Australia: The Land Where Time Began
Archaic Hominin from East Asia – First systematic Assessment of Dental Growth and Development
Several human dental traits that are typical of modern humans appear to be associated with the prolonged developmental period that is a key human attribute. Therefore there is strong interest in gaining an understanding of when, and which hominins, made their first appearance. Xing et al. used x-ray multiresolution synchrotron phase contrast microtomography to quantify dental growth and development in a juvenile of an archaic Homo that was recovered from the Xujiayao site, Northern China that was dated to 161,000 - 224,000 BP or 104,000-125,000 BP. Most aspects of the dental development of this archaic juvenile are within the range of modern humans (e.g., prolonged crown formation time and delayed eruption of the first molars), in spite of the archaic morphology of the Xujiayao hominins. The state of dental development of this juvenile archaic hominin, which at the time of death was 6.5 years, has been estimated to be that of modern children of equivalent age. These findings suggest that several factors of dental growth and development of modern humans evolved in East Asia prior to the presence of anatomically modern humans.
Humans are uniquely derived among extant primates in the prolonged period over which their physiological systems grow and develop (Bogin, 1997). It is possible to assess, through actual or virtual histology (synchrotron microtomography), with high precision, the growth and development of 1 physiological system in fossils: the dentition (Dean et al., 2001; Smith et al., 2007). Daily (short-period), as well as long period growth lines, in their hard tissues, which can be imaged nondestructively in fossil teeth that can preserve them, with synchrotron microtomography (Smith et al., (P. 20220-20225) 2007; Smith et al. (p. 6128-6133), 2007; Smith et al, 2010; Smit et al., 2015), can be preserved in fossil teeth (Smith et al., (P. 20220-20225) 2007; Smith et al. (p. 6128-6133), 2007; Smith et al, 2010; Smith et al., 2015). A recent study that used this method has shown that Australopithecus and Paranthropus species were more variable in their rate of development than had been realised previously (Smith et al., 2015), though none appear to evince the prolonged periods of dental growth and development that characterise modern humans (Dean et al., 2001; Bromage & dean, 1985).
However, according to Gao et al. the ages at which early Homo reached dental developmental stages appear to be encompassed within the range of variation of modern humans, though they generally are at the advanced end of that range (dean & Liversidge, 2015). A recent study of a single specimen suggests that with respect to Neanderthals, they also were encompassed within modern human ranges of dental development (Rosas et al., 2017). It is suggested by other studies that some individual Neanderthal specimens may have been exceptionally advanced compared to modern humans (Smith et al., 2015, P. 20220-20225; Smith et al., 2015, P. 20923-20928-5).
During the Middle to Late Pleistocene diverse hominin forms that overlapped in time with Neanderthals, most of which have been attributed to 1 (or occasionally more than 1) of these taxa/groups: Homo erectus, Homo antecessor, Homo heidelbergensis, archaic Homo, Denisovans, Neanderthals, and anatomically modern humans (AMH) (10). Gao et al. say these new archaic finds from China are complicating our understanding of the evolution of humans during this time period. Very little is known on the dental growth and development of East Asian Homo in this period of time, in spite of the surge in studies of dental development in Middle-Late Pleistocene Homo (Smith et al., 2007, P. 6128-6133; Smith et al., 2010, 20293-20298; Smith et al., 2015; Rosas et al., 2017).
In this paper Gao et al. ask: How similar or different were multiple aspects of dental growth and development of archaic hominins from East Asia from those of contemporary Neanderthals and anatomically modern humans? A first glimpse into a developmental system at a time and place in the evolution of humans that is not well known, is provided by the answer to this question. This question is addressed by this study by the use of propagation phase-contrast x-ray synchrotron microtomography (PPC-SRμCT) and laboratory microtomography (μCT) in order to assess various features of dental growth and development in archaic Homo Xujiayao 1 specimen from China in comparison with other hominins and modern humans.
The Xujiayao site, which is located in the Nihewan Basin in Northern China, produced many hominin and human fossils in the late 1970s (Wu, 1980; Chia, Wei & Li, 1979). A juvenile maxilla and unassociated mature and immature cranial material were included in the hominin remains that were recovered from the upper cultural layers (Chia, Wei & Li, 1979). Several chronometric analyses have been performed, with late Middle Pleistocene (161 – 224 ka or 104 to 125 ka ) (Chen, Yuan & Gao, 1984; Li et al., 2014). Therefore, a minimum age of more than 100 ka can be assumed, though the fossils may date to more than 200 ka. The Xujiayao hominins were identified by a consensus of a series of recent studies as Archaic Homo with a complex mosaic of morphologies, which include characteristics present in H. erectus, modern humans, and Neanderthals (Wu et al., 2014; Xing et al., 2015). Several ancestral features are displayed by the Xujiayao hominins, which include a thick cranial vault and a cranium that is built strongly, As well as robust, large teeth (12.1-15). Included among features that are derived towards a modern human condition include high and rounded temporal squama, simple occlusal and smooth buccal surfaces on the maxillary premolars, and a symmetrical P3 crown outline with a lingual cusp that is strongly reduced (Xing et al., 2015. The bony structure of the labyrinth of Xujiayao 15 temporal falls within the range for Neanderthals and differs from other members of the genus Homo (Wu et al., 2014). It has also been suggested recently, given the size of the crowns and roots of Xujiayao teeth, that they may be Denisovan (Martinόn-Torres et al., 2017).
The following suite of features characterise the dental development of modern humans:
· Slow trajectory of enamel growth,
· Compacted perikymata in the cervical half of the crown,
· Prolonged time of formation of the crown,
· Time delayed achievement of developmental stages, and
· Molar eruptive age relative to other extant primates (Dean et al., 2001; Bromage & dean, 1985; Guatelli-Steinberg & Reid, 2010; Kelly & Schwartz, 2012).
This suite of traits has not been documented as a package in other fossil hominins apart from anatomically modern Homo sapiens (Smith et al., 2007, P. 6128-6133). An in-depth analysis of the dental microstructures, growth rates, and developmental patterns conducted in this study yielded insight into possible similar mosaic patterns in its dental growth and development, and establishing where the dentition of this archaic juvenile falls on the hominin developmental spectrum, given that a mosaic pattern of morphological traits has been described for the Xujiayao individuals.
This study specifically investigates systematically the following aspects of Xujiayao dental development:
i) Long period line periodicity,
ii) Perikymata number and distribution,
iii) Crown formation time,
iv) Initiation time,
v) Root extension time,
vi) Stages of dental development in teeth relative to one another as well as the dental age relative to the dental age at death, and
vii) Estimated age at first molar eruption.
In other recent hominins and in modern humans, these aspects of dental growth and development have been well studied (eg., Smith et al., 2010, P. 20923-20928; Smith et al., 2015; Macchiarelli et al., 2006; Guatelli-Steinberg & Reid, 2010), which has shown different patterns of variation across hominin taxa. Definitions of these variables are given in data file S1.
According to Xing et al., the numbers and distribution of Perikymata vary by tooth type and across taxa of hominin from the Middle to the Late Pleistocene (Guatelli-Steinberg & Reid, 2010). Neanderthals average a smaller percentage of perikymata in the cervical half of their teeth across all tooth types, though the range overlaps with that of modern humans. A description of the number and distribution of perikymata for Xujiayao I1 and C have been published previously (Xing et al., 2015) and was referenced in this analysis. All the permanent teeth of Xujiayao fall within the range of 1 or both of the modern human groups on bivariate plots (Xing et al., 2015). The Xujiayao teeth nearly always fall outside the range of Neanderthals; the exception is P3 and P4, for which Xujiayao falls just with the range of Neanderthals.
Overall, a combination of total perikymata number and the percentage of perikymata in the cervical half of the tooth that is most similar to that of humans (and to modern southern Africans is particular). In living humans the distribution of perikymata appears to be related to changes in rates of enamel extension along the enamel-dentine junction (EDJ) (Guatelli-Steinberg et al., 2012). Xing et al suggest it is possible that the perikymata distribution patterns of individuals of Xujiayao indicates a pattern of extension rate change that is more similar to that of living humans than to that of Neanderthals, though there may be other processes of enamel formation involved (Guatelli-Steinberg et al., 2012).
Crown formation time
Cuspal and lateral enamel formation time must both be known in order to calculate the total crown formation time. Cuspal enamel formation time is calculated by using the Cuspal enamel thickness and it was compared briefly by Xing et al. across hominin groups in this study. It is usual for modern human groups to have thicker enamel than Neanderthals, though it is thinner than hominins from the Pliocene-Pleistocene (Smith et al., 2010, 20923-20928; Smith et al., 2015). Cʹ and M2 tooth types are the only tooth types of all Xujiayao teeth in which the cuspal enamel is thicker than that of Neanderthals. The Xujiayao Cʹ, P3, M1, and M2fall within the range of modern human groups; while the measurements of Cuspal thickness of P4falls above the range of modern humans and closer to that of fossils H. sapiens range. The Xujiayao juvenile has much thicker cuspal enamel (1,359 ± μm) than all other hominins that have been measured to date.
The First molar crown formation time in particular, has been suggested to be related to the pace of life history across primates (Macho, 2001), though this has been debated (Kelly & Schwartz, 2012). Neanderthals took longer, on average, to complete their crowns than do hominins from the Pliocene-Pleistocene, though they complete them in less time than do modern humans. When the ranges reported for modern humans from Southern Africa and Newcastle are combined, the Xujiayao juvenile falls within the combined modern human range for I1 and P3. The Cʹ, P4, M1, and M2 fall slightly above the combined range of recent modern humans.
The initiation times of permanent teeth exhibit a high degree of intra- and intertaxonomic variation, with the exception of M1, which consistently begins mineralisation around the time of birth. In order to explore further taxonomic trends in initiation time more data are required. The Xujiayao I1 initiated at an age of 318 ± 35 days, which is later than all available histological comparisons for modern humans and other hominins, being closest to the 206 days of an early Homo specimen. The canine initiated earlier than I1, which is the most marked result. Among fossil hominins, this is the first documented occurrence of this developmental phenomenon. In modern human samples, however, it has been shown that canines that initiate earlier than I1 do occur (Reid & Guatelli-Steinberg, 2017). The initiation age of other Xujiayao teeth, all fall in or very close to the range for modern humans.
Compared to a specimen of Homo erectus from Sangiran, Indonesia (S7-37; 934 days), the Xujiayao P4 initiated more than 100 days earlier.
Root extension rate
It was shown by Dean & Cole (Dean & Cole, 2013) that the pattern of extension rate change along the root, from the cemento-enamel junction to the root apex, differs distinctly between chimpanzees and modern humans. It is less clear what average root extension rates, as were calculated in this study, may reflect.
The Xujiayao I1 root, which was reconstructed at 6.89 mm, grew at a rate of 11.06 μm/day, which is higher than that of recent modern humans (7.93 μm/day for the first 6 mm and 8.20 μm/day for the first 7.00 mm (Dean & Vesey, 2008). At 9.74 μm/day, the M1 root extended faster than modern human roots of a similar size, for which the average extension rate is 6.28 μm/day [for the mandibular M1; see (Dean, 2007)]. It has been reported that the Sangiran S7-37 maxillary M1 root grew at a rate of 6.5 μm/day for 11.40 mm length (Dean & Liversidge, 2015). For a Neanderthal M1 the average root extension rate is 6.30 μm/day for its 1.3 mm length (Macchiarelli et al., 2006). For Jebel Irhoud 3, a hominin from the late Middle Pleistocene from North Africa, the mandibular M1 has a root that is 13.5 mm long and an extension rate of 9.60 μm/day (Smith et al., 2007, 6128-6133), which is close to the value for the Xujiayao maxillary M1.
Stages in dental development in teeth relative to one another and dental age
Development of anterior teeth relative to posterior teeth has been considered to be an “ape-like” pattern (Smith., 1994). In the relative development of anterior teeth and posterior teeth there has, however, been intraspecific variation. In fossil H. sapiens from Qafzeh, e.g., Qafzeh 10 had a delayed I1 developmental stage (Ri) relative to its M1 (RI/2), while I1 and M1 of Qafzeh 15 developed at a similar pace and approached the stage R3/4 simultaneously (Smith et al., 2010, 20923-20928). The Xujiayao I1 at stage R1/2 and M1 is at stage R3/4. 32,7% of a sample of modern human children with M1 at stage R3/4, 32.7% had I1 at stage R1/2 (dataset shared by H. M. Liversidge), which is similar to what is observed for the Xujiayao juvenile.
When the predicted development age is compared with the calculated age at death for the Xujiayao juvenile, it appears that I1 and P4 formed at a pace that was slightly faster (~1 year difference) than the model value for modern humans. When within-tooth variation is considered, however, [as per Shackelford et al. (Shackelford, Harris & Konigsberg, 2012)], the age at death that had been determined histologically of Xujiayao (6.51 ± 0.13) is included within 2 SDs of the dental age that has been predicted for I1, P4 and M2, as well as for other individual teeth. When the within-tooth as well as the between-tooth variation (the entire dentition) are considered, the age at death of the Xujiayao juvenile is very close to the median dental age that has been estimated from modern human standards and falls within 1 SD of the median attainment age for modern humans. It is indicated by these findings that the dentition of the Xujiayao juvenile does not conform to an accelerated schedule relative to that of modern humans. It is suggested by the large range of dental ages that have been estimated for each individual tooth of the Xujiayao juvenile that there is a need to be cautious when assessing dental age and/or age at death that is based on an isolated tooth verses the entire dentition.
Estimated age at M1 emergence
It has been proposed that the age of emergence of M1 is highly concordant with life history events of great apes and modern humans, such as age of first reproduction and age of weaning (Smith, 1992; Kelly & Schwartz, 2012). The age of eruption of first molars gradually shifted to later ages from Plio-Pleistocene hominins to modern humans, with most of the earlier hominins being more ape-like in the age of emergence of M1 [for Pongo; (Kelly & Schwartz, 2012)] (Plio-Pleistocene hominins and Homo erectus sensu lato) (Dean et al., 2001; Kelly & Schwartz, 2012). The average age of gingival emergence for M1 varies from 5.1 to 7.0 years in modern populations from around the world. The age of emergence of M1 in Neanderthals Krapina 46 (Max B) and Devil’s Tower 1, Gibraltar were estimated to be ~5.5 and ~5.1 years, respectively (Smith et al., 2010, 20923-20928), while the La Chaise Neanderthal M1 was reported to have its gingival emergence age at 6.7 years (Xing et al., 2015). According to the limited data for Neanderthals it may be suggested that their ages of gingival emergence for first molars fall within the variation of age in modern humans.
The juvenile Xujiayao erupted its first molar later than Plio-Pleistocene hominins, Homo erectus lato and comparably to most Neanderthals and modern humans, with an estimated year of age ~6 years for M1 gingival emergence.
The Xujiayao juveniles’ combination of dental growth and developmental features in comparative context
It remains unclear at the present when the various aspects of dental growth and development that characterise anatomically modern humans (AMH) first appeared (Dean et al., 2001; Smith et al., 2010, 20923-20998). Neither early Homo nor Homo erectus sensu lato appear to exhibit the slow maturational mode of dental growth and development of modern humans (Dean et al., 2001; Smith et al., 2015; Dean & Liversidge, 2015), when absolute timing and growth rates (i.e. crown formation time, emergence of the first molar, and the rate of formation of enamel). Relative to Plio-Pleistocene non-Homo hominins Homo erectus sensu lato is shifted more towards the condition seen in modern humans (Dean et al., 2001). It was shown (dean & Liversidge, 2015) that the range of dental development in AMH is wide enough to accommodate early Homo and H. erectus, though these early members of the genus Homo are at the advanced end of the development spectrum of AMH.
Chronological data that were derived from histology and dental development for hominins from the Neanderthal lineage, which includes H. antecessor as well as some European H. heidelbergensis, are available only for Neanderthals themselves (Smith et al., 2007; Smith et al., 2007, 20220-20225; Smith et al., 2010, 20923-20928; Rosas et al., 2017; Macchiarelli, 2006). It is indicated by the microstructures that are revealed by PPC-SRμCT that most of the Neanderthal teeth grow, on average, in shorter periods of time than those of Homo sapiens (3-5). Most Neanderthal individuals appear to lie within the advanced end of the developmental spectrum of humans, with some possibly falling below it (Smith et al., 2010, 20923-20928; Shackelford, Harris & Konigsberg, 2012), though a recent study of the El Sidrόn J1 Neanderthal demonstrates that its stage of dental development is encompassed well within the modern human ranges (Rosas et al., 2017). However the ages of Neanderthal first molar eruption fall within modern human ranges (Smith et al., 2010, 20923-20928; Macchiarelli et al., 2006). It was revealed by comparison of distribution patterns of perikymata among taxa that relative to H. sapiens, hominins in the Neanderthal lineage have a smaller percentage of their perikymata packed into the cervical halves of their crowns (Guatelli-Steinberg & Reid, 2010). The Jebel Irhoud 3 juvenile, a hominin from the late Middle Pleistocene of North Africa, which has been described as having early modern human affinities, was found to have crown formation times that were prolonged as well as developmental stages, and eruption that were comparable to those of modern humans at similar ages, though with rapid rates of root extension (Smith et al., 2007, 6128-6133). Therefore, with the Jebel Irhoud juvenile, which is believed to be an early modern human, dental development and eruption are firmly within modern human ranges.
Most aspects of dental growth and development in the Xujiayao juvenile are also within modern human ranges, with the exception of fast rates of root extension. Xujiayao 1 has prolonged times of crown formation and eruption of the first molar similar to that present in humans. The stage of dental development in Xujiayao is similar to that of modern human children of comparable age. The distribution pattern of perikymata that has a tendency to separate modern humans from Homo and Neanderthals (Guatelli-Steinberg & Reid, 2010; Xing et al., 2015) also groups the Xujiayao juvenile with modern humans. The rates of dental growth and development are generally comfortably within the ranges of modern humans (with the exception of its rapid rate of M1 root extension at late I1 initiation, therefore, though the Xujiayao juvenile has a mosaic of morphological characteristics, and retains a combination of modern and archaic features.
The dentition of Xujiayao represents the earliest appearance in the fossil record of East Asia of dental development that is comparable to that of modern humans. An exceptionally long period of childhood dependency, delayed ages at first reproduction, and a long lifespan, “modern humans live slow and die old”, are characterise modern human life history (Bogin, 1997). Investigations of the evolution of human life history have depended mainly on anatomical information that is retained in the fossil teeth of young juveniles (e.g. Smith et al., 2007, 6128-6133; Smith et al., 2007, 20220-20225; Smith et al., 2010, 20923-20928; Smith et al., 1985). In this context, the similarity of the Xujiayao juvenile to modern humans in its times of crown formation, state of dental development, and estimated age at the time of first eruption may suggest the presence of a slow life history which is comparable to that of modern humans.
Xing, S., et al. (2019). "First systematic assessment of dental growth and development in an archaic hominin (genus, <em>Homo</em>) from East Asia." Science Advances 5(1): eaau0930.
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