, C/P3 complex, and basicranium are consistently indicative of a sister relationship of Ar. ramidus with Australopithecus (and later hominids). For Ar. ramidus to be a stem species of the African ape and human clade as Sarmiento advocates, its highly derived C/P3 complex morphology, basicranial shortening, and iliac structure must have first emerged in some yet-unidentified Miocene ancestor before then reverting to an African apelike condition. Such multiple, nonparsimonious character reversals are highly unlikely.

Shouldn’t a sympathetic editor would have stopped them from including this passage? Lovejoy and colleagues’ “Great Divides” paper (2009), in the special issue of Science, was completely devoted to the argument that chimpanzees and gorillas derived most of their locomotor adaptations in parallel to each other. That includes a series of postcranial derived features ranging from the lumbar spine, wrist, hand and foot, limb proportions and the pelvis. No matter what we may think of Ardipithecus, the dentitions of chimpanzees and gorillas also evince substantial parallelism in enamel and crown morphology.

True or not, none of that is parsimonious.

I don’t see any reason why the C/P3 complex should be special evidence of relationship. Lovejoy and colleagues (2009) had given some attention to the idea that morphological characters might be genetically correlated through changes to toolkit genes. For no system is such genetic correlation as likely as for the dentition. The serial homology among neighboring teeth reflects the action of precisely the same genes in different segments established early in dental development. Moreover, unlike the case of digits and limbs, the teeth may mechanically affect each other’s development because they are adjacent to each other. That means that neither morphological reduction of the canines nor any change in their eruption schedule can be isolated from changes in the premolars.

Is it any surprise that the reduction of upper canines should result in a lack of honing wear on lower premolars? Honing is a consequence of a direct mechanical connection that becomes impossible with sufficient reduction of the canine.

Can we isolate a slight reduction in the lower third premolars from the significant reduction in the lower canines? As Suwa and colleagues (2009:95) point out, this lower canine evolution is not limited to hominins but also occurred in parallel in bonobos and some Miocene lineages:

A hominid-like incisiform LC morphology (high mesial shoulder, developed distal crest terminating at a distinct distal tubercle) is seen in some female apes (e.g., Ouranopithecus and P. paniscus), whereas the LCs of Ar. kadabba and Ar. ramidus tend to be conservative, exhibiting a strong distolingual ridge and faint distal crest, typical of the interlocking ape C/P3 complex (4) (Fig. 1 and SOM text S1).

I just don’t think that the Miocene ape record can sustain the argument that the C/P3 “complex” carries much phylogenetic weight. A bonobo-sized canine is never going to be strong evidence linking a fossil to the hominins. That’s part of why Ardipithecus remains such a doubtful case.

References

Lovejoy, C. O., Suwa, G., Simpson, S. W., Matternes, J. H., & White, T. D. (2009). The great divides: Ardipithecus ramidus reveals the postcrania of our last common ancestors with African apes. Science, 326(5949), 73-106.

Suwa, G., Kono, R. T., Simpson, S. W., Asfaw, B., Lovejoy, C. O., & White, T. D. (2009). Paleobiological implications of the Ardipithecus ramidus dentition. science, 326(5949), 69-99.

Sarmiento, E. E. (2010). Comment on the paleobiology and classification of Ardipithecus ramidus. Science, 328(5982), 1105-1105.

White TD, Suwa G, Lovejoy CO. 2010. Response to Comment on the paleobiology and classification of Ardipithecus ramidus. Science 328:1105. doi:10.1126/science.1185462