Hominin Taxic Diversity
Hominin Taxic Diversity
- Bernard Wood, Bernard WoodIndependent Scholar
- Dandy DohertyDandy DohertyIndependent Scholar
- and Eve BoyleEve BoyleGeorge Washington University
The clade (a.k.a. twig of the Tree of Life) that includes modern humans includes all of the extinct species that are judged, on the basis of their morphology or their genotype, to be more closely related to modern humans than to chimpanzees and bonobos. Taxic diversity with respect to the hominin clade refers to evidence that it included more than one species at any one time period in its evolutionary history. The minimum requirement is that a single ancestor-descendant sequence connects modern humans with the hypothetical common ancestor they share with chimpanzees and bonobos. Does the hominin clade include just modern human ancestors or does it also include non-ancestral species that are closely related to modern humans? It has been suggested there is evidence of taxic diversity within the hominin clade back to 4.5 million years ago, but how sound is that evidence?
The main factor that would work to overestimate taxic diversity is the tendency for paleoanthropologists to recognize too many taxa among the site collections of hominin fossils. Factors that would work to systematically underestimate taxic diversity include the relative rarity of hominins within fossil faunas, the realities that many parts of the world where hominins could have been living are un- or under-sampled, and that during many periods of human evolutionary history, erosion rather than deposition predominated, thus reducing or eliminating the chance that animals alive during those times would be recorded in the fossil record. Finally, some of the most distinctive parts of an animal (e.g., pelage, vocal tract, scent glands) are not likely to be preserved in the hominin fossil record, which is dominated by fragments of teeth and jaws.
- Biological Anthropology
There is overwhelming genetic (i.e., DNA) and morphological evidence that the African apes are more closely related to modern humans than is the only Asian great ape, the orangutan. There is also compelling genetic and soft-tissue morphological evidence that chimpanzees and bonobos, the two living taxa in the genus Pan, are more closely related to modern humans than to gorillas, and according to calculations based on the differences in the DNA of modern humans and chimpanzees and bonobos, it is likely that the modern human twig, or clade, separated from the clade containing chimpanzees and bonobos, our closest living relatives, c. 8–6 million years ago (Ma).
Because chimpanzees and bonobos are both only found in Africa, and because the earliest evidence for creatures that may belong to the modern human clade also comes from Africa (e.g., Brunet et al. 2002; Senut et al. 2001; White et al. 2009), Darwin’s prediction that Africa is likely to have been the continent where the modern human clade emerged was prescient.
Given the abundant evidence for a closer relationship between Pan and Homo than between Pan and Gorilla, most researchers have concluded that the modern human clade should be distinguished in the Linnaean hierarchy beneath the level of the family. Researchers who have come to that conclusion mostly now interpret the family Hominidae—hence the informal term “hominid”—more inclusively than in the pre-molecular era. Whereas previously its use was restricted to modern humans and to any fossil taxa (e.g., australopiths) that were inferred to be more closely related to modern humans than to the African apes, many now use it for all of the great apes (including modern humans).
Many researchers who have abandoned the exclusive interpretation of hominid use the subfamily Homininae for the clade that includes modern humans and chimpanzees and bonobos, and they recognize the modern human clade at the level of the tribe (i.e., Hominini)—hence the informal term “hominin.” Chimpanzees and bonobos, and any extinct taxa more closely related to chimpanzees and bonobos than to any other living taxon, have their own tribe, Panini—hence the informal term “panin.”
If we consider the metaphor of the Tree of Life, all extant species (i.e., species we can observe in the flesh) are on the ends of branches. All of the extinct species that have ever existed in the past—the vast majority of which we only know from morphological evidence and a few of which we also know from genomic evidence—lie on branches within the tree. Strictly speaking, the only extinct species that have to be within the Tree of Life are the ones on the branches that lead to extant species. Thus, because the hominin twig has only one living species, modern humans, the minimum requirement is that a single ancestor-descendant sequence connects modern humans with the hypothetical common ancestor they share with chimpanzees and bonobos. Under this minimalist “ladder-like” model at any one time in human evolutionary history, there only needs to be one hominin species, which means there would be no hominin taxic diversity (i.e., no evidence of more than one contemporary species within the hominin clade). Under this model, modern humans would have no non-ancestral relatives, and any newly discovered fossil hominin taxon in a time period for which there was no previous evidence of hominins would be assumed to be ancestral to modern humans.
At the other end of the complexity spectrum are models of human evolution that interpret the hominin clade to be as diverse and speciose (i.e., species rich) as many groups of large mammals (e.g., bovids, pigs, and elephants). In these “bushy” models, close non-ancestral relatives would potentially outnumber ancestral relatives, so instead of assuming a newly discovered fossil hominin taxon would be ancestral to modern humans, the null hypothesis would be that it is unlikely to be a modern human ancestor. All non-linear bushy interpretations of hominin evolution imply taxic diversity within the hominin clade.
Hypotheses about the existence of a lineage have to be based on reliable hypotheses about ancestor-descendant relationships. Even if there is no taxic diversity, it is not axiomatic that a series of time-successive hominin species belong to the same lineage. Merely being time successive does not mean the species are necessarily part of an ancestor-descendant sequence, and the existence of homoplasy means that reconstructing relationships from fossil evidence is not without its complications. Likewise, evidence of taxic diversity is not necessarily evidence of multiple lineages, for Foote and Raup (1996) point out that under their “budding cladogenesis” model, “an ancestral species persists after a descendant arises” (142).
Evidence for Hominin Taxic Diversity
Hominin taxic diversity in the sense we discuss it here does not refer to diachronic diversity (i.e., species-level differences through time and space). Instead, it focuses on whether there is evidence of synchronic taxonomic diversity (i.e., species-level differences across time and space) at predetermined temporal intervals since the origin of the hominin clade. Any proposal that hominin taxic diversity exists relies on the combination of hypotheses about the existence of distinct species plus the results of efforts to provide reliable information about the age of the fossils that make up the hypodigm of each species. This article leans heavily on an earlier review of hominin taxic diversity conducted by two of the present authors (Wood and Boyle 2016).
Table 1. First Appearance Dates (FAD) and Last Appearance Dates (LAD) Used to Allocate Species, Site Collections, and Individual Specimens to Time Intervals
With dating error
With dating error
Homo habilis sensu stricto
Sima de los Huesos (SH)
Source: Wood and Boyle (2016), updated 2019.
We assigned the hominin species, site collections, and individual specimens listed in Table 1 and illustrated in Figure 1 to one or more of the time intervals. The time intervals have to be long enough to potentially capture several taxa, but not so long that they are uninformative about diachronic changes in taxic diversity. The first time interval includes fossil evidence of potential hominins between c. 7 and 5 Ma. The next two span one million years (i.e., 5.0–4.0 Ma and 4.0–3.0 Ma). The next four span half a million years (i.e., 3.0–2.5 Ma, 2.5–2.0 Ma, 2.0–1.5 Ma, and 1.5–1.0 Ma), a reduction that reflects the larger numbers of hominin species that have been proposed post 3 Ma. We then consider evidence for species-level diversity within the hominin clade between 1.0 and 0.25 Ma, and finally in the interval between 0.25 Ma and the present.
We are aware that decisions about the length and the registration of the time intervals can potentially bias the outcome of the analysis, but when Wood and Boyle (2016) repeated the exercise with different lengths and registrations, the outcome was not materially different.
We exclude some hominin species that have been proposed because we and—to judge by the lack of citations—our colleagues also consider them to be too idiosyncratic to take seriously. We assigned the remaining species, site collections, and individual specimens to one or more time intervals according to each taxon’s first appearance datum (FAD), which is the date of a taxon’s first appearance in the fossil record, and its last appearance datum (LAD), which is the date of that taxon’s last occurrence in the fossil record. The allocations to time intervals are based on conservative versions of the FADs and LADs (Table 1, columns 1 and 3, and Figure 1) as determined from the published ages of the fossils.
We reviewed the evidence for taxic diversity within each time interval by making pairwise comparisons between the hominin species, site collections, and even individual fossils that have been recognized as, or suggested to be, discrete evolutionary units. We began with the taxon that has historical priority and then compared subsequently proposed taxa with that taxon, and so on. Our attempts to rank these comparisons in terms of the degree of confidence we have in any proposed species difference (Table 2) reflect our interpretation of the literature and our judgment about the strength of each case. We concede that others may well come to different decisions, but given the multiple variables involved (e.g., what anatomical regions are sampled by the hypodigm, sample size, and preservation), it was not immediately clear to us how such judgments, especially when made across more than five million years of hominin evolution, can be standardized. We continue to reflect on and investigate ways to do this more effectively.
c. 7.0–5.0 Ma
White et al. (2009) suggested that the morphological differences between Ardipithecus ramidus and both Orrorin tugenensis and Sahelanthropus tchadensis do not justify either of the latter two species being assigned to their own genus, so he proposed they should be transferred to the genus with priority (i.e., Ardipithecus) as Ardipithecus tugenensis and Ardipithecus tchadensis, respectively. However, because White et al. (2009) did not question the decision to recognize O. tugenensis and S. tchadensis as separate species, their proposal does not affect our consideration of taxic (i.e., species level) diversity.
Publications about S. tchadensis have mainly focused on defending its status as a hominin rather than the decision to recognize it as a species distinct from O. tugenensis. Zollikofer et al. (2005) and Guy et al. (2005) each emphasize the substantial (c. 2500 km) distance separating the localities where the fossil evidence of the two taxa has been found, but there is no a priori reason why the same taxon could not have existed in the two regions (see, e.g., the discussion in the section “4.0–3.0 Ma” about taxonomic diversity between Australopithecus afarensis and Australopithecus bahrelghazali). When Brunet et al. (2005) described two new mandibles belonging to S. tchadensis, they made no reference to how they compare with what is preserved of the mandibular morphology of O. tugenensis, but apart from the mandible and some positions along the maxillary tooth row, there is little overlap in the parts of the skeleton preserved in the two hypodigms.
When Haile-Selassie et al. (2004) proposed that Ardipithecus kadabba was a separate species, the authors drew attention to differences between the crown morphology of the upper canines of O. tugenensis and Ar. kadabba, yet in the summary they suggest that with respect to the dentition “Sahelanthropus and Orrorin . . . are very similar to A. kadabba” (1503). In a later review of the fossil evidence for Ar. kadabba, Haile-Selassie et al. (2009) concluded that the mandibular morphology of Sahelanthropus is “broadly compatible with that exhibited by the ALA-VP-2/10 mandible (of A. kadabba)” (208), but no evaluation of any similarities or differences between the mandibular morphology of O. tugenensis and Ar. kadabba was offered “because of the lack of detailed information” about O. tugenensis (208). With respect to the post-canine dentition, Haile-Selassie et al. (2009) concluded that “the mandibular post-canine dentition of Sahelanthropus (TM266-02-154-2) closely matches the ALA-VP-2/10 equivalent in the available P4 to M3 metrics” (218), but once again they offered no comparison with O. tugenensis. Yet, despite these acknowledged similarities, Haile-Selassie et al. (2009) do not advocate any change to the conventional taxonomy that recognizes species- and genus-level differences between O. tugenensis, S. tchadensis, and Ar. kadabba.
Given the small size of the hypodigms of the three proposed species in this time interval and the limited overlap in the parts of the skeleton represented in those hypodigms, we believe it would be unwise to uncritically assume that the fossils in this time interval sample three separate species. In our opinion, the evidence for species differences (i.e., taxic diversity) in this time interval is not as strong as is commonly assumed, which is why we score them as enjoying only moderate confidence (Table 2).
Evidence of taxic diversity within the 5.0–4.0 Ma time interval is dependent on being able to demonstrate taxonomically valent differences between Ar. ramidus and Australopithecus anamensis. Most comparisons of Ardipithecus and Australopithecus (e.g., White et al. 2009; Suwa et al. 2009) focus on the differences between Ar. ramidus and Au. afarensis, but in their diagnosis of Au. anamensis, Leakey et al. (1995) suggest that the new taxon “can be distinguished from Ardipithecus” because it has “absolutely and relatively thicker tooth enamel; upper canine buccal enamel thickened apically; molars more buccolingually expanded; first and second lower molars not markedly different in size; tympanic tube extends only to the medial edge of the postglenoid process rather than to the lateral edge or beyond it; lateral trochlear ridge of humerus weak” (565). These distinguishing features also occur in the list of inferred shared-derived characters White et al. (2009) claim distinguish Ar. ramidus from Au. anamensis (Table 1, 82–83).
Unlike the situation in the previous time interval, there is substantial overlap in the parts of the skeleton represented by the hypodigms of Ar. ramidus and Au. anamensis, and this leads us to have high confidence that there is taxic diversity in this time interval (Table 2).
In the past several decades, researchers have assembled the substantial cumulative site collection of fossils (now well over four hundred specimens) that makes up the hypodigm of Au. afarensis. There have been suggestions that the Au. afarensis hypodigm samples more than one taxon, but none of them has received support from the researchers most familiar with the evidence. Thus, any proposal for a new hominin species in the 4.0–3.0 Ma time interval must demonstrate that the morphology of the new fossil evidence lies outside the morphospace occupied by Au. afarensis.
When this test is applied to Au. bahrelghazali, while Guy et al. (2008) claim that the symphyseal outline of Au. bahrelghazali distinguishes it from Au. afarensis, others interpret the modest-sized hypodigm of Au. bahrelghazali as evidence of geographical variation within Au. afarensis. We agree with this assessment.
The proposal to establish a new species and genus, Kenyanthropus platyops, for fossil hominins discovered at West Turkana in 1998 and 1999 was based on the hypothesis that two specimens, the type KNM-WT 40000, a 3.5 Ma cranium, and the paratype, KNM-WT 38350, a 3.3 Ma partial maxilla (Leakey et al. 2001), lie outside the morphospace occupied by Au. afarensis. The case for rejecting Au. afarensis as the appropriate taxon for this material is made more complicated because the KNM-WT 40000 cranium is plastically deformed and permeated by matrix-filled cracks. White (2003) took the view that these factors are responsible for the unusual facial morphology, and he judges KNM-WT 40000 to be a taphonomically altered Au. afarensis cranium. Spoor et al. (2010) responded by making what to us is a convincing case that the matrix-filled cracking and deformation are not responsible for the observed differences. In any event, the taphonomic alteration of the bone cannot explain the dental differences between KNM-WT 40000 and Au. afarensis.
The case made by Haile-Selassie et al. (2015) that Au. deyiremeda lies outside of the morphospace of Au. afarensis has aspects in common with the argument made by Leakey et al. (2001) for K. platyops. The authors claim that, compared with Au. afarensis, the mandibular corpus of Au. deyiremeda is more robust and lacks lateral hollowing, plus the roots of the mandibular ramus and the zygomatic process of the maxilla are more anteriorly located. With respect to the dentition, they suggest that the post-canine tooth crowns are smaller and, as was the case for K. platyops, with the M1 crown being particularly small. However, for many of the differences cited by Haile-Selassie et al. (2015), the condition in Au. deyiremeda is close to or at the edge of the range of the existing site samples of Au. afarensis. As good as that hypodigm is, it does not circumscribe the range of variation in that species. In our opinion, the claim of distinctiveness would be much stronger if Haile-Selassie et al. (2015) had linked Au. deyiremeda with the foot from Burtele.
In their initial description of the Burtele foot (BRT-VP-2/73), Haile-Selassie et al. (2012) noted that the short, opposable hallux and overall morphology of the partial foot from Burtele are sound evidence that it “does not belong to the contemporaneous species Au. afarensis” (568). They suggest that the Burtele foot retains “a grasping capacity that would allow it to exploit arboreal settings” (568), making it unlike the foot of Au. afarensis that has been described as “functionally like that of modern humans” and the foot of a “committed terrestrial biped” (Ward et al. 2011, 750).
Several researchers have drawn attention to dental, facial, and mandibular differences between the early component of the Au. afarensis hypodigm from Laetoli and the geologically younger part of the hypodigm from Hadar, and to similarities between the Laetoli remains and those of Au. anamensis (e.g., Ward et al. 1999; Kimbel et al. 2006). It remains to be seen whether these similarities are sufficient evidence to sustain the hypothesis that Au. anamensis evolved via anagenesis into Au. afarensis (e.g., Haile-Selassie et al. 2010), but even if the taxa are related in this way, it would have no effect on any claims about hominin taxic diversity because the fossil records of Au. anamensis and Au. afarensis are not synchronic.
The profound structural and inferred functional differences between the Burtele foot (BRT-VP-2/73) and the foot of Au. afarensis provide the strongest evidence for hominin taxic diversity in the 4.0–3.0 Ma time interval (e.g., DeSilva et al. 2018). It is possible that the Burtele foot belongs to Ar. ramidus. We suggest that the case for distinguishing Au. afarensis from K. platyops is stronger than the one for distinguishing it from Au. deyiremeda. For one reason or another (e.g., no overlap in the regions of the body represented in the taxon samples, poor preservation), we only have low confidence that the other pairwise comparisons in this time interval provide evidence of taxic diversity (Table 2).
The first of the two species conventionally recognized in the 3.0–2.5 Ma time interval, Australopithecus africanus, was established to accommodate an immature skull recovered in 1924 from the lime works at Taungs (now called Taung) in what is now South Africa (Dart 1925). In addition to Taung, the Au. africanus hypodigm as presently interpreted includes fossils from Member 4 at Sterkfontein, Members 3 and 4 at Makapansgat, and Gladysvale, all located in what is now South Africa. It remains to be seen whether the associated skeleton StW 573 from Sterkfontein Member 2 plus the twelve hominin fossils recovered from the Jakovec Cavern (Partridge et al. 2003) belong to Au. africanus or to a different species, Australopithecus prometheus (Clarke 2008). Several researchers have commented on the unusual nature and degree of variation within the hypodigm of Au. africanus (Lockwood and Tobias 2002), but there has been scant agreement on how the specimens that make up the hypodigm would be partitioned. Clarke (2008) has consistently argued that Makapansgat and some of the Sterkfontein Member 4 components of the hypodigm of Au. africanus samples a second, more Paranthropus-like taxon. He would include Sts 1 and 71, StW 183, 252, 384, 498, and 505, and MLD 2, plus StW 573 from Sterkfontein Member 2, within the second species, which he refers to as Au. prometheus (Granger et al. 2015), thus reviving the species name Dart (1948) used for the hominin fossils from Makapansgat. The proposed differences between the second taxon and Au. africanus mainly relate to craniofacial structure and tooth size (Clarke 2008).
The next species with historical priority in the 3.0–2.5 Ma time interval, Paranthropus aethiopicus, is used by researchers who, while not recognizing Paraustralopithecus as a separate genus, consider that the >2.3 Ma hyper-megadont hominins from the Omo-Turkana Basin belong to a species that is distinct from Paranthropus boisei. As well as the type mandible, Omo 18-1967-18, the hypodigm includes a well-preserved adult cranium (KNM-WT 17000) and mandible (KNM-WT 16005) from West Turkana and isolated teeth from the Shungura Formation. Some also assign the juvenile braincase, L. 338y-6, from the Shungura Formation to this taxon. The only postcranial fossil considered part of the hypodigm of P. aethiopicus is a proximal tibia from Laetoli. Compared with P. boisei, the face of P. aethiopicus is more prognathic, the cranial base is less flexed, the incisors, as inferred from their preserved alveoli, are larger, and the post-canine teeth, especially the mandibular premolars, are less morphologically specialized than those of P. boisei (Suwa 1988).
The only other hominin from the 3.0–2.5 Ma time interval is represented by a single specimen, LD 350-1, the left side of an adult hominin mandible, found in the Lee Adoyta region of the Ledi-Geraru research area in the Afar Regional State in Ethiopia, which has been provisionally assigned to an unnamed species of Homo (Villmoare et al. 2015).
We have high confidence that there is a strong case for distinguishing Au. africanus and P. aethiopicus (Table 2). The case for distinguishing the LD 350-1 mandible from the other taxa in this time interval is not nearly as strong. We are not convinced that a case has been made for taxic diversity within the conventional hypodigm of Au. africanus (Table 2).
After Au. africanus, the hominin species with historical priority in the 2.5–2.0 Ma time interval is Zinjanthropus boisei (Leakey 1959), now usually referred to as Paranthropus boisei (Robinson 1960). It has a comprehensive craniodental fossil record that includes an especially complete and well-preserved skull from Konso in Ethiopia (Suwa et al. 1997), several well-preserved crania, and many mandibles and isolated teeth. Apart from a partial upper limb from Olduvai Gorge and two very fragmentary possible P. boisei partial skeletons from Koobi Fora, no other postcranial evidence can be attributed to P. boisei with any reliability, but some of the postcranial fossils from Bed I at Olduvai Gorge conventionally linked with Homo habilis sensu lato may belong to P. boisei (Wood 1974; Wood and Constantino 2007; DeSilva et al. 2018).
The next species in this time interval, Homo habilis, was established to accommodate non-megadont fossil hominins (OH 4, 6, 7, 8, 13, 14, and 16) recovered between 1959 and 1963 from Beds I and II at Olduvai Gorge in Tanzania (Leakey et al. 1964). The authors claimed that the cranial and dental morphology and estimated endocranial volume of that collection of specimens, plus inferences made about the dexterity and locomotion of the type of animal it sampled, were enough to both distinguish the new taxon from Au. africanus and justify its inclusion in Homo. Subsequent discoveries at Olduvai (e.g., OH 24, 62, and 65) and from other sites (e.g., Koobi Fora: KNM-ER 1470, 1802, 1805, 1813, 3735; Sterkfontein: Stw 53; Swartkrans: SK 847; Hadar: A.L. 666-1) have also been assigned to or affiliated with H. habilis. The hypodigm set out above has a relatively wide range of cranial and dental morphology (e.g., endocranial volume ranges from c. 500 to c. 800 cm3). Some researchers, who consider the cranial variation within the hypodigm set out above to be excessive in scale and unlike the pattern of intraspecific variation seen in the African ape clade, suggest that H. habilis sensu lato subsumes two taxa, Homo habilis sensu stricto and Homo rudolfensis. Most of the fossil evidence for H. habilis sensu lato is less than 2.0 Ma, but some belongs in this earlier time interval. We discuss the claims for taxic diversity within Homo habilis sensu lato in the next section (“2.0–1.5 Ma”).
The final species in the 2.5–2.0 Ma time interval, Australopithecus garhi, was established to accommodate a fragmented cranium recovered from the Hatayae Member of the Bouri Formation at the Bouri, Gamedah, and Matabaietu collection areas in the Middle Awash study area of Ethiopia (Asfaw et al. 1999). However, unlike other hyper-megadont species such as P. aethiopicus and P. boisei, the incisors and canines of Au. garhi are also large, the anterior premolar is larger than the posterior, and the enamel apparently lacks the extreme thickness seen in the former taxa. A partial skeleton with an elongated thigh and forearm was found nearby, but it is not associated with the type cranium (Asfaw et al. 1999) and the skeleton has not been formally assigned to Au. garhi.
The effective sympatry of P. boisei and H. habilis sensu lato (Leakey and Walker 1976; Wood 1991) and their synchronicity in this and the next time interval are perhaps the strongest evidence of taxic and lineage diversity in the hominin fossil record. There is also sound evidence for making a taxonomic distinction between Au. africanus and both P. boisei and H. habilis sensu lato. Although there is only one fragmented cranium for Au. garhi, the differences between it and the cranial hypodigms of Au. africanus and P. boisei suggest that the claim for it being distinct from both of these taxa is also a strong one (Table 2).
The species with historical priority in this time interval is Homo erectus. In his initial publication of the fossils recovered from the excavations at Trinil on the island of Java, Dubois (1893) referred the skullcap to Anthropopithecus erectus. At that time, Anthropopithecus was one of the genus names used for chimpanzees, and Dubois’ choice of genus name reflected his initial conviction that he had discovered the remains of a fossil ape. But a year later he had evidently changed his mind because he transferred the new species to a novel genus, Pithecanthropus. Most of the discoveries made by Ralph von Koenigswald at Sangiran, also in Java, were added to the hypodigm of P. erectus. Fossils recovered by Davidson Black and colleagues from what was then called Choukoutien (now called Zhoukoudian) in China were initially assigned to Sinanthropus pekinensis (Black 1927). But when the researchers responsible for analyzing the Indonesian and Chinese collections compared the collections, they concluded that the two regional populations were “related to each other . . . in the same way as two different races of present mankind” (von Koenigswald and Weidenreich 1939, 928). A year later, the latter author proposed the two hypodigms should be formally merged within a single genus and species, as Homo erectus pekinensis and Homo erectus javanensis, respectively (Weidenreich 1940). Subsequently, Meganthropus palaeojavanicus (Mayr 1944), Atlanthropus (Le Gros Clark 1964), and Telanthropus (Robinson 1961) were transferred to Homo erectus. Most researchers are willing to subsume all of this material into a single species, albeit one that evolves through time (e.g., Kaifu et al. 2008). Some argue there are potential species-level differences between the Sangiran–Trinil hypodigms and the evidence from Sambungmacan and Ngandong (e.g., Widianto and Zeitoun 2003), and most recently researchers have revived the proposal that a second species—but not necessarily a hominin species—should be recognized for one of the mandibles recovered from Sangiran (Zanolli et al. 2019).
The second species with historical priority in the 2.0–1.5 Ma time interval, Paranthropus robustus, was established to accommodate fossil hominins recovered from what was then referred to as the “Phase II Breccia” (now called Member 3) at Kromdraai B, in Gauteng Province, South Africa (Broom 1938). As of 2019, most of the hypodigm comes from Swartkrans (Mbs 1, 2, and 3), with other fossil evidence coming from the nearby caves of Cooper’s, Drimolen and Gondolin. Although the dentition is well represented in the hypodigm of P. robustus, many of the mandibles are crushed or distorted. The brain, face, and chewing teeth of P. robustus are larger than those of Au. africanus, yet the incisors and canines are smaller, and whereas P. robustus includes crania with ectocranial crests, there are no Au. africanus crania with unambiguous crests. What little is known about the postcranial skeleton of P. robustus suggests that the morphology of the pelvis and the hip joint is much like that of Au. africanus.
In terms of historical priority, the next species in the 2.0–1.5 Ma time interval is Homo ergaster. It was established to accommodate fossil hominins recovered from Koobi Fora that, in the judgment of the authors, did not belong in the taxa known at the time (Groves and Mazák 1975). Wood (1994) used the taxon name H. ergaster for hominin remains (e.g., KNM-ER 730, 820, and 992) that are generally more primitive and lack the more extreme expressions of some of the derived features (e.g., thick inner and outer table, sagittal keeling) seen in Asian H. erectus.
If the fossils assigned to H. habilis sensu lato (see “2.5–2.0 Ma”) sample not one, but two species, and if that second species includes KNM-ER 1470, then the next species with historical priority in this time interval is Pithecanthropus rudolfensis, subsequently transferred to Homo (Groves 1989) as Homo rudolfensis. Leakey et al. (2012) described a face (KNM-ER 62000) and two mandibles (KNM-ER 1482 and 60000) that match KNM-ER 1470, and Spoor et al. (2015) made the case that the dental arcade of the enlarged hypodigm of H. rudolfensis is distinctively different (e.g., more divergent tooth rows, flatter anterior dental arch) from the dental arcade of H. habilis sensu stricto.
The penultimate species in this time interval, Homo georgicus, was established for the hominin fossils recovered from Dmanisi (Gabounia et al. 2002). The holotype is the mandible D2600. No paratypes were formally designated, but the mandible D211, the calvaria D2280, the cranium D2282, and the skull and associated skeleton D2700 were referred to as evidence that “will complete the characteristics of the new species” (Gabounia et al. 2002, 244). Although several of the authors of the original publication (e.g., Lordkipanidze et al. 2013) no longer support a separate taxon for this material, we treat it separately in our discussion of the evidence in this time interval because the evidence from Dmanisi provides a sense of the range of variation in a hominin species within what is a relatively short interval of geological time. Overall, the Dmanisi hominins are most similar to H. erectus, and where there are differences, they involve morphology inferred to be more primitive than that seen in the latter taxon.
The final species in the 2.0–1.5 Ma time interval, Australopithecus sediba, was established to accommodate two associated skeletons, MH1, a subadult presumed male, and MH2, an adult presumed female, recovered from Malapa, Gauteng Province, in South Africa (Berger et al. 2010). Berger and colleagues suggested that Au. sediba has cranial (e.g., more globular neurocranium, gracile face), mandibular (e.g., more vertical symphyseal profile, a weak mentum osseum), dental (e.g., simple canine crown, small anterior and post-canine tooth crowns), and pelvic (e.g., acetabulocristal buttress, expanded ilium, and short ischium) morphology that departs from that seen in Au. africanus, and which is only shared with early and later Homo taxa. Carlson et al. (2011), Kivell et al. (2011), and Zipfel et al. (2011) make similar claims for the endocranial, hand, and foot morphology, respectively, of Au. sediba.
In the previous section we noted the extremely compelling evidence for taxic diversity provided by P. boisei and H. habilis sensu lato. There is also little doubt that the fossil evidence assigned to H. erectus, P. robustus, and Au. sediba samples three different species. All of these distinctions are in the high confidence category (Table 2).
We also suggest there is compelling evidence that P. boisei is distinct from P. robustus, and that H. habilis sensu lato can be distinguished from H. erectus on the basis of cranial, mandibular, dental, and postcranial differences (contra Lordkipanidze et al. 2013), but the evidence for these latter distinctions, as convincing as it is, is not as clear-cut as the case for recognizing H. erectus, P. robustus, and Au. sediba as separate species. We agree with a recent assessment of Grine et al. (2019) that “the preponderance of evidence” (171) supports the recognition of H. habilis sensu stricto and H. rudolfensis as separate taxa, but we also agree with them that the distinction is more nuanced than the ones above, leading to disagreements about which species some individual fossils should be assigned to. Hence, these pairwise comparisons are in the moderate confidence category (Table 2).
The case for making specific distinctions among H. erectus, H. ergaster, and H. georgicus is weaker still. Two categories of features are claimed to distinguish H. ergaster from H. erectus. The first comprises dental features for which H. ergaster is more primitive than H. erectus, the second includes features of the cranial vault and cranial base that are less derived in H. ergaster than in H. erectus. For example, it is claimed that H. ergaster lacks some of the more derived features of H. erectus (e.g., thickened inner and outer tables and prominent sagittal and angular tori [Wood 1984, 1991]), but other researchers dispute the distinctiveness of this material, and Spoor et al. (2007) claim that the expression of some features is related to the overall size of the cranium such that larger H. erectus crania are more likely to show the derived morphology. Therefore, we have put both of these pairwise comparisons in the low confidence category (Table 2).
In this time interval, the only addition to the species we have already reviewed is Homo antecessor. It was established to accommodate hominins recovered from level 6 of the Gran (or Trinchera) Dolina, a complex of caves in the Atapuerca hills near Burgos, Spain. The modern human-like morphology of the face and the apparent lack of derived Homo neanderthalensis features, combined with differences between the Gran Dolina hominins and H. erectus, led Bermúdez de Castro et al. (1997) to propose that the former fossils should be assigned to a new species, H. antecessor. We include H. antecessor in this time interval as well as the next for two reasons: first, because a c. 1.2–1.1 Ma partial mandible (ATE9-1) from the Sima del Elefante was provisionally assigned to this species (Carbonell et al. 2008), although Bermudez de Castro et al. (2011) subsequently concluded there was not enough evidence to assign the mandible to H. antecessor; second, because a reappraisal of the Ceprano cranium suggested that it may also belong to H. antecessor (Manzi et al. 2001).
In the previous sections, we established that the case for H. erectus, P. robustus, P. boisei, and H. habilis sensu lato being distinct species is strong enough to place all of those pairwise distinctions in the high confidence category (Table 2). Despite the claims of Lordkipanidze et al. (2013), the case for distinguishing between H. erectus and H. habilis sensu lato is strong enough for us to put it in the moderate confidence category (Table 2). We place the cases for distinguishing between H. erectus and H. ergaster and between H. antecessor and H. erectus–H. ergaster in the low confidence category (Table 2).
The species with historical priority, H. erectus, was reviewed in the 2.0–1.5 Ma time interval. The next species in this time interval, Homo heidelbergensis, was created to accommodate a hominin mandible found in 1907 in a sandpit at Mauer, near Heidelberg in Germany (Schoetensack 1908). Schoetensack concluded that the Mauer mandible’s mix of primitive (no chin, robust corpus, broad ramus, and an anterior-posteriorly deep mandibular symphysis) and derived (reduced canines and modern human-like dental proportions) features was sufficient to distinguish it from Homo sapiens, H. neanderthalensis, and what was then called Pithecanthropus erectus. But H. heidelbergensis attracted little interest until it was suggested that it may be the most appropriate species name for a group of Afro-European hominin fossils (e.g., Arago, Bodo, Kabwe, Mauer, Ndutu, and Petralona) that had traditionally been labeled as “archaic” Homo sapiens (Rightmire 1995). Mounier et al. (2009) set out the morphological grounds for recognizing H. heidelbergensis as a separate taxon and provided a definition and a differential diagnosis (243–244).
The next species with historical priority in the 1.0–0.25 Ma time interval, Homo rhodesiensis, was introduced to accommodate the cranium and limb bones (Kabwe 1 or E 686) recovered from the Broken Hill lead mine at Kabwe in what then was the British protectorate of Northern Rhodesia, now Zambia (Woodward 1921). Woodward reasoned a new species was needed because Kabwe 1 did not resemble H. erectus, H. sapiens, or H. neanderthalensis. Morphologically similar remains include fossils from Hopefield–Elandsfontein in southern Africa, Ndutu in Tanzania, Sale in North Africa, and Bodo in Ethiopia.
The next formal species in the 1.0–0.25 Ma time interval, Homo helmei, was established for the Florisbad 1 partial cranium discovered in 1932 in Florisbad in South Africa (Dreyer 1935). Those who recognize H. helmei claim that its more steeply inclined frontal bone distinguishes it from H. heidelbergensis, and its large brow ridge, more receding frontal, and low greatest breadth in the vault distinguish it from anatomically modern humans. Others have suggested that Jebel Irhoud, Ngaloba (a.k.a. LH 18), and Omo II belong to the same hypodigm.
The last formal species we will consider in this section, Homo naledi, straddles the boundary between this time interval and the next. The taxon comprises hominin remains recovered from two chambers, Dinaledi and Lesedi, in the Rising Star cave system near the site of Swartkrans, in Gauteng Province, South Africa. At the time we prepared our initial review of hominin taxic diversity (Wood and Boyle 2016), H. naledi was not included because there were no dates then (Berger et al. 2015). All of the hominin fossils in the Dinaledi Chamber were recovered from the same horizon, subunit 3b, and the sediments in that subunit were subsequently dated using optically stimulated luminescence; the capping flowstones were dated using U-Th and paleomagnetism. Ages were also obtained from three teeth belonging to H. naledi by combining U-series and electron spin resonance techniques (US-ESR). The researchers suggest that their best estimate of the age of H. naledi from the Dinaledi Chamber is the maximum age from US-ESR, which is 253 +82/-70 ka (Dirks et al. 2017). The hominins from the Lesedi Chamber are presently undated.
The fossils belonging to H. naledi, which display relatively little inter-individual variation, appear to sample a hominin with an unusual mix of characteristics. Its cranium resembles early Homo–H. ergaster, but with a smaller endocranial volume (c. >550 cm3). The dentition combines derived (i.e., modern human-like) tooth crowns with primitive mandibular premolar roots, the hand morphology is mostly derived in the direction of modern humans (Kivell et al. 2015), the pedal phalanges are curved (Harcourt-Smith et al. 2015), and the morphology of the pelvis and hip joint is relatively primitive.
The last group we consider in this time interval is the unusually complete and well-preserved collection of hominins recovered from the Sima de los Huesos, one of the many breccia-filled cave systems that make up the Cueva Mayor-Cueva del Silo within the Sierra de Atapuerca, near Burgos in northern Spain. More than 6,500 hominin specimens belonging to at least twenty-eight individuals (Arsuaga et al. 2014) have been recovered from excavations in the main cave and in the ramp that leads down to the cave. The hominin remains include numerous crania, mandibles, hundreds of teeth, a nearly complete pelvis, vertebrae, ribs, hand and foot bones, and multiple specimens of long bones. The cranial and mandibular sample shows a number of derived features of H. neanderthalensis (e.g., pronounced mid-facial prognathism, the form of the brow ridge, a flat articular eminence of the glenoid fossa, a retromolar space, and an asymmetrical configuration of the ramus of the mandible), a taxon we discuss in more detail in the next section (“0.25 Ma to the Present”). In contrast, the cranial vault is generally more primitive (e.g., large, projecting, mastoid processes, rounded neurocranium), with some incipient derived traits of H. neanderthalensis (e.g., weak expression of the suprainiac fossa). The dentition of the Sima de los Huesos hominins has affinities with the teeth of H. neanderthalensis (Gómez-Robles et al. 2015).
Recent efforts to improve the dating of the hominin-bearing sediments at Denisova Cave in the Altai region of Russia suggest that the Denisovan fossils may extend into this time interval (Jacobs et al. 2019; Douka et al. 2019), but because most of the currently known evidence is <0.25 Ma, we discuss them in the next section.
The strongest evidence for taxic diversity in the 1.0–0.25 Ma time interval are the pairwise comparisons between H. erectus and H. heidelbergensis, H. rhodesiensis, H. helmei, H. naledi, and the site sample from the Sima de los Huesos, respectively; we place them all in the high confidence category (Table 2).
As for hominin taxonomic diversity within Europe, researchers most familiar with the evidence from the Sima de los Huesos make a distinction between that site sample and the hypodigm of H. neanderthalensis, and even though they assigned the Sima de los Huesos hominins to H. heidelbergensis (Arsuaga et al. 1997), they acknowledged that H. heidelbergensis is related to H. neanderthalensis in the same way that some have suggested Au. anamensis is related to Au. afarensis (i.e., anagenetically). Those who treat the fossils from the Sima de los Huesos as evidence of an early stage of a H. neanderthalensis chronospecies include them within that taxon (Hublin 2009). We place the claims for taxonomic distinction between the Sima de los Huesos fossils and H. heidelbergensis, H. rhodesiensis, and H. helmei, respectively, in the moderate confidence category (Table 2).
While some researchers suggest that Florisbad 1 could serve as the holotype of H. helmei, most take the view there is no satisfactory diagnosis that reliably separates it from H. heidelbergensis (or from H. rhodesiensis if the distinction between H. heidelbergensis and H. rhodesiensis is accepted) or H. sapiens. Hublin et al. (2017) claim that additional evidence from Jebel Irhoud further blurs the boundary between H. helmei and H. sapiens. For these reasons, we place the claims for taxonomic distinction between H. heidelbergensis and H. rhodesiensis, and between H. heidelbergensis and H. helmei in the low confidence category (Table 2).
0.25 Ma to the Present
The species with historical priority in this time interval is Homo sapiens (Linnaeus 1758). The first widely accepted fossil evidence of modern humans came in 1868 when skeletal remains were discovered at the Cro-Magnon rock shelter at Les Eyzies de Tayac in France. Since then, discoveries of H. sapiens-like fossils have been made elsewhere in Europe (e.g., Mladec, Predmosti, and Brno), Asia and South-East Asia (e.g., Wadjak, Zhoukoudian Upper Cave, and Niah Cave), the Near East (e.g., Skhul and Djebel Qafzeh), and Australia (e.g., Willandra Lakes). The first African fossil evidence for H. sapiens came in 1924 from Singa in the Sudan, with subsequent evidence coming from Border Cave and Klasies River Mouth in South Africa, Dar es Soltane in Morocco, and Dire-Dawa, Herto, and Omo-Kibish in Ethiopia. Most recently, Hublin et al. (2017) claim that additional evidence from Jebel Irhoud strengthens the claim that hominins from that site “sample early stages of the H. sapiens clade” (289). If the Jebel Irhoud evidence were to be included, without qualification, in H. sapiens, then that taxon would extend into the previous time interval.
The next species for consideration in this time interval, Homo neanderthalensis, was established for the partial skeleton recovered in 1856 from the Kleine Feldhofer Grotte in the part of the Düssel valley named after Joachim Neander (King 1864). Discoveries made before 1856, such as the infant’s cranium from Engis in 1828 and the partial cranium from Forbes’ Quarry, Gibraltar, in 1848, were subsequently recognized as belonging to H. neanderthalensis. In the following half-century, remains attributed to H. neanderthalensis were discovered at other European sites, including La Naulette and Spy in Belgium, Šipka in Moravia, Krapina in Croatia, and Malarnaud, La Chapelle-aux-Saints, Le Moustier (lower shelter), La Ferrassie, and La Quina, among others, in France. In 1924–1926, the first H. neanderthalensis remains were found outside of Western Europe at Kiik-Koba in the Crimea, and thereafter came discoveries at Tabun Cave on Mount Carmel in the Levant, and at Teshik-Tash in central Asia. Further evidence was added after World War II, first from Shanidar in Iraq, then from Amud and Kebara in Israel, and from Dederiyeh in Syria. New fossiliferous localities continue to be discovered in Europe (e.g., Saint-Césaire and Moula-Guercy in France, Zafarraya in Spain, Vindija in Croatia, and Lakonis in Greece), Western Asia (e.g., Mezmaiskaya and Denisova in Russia), and China (e.g., Xuchang). To date, Neanderthal remains have been found throughout much of Europe below 55°N, in the Near East and in Western Asia, but no evidence has been found in North Africa.
There is sound enough evidence that H. erectus (see previously) persists at some sites until 0.25 Ma for us to consider it within this final time interval.
The next species with historical priority, Homo floresiensis (Brown et al. 2004), was established to accommodate LB1, a partial adult hominin skeleton, and LB2, an isolated left P3, recovered in 2003 from the Liang Bua cave on the island of Flores in Indonesia. More material belonging to LB1, and evidence allocated to individuals LB4–9, including LB6—a partial skeleton lacking a cranium—was recovered in 2004 (Morwood et al. 2005). The hypodigm now includes close to one hundred individually numbered specimens that are estimated to represent fewer than ten individuals. Initially, it was suggested that H. floresiensis was a dwarfed H. erectus, but the burden of subsequent analyses suggests that it may be more closely related to a more primitive hominin such as H. habilis sensu lato (Morwood and Jungers 2009). Baab (2016) provides an excellent review of the implications of the fossil evidence.
Even more recently, researchers have claimed that c. 70 kya fossil hominin remains (seven maxillary post-canine teeth, two hand bones, three foot bones, and a femur shaft) from at least three individuals, recovered from Callao Cave on the island of Luzon in the Philippines, sample a hitherto unknown hominin species, Homo luzonensis (Détroit et al. 2019).
The final evidence to be considered in this time interval is a taxon that was recognized through ancient DNA analysis before there was any morphological evidence for its existence. Researchers recovered mtDNA from the distal phalanx of the fifth (little finger) digit of a hominin hand (Denisova 3), which came from c. 48–30 ka layer 11 in Denisova Cave in the Altai Mountains in Russia. When they compared it with the equivalent mtDNA from fifty-four modern humans, one chimpanzee and one bonobo, six Neanderthals, and a single fossil H. sapiens from Kostenki (Krause et al. 2010), they concluded it came from a hominin that, while distinct from both modern humans and Neanderthals, shared a common ancestor with both species c. 1 million years ago. Distinctive Denisovan DNA has been recovered from a large-crowned maxillary molar (Denisova 8) whose crown morphology is distinct from both modern humans and Neanderthals. Meyer et al. (2015) recently published a high-coverage sequence from the same individual. Subsequently, a deciduous molar (Denisova 2) and another maxillary molar (Denisova 4) have been identified as Denisovan (Sawyer et al. 2015; Slon et al. 2015). An analysis of mtDNA of an individual from Sima de los Huesos (Meyer et al. 2014) suggested a closer affinity between the mtDNA of Denisovans and the population from Sima de los Huesos than between Denisovans and Neanderthals or Denisovans and modern humans. Meyer et al. (2016) extracted mtDNA and nuclear DNA from five Sima de los Huesos hominin specimens. The new nuclear DNA data are consistent with the hypothesis that the Sima de los Huesos hominins were more closely related to the Neanderthals than to the Denisovans and suggest that the most recent common ancestor of Neanderthals and modern humans was living between 765 and 550 ka, if not earlier (Gómez-Robles 2019). Ancient proteomic analysis links a 160 ka mandible recovered in 1980 from Xiahe, in Gansu (PRC), at the extreme eastern margin of the Tibetan plateau, with the Denisovans, and the morphology of the preserved teeth and mandibular corpus suggests that the Xiahe mandible is more primitive than H. sapiens and H. neanderthalensis and closest to the Chinese H. erectus and H. heidelbergensis (Chen et al. 2019).
Any proposal for a hominin species other than modern humans in the 0.25 Ma to the present time interval that uses morphological evidence must demonstrate that the fossil evidence lies outside the envelope of the morphological variation documented for H. sapiens. And, if more than one set of fossil evidence meets that challenge, then researchers must demonstrate that each set of fossil evidence is distinctive enough to be referred to a separate species.
There is copious morphological evidence from the cranium (e.g., large, rounded discrete brow ridges, projecting midface, angled cheeks, small mastoid process, supra-iniac fossa, and occipital bun), mandible (e.g., long corpus, retro-molar space, and asymmetric mandibular notch), dentition (e.g., large shovel-shaped incisors, distinctive occlusal and enamel-dentine junction morphology of molars and premolars, a high incidence of taurodontism), and the postcranial skeleton (e.g., long clavicle, teres minor groove extending onto the dorsal surface of the scapula, large infraspinous fossa, long, thin pubic ramus, and large joints) that H. neanderthalensis differs from H. sapiens. Even more compelling is the evidence that many of these differences are seen early in the ontogeny of H. neanderthalensis (Tillier 1982; Nelson and Thompson 2005; Coqueugniot and Hublin 2007; Ponce de León et al. 2008; Gunz et al. 2010; Smith et al. 2010). In addition, H. neanderthalensis is currently the only extinct hominin for which ancient DNA (aDNA) evidence has been recovered from many individuals across several sites, and although there is evidence of a modest amount of genetic admixture—up to 4 percent of the nuclear DNA of modern humans from outside of Africa is shared with Neanderthals—the differences between the DNA of modern humans and Neanderthals is much greater than the range of variation within modern humans. These results are compatible with either a deep split within Africa between the population that gave rise to modern Africans and a second one that gave rise to present-day non-Africans plus Neanderthals, or with the hypothesis that there was hybridization between Neanderthals and modern humans soon after the latter left Africa, perhaps in western Asia. In summary, the morphological and the genetic differences between modern humans and Neanderthals are both consistent with a species-level distinction that enjoys a high level of confidence (Table 2).
With respect to the distinctiveness of H. floresiensis, views are sharply polarized. The consensus is that if you take the hypodigm as a whole, it is most parsimoniously interpreted as evidence of a novel endemically dwarfed pre-modern Homo, or early Homo, species. Very few researchers cling to the view that the “Homo floresiensis hypodigm” samples a H. sapiens population—most likely related to the small-statured Rampasasa people who live on Flores today, some members of which just happen to be afflicted by either an endocrine disorder (see Obendorf et al. 2008 and a rebuttal by Brown 2012) or one or more of a range of syndromes that include microcephaly. Both explanations, a novel dwarfed early hominin species or a pathological subpopulation of modern humans, are exotic, but those who espouse a pathological explanation for the individuals represented by LB1–15 need to explain what pathology results in a phenotype that resembles an early Homo-like cranial vault, primitive mandibular, dental, carpal, and pedal morphology, and a brain that, while very small, apparently has none of the morphological features associated with the majority of types of microcephaly (Vannucci et al. 2011). We subscribe to the interpretation that the fossil evidence from Liang Bua is a distinctive Homo species that is clearly phenotypically distinct from all of the other taxa in this time interval, so we judge all of the pairwise comparisons involving H. floresiensis to have a high level of confidence (Table 2).
Differences between the ancient mtDNA and nuclear DNA extracted from the distal phalanx of the fifth (little finger) digit of a hominin hand and the mtDNA extracted from a large-crowned maxillary molar, both found in Denisova Cave, and the DNA of modern humans and H. neanderthalensis (Reich et al. 2011; Patterson et al. 2012; Prüfer et al. 2014) are consistent with the Denisovans, H. sapiens, and H. neanderthalensis belonging to different species. The DNA recovered from H. neanderthalensis individuals across Europe is consistently more similar to one another than any is to the DNA recovered at Denisova. On the basis of this genetic evidence, plus the dental differences between the Denisovans and contemporary taxa, we have moderate confidence that the former is a distinctive species (Table 2).
So, within the interval between 0.25 Ma to the present time, on the basis of morphological evidence we have high confidence that there are species-level differences among H. sapiens, H. neanderthalensis, H. erectus, and H. floresiensis, and there is convincing evidence from aDNA that both H. neanderthalensis and the Denisovans deserve to be recognized as separate species. There is also less strong, but still potential evidence for H. heidelbergensis in this time interval. It is also possible that H. heidelbergensis and the Denisovan aDNA sample the same taxon (Meyer et al. 2014), and it has been suggested that fossils from China, Tibet, and South East Asia may be phenotypic expressions of Denisovan aDNA.
Table 2. Assessment of the Strength of the Evidence for Taxic Diversity within the Time Intervals Described in This Article
Orrorin tugenensis vs. Sahelanthropus tchadensis
Orrorin tugenensis vs. Ardipithecus kadabba
Sahelanthropus tchadensis vs. Ardipithecus kadabba
Ardipithecus ramidus vs. Australopithecus anamensis
Australopithecus afarensis vs. Burtele foot
Australopithecus afarensis vs. Kenyanthropus platyops
Australopithecus afarensis vs. Australopithecus bahrelghazali
Australopithecus afarensis vs. Australopithecus deyiremeda
Kenyanthropus platyops vs. Australopithecus deyiremeda
Kenyanthropus platyops vs. Burtele foot
Burtele foot vs. Australopithecus deyiremeda
Australopithecus africanus vs. Paranthropus aethiopicus
Paranthropus aethiopicus vs. LD 350-1
Australopithecus africanus vs. LD 350-1
Australopithecus africanus vs. Australopithecus prometheus
Australopithecus africanus vs. Paranthropus boisei
Paranthropus boisei vs. Homo habilis sensu lato
Australopithecus garhi vs. Homo habilis sensu lato
Australopithecus africanus vs. Homo habilis sensu lato
Australopithecus africanus vs. Australopithecus garhi
Paranthropus boisei vs. Australopithecus garhi
Homo erectus vs. Paranthropus robustus
Homo erectus vs. Paranthropus boisei
Homo erectus vs. Australopithecus sediba
Paranthropus robustus vs. Homo habilis sensu lato
Paranthropus robustus vs. Paranthropus boisei
Paranthropus robustus vs. Australopithecus sediba
Paranthropus boisei vs. Homo habilis sensu lato
Paranthropus boisei vs. Australopithecus sediba
Homo habilis sensu lato vs. Australopithecus sediba
Homo habilis sensu stricto vs. Homo rudolfensis
Homo erectus vs. Homo habilis sensu lato
Homo erectus vs. Homo ergaster
Homo erectus vs. Homo georgicus
Homo erectus vs. Paranthropus robustus
Homo erectus vs. Paranthropus boisei
Paranthropus robustus vs. Homo habilis sensu lato
Paranthropus robustus vs. Homo antecessora
Paranthropus boisei vs. Homo antecessora
Homo habilis sensu lato vs. Homo antecessora
Homo erectus vs. Homo habilis sensu lato
Paranthropus robustus vs. Paranthropus boisei
Homo erectus vs. Homo ergaster
Homo erectus vs. Homo antecessor
Homo erectus vs. Homo heidelbergensis
Homo erectus vs. Homo rhodesiensis
Homo erectus vs. Homo helmei
Homo erectus vs. Sima de los Huesos
Homo erectus vs. Homo naledi
Homo heidelbergensis vs. Homo naledi
Homo rhodesiensis vs. Homo naledi
Sima de los Huesos vs. Homo naledi
Homo helmei vs. Homo naledi
Homo heidelbergensis vs. Sima de los Huesos
Homo rhodesiensis vs. Sima de los Huesos
Homo helmei vs. Sima de los Huesos
Homo heidelbergensis vs. Homo rhodesiensis
Homo heidelbergensis vs. Homo helmei
Homo sapiens vs. Homo neanderthalensis
Homo sapiens vs. Homo erectus
Homo sapiens vs. Homo heidelbergensis
Homo sapiens vs. Homo floresiensis
Homo sapiens vs. Denisovans
Homo erectus vs. Homo heidelbergensis
Homo erectus vs. Homo floresiensis
Homo neanderthalensis vs. Homo erectus
Homo neanderthalensis vs. Homo floresiensis
Homo heidelbergensis vs. Homo floresiensis
Homo neanderthalensis vs. Denisovans
Homo erectus vs. Denisovans
Homo sapiens vs. Homo luzonensis
Homo neanderthalensis vs. Homo heidelbergensis
Homo heidelbergensis vs. Denisovans
Homo floresiensis vs. Homo luzonensis
a If the partial mandible (ATE9-1) from the Sima del Elefante does not belong to H. antecessor, then these “high confidence” pairwise comparisons would fall away.
Source: Wood and Boyle (2016), updated 2019.
What Factors May Lead Researchers to Systematically Overestimate Taxic Diversity?
How sound is the evidence that, for at least the last 4.5 Ma, there is evidence of taxic diversity within the hominin clade? The relationship between the number of species that actually existed and the number of species we think we are sampling in the fossil record is an expression of the completeness (sensu Valentine 1989) of that record. Taxic diversity would be exaggerated if (a) interpretations of the alpha taxonomy of the hominin fossil record are systematically recognizing too many taxa (a.k.a. excessive “splitting”), or (b) the time ranges of those taxa are systematically being interpreted as longer than they really are. In reality, there are methodological reasons why the former may be occurring. There is little evidence to suggest that dating methods are systematically overestimating the temporal ranges of taxa.
Over-speciose taxonomic hypotheses are generated when researchers fail to understand that the existing site samples (a.k.a. hypodigms) of many early hominin taxa are too meager to realistically capture the nature and range of variation of the species in question. In an underappreciated review, Smith (2005) exposes with forensic effectiveness just how small the sample sizes of some early hominin hypodigms are, and what this means for the ability to show that when a sample of fossils is recovered from a new site it merits recognition as a new species. That being said, if new fossil evidence happens to preserve a region in which the ratio of inter- to intraspecific variation is favorable, and if the specimens are relatively complete, it is possible to demonstrate taxic diversity even with relatively small sample sizes. Indeed, there are several instances in the hominin fossil record where just one new fossil (e.g., OH 7) is so different from the fossil evidence of a synchronic species (e.g., OH 5) that the case for taxonomic distinctiveness is obvious. But, as Smith (2005) points out, not all claims for new hominin taxa are as securely based as this example. Until we have larger hypodigms for fossil hominin taxa, the procedures traditionally used in paleoanthropology (i.e., asking whether a new site sample lies outside the range of variation of the existing site samples of a taxon) are likely to lead to the over-reporting of new taxa, with the inevitable result that taxic diversity will also be over-reported (i.e., Type I error). This is because even if a species is sampled from several sites, those site samples, even ones as good as the sample of Au. afarensis from Hadar, are unlikely to capture the range of variation of the population (i.e., species) from which the samples are drawn. What researchers need to do is to find some way of using the site samples to estimate variation in the parent population. This is not a trivial task, but it is a necessary one if we are to avoid the risk of unjustified splitting.
One obvious solution is to find additional fossil evidence from new and existing sites and localities and then provide, in a timely fashion, detailed and reliable information about the new evidence. Another strategy is to expand our understanding of variation within closely related extant taxa and apply any lessons learned to interpreting the hominin fossil record. Comparative studies that collect data from large samples of the great apes for a particular region, such as the studies of dental morphology by Uchida (2004) and Pilbrow (2010), are especially helpful because they allow us to conduct the thought experiment of imagining what variation in a large sample of an early hominin species would possibly look like. Another strategy is to look at patterns of inter- and intraspecific variation within and among the extant taxa most closely related to fossil hominins. If there are any common patterns, parsimony as expressed in the principle of the phylogenetic bracket (Witmer 1995) suggests that the same pattern should also apply to fossil hominin taxa. Sound comparative evidence about inter- and intraspecific variation could then be used to generate additional criteria to help researchers make judgments about the taxonomic significance of any observed morphological differences between samples of fossil hominins.
What Factors May Lead Researchers to Systematically Underestimate Taxic Diversity?
Early Hominin Sites Cover <2 Percent of the Land Surface of Africa, So How Likely Is It that the Observed Evidence of Taxic Diversity at Those Sites Reflects the Actual Hominin Taxic Diversity Across the Continent?
Most of the projections used in commercial atlases tend to minimize the size of Africa. It is a large continent with a land surface of just over 30 million square kilometers. The regions where there are hominin fossil sites that provide the existing evidence for hominin taxic diversity generously cover only 1–2 percent of the land surface of Africa. Depending on your view about whether early hominins were more likely to have been endemic or cosmopolitan, there is a reasonable likelihood there were more hominin species within Africa as a whole than those presently sampled at existing sites in geographically restricted regions of eastern, central, and southern Africa.
Factors Other than Actual Hominin Taxic Diversity Influence the Likelihood that Hominin Taxa Will Be Recovered from a Particular Time Interval
Not all of the periods during the existence of a species are equally likely to result in a fossil record. Some periods may be represented by erosion and not sedimentation, so even if a taxon was in existence during that time, it would not have a fossil record. Even if there is sedimentation, the surface area of exposed sediment available for prospecting may vary across the actual history of a taxon, which may partly determine whether that taxon is sampled during a particular period of its existence. These effects are referred to as “rock availability.” The amount of time spent prospecting, referred to as “collection effort,” can also influence whether a taxon is recognized at a site or in a region. Maxwell et al. (2018) recently tried to estimate the impact of rock availability and collection effort on the first and last appearances of fossil hominin taxa, and thus on taxic diversity, and they concluded that both factors very likely had a profound influence.
How Common Are Hominins on the Landscape, and How Would That Affect Estimates of Taxic Diversity?
Empirical evidence suggests that hominins were relatively rare elements within the mammal fossils collected at many sites, and this is likely to translate into them being rare elements in mammalian faunas of the past. Obtaining reliable information about the incidence of hominins in site samples is a challenge for at least three reasons. First, all fossil samples are biased in one way or another. Taphonomy is the branch of science that investigates the many factors that determine how a living animal community is converted into a much different looking fossil record. Second, at open-air sites where fossils are found on the surface of exposed sediments, the collection strategy used by the researchers will determine in large part the incidence of hominins. For example, while it is almost certain that research teams will pick up and catalog all of the hominin fossils they find, they are unlikely to do this for more common mammals, such as pigs and antelopes. Thus, the incidence of hominins in the living community will be exaggerated. The hominin site with a collection strategy that is least likely to exaggerate the frequency of hominins on the landscape (all fossil mammals are collected) is the Omo, in Ethiopia, and here hominins are estimated to make up less than 1 percent of all large mammals. Last, within the sample of fossils recovered at a site, an individual animal may be represented by just one fossil or by many skeletal or dental fragments. So, this also has to be factored in to any estimates of how common or rare hominins were in the animal communities of which they were a part. When combined with the principle that “absence of evidence is not evidence of absence,” this would all suggest that relatively small site samples of fossil mammals are unlikely to show evidence of a hominin, even if it was part of the fauna at the time. Basically, you need to find a very large number of pig and antelope (suids and bovids) fossils at a site before you can be confident there were no hominins.
Does Hard Tissue-Only Evidence Systematically Underestimate the Number of Taxa?
Taxonomic hypotheses in paleontology have to be based on evidence about the hard tissues that are preserved in the fossil record. But we know from studies of living animals that many of the visual, auditory, and odiferous signals individuals use to recognize potential mates (Paterson 1985) are unlikely to leave any trace on the skeletal and dental elements that make up the fossil record. Tattersall (1993) found very little evidence of diagnostic craniodental features among widely accepted species in the genus Lemur, and similar results were obtained for guenons (Verheyen 1962) and gibbons (Chivers and Gittins 1978). It is reasonable to assume that a hard tissue-only fossil record is likely to underestimate the number of species within any group of mammals.
The Future of Hominin Taxic Diversity
Although this article has offered several examples of proposed hominin species that may not stand the test of time, our assessment is that from at least 4.4 Ma ago, there is sound evidence of taxic diversity within the hominin clade. We also suggest that if researchers focus their efforts on looking for fossils in either hitherto unexplored locations that are <4.4 Ma or in locations in earlier time periods, then it is very likely that more taxa may be found within time intervals that already show evidence for taxic diversity, and that the early time intervals that presently show less convincing evidence will be found to have more convincing evidence of taxic diversity.
- Cartmill, Matt, and Fred H. Smith. 2009. The Human Lineage. Hoboken, NJ: Wiley-Blackwell.
- Humphrey, Louise, and Chris Stringer. 2018. Our Human Story. London: Natural History Museum.
- Roberts, Alice. 2018. Evolution: The Human Story, 2nd ed. London: Dorling Kindersley.
- Stringer, Chris, and Peter Andrews. 2012. The Complete World of Human Evolution. London: Thames and Hudson.
- Wood, Bernard. 2019. Human Evolution: A Very Short Introduction, 2nd ed. Oxford: Oxford University Press.
- Arsuaga, Juan Luis, Ignacio Martínez, Lee J. Arnold, Arantxa Aranburu, Ana Gracia-Téllez, Warren D. Sharp, Rolf M. Quam, Christophe Falgueres, A. Pantoja-Pérez, James Bischoff, Eva Poza-Rey, Josep M. Parés, José Miguel Carretero, Martina Demuro, Carlos Lorenzo, Nohemi Sala, María Martinón-Torres, Nuria García, A. Alcázar de Velasco, Gloria Cuenca-Bescós, Asier Gómez-Olivencia, Davinia Moreno, Adrián Pablos, Chuan-Chou Shen, Laura Rodríguez, Ana Isabel Ortega, Rebeca García, A. Bonmatí, José-María Bermúdez de Castro, and Eudald Carbonell. 2014. “Neandertal Roots: Cranial and Chronological Evidence from Sima de los Huesos.” Science 344: 1358–1363.
- Arsuaga, Juan Luis, Ignacio Martinez, Ana Garcia, and Carlos Lorenzo. 1997. “The Sima de los Huesos Crania (Sierra de Atapuerca, Spain): A Comparative Study.” Journal of Human Evolution 33: 219–281.
- Asfaw, Berhane, Tim White, Owen Lovejoy, Bruce Latimer, Scott Simpson, and Gen Suwa. 1999. “Australopithecus garhi: A New Species of Early Hominid from Ethiopia.” Science 284: 629–635.
- Baab, Karen. 2016. “The Place of Homo floresiensis in Human Evolution.” Journal of Anthropological Sciences 94: 1–14.
- Berger, Lee R., Darryl J. de Ruiter, Steven E. Churchill, Peter Schmid, Kristian J. Carlson, Paul H. Dirks, and Job M. Kibii. 2010. “Australopithecus sediba: A New Species of Homo-Like Australopith from South Africa.” Science 328: 195–204.
- Berger, Lee R., John Hawks, Darryl J. de Ruiter, Steven E. Churchill, Peter Schmid, Lucas K. Delezene, Tracy L. Kivell, Heather M. Garvin, Scott A. Williams, Jeremy M. DeSilva, Matthew M. Skinner, Charles M. Musiba, Noel Cameron, Trenton W. Holliday, William Harcourt-Smith, Rebecca R. Ackermann, Markus Bastir, Barry Bogin, Debra Bolter, Juliet Brophy, Zachary D. Cofran, Kimberly A. Congdon, Andrew S. Deane, Mana Dembo, Michelle Drapeau, Marina C. Elliott, Elen M. Feuerriegel, Daniel Garcia-Martinez, David J. Green, Alia Gurtov, Joel D. Irish, Ashley Kruger, Myra F. Laird, Damiano Marchi, Marc R. Meyer, Shahed Nalla, Enquye W. Negash, Caley M. Orr, Davorka Radovcic, Lauren Schroeder, Jill E. Scott, Zachary Throckmorton, Matthew W. Tocheri, Caroline VanSickle, Christopher S. Walker, Pianpian Wei, and Bernhard Zipfel. 2015. “Homo naledi: A New Species of the Genus Homo from the Dinaledi Chamber, South Africa.” eLife 4: e09560.
- Bermúdez de Castro, José-María, Juan Luis Arsuaga, Eudald Carbonell, Antonio Rosas, Ignacio Martínez, and Marina Mosquera. 1997. “A Hominid from the Lower Pleistocene of Atapuerca, Spain: Possible Ancestor to Neandertals and Modern Humans.” Science 276: 1392–1395.
- Bermudez de Castro, José María, María Martinón-Torres, Aida Gómez-Robles, Leyre Prado-Simón, Laura Martín-Francés, María Lapresa, Anthony Olejniczak, and Eudald Carbonell. 2011. “Early Pleistocene Human Mandible from Sima del Elefante (TE) Cave Site in Sierra de Atapuerca (Spain): A Comparative Morphological Study.” Journal of Human Evolution 61: 12–25.
- Black, Davidson. 1927. “On a Lower Molar Hominid Tooth from Chou-kou-tien Deposit.” Acta Palaeontologica Sinica 7: 1–28.
- Broom, Robert. 1938. “The Pleistocene Anthropoid Apes of South Africa.” Nature 142: 377–379.
- Brown, Peter. 2012. “LB1 and LB6 Homo floresiensis Are Not Modern Human (Homo sapiens) Cretins.” Journal of Human Evolution 62: 201–224.
- Brown, Peter, Thomas Sutikna, Michael J. Morwood, Raden P. Soejono, Jatmiko, E. Wayhu Saptomo, and Rokus Awe Due. 2004. “A New Small-Bodied Hominin from the Late Pleistocene of Flores, Indonesia.” Nature 431: 1055–1061.
- Brunet, Michel, Franck Guy, David Pilbeam, Daniel Lieberman, Andossa Likius, Hassane T. Mackaye, Marcia Ponce de León, Christoph Zollikofer, and Patrick Vignaud. 2005. “New Material of the Earliest Hominid from the Upper Miocene of Chad.” Nature 434: 752–755.
- Brunet, Michel, Franck Guy, David Pilbeam, Hassane Taisso Mackaye, Andossa Likius, Djimdoumalbaye Ahounta, Alain Beauvilain, Cécile Blondel, Herve´ Bocherens, Jean-Renaud Boisserie, Louis De Bonis, Yves Coppens, Jean Dejax, Christiane Denys, Philippe Duringer, Ve´ra Eisenmann, Gongdibe´ Fanone, Pierre Fronty, Denis Geraads, Thomas Lehmann, Fabrice Lihoreau, Antoine Louchart, Adoum Mahamat, Gildas Merceron, Guy Mouchelin, Olga Otero, Pablo Pelaez Campomanes, Marcia Ponce De Leon, Jean-Claude Rage, Michel Sapanet, Mathieu Schuster, Jean Sudre, Pascal Tassy, Xavier Valentin, Patrick Vignaud, Laurent Viriot, Antoine Zazzo, and Christoph Zollikofer. 2002. “A New Hominid from the Upper Miocene of Chad, Central Africa.” Nature 418: 145–151.
- Carbonell, Eudald, José M Bermúdez de Castro, Josep M. Parés, Alfredo Pérez-González, Gloria Cuenca-Bescós, Andreu Ollé, Marina Mosquera, Rosa Huguet, Jan van der Made, Antonio Rosas, Robert Sala, Josep Vallverdú, Nuria García, Darryl E. Granger, María Martinón-Torres, Xosé P. Rodríguez, Greg M. Stock, Josep M. Vergès, Ethel Allué, Francesc Burjachs, Isabel Cáceres, Antoni Canals, Alfonso Benito, Carlos Díez, Marina Lozano, Ana Mateos, Marta Navazo, Jesús Rodríguez, Jordi Rosell, and Juan L. Arsuaga. 2008. “The First Hominin of Europe.” Nature 452: 465–469.
- Carlson, Kristian J., Dietrich Stout, Tea Jashashvili, Darryl J. de Ruiter, Paul Tafforeau, Keely Carlson, and Lee R. Berger. 2011. “The Endocast of MH1, Australopithecus sediba.” Science 333: 1402–1407.
- Chen, Fahu, Frido Welker, Chuan-Chou Shen, Shara E. Bailey, Inga Bergmann, Simon Davis, Huan Xia, Hui Wang, Roman Fischer, Sarah E. Freidline, Tsai Luen Yu, Matthew M. Skinner, Stefanie Stelzer, Guangrong Dong, Qiaomei Fu, Guanghui Dong, Jian Wang, Dongju Zhang, and Jean Jacques Hublin. 2019. “A Late Middle Pleistocene Denisovan Mandible from the Tibetan Plateau.” Nature 569: 409–441.
- Chivers, David J., and S. P. Gittins. 1978. “Diagnostic Features of Gibbon Species.” International Zoo Yearbook 18: 157–164.
- Clarke, Ronald J. 2008. “Latest Information on Sterkfontein’s Australopithecus Skeleton and a New Look at Australopithecus.” South African Journal of Science 104: 443–449.
- Coqueugniot, Hélène, & Jean-Jacques Hublin. 2007. “Endocranial Volume and Brain Growth in Immature Neandertals.” Periodicum Biologorum 109: 379–385.
- Dart, Raymond. 1925. “Australopithecus africanus: The Man-Ape from South Africa.” Nature 115: 195–199.
- Dart, Raymond. 1948. “The Makapansgat Proto-Human Australopithecus prometheus.” American Journal of Physical Anthropology 6: 259–284.
- DeSilva, Jeremy, Ellison McNutt, Julien Benoit, and Bernhard Zipfel. 2018. “One Small Step: A Review of Plio-Pleistocene Hominin Foot Evolution.” American Journal of Physical Anthropology 168: 63–140.
- Détroit, Florent, Armand Salvador Mijares, Julien Corny, Guillaume Daver, Clément Zanolli, Eusebio Dizon, Emil Robles, Rainer Grün, and Philip J. Piper. 2019. “A New Species of Homo from the Late Pleistocene of the Philippines.” Nature 568: 181–186.
- Dirks, Paul H., Eric M. Roberts, Hannah Hilbert-Wolf, Jan D. Kramers, John Hawks, Anthony Dosseto, Mathieu Duval, Marina Elliott, Mary Evans, Rainer Grün, John Hellstrom, Andy I. Herries, Renaud Joannes-Boyau, Tebogo V. Makhubela, Christa J. Placzek, Jessie Robbins, Carl Spandler, Jelle Wiersma, Jon Woodhead, and Lee R. Berger. 2017. “The Age of Homo naledi and Associated Sediments in the Rising Star Cave, South Africa.” eLife 6: e24231.
- Douka, Katerina, Viviane Slon, Zenobia Jacobs, Christopher Bronk Ramsey, Michael V. Shunkov, Anatoly P. Derevianko, Fabrizio Mafessoni, Maxim B. Kozlikin, Bo Li, Rainer Grün, Daniel Comeskey, Thibaut Devièse, Samantha Brown, Bence Viola, Leslie Kinsley, Michael Buckley, Matthias Meyer, Richard G. Roberts, Svante Pääbo, Janet Kelso, and Tom Higham. 2019. “Age Estimates for Hominin Fossils and the Onset of the Upper Palaeolithic at Denisova Cave.” Nature 565: 640–644.
- Dreyer, Thomas F. 1935. “A Human Skull from Florisbad, Orange Free State, with a Note on the Endocranial Cast, by C. U. Ariëns Kappers.” Proceedings of the Royal Academy of Sciences at Amsterdam 38: 119–128.
- Dubois, Eugene. 1893. “Palaeontologische onderzoekingen op Java.” Versl Mijnwez Batavia 10: 10–14.
- Foote, Mike, and David M. Raup. 1996. “Fossil Preservation and the Stratigraphic Ranges of Taxa.” Paleobiology 22: 121–140.
- Gabounia, Léo, Marie-Antoinette de Lumley, Abesalom Vekua, David Lordkipanidze, and Henry de Lumley. 2002. “Découverte d’un nouvel hominidé à Dmanissi (Transcaucasie, Géorgie).” Comptes Rendus Palevol 1: 243–253.
- Gómez-Robles, Aida. 2019. “Dental Evolutionary Rates and Its Implications for the Neanderthal–Modern Human Divergence.” Science Advances 5: eaaw1268.
- Gómez-Robles, Aida, José María Bermúdez de Castro, María Martinón-Torres, Leyre Prado-Simón, and Juan Luis Arsuaga. 2015. “A Geometric Morphometric Analysis of Hominin Lower Molars: Evolutionary Implications and Overview of Postcanine Dental Variation.” Journal of Human Evolution 82: 34–50.
- Granger, Darryl E., Ryan J. Gibbon, Kathleen Kuman, Ronald J. Clarke, Laurent Bruxelles, and Marc W. Caffee. 2015. “New Cosmogenic Burial Ages for Sterkfontein Member 2 Australopithecus and Member 5 Oldowan.” Nature 522: 85–88.
- Grine, Frederick E., Meave G. Leakey, Patrick N. Gathogo, Frank H. Brown, Carrie S. Mongle, Deming Yang, William L. Jungers, and Louise N. Leakey. 2019. “Complete Permanent Mandibular Dentition of Early Homo from the Upper Burgi Member of the Koobi Fora Formation, Ileret, Kenya.” Journal of Human Evolution 131: 152–175.
- Le Gros Clark, Wilfrid E. 1964. The Fossil Evidence for Human Evolution: An Introduction to the Study of Palaeoanthropology, 2nd ed. Chicago: University of Chicago Press.
- Groves, Colin P. 1989. A Theory of Human and Primate Evolution. Oxford: Clarendon Press.
- Groves, Colin P., and Vratislav Mazák. 1975. “An Approach to the Taxonomy of the Hominidae: Gracile Villafranchian Hominids of Africa.” Casopis pro Mineralogii a Geologii 20: 225–247.
- Gunz, Philipp, Simon Neubauer, Bruno Maureille, and Jean-Jacques Hublin. 2010. “Brain Development After Birth Differs between Neanderthals and Modern Humans.” Current Biology 20 (21): R921–922.
- Guy, Franck, Daniel Lieberman, David Pilbeam, Marcia Ponce de León, Andossa Likius, Hassane T. Mackaye, Patrick Vignaud, Christoph Zollikofer, and Michel Brunet. 2005. “Morphological Affinities of the Sahelanthropus tchadensis (Late Miocene Hominid from Chad) Cranium.” Proceedings of the National Academy of Sciences of the United States of America 102: 18836–18841.
- Guy, Franck, Hassane-Taïsso Mackaye, Andossa Likius, Patrick Vignaud, Matthieu Schmittbuhl, and Michel Brunet. 2008. “Symphyseal Shape Variation in Extant and Fossil Hominoids, and the Symphysis of Australopithecus bahrelghazali.” Journal of Human Evolution 55: 37–47.
- Haile-Selassie, Yohannes, Luis Gibert, Stephanie M. Melillo, Timothy M. Ryan, Mulugeta Alene, Alan Deino, Naomi E. Levin, and Beverly Z. Saylor. 2015. “New Species from Ethiopia Further Expands Middle Pliocene Hominin Diversity.” Nature 521: 483–488.
- Haile-Selassie, Yohannes, Beverly Saylor, Alan Deino, Mulugeta Alene, and Bruce Latimer. 2010. “New Hominid Fossils from Woranso-Mille (Central Afar, Ethiopia) and Taxonomy of Early Australopithecus.” American Journal of Physical Anthropology 141: 406–417.
- Haile-Selassie, Yohannes, Beverly Saylor, Alan Deino, Naomi E. Levin, Mulugeta Alene, and Bruce M. Latimer. 2012. “A New Hominin Foot from Ethiopia Shows Multiple Pliocene Bipedal Adaptations.” Nature 483: 565–569.
- Haile-Selassie, Yohannes, Gen Suwa, and Tim White. 2004. “Late Miocene Teeth from Middle Awash, Ethiopia, and Early Hominid Dental Evolution.” Science 303: 1503–1505.
- Haile-Selassie, Yohannes, Gen Suwa, and Tim White. 2009. “Hominidae.” In Ardipithecus kadabba Late Miocene Evidence from the Middle Awash Ethiopia, edited by Yohannes Haile-Selassie and Giday WoldeGabriel, 159–236. Berkeley, CA: University of California Press.
- Harcourt-Smith, William E. H., Zachary Throckmorton, Kimberly A. Congdon, Bernhard Zipfel, Andrew S. Deane, Michèle S. M. Drapeau, Steven E. Churchill, Lee R. Berger, and Jeremy M. DeSilva. 2015. “The Foot of Homo naledi.” Nature Communications 6: 8432.
- Hublin, Jean-Jacques. 2009. “The Origin of Neandertals.” Proceedings of the National Academy of Sciences of the United States of America 106: 16022–16027.
- Hublin, Jean-Jacques, Abdelouahed Ben-Ncer, Shara E. Bailey, Sarah E. Freidline, Simon Neubauer, Matthew M. Skinner, Inga Bergmann, Adeline Le Cabec, Stefano Benazzi, Katerina Harvati, and Philipp Gunz. 2017. “New Fossils from Jebel Irhoud, Morocco and the Pan-African Origin of Homo sapiens.” Nature 546: 289–292.
- Jacobs, Zenobia, Bo Li, Michael V. Shunkov, Maxim B. Kozlikin, Nataliya S. Bolikhovskaya, Alexander K. Agadjanian, Vladimir A. Uliyanov, Sergei K. Vasiliev, Kieran O’Gorman, Anatoly P. Derevianko, and Richard G. Roberts. 2019. “Timing of Archaic Hominin Occupation of Denisova Cave in Southern Siberia.” Nature 565: 594–599.
- Kaifu, Yousuke, Fachroel Aziz, Etty Indriati, Teuku Jacob, Iwan Kurniawan, and Hisao Baba. 2008. “Cranial Morphology of Javanese Homo erectus: New Evidence for Continuous Evolution, Specialization, and Terminal Extinction.” Journal of Human Evolution 55: 551–580.
- Kimbel, William H., Charles A. Lockwood, Carol V. Ward, Meave G. Leakey, Yoel Rak, and Donald C. Johanson. 2006. “Was Australopithecus anamensis Ancestral to A. afarensis? A Case of Anagenesis in the Hominin Fossil Record.” Journal of Human Evolution 51: 134–152.
- King, William. 1864. “The Reputed Fossil Man of the Neanderthal.” Quarterly Journal of Science 1: 88–97.
- Kivell, Tracy L., Andrew S. Deane, Matthew W. Tocheri, Caley M. Orr, Peter Schmid, John Hawks, Lee R. Berger, and Steven E. Churchill. 2015. “The Hand of Homo naledi.” Nature Communications 6: 8431.
- Kivell, Tracy L., Job M. Kibii, Steven E. Churchill, Peter Schmid, and Lee R. Berger. 2011. “Australopithecus sediba Hand Demonstrates Mosaic Evolution of Locomotor and Manipulative Abilities.” Science 333: 1411–1417.
- von Koenigswald, Gustav Heinrich, and Franz Weidenreich. 1939. “The Relationship between Pithecanthropus and Sinanthropus.” Nature 144: 926–929.
- Krause, Johannes, Qiaomei Fu, Jeffrey M. Good, Bence Viola, Michael V. Shunkov, Anatoli P. Derevianko, and Svante Pääbo. 2010. “The Complete Mitochondrial DNA Genome of an Unknown Hominin from Southern Siberia.” Nature 464: 894–897.
- Leakey, Louis S. B. 1959. “A New Fossil Skull from Olduvai.” Nature 184: 491–493.
- Leakey, Louis S. B., Phillip V. Tobias, and John Russell Napier. 1964. “A New Species of the Genus Homo from Olduvai Gorge.” Nature 202: 7–9.
- Leakey, Meave G., Craig S. Feibel, Ian McDougall, and Alan Walker. 1995. “New Four-Million-Year-Old Hominid Species from Kanapoi and Allia Bay, Kenya.” Nature 376: 565–571.
- Leakey, Meave G., Fred Spoor, Frank H. Brown, Patrick N. Gathogo, Christopher Kiarie, Louise N. Leakey, and Ian McDougall. 2001. “New Hominin Genus from Eastern Africa Shows Diverse Middle Pliocene Lineages.” Nature 410: 433–440.
- Leakey, Meave G., Fred Spoor, M. Christopher Dean, Craig S. Feibel, Susan C. Antón, Christopher Kiarie, and Louise N. Leakey. 2012. “New Fossils from Koobi Fora in Northern Kenya Confirm Taxonomic Diversity in Early Homo.” Nature 488: 201–204.
- Leakey, Richard E. F., and Alan Walker. 1976. “Australopithecus, Homo erectus and the Single Species Hypothesis.” Nature 261: 572–574.
- Li, Zhan-Yang, Xiu-Jie Wu, Li-Ping Zhou, Wu Liu, Xing Gao, Xiao-Mei Nian, and Erik Trinkaus. 2017. “Late Pleistocene Archaic Human Crania from Xuchang, China.” Science 355: 969–972.
- Linnaeus, Carl. 1758. Systema Naturae. Stockhom: Laurentii Salvii.
- Lockwood, Charles A., and Phillip V. Tobias. 2002. “Morphology and Affinities of New Hominin Cranial Remains from Member 4 of the Sterkfontein Formation, Gauteng Province, South Africa.” Journal of Human Evolution 42: 389–450.
- Lordkipanidze, David, Marcia Ponce de León, Ann Margvelashvili, Yoel Rak, G. Philip Rightmire, Abesalom Vekua, and Christoph P. Zollikofer. 2013. “A Complete Skull from Dmanisi, Georgia, and the Evolutionary Biology of Early Homo.” Science 342: 326–331.
- Manzi, Giorgio, Francesco Mallegni, and Antonio Ascenzi. 2001. “A Cranium for the Earliest Europeans: Phylogenetic Position of the Hominid from Ceprano, Italy.” Proceedings of the National Academy of Sciences of the United States of America 98: 10011–10016.
- Maxwell, Simon J., Philip J. Hopley, Paul Upchurch, and Christophe Soligo. 2018. “Sporadic Sampling, Not Climatic Forcing, Drives Observed Early Hominin Diversity.” Proceedings of the National Academy of Sciences of the United States of America 115 (19): 4891–4896.
- Mayr, Ernst. 1944. “On the Concepts and Terminology of Vertical Subspecies and Species.” Common Problems of Genetics, Paleontology and Systematics Bulletin 2: 11–16.
- Meyer, Matthias, Juan-Luis Arsuaga, Cesare de Filippo, Sarah Nagel, Ayinuer Aximu-Petri, Birgit Nickel, Ignacio Martínez, Ana Gracia, José María Bermúdez de Castro, Eudald Carbonell, Bence Viola, Janet Kelso, Kay Prüfer, and Svante Pääbo. 2016. “Nuclear DNA Sequences from the Middle Pleistocene Sima de los Huesos Hominins.” Nature 531: 504–507.
- Meyer, Matthias, Qiaomei Fu, Ayinuer Aximu-Petri, Isabelle Glocke, Birgit Nickel, Juan-Luis Arsuaga, Ignacio Martínez, Ana Gracia, José María de Castro, Eudald Carbonell, and Svante Pääbo. 2014. “A Mitochondrial Genome Sequence of a Hominin from Sima de los Huesos.” Nature 505: 403–406.
- Meyer, Matthias, Martin Kircher, Marie-Theres Gansauge, Heng Li, Fernando Racimo, Swapan Mallick, Joshua G. Schraiber, Flora Jay, Kay Prüfer, Cesare de Filippo, Peter H. Sudmant, Can Alkan, Qiaomei Fu, Ron Do, Nadin Rohland, Arti Tandon, Michael Siebauer, Richard E. Green, Katarzyna Bryc, Adrian W. Briggs, Udo Stenzel, Jesse Dabney, Jay Shendure, Jacob Kitzman, Michael F. Hammer, Michael V. Shunkov, Anatoli P. Derevianko, Nick Patterson, Aida M. Andrés, Evan E. Eichler, Montgomery Slatkin, David Reich, Janet Kelso, and Svante Pääbo. 2015. “A High-Coverage Genome Sequence from an Archaic Denisovan Individual.” Science 338: 222–226.
- Morwood, Michael J., Peter Brown, Jatmiko, T. Sutikna, E. Wahyu Saptomo, Kira E. Westaway, Rokus Awe Due, Richard G. Roberts, Toshinari Maeda, Sri Wasisto, and T. Djubiantono. 2005. “Further Evidence for Small-Bodied Hominins from the Late Pleistocene of Flores, Indonesia. Nature 437: 1012–1017.
- Morwood, Michael J., and William L. Jungers. 2009. “Conclusions: Implications of the Liang Bua Excavations for Hominin Evolution and Biogeography.” Journal of Human Evolution 57: 640–648.
- Mounier, Aurélien, François Marchal, and Silvana Condemi. 2009. “Is Homo heidelbergensis a Distinct Species? New Insight on the Mauer Mandible.” Journal of Human Evolution 56: 219–246.
- Nelson, Andrew J., and Jennifer L. Thompson. 2005. “Le Moustier 1 and the Interpretation of Stages in Neandertal Growth and Development.” In The Neandertal Adolescent Le Moustier, edited by Hannes Ullrich, 328–338. Staatliche Museen zu Berlin, Berlin.
- Obendorf, Peter J., Charles E. Oxnard, and Ben J. Kefford. 2008. “Are the Small Human-like Fossils Found on Flores Human Endemic Cretins?” Proceedings of the Royal Society B 275: 1287–1296.
- Partridge, Tim C., Darryl E. Granger, Mark W. Caffee, and Ronald J. Clarke. 2003. “Lower Pliocene Hominid Remains from Sterkfontein.” Science 300: 607–612.
- Paterson, Hugh E. H. 1985. “The Recognition Concept of Species.” In Species and Speciation, edited by Elisabeth Vrba. Pretoria, South Africa: Transvaal Museum Monograph No. 4.
- Patterson, Nick, Priya Moorjani, Yontao Luo, Swapan Mallick, Nadin Rohland, Yiping Zhan, Teri Genschoreck, Teresa Webster, and Devid Reich. 2012. “Ancient Admixture in Human History.” Genetics 192: 1065–1093.
- Pilbrow, Varsha. 2010. “Dental and Phylogeographic Patterns of Variation in Gorillas.” Journal of Human Evolution 59: 16–34.
- Ponce de León, Marcia S., Lubov Golovanova, Vladimir Doronichev, Galina Romanova, Takeru Akazawa, Osamu Kondo, Hajime Ishida, and Christoph P. Zollikofer. 2008. “Neanderthal Brain Size at Birth Provides Insights into the Evolution of Human Life History.” Proceedings of the National Academy of Sciences of the United States of America 105: 13764–13768.
- Prüfer, Kay, Fernando Racimo, Nick Patterson, Flora Jay, Sriram Sankararaman, Susanna Sawyer, Anja Heinze, Gabriel Renaud, Peter H. Sudmant, Cesare de Filippo, Heng Li, Swapan Mallick, Michael Dannemann, Qiaomei Fu, Martin Kircher, Martin Kuhlwilm, Michael Lachmann, Matthias Meyer, Matthias Ongyerth, Michael Siebauer, Christoph Theunert, Arti Tandon, Priya Moorjani, Joseph Pickrell, James C. Mullikin, Samuel H. Vohr, Richard E. Green, Ines Hellmann, Philip L. Johnson, Hélène Blanche, Howard Cann, Jacob O. Kitzman, Jay Shendure, Evan E. Eichler, Ed S. Lein, Trygve E. Bakken, Liubov V. Golovanova, Vladimir B. Doronichev, Michael V. Shunkov, Anatoli P. Derevianko, Bence Viola, Montgomery Slatkin, David Reich, Janet Kelso, and Svante Pääbo. 2014. “The Complete Genome Sequence of a Neanderthal from the Altai Mountains.” Nature 505: 43–49.
- Reich, David, Nick Patterson, Martin Kircher, Frederick Delfin, Madhusudan R. Nandineni, Irina Pugach, Albert Min-Shan Ko, Ying-Chin Ko, Timothy A. Jinam, Maude E. Phipps, Naruya Saitou, Andreas Wollstein, Manfred Kayser, Svante Pääbo, and Mark Stoneking. 2011. “Denisova Admixture and the First Modern Human Dispersals into Southeast Asia and Oceania.” American Journal of Human Genetics 89: 1–13.
- Rightmire, G. Philip. 1995. “Geography, Time and Speciation in Pleistocene Homo.” South African Journal of Science 91: 450–454.
- Robinson, John T. 1960. “The Affinities of the New Olduvai Australopithecine.” Nature 186: 456–458.
- Robinson, John T. 1961. “The Australopithecines and Their Bearing on the Origin of Man and of Stone Tool-Making.” South African Journal of Science 57: 3–13.
- Sawyer, Susanna, Gabriel Renaud, Bence Viola, Jean-Jacques Hublin, Marie-Theres Gansauge, Michael V. Shunkov, Anatoly P. Derevianko, Kay Prüfer, Janet Kelso, and Svante Pääbo. 2015. “Nuclear and Mitochondrial DNA Sequences from Two Denisovan Individuals.” Proceedings of the National Academy of Sciences of the United States of America 112 (51): 15696–15700.
- Schoetensack, Otto. 1908. Der Unterkiefer des Homo heidelbergensis aus den Sanden von Mauer bei Heidelberg. Leipzig: W. Engelmann.
- Senut, Brigitte, Martin Pickford, Dominique Gommery, Pierre Mein, Kiptalam Cheboi, and Yves Coppens. 2001. “First Hominid from the Miocene (Lukeino Formation, Kenya).” Comptes Rendus Académie Science 332: 137–144.
- Slon, Viviane, Susanna Sawyer, Gabriel Renaud, Bence Viola, Jean-Jacques Hublin, Marie-Theres Gansauge, Michael V. Shunkov, Anatoly P. Derevianko, Matthias Meyer, Kay Prüfer, J. Kelso, and Svante Pääbo. 2015. “Genetic Analysis of Three Denisovan Individuals from Altai Mountains (Siberia).” Proceedings of the European Society for the Study of Human Evolution 4: 207.
- Smith, Richard J. 2005. “Species Recognition in Paleoanthropology: Implications of Small Sample Sizes.” In Interpreting the Past: Essays on Human, Primate, and Mammal Evolution in Honor of David Pilbeam, edited by Daniel E. Lieberman, Richard J. Smith, and Jay Kelley, 207–219. Boston: Brill Academic.
- Smith, Tanya M., Paul Tafforeau, Donald J. Reid, Joane Pouech, Vincent Lazzari, John P. Zermeno, Debbie Guatelli-Steinberg, Anthony J. Olejniczak, Almut Hoffman, Jakov Radovčić, Masrour Makaremi, Michel Toussaint, Chris Stringer, and Jean-Jacques Hublin. 2010. “Dental Evidence for Ontogenetic Differences between Modern Humans and Neanderthals.” Proceedings of the National Academy of Sciences of the United States of America 107: 20923–20928.
- Spoor, Fred, Philipp Gunz, Simon Neubauer, Stefanie Stelzer, Nadia Scott, Amandus Kwekason, and M. Christopher Dean. 2015. “Reconstructed Homo habilis Type OH 7 Suggests Deep-Rooted Species Diversity in Early Homo.” Nature 519: 83–86.
- Spoor, Fred, Meave G. Leakey, Patrick N. Gathogo, Frank H. Brown, Susan Anton, Ian McDougall, Christopher Kiarie, Frederick K. Manthi, and Louise N. Leakey. 2007. “Implications of New Early Homo Fossils from Ileret, East of Lake Turkana, Kenya.” Nature 448: 688–691.
- Spoor, Fred, Meave G. Leakey, and Louise N. Leakey. 2010. “Hominin Diversity in the Middle Pliocene of Eastern Africa: The Maxilla of KNM-WT 40000.” Philosophical Transactions of the Royal Society B 365: 3377–3388.
- Suwa, Gen. 1988. “Evolution of the ‘Robust’ Australopithecines in the Omo Succession: Evidence from Mandibular Premolar Morphology.” In Evolutionary History of the “Robust” Australopithecines, edited by Frederick E. Grine, 199–222. New York: Aldine de Gruyter.
- Suwa, Gen, Berhane Asfaw, Yonas Beyene, Tim White, Shigehiro Katoh, Shinji Nagaoka, Hideo Nakaya, Kazuhiro Uzawa, Paul Renne, and Giday WoldeGabriel. 1997. “The First Skull of Australopithecus boisei.” Nature 389: 489–492.
- Suwa, Gen, Reiko T. Kono, Scott W. Simpson, Berhane Asfaw, C. Owen Lovejoy, and Tim D. White. 2009. “Paleobiological Implications of the Ardipithecus ramidus Dentition.” Science 326: 69–99.
- Tattersall, Ian. 1993. “Speciation and Morphological Differentiation in the Genus Lemur.” In Species, Species Concepts and Primate Evolution, edited by William H. Kimbel and Lawrence Martin, 163–176. New York: Plenum Press.
- Tillier, Anne-marie. 1982. “Les enfants néanderthaliens de Devil’s Tower (Gibraltar).” Zeitschrift für Morphologie und Anthropologie 73: 125–148.
- Uchida, Akiko. 2004. Craniodental Variation Among the Great Apes. Cambridge, MA: Harvard University Press.
- Valentine, James W. 1989. “How Good Was the Fossil Record? Clues from the Californian Pleistocene.” Paleobiology 15: 83–94.
- Vannucci, Robert C., Todd F. Barron, and Ralph L. Holloway. 2011. “Craniometric Ratios of Microcephaly and LB1, Homo floresiensis, Using MRI and Endocasts.” Proceedings of the National Academy of Sciences of the United States of America 108: 14043–14048.
- Verheyen, Walter N. 1962. Contribution a la Craniologie Comparee des Primates. Les Genres Colobus Illiger 1811 et Cercopithecus Linne 1758. Tervuren, Belgium: Musee Royal de l’Afrique Centrale.
- Villmoare, Brian, William H. Kimbel, Chalachew Seyoum, Christopher J. Campisano, Erin N. DiMaggio, John Rowan, David R. Braun, J. Ramón Arrowsmith, and Kaye E. Reed. 2015. “Early Homo at 2.8 Ma from Ledi-Geraru, Afar, Ethiopia.” Science 347: 1352–1355.
- Ward, Carol, William H. Kimbel, and Donald C. Johanson. 2011. “Complete Fourth Metatarsal and Arches in the Foot of Australopithecus afarensis.” Science 331: 750–753.
- Ward, Carol, Meave G. Leakey, and Alan Walker. 1999. “The New Hominid Species Australopithecus anamensis.” Evolutionary Anthropology 7: 197–205.
- Weidenreich, Franz. 1940. “Some Problems Dealing with Ancient Man.” American Anthropology 42: 375–383.
- White, Tim. 2003. “Early Hominids—Diversity or Distortion?” Science 299: 1994–1997.
- White, Tim, Berhane Asfaw, Yonas Beyene, Yohannes Haile-Selassie, Owen Lovejoy, Gen Suwa, and Giday WoldeGabriel. 2009. “Ardipithecus ramidus and the Paleobiology of Early Hominids.” Science 326: 64–86.
- Widianto, Harry, and Valery Zeitoun. 2003. “Morphological Description, Biometry and Phylogenetic Position of the Skull of Ngawi 1 (East Java, Indonesia).” International Journal of Osteoarchaeology 13: 339–351.
- Witmer, Lawrence M. 1995. “The Extant Phylogenetic Bracket and the Importance of Reconstructing Soft Tissues in Fossils.” In Functional Morphology in Vertebrate Paleontology, edited by Jeff J. Thomason, 19–33. Cambridge, UK: Cambridge University Press.
- Wood, Bernard A. 1974. “Olduvai Bed I Post-Cranial Fossils: A Reassessment.” Journal of Human Evolution 3: 373–378.
- Wood, Bernard A. 1984. “The Origins of Homo erectus.” Courier Forschungsinstitut Senckenberg 69: 99–111.
- Wood, Bernard A. 1991. Koobi Fora Research Project. Vol. 4. Hominid Cranial Remains. Oxford: Clarendon Press.
- Wood, Bernard A. 1994. “Taxonomy and Evolutionary Relationship of Homo erectus.” Courier Forschungsinstitut Senckenberg 171: 159–165.
- Wood, Bernard A., and Eve K. Boyle. 2016. “Hominin Taxic Diversity: Fact or Fantasy?” American Journal of Physical Anthropology 159: 37–78.
- Wood, Bernard A., and Paul Constantino. 2007. “Paranthropus boisei: Fifty Years of Evidence and Analysis.” Yearbook of Physical Anthropology 50: 106–132.
- Woodward, Arthur Smith. 1921. “A New Cave Man from Rhodesia, South Africa.” Nature 108: 371–372.
- Zanolli, Clément, Ottmar Kullme, Jay Kelley, Anne-Marie Bacon, Fabrice Demeter, Jean Dumoncel, Luca Fiorenza, Frederick E. Grine, Jean-Jacques Hublin, Anh Tuan Nguyen, Thi Mai Huong Nguyen, Lei Pan, Burkhard Schillinger, Friedemann Schrenk, Matthew M. Skinner, Xueping Ji, and Roberto Macchiarelli. 2019. “Evidence for Increased Hominid Diversity in the Early to Middle Pleistocene of Indonesia.” Nature Ecology & Evolution 3: 755–764.
- Zipfel, Bernhard, Jeremy M. DeSilva, Robert S. Kidd, Kristian J. Carlson, Steven E. Churchill, and Lee R. Berger. 2011. “The Foot and Ankle of Australopithecus sediba.” Science 333: 1417–1420.
- Zollikofer, Christoph P. E., Marcia S. Ponce de León, Daniel E. Lieberman, Franck Guy, David Pilbeam, Andossa Likius, Hassane T. Mackaye, Patrick Vignaud, and Michel Brunet. 2005. “Virtual Cranial Reconstruction of Sahelanthropus tchadensis.” Nature 434: 755–759.