Hominins and the Emergence of the Modern Human Brain

CHAPTER 14

Hominins and the emergence of the modern human brain

Alexandra de Sousa* and Eugénia Cunha

Department of Life Sciences, Forensic Sciences Center, University of Coimbra, Coimbra, Portugal

Abstract: Evidence used to reconstruct the morphology and function of the brain (and the rest of the central nervous system) in fossil hominin species comes from the fossil and archeological records. Although the details provided about human brain evolution are scarce, they benefit from interpretations informed by interspecific comparative studies and, in particular, human pathology studies. In recent years, new information has come to light about fossil DNA and ontogenetic trajectories, for which pathology research has significant implications. We briefly describe and summarize data from the paleoarcheological and paleoneurological records about the evolution of fossil hominin brains, including behavioral data most relevant to brain research. These findings are brought together to characterize fossil hominin taxa in terms of brain structure and function and to summarize brain evolution in the human lineage.

Keywords: evolution; endocast; fossil hominin; paleoneurology; cognition; paleoarcheology.

Introduction progress in archeology, ancient DNA, and life history. The combination of paleoneurological, A major obstacle to understanding the evolution paleoarcheological, paleogenetic, and ontogenetic of the human brain is that it is a soft tissue evidence, informed by comparative studies and not directly preserved in the fossil record, pathology research, is reviewed here to recon- although information about its size and shape is struct the evolution of the human brain. preserved in natural endocasts and fossilized “Hominins” include extant humans (herewith neurocrania. Recent insights have come from referred to as “humans” or “recent anatomically modern Homo sapiens—rAMHS”) and all extinct species that are more closely related to humans than to any other living taxon; “Panins” include *Corresponding author. chimpanzees, bonobos, and all fossil species more E-mail: [email protected] closely related to them than to humans. The

DOI: 10.1016/B978-0-444-53860-4.00014-3 293 294 hominin clade dates back to the most recent com- Although humans are more closely related to mon ancestor (MRCA) of humans, chimpanzees, panins than to any other living animals, it is usual and bonobos, via the appearance of the first to compare them to the “apes,” a group defined hominins ca. 8–4Ma. Anatomically modern Homo on the basis of behavioral and anatomical sapiens (AMHS), encompassing both fossil similarities. Apes include the great apes (panins (fAMHS) and recent (rAMHS) members, and gorillas in Africa, orangutans in Asia) and emerged from this clade a little over 190ka the lesser apes (gibbons). Apes and humans (McDougall et al., 2005). The emergence of the together comprise the “hominoids.” human brain is reviewed here with respect to differ- Panins (especially chimpanzees) are used as a ent hominin taxa, based on a speciose taxonomy proxy for the ancestral hominin state, unless indi- (Table 1), as described previously (de Sousa and cated otherwise. In order to determine whether a Wood, 2007; see also Wood and Lonergan, 2008). feature is “primitive” or “derived” within the Interpretations of fossil hominin brain structure hominin clade, it is necessary to consider the brain and function benefit from ongoing comparative morphology of the hominin–panin MRCA, which and pathology studies. Comparative samples are would have possessed all shared derived features used to determine interspecific trends, for exam- of extant humans, chimpanzees, and bonobos but ple, to estimate the degree of encephalization. would lack those features acquired solely along Comparisons between living species improve our either the panin or the hominin lineages. It is partic- understanding of how the brain works and indi- ularly difficult to reconstruct the brain of the cate any unique attributes of the human brain. hominin–panin MRCA because a panin fossil

Table 1. Approximate date ranges for fossil hominin species, which are defined according to both speciose and short taxonomies

Speciose taxonomy Short taxonomy Approximate date range

Possible hominins Sahelanthropus tchadensis Ardipithecus ramidus s.l. 7Ma Orrorin tugenensis Ardipithecus ramidus s.l. 6Ma Ardipithecus kadabba Ardipithecus ramidus s.l. 5.8–5.2Ma Ardipithecus ramidus Ardipithecus ramidus s.l. 4.5–4.3Ma Archaic hominins Australopithecus anamensis Australopithecus afarensis s.l. 4.2–3.9Ma Australopithecus afarensis Australopithecus afarensis s.l. 3.7–3Ma Australopithecus bahrelghazali Australopithecus afarensis s.l. 3.5–3.0Ma Kenyanthropus platyops Kenyanthropus platyops 3.5–3.3Ma Australopithecus africanus Australopithecus africanus 3–2.4Ma Australopithecus sediba Australopithecus sediba 1.95Ma Megadont archaic hominins Australopithecus garhi Australopithecus garhi 2.5Ma Paranthropus aethiopicus Paranthropus boisei s.l. 2.5–2.3Ma Paranthropus boisei s.s. Paranthropus boisei s.l. 2.3–1.4Ma Paranthropus robustus Paranthropus robustus 2.0–1.5Ma Transitional hominins Homo habilis s.s. Homo habilis s.l. 2.4–1.4Ma Homo rudolfensis Homo habilis s.l. 2.4–1.6Ma Premodern Homo Homo erectus s.s. Homo erectus s.l. 1.9–1.5Ma Homo ergaster Homo erectus s.l. 1.8Ma–30ka Homo antecessor Homo antecessor 780–500ka Homo heidelbergensis Homo sapiens s.l. 600–100ka Homo neanderthalensis Homo sapiens s.l. 200–28ka Homo floresiensis Homo floresiensis 74–17ka Anatomically modern Homo Homo sapiens s.s. Homo sapiens s.l. 195ka–present

Note: s.s., sensu stricto; s.l., sensu lato. 295 record was completely unknown until recently which now bears his name (Dronkers et al., 2007). (McBrearty and Jablonski, 2005). So, for practical Similarly, human pathologies are increasingly purposes, the brains and behaviors of panins are attributed to genetic causes, such as mutations in assumed to be equivalent to those primitive for gene sequences, or changes in gene copy number. hominins. Pathologies which interrupt the function of Traveling from past to present in the hominin human-specific behaviors have drawn special fossil record, species appear which are increasingly attention in brain evolution research. Microceph- related to humans (although there exists evidence aly and the severe speech and language disorder for at least one other major hominin lineage, the of the KE family highlight mechanisms which may megadont archaic hominins). Hominins which are be responsible for human-specific brain structure phylogenetically closest to humans are presumably and function, and the possibility that these less panin-like and more humanlike. For this rea- pathologies are atavisms has been discussed son, intraspecific comparisons, usually between (Fisher and Marcus, 2006; Jackson et al., 2002). clinical cases and neurotypical humans, are used Autism, a neurodevelopmental disorder to assess variation at low taxonomic levels. characterized by impaired social interaction for which a clinical definition is ongoing (Charman et al., 2010; Happe et al., 2006), is referenced in stud- Pathology’s contributions to brain ies of fossil hominin brain structure and function, evolution research either as an analogy for developmental differences between closely related species or as a potentially Pathology (here defined broadly to include the study atavistic indication of actual primitive phenotypes. of all clinically abnormal conditions including For example, an autistic child lacking language cre- injuries, disabilities, disorders, syndromes, and ated naturalistic artwork much like that from the infections) has enlightened our understanding of Upper Paleolithic, on the basis of which it was hominin brain evolution in two major ways. First, suggested that fAMHS could have also lacked fully pathologies highlight human biological mechanisms. modern cognition (Humphrey, 1998). Second, an understanding of the anatomical (and behavioral) manifestations of pathologies is necessary for correctly interpreting the fossil (and arche- Recognizing pathology in fossils ological) record. These major categories of contributions are described here, and further Pathology has always had a role in paleoanthropol- examples of how pathologies play into ogy. At the time of the first acknowledgment of a fos- interpretations of fossil hominin brains can be found sil hominin species, H. neanderthalensis,the elsewhere in this chapter. prominent pathologist Rudolf Virchow wrote off the distinct anatomy as features of aging, arthritis, fracture, and rickets (Cartmill and Smith, 2009). Pathologies mark neural and genetic mechanisms Virchow’s interpretation was quashed after additional specimens were found to show the same dis- Pathological studies have made significant con- tinct morphology. Pathological explanations tributions to neuroscience. Early brain mapping continue to be put forward for H. neanderthalensis, was conducted by associating behavioral deficits including vitamin D deficiency (Ivanhoe, 1970)and to regions of physical brain damage. For example, cretinism (Dobson, 1998), although these Paul Broca found that two stroke patients who hypotheses are not generally accepted. had lost speech ability both had damage to the pos- Most recently, a scatter of pathologies have been terior inferior frontal gyrus at autopsy, a region proposed to describe the morphology of H. 296 floresiensis, including Laron syndrome (Hershkovitz trauma, and pathology (Bonmati et al., 2010; Gracia et al., 2007), cretinism (Obendorf et al., 2008; et al., 2011) have been interpreted as evidence of Oxnard et al., 2010), and microcephaly and dwarfism humanlike social and cognitive capacities (Spikins (Martin et al., 2006), or microcephaly in a pygmoid et al., 2010). population (Jacob et al., 2006). All these have sub- sequently been addressed (Falk et al., 2007, 2009a, b; Jungers et al., 2009). There is much yet to glean Fossil hominin brain size from the discovery of H. floresiensis, a species which has quickly achieved a special position in neurosci- Human mean adult’s (21- to 39-year-old) brain ence and paleoanthropology through its challenge weight is 1450g for males and 1290g for females to prevailing notions about brain size, organization, (Fig. 1; Table 2)(Dekaban and Sadowsky, 1978). and function (Cunha and Silva, 2005). The interpre- Chimpanzee mean adolescent and young adult tation of H. floresiensis faces similar challenges as (7–30 years) brain weight is 406g for males and 368 with H. neanderthalensis, although it is further com- g for females (Herndon et al., 1999). It is expected plicated by the poor preservation of skeletal mate- that the averages used here are higher than in other rial and DNA on a tropical island. Identifying autopsy samples, which include a majority of pathology also has direct implications for assessing individuals with advanced age. In both species, brain behavior. Specimens of H. neanderthalensis and weight decreases in older adults (Resnick et al., Homo heidelbergensis showing advanced age, 2003), for example, Dekaban and Sadowsky (1978)

1750 1650 1550 1450 1350 1250 1150 1050 950 850 Brain mass (g) Brain 750 650 550 450 350 250 7.00 6.00 5.00 4.00 3.00 2.00 1.00 0.00 FAD (Ma)

S. tchadensis Au. africanus H. habilis P. robustus H. erectus H. neanderthalensis Ar. ramidus Au. garhi H. rudolfensis Au. sediba H. antecessor H. sapiens Au. afarensis P. aethiopicus P. boisei H. ergaster H. heidelbergensis H. floresiensis

Fig. 1. Chimpanzee male (open triangle) and female (open circle) and rAMHS male (open diamond) and female (open square) brain weight means are plotted, with Y-axis bars and dashed lines showing ranges within two standard deviations. Fossil hominin brain weight individual specimen values are plotted with Y-axis bars showing range within two standard deviations from the mean. For more information, see Table 2. Table 2. Absolute and relative brain size values for fossil and extant panin and hominin taxa

No. endocranial Mean Minimum Maximum Minimum Mean FAD vols. or endocranial endocranial endocranial Mean brain Maximum Brain body wt. Taxona (mya) brain wts. vol. (cm3) vol. (cm3) vol. (cm3) brain wt. (g)b wt. (g) brain wt. (g) wt. SD (kg)c EQd

Pan troglodytes (M) 17 406 347 530 39 58 1.65 Pan troglodytes (F) 17 368 308 458 37 43 1.88 rAMHS (M) 351 1450 1343 1526 20 70 5.10 rAMHS (F) 201 1290 1239 1366 30 57 5.35 S. tchadensis 7.0 1 365 363 Au. afarensis 3.7 5 446 387 550 442 385 542 69 38 2.50 Au. afarensis (M?) 3.7 2 521 492 550 514 486 542 40 45 2.56 Au. afarensis (F?) 3.7 3 396 387 400 393 385 397 7 29 2.69 Au. africanus 3.0 9 460 428 515 455 424 508 33 34 2.78 Au. garhi 2.5 1 450 446 P. aethiopicus 2.5 1 410 407 H. habilis 2.4 6 609 509 687 599 503 674 60 33 3.72 H. rudolfensis 2.4 3 776 750 825 758 734 805 41 55 3.21 P. boisei 2.3 10 488 400 545 483 397 537 43 41 2.54 P. robustus 2.0 4 533 450 650 525 446 638 82 36 3.07 Au. sediba 2.0 1 420 363 H. erectus 1.9 36 991 727 1260 963 712 1218 134 58 3.94 H. ergaster 1.8 6 763 600 900 746 590 877 111 64 2.81 H. ergaster (Africa) 1.8 3 851 804 900 830 785 877 46 64 3.12 H. ergaster 1.8 3 675 600 775 662 590 758 86 (Dmanisi) H. antecessor 0.78 1 1000 972 H. heidelbergensis 0.60 21 1242 880 1450 1200 858 1397 131 71 4.21 H. neanderthalensis 0.20 27 1404 1172 1740 1353 1135 1669 153 72 4.67 H. sapiens 0.20 79 1463 1090 1880 1408 1057 1799 124 64 5.30 H. floresiensis 0.07 1 417 414 26 3.10 aSources as follows: Chimpanzee brain and body weights from individuals 7–30 years, from Herndon et al. (1999). rAMHS brain and body weights from adults 21–39 years (except min. and max. brain weights, which are for 20–30 years), from Dekaban and Sadowsky (1978). In both datasets, “brain weight” is taken from fresh autopsy specimens and includes brain tissue as well as leptomeninges and CSF. See Appendix for references of the volumes on which fossil hominin species data are based. bFossil endocranial volumes were converted into brain weights after Ruff et al. (1997). cMean body weights are from Skinner and Wood (2006). dAfter Martin (1981) and Ruff et al. (1997). Extant taxon EQs are means of individual EQs. Fossil taxon sample mean EQs are obtained from each taxon’s mean brain weight and mean body weight estimates. EQs obtained by either method are very similar and have been used interchangeably (e.g., Ruff et al., 1997). 298 reported a 7.4% (100g) decrease in human brain neurocranial cavity) and fossilized cranial skeletal weight between 20–30 years and 70–80 years. remains. Convolutional details are notoriously dif- Although in living species males and females often ficult to interpret (Holloway, 1966; Symington, have significantly different brain sizes, it is not possi- 1916). A feature may be the impression of a sulcus, ble to know the sex of fossils with certainty, and sta- a blood vessel, or a skeletal suture, or it may be an tistical methods of sexing are not possible for the artifact, and observers may offer genuinely differ- small samples of early hominin crania. Here, fossil ent interpretations of what the same feature specimens are not sexed but are compared to extant represents (Connolly, 1950; Falk, 1980b). Aspects species data in which sex is known (Fig. 1). All statis- of brain morphology of hominin species inferred tical comparisons from this dataset (given in text) from fossil endocranial data are summarized here are derived from a Kruskal–Wallis test of and in Table 3 (see also Chapter 12). significance. Not all researchers are convinced that the detailed Previously, absolute brain size has been used to morphology of endocasts has functional relevance. determine a cerebral rubicon criterion for inclusion At one time, paleoneurology took for granted that in the genus Homo, variably set between 600 and sulci delimit functional or somatotopic cortical areas 800cm3 (Leakey et al., 1964). Until recently, abso- (see Radinsky, 1972, and references therein). It is lute brain size was thought to lack biological signifi- not understood, however, that primate brains cance, as it does not give an indication of degree of exhibit a substantial amount of intraspecific encephalization, or the number of “extra neurons” variability in sulcal anatomy and cytoarchitectural (Jerison, 1973; Martin, 1990). However, a recent boundaries (Geyer et al., 2001, Rademacher et al., study has found that absolute brain size predicts cog- 2001, Amunts et al., 2007). There are some cases in nitive ability in primates, whereas encephalization which the relationship between a sulcal landmark quotient (EQ, a measure of brain weight relative to and functional area border is maintained, at least body size) does not (Deaner et al., 2007). Many within a species (Holloway et al., 2003), but in other aspects of brain morphology such as brain compo- cases, it varies within species (Sherwood et al., 2003). nent volumes and degree of gyrification scale to Extant primates’ brains and endocrania are used to absolute brain size (Semendeferi and Damasio, make inferences about fossil hominins’ brains, but 2000; Semendeferi et al., 2002; Weaver, 2005; Zilles data from apes are rare, so most inferences should et al., 1988, 1989), so it is an important consideration be treated as preliminary. when making comparisons between the morphology of fossil endocasts. Fossil hominin species mean brain weights and Left-occipital right-frontal petalia EQs were estimated using allometric equations (Table 1; for a discussion of methods, see de A petalia is a protrusion of one cerebral hemi- Sousa, 2008; de Sousa and Wood, 2007). We used sphere relative to the other. The left-occipital Ruff et al.’s (1997) formula, based on Martin right-frontal (LORF) petalia is an asymmetrical (1981), and used Ruff et al.’s (1997) calculation pattern in which there is a wider and more poste- for estimating brain weight from endocranial vol- riorly protruding left-occipital pole, and a wider ume, based on Martin (1990). and more rostrally protruding right-frontal lobe. The LORF petalia is typical of humans and is statistically related to right-handedness —that is, Fossil hominin brain morphology left-handed and ambidextrous people are more likely to be symmetrical or have the opposite pat- Inferences can be made about the size and shape of tern (Le May, 1976). It is not clear whether apes the brain from natural endocasts (casts of the exhibit humanlike petalias. Le May (1976) and 299

Table 3. Brain morphology of fossil hominin species inferred from fossil endocranial data

Taxon FAD LORF Fronto- Orbital Broca’s Neurocranial Temporal Lunate Relative size (Ma) petaliaa orbital surface of the cap globularitye pole sulcus of cerebellum sulcusb frontal lobec regiond morphologyf positiong (CQ)h

P. troglodytes P P P P P P P 1.2 rAMHS HHH HH H H 1 Au. afarensis 3.7 I –– I ––P/H – Au. africanus 3h P h h – h H 0.8 P. aethiopicus 2.5 h – P –– P –– H. habilis s.s. 2.4 P P – I –––1 H. rudolfensis 2.4 H H – H –––0.9 P. boisei s.s. 2.3 h – P –– PH1 P. robustus 2I – P –– PH– H. erectus s.s. 1.9 H –– HP – H 0.9 H. ergaster 1.8 H –– I –––0.9 H. heidelbergensis 0.60 H –– HP – H 0.8 H. neanderthalensis 0.20 H –– HP – H 0.7 H. sapiens s.s. 0.20 H –– HH – H 0.7 H. floresiensis 0.07 H H H I – H –

Notes: –, no relevant evidence; I, insufficient evidence; H, humanlike morphology either described or inferred; h, incipient humanlike morphology either described or inferred; P, panin-like morphology either described or inferred. Panin-like (P) and humanlike (H) morphology as follows. Refer to text for a more details. aLeft-occipital right-frontal petalial pattern (P) infrequent, rarely involves both frontal and occipital lobes; (H) usual. bFronto-orbital sulcus (P) present; (H) absent. cOrbitofrontal region (P) beak shaped; (H) blunt and expanded. dAsymmetrical Broca’s area (P) not asymmetrically enlarged; (H) L>R asymmetry. eEndocast shape (P) “archaic”; (H) globular, suggests expanded parietal. fTemporal pole morphology (P) rounded; (H) expanded in anterior and lateral directions. gLunate sulcus position (P) anterior (some variability); (H) more posterior. hMean CQ values, calculated from specimen CQ values (LSR-05 in Weaver, 2001).

Le may et al. (1982) found that petalias are also 1993; Holloway et al., 2004a), H. erectus common in great apes. However, Holloway and (Broadfield et al., 2001; Holloway, 1980; Holloway de Lacoste-Lareymondie (1982) found them to et al., 2004a). A pronounced but reversed (ROLF) be less frequent than in humans and rarely involv- petalia pattern has been described for H. flo- ing both the frontal and the occipital lobes but resiensis and may be related to left-handedness noted a high incidence of left-occipital petalias (Falk et al., 2005, 2009b). Small LORF petalias in gorillas. In a more recent MR study, however, have been described for Australopithecus Hopkins and Marino (2000) found that great apes africanus, Paranthropus boisei, and Paranthropus display humanlike right-frontal and left-occipital aethiopicus (Holloway et al., 2004a). H. habilis petalias. specimens all lack humanlike LORF petalias. Humanlike LORF petalias are also usual in H. (Holloway et al., 2004a; Tobias, 1987). There is heidelbergensis, H. neanderthalensis, H. sapiens insufficient evidence for describing petalias in (Holloway et al, 2004a). LORF petalias are also Australopithecus afarensis, although there may be attributed to specimens of H. rudolfensis evidence of a slight left-occipital petalia in one (Holloway, 1983), H. ergaster (Begun and Walker, specimen, AL 333–45 (Holloway et al., 2004a). 300

Orbital frontal lobe shape human prefrontal cortex has a higher than expected white-to-gray matter ratio The orbital surface of the frontal lobe is blunt and (Schoenemann et al., 2005). Inferences about the expanded in humans. In contrast, it is described prefrontal cortex are disputed because this region as beaked and pointed in the African apes. This is difficult to delimit (Semendeferi et al., 2002; She- region corresponds to part of BA10, which is rwood et al., 2005). It is possible that the human involved in planning future actions, abstract frontal lobe scales to brain size, although the pre- thinking, and undertaking initiatives (Sem- frontal cortex is enlarged proportionally within it. endeferi et al., 2001). The human BA10 is Humanlike morphology, in which the fronto- characterized by increased horizontal spacing orbital sulcus is absent, has been reported for H. between cell bodies (Semendeferi et al., 2011), rudolfensis (Falk, 1983) and H. floresiensis (Falk and a larger volume than expected for an ape of et al., 2005). An apelike fronto-orbital sulcus has human brain size (but the residual [6%] is less been reported for Au. africanus and H. habilis striking than for other regions; Holloway, 2002). (Falk, 1980a, 1983). The prefrontal cortex in the region of BA10 is expanded in two large convolutions that straddle the rostrodorsal midline between the frontal lobes Broca’s cap in H. floresiensis, unlike neurotypical (non-microcephalic) H. sapiens, in whom BA10 is enlarged Broca’s cap, as seen on endocasts, represents but not manifested in such convolutions (Falk, portions of Brodmann’s areas (BAs) 47 and 45 2009; Falk et al., 2005). This region is also as identified on human brains (Broadfield et al., somewhat expanded in Au. africanus (Smith, 2001; Chapter 12). Broca’s cap overlaps (but does 1927), but not in P. aethiopicus, P. boisei, and not exactly correspond to) Broca’s language area. Paranthropus robustus (Falk et al., 2000). Broca’s area corresponds to BA45 and BA44, (respectively, pars triangularis and pars oper- cularis of the inferior frontal gyrus; Aboitiz and Fronto-orbital sulcus Garcia, 1997). In the majority of humans, the left hemisphere is dominant for language, and BA44 The fronto-orbital (orbitofrontal) sulcus typically (but not BA45) on the left hemisphere is asym- incises the orbitolateral border of the frontal lobe metrically enlarged in comparison to the contra- of African apes but is not present on human brains lateral BA44 (Amunts et al., 1999). Although an (Connolly, 1950; Falk, 1980a; Chapter 12). enlarged Broca’s cap is a characteristic of According to Connolly (1950), opercular expan- humans, it might also occur, albeit more rarely, sion of the frontal lobe during hominin evolution in apes (Holloway, 1996). covered this sulcus and caused it to shift caudally, Questions persist about whether the homo- where it became part of the anterior limiting sulcus logue of Broca’s area in apes exhibits humanlike of the insula. The human frontal lobe (Semendeferi asymmetry (Cantalupo and Hopkins, 2001; and Damasio, 2000; Semendeferi et al., 1997) and Holloway, 1996; Sherwood et al., 2003). A recent its cortex (Semendeferi et al., 2002) have volumes study of minicolumn size in BA44 and BA45 has expected for an ape of similar brain size. It has been indicated that apes lack a species-level pattern suggested that the human prefrontal cortex is larger of asymmetries like that seen in humans than expected for a primate with a similar sized (Schenker et al., 2008). Investigators draw atten- brain (Deacon, 1997), supported by the finding of tion to humanlike Broca’s cap asymmetry in fossil increased gyrification in this region (Rilling and hominins, in particular, in specimens in which the Insel, 1999). It has further been suggested that the left side is larger than its homologue on the right 301

(L>R). They also describe overall size and Temporal poles convolutional detail—particularly in fossils where only one hemisphere is present. Because a Bro- Falk et al. (2005, 2000) described human endocasts ca’s area L>R asymmetry is a characteristic of as having temporal poles which are extended in the most humans, and most humans are right-handed, anterior and lateral directions, whereas African it is related to right-handedness and attention apes have rounded temporal poles. More generally, is drawn to fossil hominins with both Broca’s area human temporal lobes are larger in total volume, L>R and LORF L>R asymmetries. white matter volume, and surface area than pre- Attention is drawn to fossil hominins in which dicted for an ape of similar brain size (Rilling and there is a pattern of both Broca’s area and LORF Seligman, 2002). In humans, the anterior lateral L>R asymmetries, presumably because these temporal pole, particularly in the left hemisphere, L>R asymmetries are characteristic of humans, is involved in face recognition and naming and most humans are both right-handed and (Damasio et al., 1996; Grabowski et al., 2001). left-lateralized for language. Broca’s area’s The corresponding monkey area, TG, also involvement in hand movement (Fadiga and functions in visual learning and recognition (Horel Craighero, 2006) as well as language is the basis et al., 1984; Nakamura and Kubota, 1995). of the mirror system hypothesis which sees Enlarged temporal lobes in fossil hominins are laterality for handedness as a precursor to lan- considered to be humanlike, in contrast to the guage (Arbib, 2005; Rizzolatti and Arbib, 1998). smaller temporal lobes of apes (Dart, 1940; Falk However, the anatomical pattern of asymmetry et al., 2000; Smith, 1927). Falk and others have in Broca’s area is variable and poorly understood made two different categories of observations in relation to the functional asymmetries of lan- about temporal lobe size, where the information is guage and handedness (Keller et al., 2009). Fur- available. First, they have described the temporal ther, brain surface morphology does not provide poles of rAMHS and Au. africanus as pointed due consistent landmarks for identifying the to the forward projections of the poles beyond the cytoarchitectonic borders of Broca’s region, par- anterior borders of sella turcica, and the distances ticularly when making comparisons between spe- between the poles. In contrast, in P. boisei, cies (Falk, 2007; Sherwood et al., 2003). P. robustus, and P. aethiopicus, the temporal lobes A clearly delimited, humanlike Broca’s cap are rounded and apelike (Falk et al., 2000). exhibiting L>R asymmetry is usual in H. Second, the unusually wide temporal lobes of H. heidelbergensis, H. neanderthalensis, and H. sapiens floresiensis are indicated by the overall endocast (Holloway et al., 2004a). It has also has been breadth/width, which exceeds that of any human, reported in specimens of H. rudolfensis (Begun ape, or fossil hominin endocast measured, due to and Walker, 1993; Holloway, 1983; Holloway the lateral expansion of the caudal part of the tem- et al., 2004a; Tobias, 1975) and H. erectus poral lobes (Falk et al., 2005, 2009b). However, (Broadfield et al., 2001; Holloway et al., 2004a). consistent with its small cranial capacity, the dis- The Broca’s cap region demonstrates a trend tance between temporal poles in H. floresiensis is toward a humanlike pattern in Au. africanus only slightly higher than that of Au. afarensis and (Holloway et al., 2004a). Descriptions of the less than that of rAMHS (Falk et al., 2005). Broca’s cap region have been insufficient or incon- clusive in Au. afarensis (Holloway et al., 2004a), H. habilis (Holloway et al., 2004a; Tobias, 1987), Lunate sulcus position H. ergaster (Begun and Walker, 1993; Holloway et al., 2004a), and H. floresiensis (Falk The lunate sulcus (LS) is within the secondary et al., 2005). visual area of apes, close to the anterior border of 302 the primary visual cortex, BA17. The position of 1947; Tobias, 1991). In contrast, it has been the LS has long been used to estimate BA17 size, asserted that Stw 505 provides better evidence and LS position correlates with cytoarchitecturally of a posteriorly positioned LS in Au. afarensis defined total BA17 volume in apes (de Sousa (Holloway et al., 2004b). In addition, posteriorly et al., 2010a). In chimpanzees, the LS marks the positioned lunate sulci have been inferred from anterior extent of BA17, even in cases where the the fossil endocasts of P. boisei, P. robustus, H. LS is in an unusual position for the species erectus, H. heidelbergensis, H. neanderthalensis, (Holloway et al., 2003). and H. sapiens (Holloway et al., 2004a). It is BA17 is the histologically defined cortical area suggested that in Au. afarensis, as in chimpanzees, which is most reduced in humans, based on pre- the LS may be variably in a posterior or anterior dictions for an ape of similar brain size. Humans position (Holloway et al., 2004a, 2003). have a substantially smaller (121%) BA17 than expected for a nonhuman primate of similar brain Parietal lobe expansion size (Holloway, 1992), a finding which is supported even when phylogeny is controlled for de Sousa The relative reduction of BA17 is associated with et al. (2010a). Although chimpanzees typically the relative expansion of the posterior parietal have a relatively larger BA17 than do humans, a association cortex. The posterior parietal lobe is minority of chimpanzees show repositioning of concerned with several aspects of sensory pro- the LS to a more humanlike posterior position cessing and sensorimotor integration (Hyvarinen, and therefore might also have reduced BA17 1981; Lynch, 1980). The superior parietal lobule volumes (Holloway et al., 2003). Holloway et al. subcomponent is involved in visuomotor tasks, (2003) use this point to argue that the hypothetical including finger movements (Shibata and panin–hominin MRCA must also have had within Ioannides, 2001) and visual attention (Yantis its population individuals with reduced primary et al., 2002). The superior parietal lobule (BA7) visual cortices, so one would expect this condition functions in spatial cognition and demonstrates dif- in early hominins such as Au. afarensis. The LS ferential activation during an Oldowan toolmaking may be unique among the cortical sulci visible on task (Stout et al., 2000). The inferior parietal lobule endocasts in that it may provide information about is involved in language and calculation abilities, the proportion of cortex allocated to distinct func- and it is greatly expanded in humans compared to tional categories, and provide an estimate of the monkeys (Simon et al., 2002). Derived human aforementioned ratio of association to sensory cor- behaviors involving the posterior parietal lobe tex (Holloway, 1966, 1968). include enhanced social behavior including com- Inferences about LS position are based on munication, toolmaking, and tool-use (Holloway observations of the LS itself, and also (or alterna- et al., 2004a). It is suggested that the unique globu- tively) on the position of the interparietal sulcus, lar shape of the neurocranium of AMHS is related which abuts the LS. Dart (1925) described a to an additional expansion of the parietal lobe and humanlike posteriorly positioned LS on a small, may be associated with the manufacture of more early hominin endocast (the Taung child, Au. sophisticated tools and refined language ability africanus), and in doing so began a long debate (Bruner, 2004; Bruner et al., 2003). over the identification and location of the LS (Falk, 1980a, 1985; Holloway, 1975; Keith, 1931; Le Gros Clark et al., 1936; Schepers, 1946). In Cerebellum size fact, many authors note that it is impossible to know the LS position in Taung with certainty The cerebellum is well known for its functions in (Falk, 2009; Holloway, 1985; Le Gros Clark, motor control such as coordination, precision, 303 and accurate timing; however, recent attention Tool-use has been brought to the evolution of the cerebellum because the neocerebellum has been Comparative studies of material culture have spe- implicated in cognitive tasks, and there is a differ- cific implications for understanding fossil hominin ential expansion of the lateral cerebellum (largely taxa because tool-use and production are the neocerebellum) in hominoids compared to other earliest (and also the most extensive) category anthropoids (MacLeod et al., 2003; Chapter 8). of hominin behavioral evidence. Chimpanzee The human cerebellum is smaller than would be archeology informs our interpretation of behavior expected for an ape of similar brain size (Rilling as represented in the archeological record. and Insel, 1998; Semendeferi and Damasio, In particular, information about tool-use in 2000). A cerebellar quotient (CQ¼actual/pre- chimpanzees and humans is used to reconstruct dicted value) was obtained when rAMHS cere- the behaviors of the hominin–panin MRCA bellar volume (determined from posterior (Haslam et al., 2009). cranial fossa volume) was regressed against brain Chimpanzees are the apes that use tools most volume (determined from endocranial capacity) extensively in the wild. Chimpanzees use stone minus cerebellar volume (Weaver, 2005). The dif- “hammers” to crack open nuts and modify twigs ference between human and great ape relative for termite hunting (Goodall, 1986) and have cerebellar volumes is statistically significant, recently been observed to hunt small primates although less dramatic when considered among with spears (Pruetz and Bertolani, 2007). As is the range of inferred relative cerebellar volumes the case with hominins, tool-use in chimps is of fossil hominins (Weaver, 2005). The relative socially learned (Whiten and van Schaik, 2007). cerebellum size of rAMHS is estimated to be sim- Chimpanzee nut-cracking leaves a recoverable ilar to or larger than that of earlier hominins. material record of stone and plant remains However, fAMHS and H. neanderthalensis have (Mercader et al., 2002). The material culture of the smallest mean CQs, indicating a recent chimpanzees can be used to reconstruct opera- increase in relative cerebellum size to that of tional sequences showing their utilization, and rAMHS (Weaver, 2005). these are distinguishable between different chimpanzee cultural groups (Carvalho et al., 2008, 2009). It has been hypothesized that even the earliest hominins used tools, made of stone or Archeological implications for fossil brain other materials, prior to the earliest evidence for function stone tool making (Panger et al., 2002). The earliest known evidence of stone tool-use, The fossil hominin archeological record contains inferred indirectly on the basis of cuts and percus- a wealth of information about the emergence of sion related to the consumption of animal tissues, human-specific behaviors. Given their special rel- is from before 3.39Ma at Dikika, Ethiopia and is evance to understanding hominin brain evolution, attributed to Au. afarensis, which was the only the earliest evidence for the following human-spe- hominin present in the area at that time cific behaviors are discussed here and (McPherron et al., 2010). Although the full extent summarized in Table 4: (1) tool-use, (2) inten- of tool-use in Au. afarensis is uncertain, at pres- tionally manufactured stone tools, (3) symmetri- ent, the evidence supports the conclusion that cal tools, (4) handedness among toolmakers, and they used tools. However, whether or not they (5) symbolic activity (burials, abstract intentionally made tools is an open question. representations, personal ornamentation, and fig- Unlike humans, chimpanzees are not known to urative representations). intentionally manufacture stone tools in the wild. Table 4. Behaviors of fossil hominin species inferred from the archeological record

Intentional Handedness Symmetry Sound- FAD Tool- tool (across in tool Abstract modifying Figurative Taxon (mya) use manufacture populations) morphology Symbolism Burial Ornamentation representation instruments representation

P. troglodytes A rAMHS A Au. afarensis 3.7 U Au. africanus 3UU Au. garhi 2.5 U U P. aethiopicus 2.5 U U H. habilis s.s. 2.4 U U U H. rudolfensis 2.4 U U P. boisei s.s. 2.3 U U U P. robustus 2UU H. erectus s.s. 1.9 A A A A H. ergaster 1.8 A A U A H. antecessor 0.70 A A A H. 0.60 A A A A heidelbergensis H. 0.20 A A A A AAA U U U neanderthalensis H. sapiens s.s. 0.20 A A A A AAA A A A H. floresiensis 0.07 A A

Notes: A, associated with behavior in archeological record; U, uncertain association, for which it is a candidate species. 305

In captivity, it is possible to train a bonobo to pro- Handedness duce by hard-hammer percussion fragments for food consumption use, using a stone-flaking All human populations are characterized by hav- method less advanced than the Oldowan (Schick ing a right-handed majority. Handedness in apes et al., 1999; Toth et al., 1993). is less regular, and although it may occur at the level of populations (Hopkins et al., 2003), the pattern is not consistent across an entire species Intentionality (Uomini, 2009) and continues to be debated (Hopkins et al., 2011). Oldowan tools from Gona, Ethiopia, from 2.6 to Evidence of population-level right-handedness 2.5Ma are the oldest direct evidence of stone tool was proposed for an Oldowan assemblage, dated making (Semaw et al., 1997). These tools are not to 1.9–1.4Ma, from Koobi Fora, Kenya (Toth, in direct association with any hominin species, 1985). This is not in direct association with any although Australopithecus garhi occurred contem- hominin species, although the candidate species poraneously a short distance away (Asfaw et al., are H. habilis, H. ergaster,andP. boisei. On the 1999; de Heinzelin et al., 1999). However, any of basis of lithic morphology, population-level several species which occurred at this time might right-handedness has been proposed for H. have made them. Early Homo is often credited erectus, H. neanderthalensis,andH. sapiens for the earliest stone tool making, and thus (Uomini, 2009). It has also been suggested for starting a tradition that continued in the undis- H. neanderthalensis and H. heidelbergensis on puted toolmaking members of its genus including the basis of dental microwear patterns (Frayer rAMHS (Plummer, 2004; Toth and Schick, 2009). et al., 2011a,b; Lozano et al., 2009). The earliest hominin specimen associated with tools is AL 666-1, which may be an early member of the genus Homo (Kimbel et al., 1996). How- Symmetry ever, non-Homo hominids have also been put forward as potential toolmakers because they are The production of lithics with symmetrical (or synchronic with lithic industries (de Heinzelin otherwise standardized) shape has not been et al., 1999; Kuman and Clarke, 2000), share a observed in extant species other than H. sapiens. trend toward brain size increase (Elton et al., However, the cognitive implications of this 2001), and may have had hand morphology com- human-specific behavior are strongly disputed. patible with tool-use (Ricklan, 1987; Susman, A technological industry spanning one million 1994, 1998; but see Tocheri et al., 2008). years and several continents, the Acheulean, is Australopithecus garhi, Au. africanus, K. platyops, generally typified according to the existence of P. aethiopicus, P. boisei, P. robustus, H. habilis, bifacially and bilaterally symmetrical teardrop- and H. rudolfensis have all been implicated as shaped lithics and is the focus of dispute. It has potential creators of the earliest Oldowan. The been suggested that symmetrical standardization earliest definite toolmaker is H. ergaster, a species of lithics signifies the ability to impose a pre- which is associated with both late Oldowan and determined form on a piece of stone, and by early Acheulean (Kuman and Clarke, 2000; extrapolation cognitive capacities for planning Plummer, 2004). In addition, stone tools have and perhaps language ability (Gowlett, 2006). been found in association with the skeletal However, it has been suggested that Acheulean remains of H. ergaster, H. erectus, H. antecessor, tools are, for the most part, not particularly sym- H. heidelbergensis, H. neanderthalensis, H. flo- metrical (Clark and Riel-Salvatore, 2005), vary resiensis, and H. sapiens. in form according to raw material and production 306 intensity (McPherron, 2000), and may have been advent of writing. Burial, ornamentation, and cores rather than end-products (Davidson and abstract or figurative auditory and visual Noble, 1993). Further, the manufacture of sym- representations (art and music) are often cited metrical objects is not distinct to humans, as apes as evidence of early symbolic capacity. However, may produce radially symmetrical sleeping nests none of these is necessarily symbolic (Duff (Wynn and McGrew, 1989). The earliest et al., 1992); therefore, it is common to look more handaxes are from 1.6 to 1.7Ma, from eastern broadly for evidence for symbolic behavior. It has and southern Africa, and include 1.7Ma tools at been argued that symbolic behaviors appeared as Konso-Gardula, Ethiopia (Asfaw et al., 1992) a synchronic “package,” coincident with a cogni- and 1.6Ma tools at Sterkfontein, South Africa tive “revolution” (Klein, 1999, 2003), although (Gibbon et al., 2009). The Acheulean is normally most archeologists prefer a model in which attributed to H. ergaster and African H. erectus. attributes of symbolic behavior appear gradually. H. antecessor, H. heidelbergensis, H. The timeframe may have encompassed speciation neanderthalensis, and early AMHS are also events, and sequential species may have differed associated with symmetrical handaxes (Clark in the biological basis of behavior (McBrearty et al., 2003; McPherron, 2000). In addition, and Brooks, 2000). However, demographic and rAMHS and H. floresiensis are also associated ecological variables could have contributed to with symmetrical tool morphologies. the appearance and patterning of new behaviors even in the absence of biological changes (Powell et al., 2009). Symbolism The earliest evidence of probable symbolic behavior of any kind is the use of pigments, pre- The fabrication of material symbols is unique to sumably in personal ornamentation or art. The humans among extant species. The quintessential earliest known occurrence of pigment use is at symbol system, language, is human specific, but Pinnacle Point, South Africa, 164ka, attributed symbolism is defined more broadly to include any to H. sapiens (Marean et al., 2007). arbitrary assignment of meaning to a thing that Burial: The oldest purposeful burials are H. bears no necessary resemblance to its referent sapiens from Qafzeh and Skhul, Israel, 115ka (Pierce, 1932). Aspects of symbolic capacity exist (Grun et al., 2005). Two species, H. sapiens and in apes, including language in a captive bonobo H. neanderthalensis, are associated with purpose- (Benson et al., 2002), auditory communication in ful burials (Riel-Salvatore and Clark, 2001). wild chimpanzees (Boesch, 1991), and juvenile Ornamentation: More robust evidence of per- female chimpanzees carrying sticks as if they were sonal ornamentation is the use of shell beads, infants (Kahlenberg and Wrangham, 2010). This which occurred in similar patterns at several mid- has prompted examination of any particular dle stone age sites in North Africa (Bouzouggar aspects of symbolic behavior which may in fact be et al., 2007; Vanhaereny et al., 2006) and Sub- human specific (Deacon, 1997; Mignault, 1985). Saharan Africa (d’Errico et al., 2005; Because wild chimpanzees are not known to manu- Henshilwood et al., 2009), and Western Asia facture symbolic artifacts, at least this aspect of (Bar-Yosef Mayer et al., 2009; Vanhaereny symbolic behavior seems to be exclusively hominin. et al., 2006). Of these, the earliest are the There is no definitive way in which symbolism perforated shells from Skhul, Israel, from 100 to is physically represented, making it difficult to 135ka, associated with H. sapiens (Vanhaereny identify archeologically. Language is the likely et al., 2006). Two species, H. sapiens and H. predecessor to all forms of symbolic behavior, neanderthalensis, are associated with ornamenta- but it is not identifiable archeologically until the tion. The latter is associated with beads made of 307 pierced shells and teeth (Zilhão, 2007; Zilhao intergroup contact may have inspired their crea- et al., 2010) and may have used feathers as tion (Conard, 2010; d’Errico and Stringer, 2011). ornaments (Peresani et al., 2011). Abstract representation: The earliest evidence of abstract representation are deliberately Neuroimaging fossil hominin archeology engraved ochre pieces from Blombos Cave, South Africa, dated to 75ka (Henshilwood et al., 2002, An approach which links hominin brains to 2009). Two species, H. sapiens and H. behaviors entails the neuroimaging of humans neanderthalensis, are associated with abstract engaged in tool-use and toolmaking. Such studies visual and auditory representations (Soressi and identify regions involved in fossil hominin-like d’Errico, 2007), although in the latter species the toolmaking. Toolmaking by experienced evidence is far less robust. toolmakers differs from that of inexperienced Sound-modifying instruments: The oldest undis- toolmakers in that there is more activation in puted intentionally crafted sound-modifying regions of language and manual praxis circuits, instruments are bone flutes, thought to be musical including parietofrontal regions in both the instruments, attributed to over 35ka from Hohle hemispheres and the right hemisphere homologue Fels, Germany (Conard et al., 2009). Undisputed of Broca’s area (Stout et al., 2008). Also of inter- examples of intentionally crafted musical est are differences in brain activation according to instruments have been found in association with toolmaking method, demonstrating the differen- H. sapiens only (d’Errico and Lawson, 2006). tial cognitive demands of different technological Figurative representation: There are several industries. For example, the observation of candidates for the oldest figurative Acheulean toolmaking, compared with Oldowan representations (i.e., for which the intentionality toolmaking, corresponds to increased activation is undisputed and which are thus interpreted as of left anterior intraparietal and inferior frontal “art”), all dating to 60–30ka. There is a great deal sulci, which are regions of the brain involved in of dispute about precise dates, however, and the “action understanding” (Stout et al., 2011). time frame is relatively narrow, so the earliest Unfortunately, thus far, it has proved difficult examples are provided here. The oldest possible to do functional neuroimaging of tool-use and date for figurative representations come from manufacture in apes. Comparisons between painted slabs depicting animals, in the Apollo 11 humans and macaques during tool-use (and Cave, which is dated to 18–34ka but argued to related activities) may highlight regions of inter- have a date older than 59ka based on their Mid- est for future studies. For example, a rostral sec- dle Stone Age context in Namibia (McBrearty tor of the left inferior parietal lobule active and Brooks, 2000, Wendt, 1974, 1975). Also dur- during the observation of tool-use by humans, ing this time frame, rock paintings depicting but not macaques, has been identified through animals from Grotte Chauvet, France are dated functional neuroimaging (Peeters et al., 2009). up to 32 ka, and figurines from Hohle Fels Cave The archeological record is not limited to tool- date to older than 30ka (Conard, 2003, 2010). making, and there exists additional potential for Undisputed examples of figurative art have been identifying the neural correlates of other human- found in association with H. sapiens only. How- specific activities known to exist in fossil ever, no specific taxon is associated with the hominins. Notably, artifacts as early as the earliest figurative representations. It has been Acheulean may provide information about suggested that archaic humans such as H. esthetics in early hominins. Further research neanderthalensis had the potential to create figu- may reveal how transitions in the fossil hominin rative representations and/or that H. sapiens’ archeological record in both the technology and 308 the production of art and ornamentation are in language and brain size, respectively: FOXP2 related to the neural correlates of esthetic behav- and microcephalin (MCPH1). FOXP2 is ior in humans as well as nonhumans. implicated in a severe form of speech and language disorder which is associated with a heterozygous Fossil brain genetics missense mutation at the locus SPCH1 (Fisher et al., 1998). FOXP2 may be essential for normal Ancient DNA sequences provide evidence which language and speech function (Lai et al., 2001; can be used in conjunction with archeological and MacDermot et al., 2005). Two amino acid sub- paleontological evidence to reconstruct the struc- stitutions appeared in FOXP2 in hominins after ture and function of fossil hominin brains. Interest- the divergence from the hominin–panin MRCA ingly, human-specific cognition and brain and are found in H. sapiens (Enard et al., 2002), morphology may be the product of contributions H. neanderthalensis (Krause et al., 2007), and the from multiple hominin lineages, either directly Denisovans (Hawks, 2011a). through genomic contributions or through social Homozygosis of loss-of-function mutations in and cultural interactions. Recently, it has been MCPH1 causes a condition known as primary suggested that H. neanderthalensis may have con- microcephaly, associated with severe (three- to tributed 1–4% of the genomes of living Eurasian fourfold) reduction in brain volume (Jackson H. sapiens (Green et al., 2010) and a separate, genet- et al., 2002). A derived group of haplotypes at ically defined species, from 50 to 30ka in Denisova the MCPH1 locus (haplogroup D) occurs in 70% cave, Russia, may have contributed 4% of the of H. sapiens but is estimated to have appeared rel- genomes of living Melanesian H. sapiens (Reich atively recently (14–62ka) (Evans et al., 2005). It et al., 2010). As mentioned in the section on archeol- was proposed that the rapid increase of this genetic ogy, intergroup contact may have driven behavioral variant indicates that it was positively selected for changes at the cultural and/or genetic levels. in H. sapiens and appeared due to admixture with Genes associated with neurological conditions other hominin species—originally suggested to be give insight into the mechanisms influencing the H. neanderthalensis, because of the lower fre- evolution of brain structure and function. quency of haplotype D in Sub-Saharan Africa Differences between the genomes of H. (Evans et al., 2005, 2006). However, in spite of its neanderthalensis and H. sapiens have been recent predominance, no particular function is identified and could potentially be linked to spe- attributed to the novel variant; in fact, a recent cies-specific cognition. Of these, several genes study found no evidence linking MCPH1 to brain associated with human neurological disorders size evolution (Montgomery et al., 2011). Further, were inferred to show evidence of positive all specimens with known sequences for the gene selection in H. sapiens since the time of diver- in H. neanderthalensis show the ancestral variant gence with H. neanderthalensis. These are (Green et al., 2010; Lari et al., 2010). The DYRK1A, a gene associated with Down syn- Denisovans also show the ancestral variant drome; NRG, a gene associated with schizophre- (Hawks, 2011b). nia; and CADPS2 and AUTS2, both associated with autism (Green et al., 2010). Further analyses are needed to indicate the specific functional, and potentially cognitive, significance of any of these Fossil brain ontogeny mutations. Two genes related to cognitive function have Humans and chimpanzees differ in their patterns been specifically investigated in H. of brain growth (increase in size) and develop- neanderthalensis because of their probable roles ment (change in shape) (see Chapter 13). Most 309 obviously, there is a difference between the total development, the patterns of development are growth of the brain, indicated by the three- to similar (Neubauer et al., 2010). H. fourfold larger adult brain volume of humans neanderthalensis resembles chimpanzees in that than chimpanzees. However, this may seem it lacks the AMHS globularization phase (Gunz surprising given that the duration of postnatal et al., 2010). In spite of the primitive brain shape brain growth is similar in humans and development of H. neanderthalensis, its growth chimpanzees. Several factors explain this. First, appears further “derived” along the hominin humans have larger brains at birth (DeSilva and trend than rAMHS due to a larger adult brain Lesnik, 2006). Second, postnatally, the human size and a more rapid postnatal brain growth brain grows proportionally more, expanding by a period. factor of 3.3, compared with 2.5 in chimpanzees It has been suggested that differences between (DeSilva and Lesnik, 2006). Third, postnatally, a H. neanderthalensis and rAMHS in brain mor- greater absolute volume of additional brain tissue phology and cognition have parallels in the is produced in humans than in chimpanzees differences between autistic versus neurotypical (DeSilva and Lesnik, 2006). Fourth, in the early individuals (Neubauer et al., 2010). That is, H. postnatal period, humans have a higher growth neanderthalensis, like autistic individuals, has rate (Leigh, 2004). Few juvenile cranial capacities been suggested to have undergone an early post- are known, making it very difficult to ascertain natal spurt in brain development. The irregular anything about brain development in early developmental trajectory of autistics results in hominins. The earliest species for which the brain more short-distance connections and larger abso- growth trajectory is studied in detail is H. erectus. lute brain size, whereas the developmental trajec- H. erectus has been suggested to have a chimpan- tory of neurotypicals results in longer-distance zee-like brain growth rate based on the juvenile connections and smaller brain size (Courchesne Mojokerto specimen (Coqueugniot et al., 2004), et al., 2010; Lewis and Elman, 2008). but this has been met with skepticism due to diffi- culty in accurately aging the specimen, and because the Nariokotome boy suggests a more Bringing together evidence for fossil hominin humanlike growth pattern (DeSilva and Lesnik, brain structure and function 2006; Leigh, 2006). There is better evidence for determining the growth trajectory of H. Possible hominins neanderthalensis, which seems to have had growth rates during early infancy which were even higher We know very little about the brains and than those of humans, and resulted in larger adult behaviors of possible hominin species, and there brain sizes but not in earlier completion of brain is no basis on which they seem to be derived in growth (Ponce de Leon et al., 2008). This pattern comparison to a panin ancestral condition. is suggested to also apply to fAMHS because they Sahelanthropus tchadensis is the earliest possible have large brains, although growth rates have not hominin and it is also the hominin species with been demonstrated for them using fossil samples the smallest mean brain volume, which falls just (Ponce de Leon et al., 2008). below the female chimpanzee mean (but note Human brains also differ from those of that specimens of P. aethiopicus, Au. garhi,and chimpanzees in overall shape (Aldridge, 2011). H. floresiensis plot around the male chimpanzee Developmental patterns differ between humans mean). The lack of archeological data is consis- and chimpanzees during the stage directly after tent with what would be expected for a very early birth in that only humans undergo a hominin, or, for that matter, a member of any “globularization” phase; although, later in great ape lineage. 310

Archaic hominins: Reintroducing “Man the chimpanzees, they may have used tools; however, Toolmaker” unlike chimpanzees, it is likely they used tools to butcher animals. The notion that the human lineage could be defined Many aspects of humanlike endocast morphol- according to toolmaking was quashed with the dis- ogy make an appearance in Au. africanus, including covery of Au. afarensis, which shares humanlike (1) evidence for a reduced BA17, (2) frontal lobes postcranial anatomy and bipedal locomotion but that are expanded orbitally and a prefrontal cortex lacks the big brains and behaviors of humans. How- that appears squared off rostrolaterally when ever, more recent findings indicate that Au. viewed dorsally, (3) anteriorly expanded, laterally afarensis was likely a tool-user and Au. garhi was pointed temporal poles, (4) an incipient LORF likely a toolmaker. As noted, chimpanzees have petalial pattern, and (5) a humanlike Broca’s cap their own material culture. These recent findings region. Although these features are not as pro- suggest that tool associations may be expected even nounced as in humans, they can be interpreted as for probable hominins, regardless of brain size. being derived in the direction of humans. The rea- This, in turn, suggests that it would be worthwhile son for their occurrence in this taxon is uncertain to investigate the relationship between early, subtle but may be influenced by brain size increase, and changes in brain size and organization and material it is quite possibly related to exceptional preserva- culture. For example, possible differences in brain tion of brain morphology in Au. africanus. The organization within panins (cf. de Sousa et al., appearance of several aspects of modern brain 2010a,b) could be related to tool behaviors. morphology in Au. africanus complement the fact The earliest detectable aspect of humanlike that this taxon is the first to have a brain size signifi- brain morphology is the reduction of BA17. A cantly different from chimpanzees. The Au. posterior LS has been reported for some Au. africanus sample is significantly different from the afarensis specimens, although it is variable within combined sex sample (p<0.001), and the the taxon. Given the small sample, it is difficult to male (p¼0.001) and the female (p<0.001) sub- tell whether the Au. afarensis brain really is samples of chimpanzees. This finding is further derived in the direction of the human brain, or evidenced by the Au. afarensis EQ (2.5) which is whether it expresses variability similar to that well above that for chimpanzees and equals that seen in chimpanzees. The Au. afarensis mean of P. boisei. brain mass is not significantly different from the However, the Au. africanus brain differs con- combined sex sample of chimpanzees (p¼0.093) siderably from the human brain, and any nor from the male chimpanzee sample (p¼ similarities are not considered sufficient to sug- 0.456), although it is significantly larger than the gest humanlike brain structure and function in female chimpanzee sample (p¼0.011), although Au. africanus. Au. africanus appears later in the the EQs of Au. afarensis (2.5) and Au. africanus fossil record than Au. afarensis and there exists (2.8) are well above those for chimpanzees (male some possibility that it could have manufactured EQ¼1.7; female EQ¼1.9). Given small samples, Oldowan tools. Australopithecus brain size and one cannot be certain whether this variation is structure are rarely related to derived cognitive in fact a change from the variation seen in capacities. chimpanzees. Further, humanlike endocranial anatomy in Au. afarensis might be a preadapta- tion which only acquires its modern functions in Megadont archaic hominins: Potential parallels Au. africanus, H. rudolfensis, or in even later hominins. Behaviorally, Au. afarensis could be The P. boisei mean estimated brain weight (483g) derived compared to chimpanzees: Like is larger than that of P. aethiopicus (407g) and 311 somewhat larger than those of Au. africanus (455 humanlike cognitive capacities. Most notably, g) and Au. afarensis (442g). Further, the majority these features are suggestive of language ability of the P. boisei specimens fall outside two stan- and right-handedness—coincident with the first dard deviations of the male chimpanzee mean. stone tools which apparently were made by Therefore, it is inferred that P. boisei has right-handed hominins. The LORF petalial pat- increased its absolute brain size relative to the tern and Broca’s cap region have become increas- primitive condition. The P. boisei mean is not sig- ingly humanlike in H. rudolfensis, the earliest nificantly different (p¼0.357) from that of the taxon for which there is strong evidence for later occurring P. robustus sample, even though humanlike brain organization. In addition, H. the latter attains a much higher maximum value rudolfensis is the earliest taxon not to have a (638g) and has a much higher mean (525g). P. fronto-orbital sulcus (but the evidence is based boisei and P. robustus have EQs that are higher on very little endocranial morphology). Interest- than those for male and female chimpanzees. ingly, there is no good evidence for a humanlike However, the P. boisei EQ is smaller than the LORF petalial pattern and a Broca’s cap region Au. africanus and it is similar to the Au. afarensis in H. habilis. Instead, there is evidence of an Afri- value. Given the lack of postcranial evidence, one can apelike fronto-orbital sulcus. This is cannot be certain that EQ has increased from P. associated with the earliest brain weights that aethiopicus to later Paranthropus taxa. These data exceed expectations for chimpanzees, and an are, however, consistent with the suggestion of a EQ higher than that of earlier taxa. temporal trend for brain size increase within the Relative brain weight in both H. habilis and H. Paranthropus lineage (Elton et al., 2001). rudolfensis is greater than that in Australopithecus There is little evidence suggesting humanlike and Paranthropus, and they approach the values reorganization of the Paranthropus brain. In par- for H. erectus (EQ¼3.9). By the time of the ticular, slight LORF petalial patterns are found in appearance of H. rudolfensis and H. habilis, both P. aethiopicus and P. boisei, and a posteriorly absolute and relative brain size have clearly positioned LS has been identified in P. boisei. departed from the Pan-like condition. H. habilis The evidence does not suggest that the and H. rudolfensis are significantly different in Paranthropus brain becomes increasingly human- brain weight (p¼0.02), and the entire range of like over time, as is the case for Homo. Further, H. rudolfensis values plot above the range of H. Paranthropus retains an apelike beak-shaped habilis values. However, H. habilis has a higher orbital surface of frontal lobe and rounded tem- EQ than H. rudolfensis and also has brain weight poral poles, differentiating it from Au. africanus values outside of those expected for chimpanzees. and AMHS. The humanlike endocranial features As yet, it is not possible to tell whether the more seen in Paranthropus most likely reflect a shared humanlike brain morphology of H. rudolfensis, ancestry with the human lineage. Similarly, brain compared to H. habilis is, or is not, size related. size increase in Paranthropus is probably the con- Early Homo has been described as linking sev- tinuation of a trend beginning in the AMHS- eral aspects of the brain (absolute size, Paranthropus MRCA. encephalization trend, humanlike morphology— in particular, related to lateralization) to behaviors (intentionality, handedness). However, Transitional hominins: Intelligent, the archeological associations are uncertain, and assuming we are related... the endocranial evidence is scarce. Doubt has been cast on the Homo-status of early Homo on The more humanlike brain morphology of H. the basis of its australopith-like postcrania and rudolfensis is generally taken as evidence of more dentition (Wood and Collard, 1999), and it has 312 even been suggested that their brains require are not identical to those of rAMHS. Parietal downsizing (Bromage et al., 2008). More lobe expansion that is related to brain reliable data about the brains and behaviors globularization (Bruner et al., 2003) and occurs of early Homo would shed much light on defini- during a novel postnatal developmental stage tive aspects of brain evolution in the human (Gunz et al., 2010) distinguishes both fossil and lineage. recent AMHS from H. neanderthalensis and other hominins. However, fAMHS more closely resembles H. neanderthalensis than rAMHS in hav- Premodern Homo: Making space for ing larger brains (and by extrapolation, a H. floresiensis similarly brain growth trajectory) and smaller relative cerebellum sizes. Further, behavioral H. erectus and H. ergaster tend to share the distinctions between fAMHS and H. humanlike endocranial features found in H. neanderthalensis are becoming blurred as new rudolfensis. Absolute and relative brain sizes in studies reveal increasingly early symbolic H. floresiensis are thought to have decreased from behaviors, including some associated with H. the ancestral condition (Brown et al., 2004). H. neanderthalensis (d’Errico and Stringer, 2011). In floresiensis had a very small brain (414g), with fact, the earliest art is not directly associated with an EQ (3.0) much lower than that of one of its AMHS, or any other hominin species. Finally, the presumed close relatives, H. erectus. Interestingly, most recent genetic analyses (Green et al., 2010; its EQ is higher than the one listed here for H. Reich et al., 2010), as well as some archeological ergaster (2.8—includes Dmanisi) and only slightly and morphological studies (Duarte et al., 1999, lower than the EQ for African H. ergaster (3.1). Zilhão, 2006) have suggested admixture between Body weight estimates obtained from Dmanisi fAMHS and other contemporary species, includ- postcranial remains will refine the H. ergaster ing H. neanderthalensis. The biological and cul- EQ. Given that H. ergaster is thought to have tural factors which define brain structure and expanded its range outside of Africa, evidence function in rAMHS might not best be revealed from the relative brain size alone suggest that it by comparing H. neanderthalensis to fAMHS. rather than H. erectus may be the sister-taxon of Rather, more comparisons are needed between H. floresiensis. If so, this would indicate that EQ fAMHS and rAMHS. did not actually decrease in H. floresiensis—solv- Hominin behavior may have changed more ing one of the major puzzles of this taxon (Brown dramatically from the early to late Upper Paleo- et al., 2004). H. floresiensis possesses many lithic than during the Middle to Upper Paleo- features which are derived relative to an apelike lithic “transition” (Riel-Salvatore and Clark, condition, although several of these already 2001). Studies making such a distinction might existed in the H. erectus. explain why the makers of late Upper Paleolithic cave art resemble rAMHS in drawing animal limb joints (Biederman and Kim, 2008), Anatomically modern Homo: while early Upper Paleolithic art may more When “modern” is not “recent” closely approximate autistic rather than neurotypical productions (Humphrey, 1998). Although fAMHS is included in our species on Because these comparisons involve members of the basis of anatomy (and possibly DNA; a single species, they will rely even more Caramelli et al., 2008) that is indistinguishable heavily on pathology and other interindividual from rAMHS, the evidence reviewed here sug- comparisons in neural and psychological gest that the brains and behaviors of fAMHS sciences. 313

Conclusions the approach taken was to all specimens for which an estimate could be found, noting the reliability The data suggest that while fully humanlike brain is variable. morphology only occurs in rAMHS, many aspects S. tchadensis: Based on TM 266-01-060-1 of human brain morphology are present in earlier (Zollikofer et al., 2005). forms. Further, encephalization in the human Ar. ramidus: Based on ARA-VP-6/500 (Suwa lineage may have begun as early as Au. afarensis, et al., 2009). and it was more evident in Au. africanus (in par- Au. afarensis s.s.: Based on AL 162-28, AL 288- allel to the encephalization of Paranthropus) and 1, AL 333-105, AL 333-45, AL 444-2 (Holloway had definitely occurred by the time of the appear- et al., 2004a). ance of H. habilis and H. rudolfensis. Interest- Au. africanus: Based on STW 505 (Conroy ingly, brain size increase and the appearance of et al., 1998), MLD 1, STS 19, STS 5, STS 60, some aspects of humanlike brain morphology STS 71, Taung, Type 2 (Holloway et al., 2004a), occur in at least two hominin lineages. Both MLD 37/38 (Neubauer et al., 2004). Paranthropus and Homo have absolutely and rel- Au. garhi: Based on Bou-VP-12/130 (Holloway atively significantly larger brains than et al., 2004a). Australopithecus. However, only in Homo does P. aethiopicus: Based on KNM-WT 17000 brain size increase occur in parallel with the (Holloway et al., 2004a). acquisition of humanlike brain morphology. H. P. boisei s.s.: Based on Omo-323-1976-896 floresiensis provides striking evidence that within (Falk et al., 2000), KNM-ER 406 (Holloway, Homo brain size and morphology may have 1988 [in Falk et al., 2000]), KGA-10-525, KNM- become disassociated. New evidence of possible ER 23000, KNM-ER 407, KNM-ER 732, KNM- continuity between the brains and behaviors of WT 13750, KNM-WT 17400, OH 5, Omo L- fAMHS and contemporaneous hominins also 338Y-6 (Holloway et al., 2004a). indicate that further changes may have taken P. robustus: Based on TM 1517 (Broom and place more recently in our species. New lines of Robinson, 1948), SK 1585, SK 54, SK 859 research are shedding light on the biological and (Holloway et al., 2004a). cultural factors resulting in recent human brain Au. sediba: Based on MH1 (Berger et al., structure and function. 2010). H. rudolfensis: Based on KNM-ER 1470, KNM-ER 1590, KNM-ER 3732 (Holloway et al., Acknowledgment 2004a). H. habilis s.s.: Based on KNM-ER 1813, KNM- Fundação para a Ciência e a Tecnologia (SFRH/ ER 1805, OH 7, OH 13, OH 16, OH 24 BPD/43518/2008) supported this research. The (Holloway et al., 2004a). chapter was substantially improved by editorial H. erectus s.s.: Based on Modjokerto 1 (Anton, suggestions from Dean Falk and Michel Hofman. 1997), Sangiran IX (Anton, 2003), Zhoukoudian V(Chiu et al., 1973), Gongwangling 1, Hexian, Narmada 1, Ngandong 1, Ngandong 6 (5), Appendix Ngandong 7, Ngandong (10), Ngandong 13 (11), Ngandong 14 (12), Ngawi, OH 9, OH 12, Notes for brain size data as used in Table 2. Sambungmacan 1, Sambungmacan 3, Fossil hominin endocranial volume Sambungmacan 4, Sangiran 2, Sangiran 3, measurements were taken from reviews as well Sangiran 4, Sangiran 10, Sangiran 12, Sangiran other papers. In order to maximize sample size, 17, Trinil 2 (1891), Zhoukoudian, Zhoukoudian 314

I, Zhoukoudian III (E), Zhoukoudian III (L), Nazlet Khater 2, Oberkassel 1, Oberkassel 2, Zhoukoudian VI (Holloway et al., 2004a), Bou- Omo-Kibbish 2, Pataud 1, Pavlov 1, Predmosti 3, VP-2/66, Buia (UA 31), Ceprano (Lee and Predmosti 4, Predmosti 9, Predmosti 10, Qafzeh Wolpoff, 2003), Nanjing 1 (Liu et al., 2005), 11, Qafzeh 6, Qafzeh 9, San Teodoro 1, San Poloyo PL-1 (Mowbray et al., 2000), Teodoro 2, San Teodoro 3, San Teodoro 5, Singa Zhoukoudian II (Weidenreich, 1943). 1, Skhul 1, Skhul 4, Skhul 5, Skhul 9, St. Germain- H. ergaster: Based on D2280, D2282, KNM-ER la-Riviere 1, Sungir 1, Sungir 2, Sungir 3, Sungir 5, 3733, KNM-ER 3883, KNM-WT 15000 Veyrier 1, Yinkou, Zhoukoudian (Upper Cave) 1, (Holloway et al., 2004a), D2700 (Lee and Zhoukoudian (Upper Cave) 2, Zhoukoudian Wolpoff, 2003). (Upper Cave) 3 (Holloway et al., 2004a), Eliye H. antecessor: Based on ATD-15 (Bermudez de Springs 11693, Omo-Kibbish 1, Paderbourne Castro et al., 1997). (Lee and Wolpoff, 2003), Arene Candide 1, H. heidelbergensis: Based on Steinheim Arene Candide 1-IP, Arene Candide 2, Arene (Rightmire, 2004), Florisbad (Aiello and Dean, Candide 4, Arene Candide 5, Asselar, Barma 1990), Vertesszollos II (Delson et al., 2000), Grande 2 (Ruff et al., 1997), Dolni Vestonice 8, Arago (composite), Atapuerca 4, Atapuerca 5, Dolni Vestonice 15, Dolni Vestonice 16 Atapuerca 6, Bodo, Broken Hill 1, Dali 1, (Schwartz and Tattersall, 2002), BOU-VP-16/1 Ehringsdorf, Jinniushan 1, Guomde, Lazaret, Pet- (White et al., 2003). ralona 1, Reilingen, Sale, SAM-PQ-EH1, H. floresiensis: Based on LB1 (Falk et al., 2005). Swanscombe, Yunxian (1 and 2) (Holloway et al., 2004a), Ndutu 1 (Rightmire, 1983 [in Rightmire, 2004]). H. neanderthalensis: Based on Krapina 4 Abbreviations (Delson et al., 2000), Ehringsdorf 9, Gibraltar 1, Le Moustier 1 (Grimaud-Hervé, 1997), Amud 1, AMHS anatomically modern Homo sapiens Biache-Saint Vaast, Engis 2, Ganovce 1, Gibraltar fAMHS fossil anatomically modern Homo 2, Krapina (4) 2, Krapina (4) 3, Krapina 6, La sapiens Chapelle-aux-Saints 1, La Ferrassie 1, La Quina rAMHS recent anatomically modern Homo 18, La Quina 5, Monte Circeo I, Neanderthal, sapiens Saccopastore I, Saccopastore II, Shanidar 5, Spy CQ cerebellar quotient I, Spy II, Tabun I, Teshik-Tash 1 (Holloway EQ encephalization quotient et al., 2004a), Fontéchevade, Shanidar 1 (Lee FAD first appearance datum and Wolpoff, 2003). L>R left larger than right H. sapiens s.s.: Based on Eyasi 1 (Easi) (Con- LORF left-occipital right-frontal roy, 1997), Kanjera 1 (Brauer, 1984), Border LS lunate sulcus Cave 1, Brno I, Brno II, Brno III, Bruniquel 2, MRCA most recent common ancestor Cap Blanc 1, Chancelade, Combe Capelle, Cro- Magnon I, Cro-Magnon III, Dolni Vestonice 3, References Dolni Vestonice 14, Dolni Vestonice 18, Dolni Vestonice 20, Dolni Vestonice 21, Grotte des Aboitiz, F., & Garcia, R. (1997). The anatomy of language – Enfants 4, Grotte des Enfants 5, Grotte des revisited. Brain Research Reviews, 30, 171 183. Aiello, L., & Dean, C. (1990). An introduction to human evo- Enfants 6, Herto 1/16, Jebel Irhoud 1, Jebel lutionary anatomy. London; San Diego: Academic Press. Irhoud 2, Kostenki 14, Kostenki 2, LH 18, Aldridge, K. (2011). Patterns of differences in brain morphol- Liujiang, Minatogawa 1, Minatogawa 2, ogy in humans as compared to extant apes. Journal of Minatogawa 4, Mladec 1, Mladec 2, Mladec 5, Human Evolution, 60,94–105. 315

Amunts, K., Schleicher, A., Burgel, U., Mohlberg, H., Bouzouggar, A., Barton, N., Vanhaeren, M., D’Errico, F., Uylings, H. B., & Zilles, K. (1999). Broca’s region revisited: Collcutt, S., Higham, T., et al. (2007). 82,000-year-old shell Cytoarchitecture and intersubject variability. The Journal of beads from North Africa and implications for the origins Comparative Neurology, 412, 319–341. of modern human behavior. Proceedings of the National Amunts, K., Schleicher, A., & Zilles, K. (2007). Academy of Sciences of the United States of America, 104, Cytoarchitecture of the cerebral cortex - More than localiza- 9964–9969. tion. Neuroimage, 37, 1061. Brauer, G. (1984). A craniological approach to the origin of Anton, S. C. (1997). Developmental age and taxonomic affin- anatomically modern Homo sapiens in Africa and ity of the Mojokerto child, Java, Indonesia. American Jour- implications for the appearance of modern Europeans. In nal of Physical Anthropology, 102, 497–514. F. Spencer (Ed.), The origin of modern humans: A world Anton, S. C. (2003). Natural history of Homo erectus. Year- survey of the fossil evidence (pp. 327–410). New York: Alan book of Physical Anthropology, 46, 126–170. R. Liss. Arbib, M. A. (2005). From monkey-like action recognition to Broadfield, D. C., Holloway, R. L., Mowbray, K., Silvers, A., human language: An evolutionary framework for neu- Yuan, M. S., & Marquez, S. (2001). Endocast of rolinguistics. The Behavioral and Brain Sciences, 28, Sambungmacan 3 (Sm 3): A new Homo erectus from 105–124 (discussion 125–67). Indonesia. Anatomical Record, 262, 369–379. Asfaw, B., Beyene, Y., Suwa, G., Walter, R. C., White, T. D., Bromage, T. G., McMahon, J. M., Thackeray, J. F., Woldegabriel, G., et al. (1992). The earliest Acheulean from Kullmer, O., Hogg, R., Rosenberger, A. L., et al. (2008). Konso-Gardula. Nature, 360, 732. Craniofacial architectural constraints and their Asfaw, B., White, T., Lovejoy, O., Latimer, B., Simpson, S., & importance for reconstructing the early Homo skull KNM- Suwa, G. (1999). Australopithecus garhi: A new species of ER 1470. The Journal of Clinical Pediatric Dentistry, 33, early hominid from Ethiopia. Science, 284, 629–635. 43–54. Bar-Yosef Mayer, D. E., Vandermeersch, B., & Bar-Yosef, O. Broom, R., & Robinson, J. T. (1948). Size of the brain in the (2009). Shells and ochre in Middle Paleolithic Qafzeh Cave, ape-man, Plesianthropus. Nature, 161, 438. Israel: Indications for modern behavior. Journal of Human Brown, P., Sutikna, T., Morwood, M. J., Soejono, R. P., Evolution, 56, 307–314. Jatmiko, , Saptomo, E. W., et al. (2004). A new small-bodied Begun, D. R., & Walker, A. (1993). The endocast. In A. hominin from the Late Pleistocene of Flores, Indonesia. Walker & R. Leakey (Eds.), The Nariokotome Homo Nature, 431, 1055–1061. erectus skeleton (pp. 326–358). Cambridge, MA: Harvard Bruner, E. (2004). Geometric morphometrics and University Press. paleoneurology: Brain shape evolution in the genus Homo. Benson, J., Greaves, W., O’Donnell, M., & Taglialatela, J. Journal of Human Evolution, 47, 279–303. (2002). Evidence for symbolic language processing in a Bruner, E., Manzi, G., & Arsuaga, J. L. (2003). bonobo (Pan paniscus). Journal of Consciousness Studies, Encephalization and allometric trajectories in the genus 9,33–56. Homo: Evidence from the Neandertal and modern lineages. Berger, L. R., de Ruiter, D. J., Churchill, S. E., Schmid, P., Proceedings of the National Academy of Sciences of the Carlson, K. J., Dirks, P. H., et al. (2010). Australopithecus United States of America, 100, 15335–15340. sediba: A new species of Homo-like australopith from South Cantalupo, C., & Hopkins, W. D. (2001). Asymmetric Broca’s Africa. Science, 328, 195–204. area in great apes. Nature, 414, 505. Bermudez de Castro, J. M., Arsuaga, J. L., Carbonell, E., Caramelli, D., Milani, L., Vai, S., Modi, A., Pecchioli, E., Rosas, A., Martinez, I., & Mosquera, M. (1997). A hominid Girardi, M., et al. (2008). A 28,000 years old Cro-Magnon from the lower Pleistocene of Atapuerca, Spain: Possible mtDNA sequence differs from all potentially contaminating ancestor to Neandertals and modern humans. Science, 276, modern sequences. PloS One, 3, e2700. 1392–1395. Cartmill, M., & Smith, F. H. (2009). The human lineage. Biederman, I., & Kim, J. G. (2008). 17,000 years of depicting Hoboken, NJ: Wiley-Blackwell. the junction of two smooth shapes. Perception, 37, 161–164. Carvalho, S., Cunha, E., Sousa, C., & Matsuzawa, T. (2008). Boesch, C. (1991). Symbolic communication in wild Chaînes opératoires and resource-exploitation strategies in chimpanzees? Human Evolution, 6,81–89. chimpanzee (Pan troglodytes) nut cracking. Journal of Bonmati, A., Gomez-Olivencia, A., Arsuaga, J. L., Human Evolution, 55, 148–163. Carretero, J. M., Gracia, A., Martinez, I., et al. (2010). Mid- Carvalho, S., Biro, D., McGrew, W. C., & Matsuzawa, T. dle Pleistocene lower back and pelvis from an aged human (2009). Tool-composite reuse in wild chimpanzees (Pan individual from the Sima de los Huesos site, Spain. Pro- troglodytes): archaeologically invisible steps in the techno- ceedings of the National Academy of Sciences of the United logical evolution of early hominins?. Animal Cognition, 12 States of America, 107, 18386–18391. (Suppl 1), S103–S114. 316

Charman, T., Jones, C. R., Pickles, A., Simonoff, E., Baird, G., Damasio, H., Grabowski, T. J., Tranel, D., Hichwa, R. D., & & Happe, F. (2010). Defining the cognitive phenotype of Damasio, A. R. (1996). A neural basis for lexical retrieval. autism. Brain Research, 1380,10–21. Nature, 380, 499–505. Chiu, C., Ku, Y., Chang, Y., & Chang, S. (1973). Peking man Dart, R. A. (1925). Australopithecus africanus: The man-ape of fossils and cultural remains newly discovered at South Africa. Nature, 115, 195–199. Choukoutien. Vertebrata Palasiatica, 11, 109–131. Dart, R. A. (1940). The status of Australopithecus. American Clark, J. D., Beyene, Y., Woldegabriel, G., Hart, W. K., Journal of Physical Anthropology, 26, 167–186. Renne, P. R., Gilbert, H., et al. (2003). Stratigraphic, chro- Davidson, I., & Noble, W. (1993). Tools and language in nological and behavioural contexts of Pleistocene Homo human evolution. In K. Gibson & T. Ingold (Eds.), Tools, sapiens from Middle Awash, Ethiopia. Nature, 423, 747–752. language and cognition in human evolution (pp. 363–388). Clark, G. A., & Riel-Salvatore, J. (2005). Observations on sys- Cambridge: Cambridge University Press. tematics in Paleolithic archaeology. In E. Hovers & S. L. de Heinzelin, J., Clark, J. D., White, T., Hart, W., Renne, P., Kuhn (Eds.), Transitions before the transition (pp. 29–56). Woldegabriel, G., et al. (1999). Environment and behavior New York: Springer. of 2.5-million-year-old Bouri hominids. Science, 284, Conard, N. J. (2003). Palaeolithic ivory sculptures from south- 625–629. western Germany and the origins of figurative art. Nature, de Sousa, A. A. (2008). Hominoid brain organization: 426, 830–832. Histometric and morphometric comparisons of visual Conard, N. J. (2010). Cultural modernity: Consensus or conun- brain structures. Ph.D., The George Washington University. drum? Proceedings of the National Academy of Sciences of de Sousa, A. A., Sherwood, C. C., Mohlberg, H., Amunts, K., the United States of America, 107, 7621–7622. Schleicher, A., Macleod, C. E., et al. (2010a). Hominoid Conard, N. J., Malina, M., & Munzel, S. C. (2009). New flutes visual brain structure volumes and the position of the lunate document the earliest musical tradition in southwestern sulcus. Journal of Human Evolution, 58, 281–292. Germany. Nature, 460, 737–740. de Sousa, A. A., Sherwood, C. C., Schleicher, A., Amunts, K., Connolly, C. J. (1950). External morphology of the primate Macleod, C. E., Hof, P. R., et al. (2010b). Comparative brain. Springfield, IL: C.C. Thomas. cytoarchitectural analyses of striate and extrastriate areas Conroy, G. C. (1997). Reconstructing human origins: A mod- in hominoids. Cerebral Cortex, 20, 966–981. ern synthesis. New York: W.W. Norton & Company. de Sousa, A., & Wood, B. A. (2007). The hominin fossil record Conroy, G. C., Weber, G. W., Seidler, H., Tobias, P. V., and the emergence of the modern human central nervous Kane, A., & Brunsden, B. (1998). Endocranial capacity in system. In J. H. Kaas & T. M. Preuss (Eds.), Evolution of an early hominid cranium from Sterkfontein, South Africa. nervous systems, Vol. 4: The evolution of primate nervous Science, 280, 1730–1731. systems (pp. 291–336). Oxford: Academic Press. Coqueugniot, H., Hublin, J. J., Veillon, F., Houet, F., & Deacon, T. W. (1997). The symbolic species: The co-evolution of Jacob, T. (2004). Early brain growth in Homo erectus and language and the brain. New York: W.W. Norton & Company. implications for cognitive ability. Nature, 431, 299–302. Deaner, R. O., Isler, K., Burkart, J., & van Schaik, C. (2007). Courchesne, E., Campbell, K., & Solso, S. (2010). Brain Overall brain size, and not encephalization quotient, best growth across the life span in autism: Age-specific changes predicts cognitive ability across non-human primates. Brain, in anatomical pathology. Brain Research, 1380, 138–145. Behavior and Evolution, 70, 115–124. Cunha, E., & Silva, H. P. (2005). A recente descoberta paleo- Dekaban, A. S., & Sadowsky, D. (1978). Changes in brain antropológica da Ilha das Flores: alguns comentários. weights during the span of human life: Relation of brain Antropo, [Online], 10. Available from: http://www.didac. weights to body heights and body weights. Annals of Neu- ehu.es/antropo/10/10-3/Cunha.pdf. rology, 4, 345–356. D’Errico, F., Henshilwood, C., Vanhaeren, M., & van Delson, E., Tattersall, I., Couvering, J. A. V., & Brooks, A. S. Niekerk, K. (2005). Nassarius kraussianus shell beads from (2000). Encyclopedia of human evolution and prehistory. Blombos Cave: Evidence for symbolic behaviour in the Mid- New York: Garland/Taylor & Francis. dle Stone Age. Journal of Human Evolution, 48,3–24. Desilva, J., & Lesnik, J. (2006). Chimpanzee neonatal brain D’Errico, F., & Lawson, G. (2006). The Sound Paradox. How size: Implications for brain growth in Homo erectus. Journal to assess the acoustic significance of archaeological evi- of Human Evolution, 51, 207–212. dence? In C. S. G. Lawson (Ed.), Archaeoacustics Dobson, J. E. (1998). The iodine factor in health and evolu- (pp. 41–57). Cambridge, UK: McDonald Institute. tion. Geographical Review, 88,3–28. D’Errico, F., & Stringer, C. B. (2011). Evolution, revolution or Dronkers, N. F., Plaisant, O., Iba-Zizen, M. T., & saltation scenario for the emergence of modern cultures? Cabanis, E. A. (2007). Paul Broca’s historic cases: High res- Philosophical Transactions of the Royal Society B: Biological olution MR imaging of the brains of Leborgne and Lelong. Sciences, 366, 1060–1069. Brain, 130, 1432–1441. 317

Duarte, C., Mauricio, J., Pettitt, P. B., Souto, P., Trinkaus, E., and Homo floresiensis. Proceedings of the National Academy van der Plicht, H., et al. (1999). The early Upper Paleolithic of Sciences of the United States of America, 104, 2513–2518. human skeleton from the Abrigo do Lagar Velho (Portugal) Falk, D., Hildebolt, C., Smith, K., Morwood, M. J., Sutikna, T., and modern human emergence in Iberia. Proceedings of the Jatmiko, et al. (2009). LB1’s virtual endocast, microcephaly, National Academy of Sciences, 96, 7604–7609. and hominin brain evolution. Journal of Human Evolution, Duff, A. I., Clark, G. A., & Chadderdon, T. J. O. (1992). Sym- 57, 597–607. bolism in the early Paleolithic: A conceptual odyssey. Falk, D., Redmond, J. C., Jr., Guyer, J., Conroy, C., Cambridge Archaeological Journal, 2, 211–229. Recheis, W., Weber, G. W., et al. (2000). Early hominid Elton, S., Bishop, L. C., & Wood, B. (2001). Comparative con- brain evolution: A new look at old endocasts. Journal of text of Plio-Pleistocene hominin brain evolution. Journal of Human Evolution, 38, 695–717. Human Evolution, 41,1–27. Fisher, S. E., & Marcus, G. F. (2006). The eloquent ape: Enard, W., Przeworski, M., Fisher, S. E., Lai, C. S., Wiebe, V., Genes, brains and the evolution of language. Nature Kitano, T., et al. (2002). Molecular evolution of FOXP2, a Reviews. Genetics, 7,9–20. gene involved in speech and language. Nature, 418, 869–872. Fisher, S. E., Vargha-Khadem, F., Watkins, K. E., Evans, P. D., Gilbert, S. L., Mekel-Bobrov, N., Monaco, A. P., & Pembrey, M. E. (1998). Localisation of a Vallender, E. J., Anderson, J. R., Vaez-Azizi, L. M., et al. gene implicated in a severe speech and language disorder. (2005). Microcephalin, a gene regulating brain size, con- Nature Genetics, 18, 168–170. tinues to evolve adaptively in humans. Science, 309, Frayer, D. W., Fiore, I., Lalueza-Fox, C., Radovcic, J., & 1717–1720. Bondioli, L. (2011a). Right handed Neandertals: Vindija Evans, P. D., Mekel-Bobrov, N., Vallender, E. J., and beyond. Journal of Anthropological Sciences, 88, Hudson, R. R., & Lahn, B. T. (2006). Evidence that the 113–127. adaptive allele of the brain size gene microcephalin Frayer, D. W., Lozano, M., Bermudez DE Castro, J. M., introgressed into Homo sapiens from an archaic Homo line- Carbonell, E., Arsuaga, J. L., Radovcic, J., et al. (2011b). age. Proceedings of the National Academy of Sciences of the More than 500,000 years of right-handedness in Europe. United States of America, 103, 18178–18183. Laterality, 1–19. Fadiga, L., & Craighero, L. (2006). Hand actions and speech Geyer, S., Schleicher, A., Schormann, T., Mohlberg, H., representation in Broca’s area. Cortex, 42, 486–490. Bodegard, A., Roland, P. E., & Zilles, K. (2001). Integration Falk, D. (1980a). A reanalysis of the South African of microstructural and functional aspects of human somato- australopithecine natural endocasts. American Journal of sensory areas 3a, 3b, and 1 on the basis of a computerized Physical Anthropology, 53, 525–539. brain atlas. Anatomy and Embryology (Berl), 204, 351–366. Falk, D. (1980b). Hominid brain evolution: The approach Gibbon, R. J., Granger, D. E., Kuman, K., & Partridge, T. C. from paleoneurology. Yearbook of Physical Anthropology, (2009). Early Acheulean technology in the Rietputs Forma- 23,93–107. tion, South Africa, dated with cosmogenic nuclides. Journal Falk, D. (1983). Cerebral cortices of East-African early of Human Evolution, 56, 152–160. hominids. Science, 221, 1072–1074. Goodall, J. (1986). The chimpanzees of Gombe: Patterns of Falk, D. (1985). Apples, oranges, and the lunate sulcus. Amer- behavior. Boston: Bellknap Press of the Harvard University ican Journal of Physical Anthropology, 67, 313–315. Press. Falk, D. (2007). The evolution of Broca’s area. IBRO History Gowlett, J. A. J. (2006). The elements of design form in Acheulian of Neuroscience, [Online]. Available from: http://www.ibro. bifaces: Modes, modalities, rules and languag. In N. Goren- org/Pub/Pub_Main_Display.asp?LC_Docs_ID¼3145. Inbar & G. Sharon (Eds.), Axe age: Acheulian tool-making Falk, D. (2009). The natural endocast of Taung from quarry to discard (pp. 203–221). London: Equinox. Australopithecus africanus: Insights from the unpublished Grabowski, T. J., Damasio, H., Tranel, D., Ponto, L. L., papers of Raymond Arthur Dart. American Journal of Phys- Hichwa, R. D., & Damasio, A. R. (2001). A role for left ical Anthropology, 140,49–65. temporal pole in the retrieval of words for unique entities. Falk, D., Hildebolt, C., Smith, K., Jungers, W., Larson, S., Human Brain Mapping, 13, 199–212. Morwood, M., et al. (2009). The type specimen (LB1) of Gracia, A., Martinez-Lage, J. F., Arsuaga, J. L., Martinez, I., Homo floresiensis did not have Laron syndrome. American Lorenzo, C., & Perez-Espejo, M. A. (2011). The earliest evi- Journal of Physical Anthropology, 140,52–63. dence of true lambdoid craniosynostosis: the case Falk, D., Hildebolt, C., Smith, K., Morwood, M. J., Sutikna, T., of "Benjamina", a Homo heidelbergensis child. Child's Brown, P., et al. (2005). The brain of LB1, Homo flo- Nervous System, 26, 723–727. resiensis. Science, 308, 242–245. Green, R. E., Krause, J., Briggs, A. W., Maricic, T., Falk, D., Hildebolt, C., Smith, K., Morwood, M. J., Sutikna, T., Stenzel, U., Kircher, M., et al. (2010). A draft sequence of Jatmiko, et al. (2007). Brain shape in human microcephalics the Neandertal genome. Science, 328, 710–722. 318

Grimaud-Hervé, D. (1997). L’évolution de l’encéphale chez Holloway, R. L. (1985). The past, present, and future signifi- Homo erectus et Homo sapiens. Paris: CNRS éditions. cance of the lunate sulcus. In P. V. Tobias, V. Strong & H. Grun, R., Stringer, C., McDermott, F., Nathan, R., Porat, N., White (Eds.), Hominid evolution: Past, present and future. Robertson, S., et al. (2005). U-series and ESR analyses of New York: A.R. Liss. bones and teeth relating to the human burials from Skhul. Holloway, R. L. (1992). The failure of the gyrification index Journal of Human Evolution, 49, 316–334. (GI) to account for volumetric reorganization in the evolu- Gunz, P., Neubauer, S., Maureille, B., & Hublin, J. J. (2010). tion of the human brain. Journal of Human Evolution, 22, Brain development after birth differs between Neanderthals 163. and modern humans. Current Biology, 20, R921–R922. Holloway, R. L. (1996). Evolution of the human brain. In A. Happe, F., Ronald, A., & Plomin, R. (2006). Time to give up Lock & C. R. Peters (Eds.), Handbook of human symbolic on a single explanation for autism. Nature Neuroscience, 9, evolution. New York: Clarendon Press. 1218–1220. Holloway, R. L. (2002). Brief communication: How much Haslam, M., Hernandez-Aguilar, A., Ling, V., Carvalho, S., de larger is the relative volume of area 10 of the prefrontal cor- la Torre, I., Destefano, A., et al. (2009). Primate archaeol- tex in humans? American Journal of Physical Anthropology, ogy. Nature, 460, 339–344. 118, 399–401. Hawks, J. (2011a). Denisova FOXP2 status. John Hawks Web- Holloway, R. L., Broadfield, D. C., & Yuan, M. S. (2003). log, [Online]. Available from: http://johnhawks.net/weblog/ Morphology and histology of chimpanzee primary visual reviews/denisova/foxp2-denisova-humanlike-2011.html. striate cortex indicate that brain reorganization predated Hawks, J. (2011b). Denisova microcephalin status. John brain expansion in early hominid evolution. Anatomical Hawks Weblog, [Online]. Available from: http://johnhawks. Record, 273A, 594–602. net/weblog/reviews/denisova/denisova-mcph1-2011.html. Holloway, R. L., Broadfied, D. C., & Yuan, M. (2004a). The Henshilwood, C. S., D’Errico, F., & Watts, I. (2009). Engraved human fossil record, volume three: Brain endocasts—The ochres from the Middle Stone Age levels at Blombos Cave, paleoneurological evidence. Hoboken, NJ: John Wiley & South Africa. Journal of Human Evolution, 57,27–47. Sons Inc. Henshilwood, C. S., D’Errico, F., Yates, R., Jacobs, Z., Holloway, R. L., Clarke, R. J., & Tobias, P. V. (2004b). Poste- Tribolo, C., Duller, G. A., et al. (2002). Emergence of mod- rior lunate sulcus in Australopithecus africanus: Was Dart ern human behavior: Middle Stone Age engravings from right? Comptes Rendus Palevol, 3, 287–293. South Africa. Science, 295, 1278–1280. Holloway, R. L., & De Lacoste-Lareymondie, M. C. (1982). Herndon, J. G., Tigges, J., Anderson, D. C., Klumpp, S. A., & Brain endocast asymmetry in pongids and hominids: Some McClure, H. M. (1999). Brain weight throughout the life preliminary findings on the paleontology of cerebral domi- span of the chimpanzee. The Journal of Comparative Neu- nance. American Journal of Physical Anthropology, 58, rology, 409, 567–572. 101–110. Hershkovitz, I., Kornreich, L., & Laron, Z. (2007). Compara- Hopkins, W. D., Hook, M., Braccini, S., & Schapiro, S. J. tive skeletal features between Homo floresiensis and (2003). Population-level right handedness for a coordinated patients with primary growth hormone insensitivity (Laron bimanual task in chimpanzees: Replication and extension in syndrome). American Journal of Physical Anthropology, a second colony of apes. International Journal of Primatol- 134, 198–208. ogy, 24, 677–689. Holloway, R. L. (1966). Cranial capacity, neural reorganiza- Hopkins, W. D., & Marino, L. (2000). Asymmetries in cerebral tion, and hominid evolution—Search for more suitable width in nonhuman primate brains as revealed by magnetic parameters. American Anthropologist, 68, 103–121. resonance imaging (MRI). Neuropsychologia, 38, 493–499. Holloway, R. L. (1968). The evolution of the primate brain: Hopkins, W. D., Phillips, K. A., Bania, A., Calcutt, S. E., Some aspects of quantitative relations. Brain Research, 7, Gardner, M., Russell, J., et al. (2011). Hand preferences 121–172. for coordinated bimanual actions in 777 great apes: Holloway, R. L. (1975). Early hominid endocasts: Volumes, Implications for the evolution of handedness in hominins. morphology and significance. In R. Tuttle (Ed.), Primate Journal of Human Evolution, 60, 605–611. functional morphology and evolution. The Hague: Mouton. Horel, J. A., Voytko, M. L., & Salsbury, K. G. (1984). Visual Holloway, R. L. (1980). Indonesian “Solo” (Ngandong) learning suppressed by cooling the temporal pole. Behav- endocranial reconstructions: Some preliminary observations ioral Neuroscience, 98, 310–324. and comparisons with Neandertal and Homo erectus groups. Humphrey, N. (1998). Cave art, autism, and the evolution of the American Journal of Physical Anthropology, 53, 285–295. human mind. Cambridge Archaeological Journal, 8, 165–191. Holloway, R. L. (1983). Human paleontological evidence rele- Hyvarinen, J. (1981). Regional distribution of functions in vant to language behavior. Human Neurobiology, 2, parietal association area 7 of the monkey. Brain Research, 105–114. 206, 287–303. 319

Ivanhoe, F. (1970). Was Virchow right about Neandertal? Le Gros Clark, W. E., Cooper, D. M., & Zuckerman, S. Nature, 227, 577–579. (1936). The endocranial cast of the chimpanzee. Journal of Jackson, A. P., Eastwood, H., Bell, S. M., Adu, J., Toomes, C., the Royal Anthropological Institute of Great Britain and Carr, I. M., et al. (2002). Identification of microcephalin, a Ireland, 66, 249–268. protein implicated in determining the size of the human Le May, M. (1976). Morphological cerebral asymmetries of brain. American Journal of Human Genetics, 71, 136–142. modern man, fossil man and nonhuman primates. Annals Jacob, T., Indriati, E., Soejono, R. P., Hsu, K., Frayer, D. W., of the New York Academy of Sciences, 280, 349–366. Eckhardt, R. B., et al. (2006). Pygmoid Australomelanesian Le May, M., Billig, M. S., & Geschwind, N. (1982). Homo sapiens skeletal remains from Liang Bua, Flores: Asymmetries in the brains and skulls of nonhuman Population affinities and pathological abnormalities. Pro- primates. In E. Armstrong & D. Falk (Eds.), Primate brain ceedings of the National Academy of Sciences of the United evolution: Methods and concepts (pp. 263–278). New York: States of America, 103, 13421–13426. Plenum Press. Jerison, H. J. (1973). Evolution of the brain and intelligence. Leakey, L. S. B., Tobias, P. V., & Napier, J. R. (1964). A new New York: Academic Press. species of genus Homo from Olduvai Gorge. Nature, 202,7–9. Jungers, W. L., Falk, D., Hildebolt, C., Smith, K., Prior, F., Lee, S. H., & Wolpoff, M. H. (2003). The pattern of evolution Tocheri, M. W., et al. (2009). The hobbits (Homo flo- in Pleistocene human brain size. Paleobiology, 29, 186–196. resiensis) were not cretins. American Association of Physical Leigh, S. R. (2004). Brain growth, life history, and cognition in Anthropologists, 138(S48), 244. primate and human evolution. American Journal of Prima- Kahlenberg, S. M., & Wrangham, R. W. (2010). Sex tology, 62, 139–164. differences in chimpanzees’ use of sticks as play objects Leigh, S. R. (2006). Brain ontogeny and life history in Homo resemble those of children. Current Biology, 20, erectus. Journal of Human Evolution, 50, 104–108 (author R1067–R1068. reply 109–13). Keith, A. (1931). New discoveries relating to the antiquity of Lewis, J. D., & Elman, J. L. (2008). Growth-related neural man. New York: Williams and Norgate. reorganization and the autism phenotype: A test of the Keller, S. S., Crow, T., Foundas, A., Amunts, K., & hypothesis that altered brain growth leads to altered connec- Roberts, N. (2009). Broca’s area: Nomenclature, anatomy, tivity. Developmental Science, 11, 135–155. typology and asymmetry. Brain and Language, 109,29–48. Liu, W., Zhang, Y., & Wu, X. (2005). Middle Pleistocene Kimbel, W. H., Walter, R. C., Johanson, D. C., Reed, K. E., human cranium from Tangshan (Nanjing), Southeast China: Aronson, J. L., Assefa, Z., et al. (1996). Late Pliocene A new reconstruction and comparisons with Homo erectus Homo and Oldowan tools from the Hadar Formation (Kada from Eurasia and Africa. American Journal of Physical Hadar member), Ethiopia. Journal of Human Evolution, 31, Anthropology, 127, 253–262. 549–561. Lozano, M., Mosquera, M., De Castro, J. M. B., Arsuaga, J. L. Klein, R. G. (1999). The human career: Human biological and & Carbonell, E. 2009. Right handedness of Homo cultural origins. Chicago: University of Chicago Press. heidelbergensis from Sima de los Huesos (Atapuerca, Spain) Klein, R. G. (2003). Whither the Neanderthals? Science, 299, 500,000 years ago. Evolution and Human Behavior, 30, 1525–1527. 369–376. Krause, J., Lalueza-Fox, C., Orlando, L., Enard, W., Lynch, J. C. (1980). The functional organization of posterior Green, R. E., Burbano, H. A., et al. (2007). The derived parietal association cortex. The Behavioral and Brain FOXP2 variant of modern humans was shared with Sciences, 3, 485–534. Neandertals. Current Biology, 17, 1908–1912. Macdermot, K. D., Bonora, E., Sykes, N., Coupe, A. M., Kuman, K., & Clarke, R. J. (2000). Stratigraphy, artefact Lai, C. S., Vernes, S. C., et al. (2005). Identification of industries and hominid associations for Sterkfontein, mem- FOXP2 truncation as a novel cause of developmental ber 5. Journal of Human Evolution, 38, 827–847. speech and language deficits. American Journal of Human Lai, C. S., Fisher, S. E., Hurst, J. A., Vargha-Khadem, F., & Genetics, 76, 1074–1080. Monaco, A. P. (2001). A forkhead-domain gene is mutated Macleod, C. E., Zilles, K., Schleicher, A., Rilling, J. K., & in a severe speech and language disorder. Nature, 413, Gibson, K. R. (2003). Expansion of the neocerebellum in 519–523. Hominoidea. Journal of Human Evolution, 44, 401–429. Lari, M., Rizzi, E., Milani, L., Corti, G., Balsamo, C., Vai, S., Marean, C. W., Bar-Matthews, M., Bernatchez, J., Fisher, E., et al. (2010). The microcephalin ancestral allele in a Nean- Goldberg, P., Herries, A. I., et al. (2007). Early human use derthal individual. PloS One, 5, e10648. of marine resources and pigment in South Africa during Le Gros Clark, W. E. (1947). Observations on the anatomy of the Middle Pleistocene. Nature, 449, 905–908. the fossil Australopithecinae. Journal of Anatomy, 81, Martin, R. D. (1981). Relative brain size and basal metabolic 300–333. rate in terrestrial vertebrates. Nature, 293,57–60. 320

Martin, R. D. (1990). Primate origins and evolution: A phylo- Oxnard, C., Obendorf, P. J., & Kefford, B. J. (2010). Post-cra- genetic reconstruction. London/New Jersey: Chapman Hall/ nial skeletons of hypothyroid cretins show a similar Princeton University Press. anatomical mosaic as Homo floresiensis. PloS One, 5, Martin, R. D., Maclarnon, A. M., Phillips, J. L., & e13018. Dobyns, W. B. (2006). Flores hominid: New species or Panger, M. A., Brooks, A. S., Richmond, B. G., & Wood, B. microcephalic dwarf? Anatomical Record, 288, 1123–1145. (2002). Older than the Oldowan? Rethinking the emergence McBrearty, S., & Brooks, A. (2000). The revolution that of hominin tool use. Evolutionary Anthropology, 11, wasn’t: A new interpretation of the origin of modern human 235–245. behavior. Journal of Human Evolution, 39, 453–563. Peeters, R., Simone, L., Nelissen, K., Fabbri-Destro, M., McBrearty, S., & Jablonski, N. G. (2005). First fossil chimpan- Vanduffel, W., Rizzolatti, G., et al. (2009). The representa- zee. Nature, 437, 105–108. tion of tool use in humans and monkeys: Common and McDougall, I., Brown, F. H., & Fleagle, J. G. (2005). Strati- uniquely human features. The Journal of Neuroscience, 29, graphic placement and age of modern humans from Kibish, 11523–11539. Ethiopia. Nature, 433, 733–736. Peirce, C. S. (1932). The icon, index, and symbol. In C. Har- McPherron, S. P. (2000). Handaxes as a measure of the mental tshorne & P. Weis (Eds.), The collected papers of Charles Sand- capabilities of early hominids. Journal of Archaeological Sci- ers Peirce, Vol. II (pp. 156–173). Cambridge, MA: Harvard. ence, 27, 655–663. Peresani, M., Fiore, I., Gala, M., Romandini, M., & McPherron, S. P., Alemseged, Z., Marean, C. W., Wynn, J. G., Tagliacozzo, A. (2011). Late Neandertals and the inten- Reed, D., Geraads, D., et al. (2010). Evidence for tional removal of feathers as evidenced from bird bone stone-tool-assisted consumption of animal tissues before taphonomy at Fumane Cave 44 ky B.P., Italy. Proceedings 3.39 million years ago at Dikika, Ethiopia. Nature, 466, of the National Academy of Sciences of the United States of 857–860. America, 108, 3888–3893. Mercader, J., Panger, M., & Boesch, C. (2002). Excavation of a Plummer, T. (2004). Flaked stones and old bones: Biological chimpanzee stone tool site in the African rainforest. Science, and cultural evolution at the dawn of technology. American 296, 1452–1455. Journal of Physical Anthropology, 125, 118–164. Mignault, C. (1985). Transition between sensorimotor and Ponce de Leon, M. S., Golovanova, L., Doronichev, V., symbolic activities in nursery-reared chimpanzees (Pan Romanova, G., Akazawa, T., Kondo, O., et al. (2008). Nean- troglodytes). Journal of Human Evolution, 14, 747–758. derthal brain size at birth provides insights into the evolution Montgomery, S. H., Capellini, I., Venditti, C., Barton, R. A., & of human life history. Proceedings of the National Academy Mundy, N. I. (2011). Adaptive evolution of four microceph- of Sciences of the United States of America, 105, 13764–13768. aly genes and the evolution of brain size in Powell, A., Shennan, S., & Thomas, M. G. (2009). Late Pleis- anthropoid primates. Molecular Biology and Evolution, 28, tocene demography and the appearance of modern human 625–638. behavior. Science, 324, 1298–1301. Mowbray, K., Marquez, S., & Anton, S. (2000). The newly Pruetz, J. D., & Bertolani, P. (2007). Savanna chimpanzees, recovered Poloyo hominin (PL-1) from Java. American Pan troglodytes verus, hunt with tools. Current Biology, 17, Journal of Physical Anthropology Supplement, 30, 233. 412–417. Nakamura, K., & Kubota, K. (1995). Mnemonic firing of Radinsky, L. (1972). Endocasts and studies of primate brain neurons in the monkey temporal pole during a visual recog- evolution. In R. Tuttle (Ed.), The functional and evolution- nition memory task. Journal of Neurophysiology, 74, ary biology of primates. Chicago: Aldine-Atherton Inc. 162–178. Rademacher, J., Burgel, U., Geyer, S., Schormann, T., Neubauer, S., Gunz, P., & Hublin, J. J. (2010). Endocranial Schleicher, A., Freund, H. J., & Zilles, K. (2001). Variability shape changes during growth in chimpanzees and humans: and asymmetry in the human precentral motor system. A A morphometric analysis of unique and shared aspects. cytoarchitectonic and myeloarchitectonic brain mapping Journal of Human Evolution, 59, 555–566. study. Brain, 124, 2232–2258. Neubauer, S., Gunz, P., Mitteroecker, P., & Weber, G. W. Reich, D., Green, R. E., Kircher, M., Krause, J., Patterson, N., (2004). Three-dimensional digital imaging of the partial Durand, E. Y., et al. (2010). Genetic history of an archaic Australopithecus africanus endocranium MLD 37/38. Cana- hominin group from Denisova Cave in Siberia. Nature, dian Association of Radiologists Journal, 55, 271–278. 468, 1053–1060. Obendorf, P. J., Oxnard, C. E., & Kefford, B. J. (2008). Are Resnick, S. M., Pham, D. L., Kraut, M. A., Zonderman, A. B., the small human-like fossils found on Flores human endemic & Davatzikos, C. (2003). Longitudinal magnetic resonance cretins? Proceedings of the Royal Society of London Series imaging studies of older adults: A shrinking brain. The Jour- B-Biological Sciences, 275, 1287–1296. nal of Neuroscience, 23, 3295–3301. 321

Ricklan, D. E. (1987). Functional anatomy of the hand of Semendeferi, K., & Damasio, H. (2000). The brain and its Australopithecus africanus. Journal of Human Evolution, main anatomical subdivisions in living hominoids using mag- 16, 643–664. netic resonance imaging. Journal of Human Evolution, 38, Riel-Salvatore, J., & Clark, G. A. (2001). Grave markers: Mid- 317–332. dle and Early Upper Paleolithic burials and the use of Semendeferi, K., Damasio, H., Frank, R., & van chronotypology in contemporary Paleolithic research. Cur- Hoesen, G. W. (1997). The evolution of the frontal lobes: rent Anthropology, 42, 449–479. A volumetric analysis based on three-dimensional Rightmire, G. P. (2004). Brain size and encephalization in reconstructions of magnetic resonance scans of human and early to mid-Pleistocene Homo. American Journal of Physi- ape brains. Journal of Human Evolution, 32, 375–388. cal Anthropology, 124, 109–123. Semendeferi, K., Lu, A., Schenker, N., & Damasio, H. (2002). Rilling, J. K., & Insel, T. R. (1998). Evolution of the cerebel- Humans and great apes share a large frontal cortex. Nature lum in primates: Differences in relative volume among Neuroscience, 5, 272–276. monkeys, apes and humans. Brain, Behavior and Evolution, Semendeferi, K., Teffer, K., Buxhoeveden, D. P., Park, M. S., 52, 308–314. Bludau, S., Amunts, K., et al. (2011). Spatial organization of Rilling, J. K., & Insel, T. R. (1999). The primate neocortex in neurons in the frontal pole sets humans apart from great comparative perspective using magnetic resonance imaging. apes. Cerebral Cortex, 21(7), 1485–1497. Journal of Human Evolution, 37, 191–223. Sherwood, C. C., Broadfield, D. C., Holloway, R. L., Rilling, J. K., & Seligman, R. A. (2002). A quantitative mor- Gannon, P. J., & Hof, P. R. (2003). Variability of Broca’s phometric comparative analysis of the primate temporal area homologue in African great apes: Implications for lan- lobe. Journal of Human Evolution, 42, 505–533. guage evolution. Anatomical Record, 271A, 276–285. Rizzolatti, G., & Arbib, M. A. (1998). Language within our Sherwood, C. C., Holloway, R. L., Semendeferi, K., & grasp. Trends in Neurosciences, 21, 188–194. Hof, P. R. (2005). Is prefrontal white matter enlargement a Ruff, C. B., Trinkaus, E., & Holliday, T. W. (1997). Body mass human evolutionary specialization? Nature Neuroscience, 8, and encephalization in Pleistocene Homo. Nature, 387, 537–538. 173–176. Shibata, T., & Ioannides, A. A. (2001). Contribution of the Schenker, N. M., Buxhoeveden, D. P., Blackmon, W. L., human superior parietal lobule to spatial selection process: Amunts, K., Zilles, K., & Semendeferi, K. (2008). A com- An MEG study. Brain Research, 897, 164–168. parative quantitative analysis of cytoarchitecture and mini- Simon, O., Mangin, J. F., Cohen, L., Le Bihan, D., & columnar organization in Broca’s area in humans and great Dehaene, S. (2002). Topographical layout of hand, eye, cal- apes. The Journal of Comparative Neurology, 510, 117–128. culation, and language-related areas in the human parietal Schepers, G. W. H. (1946). The endocranial casts of the South lobe. Neuron, 33, 475–487. African apemen. In R. Broom & G. W. H. Schepers (Eds.), Skinner, M., & Wood, B. (2006). The evolution of modern The South African fossil apemen: The Australopithecinae. human life history—A paleontological perspective. In K. Pretoria: Transvaal Museum. Hawkes & R. Paine (Eds.), The evolution of modern human Schick, K. D., Toth, N., Garufi, G., Savage-Rumbaugh, E., life history. Santa Fe: School of American research. Rumbaugh, D., & Sevcik, R. (1999). Continuing Smith, G. E. (1927). Evolution of man: Essays. London: investigations into the stone tool-making and tool-using Oxford University Press. capabilities of a Bonobo (Pan paniscus). Journal of Archae- Soressi, M., & D’errico, F. (2007). Pigments, gravures, parures: ological Science, 26, 821–832. Les comportements symboliques controversés des Schoenemann, P. T., Sheehan, M. J., & Glotzer, L. D. (2005). Néandertaliens. In B. Vandermeersch & B. Maureille Prefrontal white matter volume is disproportionately larger (Eds.), Les Néandertaliens. Biologie et cultures, (Vol. 23), in humans than in other primates. Nature Neuroscience, 8, (pp. 297–309). Paris: Éditions du CTHS. 242–252. Spikins, P. A., Rutherford, H. E., & Needham, A. P. (2010). Schwartz, J. H., & Tattersall, I. (2002). The human fossil From homininity to humanity: Compassion from the earliest record, volume 1. Terminology and craniodental morphology archaics to modern humans. Time and Mind, 3, 303–325. of genus Homo (Europe). New York: Wiley-Liss. Stout, D., Passingham, R., Frith, C., Apel, J., & Chaminade, T. Semaw, S., Renne, P., Harris, J. W., Feibel, C. S., (2011). Technology, expertise and social cognition in human Bernor, R. L., Fesseha, N., et al. (1997). 2.5-million-year- evolution. The European Journal of Neuroscience, 33, old stone tools from Gona, Ethiopia. Nature, 385, 333–336. 1328–1338. Semendeferi, K., Armstrong, E., Schleicher, A., Zilles, K., & Stout, D., Toth, N., Schick, K., & Chaminade, T. (2008). Neural van Hoesen, G. W. (2001). Prefrontal cortex in humans correlates of Early Stone Age toolmaking: Technology, lan- and apes: A comparative study of area 10. American Journal guage and cognition in human evolution. Philosophical Trans- of Physical Anthropology, 114, 224–241. actions of the Royal Society of London B, 363, 1939–1949. 322

Stout, D., Toth, N., Schick, K., Stout, J., & Hutchins, G. Weaver, A. H. (2005). Reciprocal evolution of the cerebellum (2000). Stone tool-making and brain activation: Position and neocortex in fossil humans. Proceedings of the National emission tomography (PET) studies. Journal of Archaeolog- Academy of Sciences of the United States of America, 102, ical Science, 27, 1215–1223. 3576–3580. Susman, R. L. (1994). Fossil evidence for early hominid tool Weidenreich, F. (1943). The skulls of Sinanthropus pekinensis: use. Science, 265, 1570–1573. A comparative study on a primitive hominid skull. Susman, R. L. (1998). Hand function and tool behavior in Palaeontologia Sinica, Series D, 10,1–485. early hominids. Journal of Human Evolution, 35,23–46. Wendt, W. E. (1974). “Art mobilier” aus der Apollo 11-Grotte Suwa, G., Asfaw, B., Kono, R. T., Kubo, D., Lovejoy, C. O., & in Südwest-Afrika. Acta praehistorica et archaeologica, 5,1–42. White, T. D. (2009). The Ardipithecus ramidus skull and its Wendt, W. E. (1975). "Art Mobilier" from the Apollo 11 implications for hominid origins. Science, 326, 68e1–68e7. Cave, South West Africa: Africa's oldest dated works of Symington, J. (1916). Endocranial casts and brain form: A crit- art. South African Archaeological Bulletin, 31,5–11. icism of some recent speculations. Journal of Anatomy and White, T., Asfaw, B., Degusta, D., Gilbert, H., Richards, G. D., Physiology, 11, 111–130. Suwa, G., et al. (2003). Pleistocene Homo sapiens from Tobias, P. V. (1975). Brain evolution in the Hominoidea. In Middle Awash, Ethiopia. Nature, 423, 742–747. R. H. Tuttle (Ed.), Primate functional morphology and evo- Whiten, A., & van Schaik, C. P. (2007). The evolution of ani- lution. The Hague: Mouton. mal “cultures” and social intelligence. Philosophical Trans- Tobias, P. V. (1987). The brain of Homo habilis: A new level actions of the Royal Society B: Biological Sciences, 362, 603. of organization in cerebral evolution. Journal of Human Wood, B., & Collard, M. (1999). The human genus. Science, Evolution, 16, 741. 284,65–71. Tobias, P. V. (1991). Olduvai Gorge, Volume 4. The skulls, Wood, B., & Lonergan, N. (2008). The hominin fossil record: endocasts and teeth of Homo habilis. Cambridge: Cambridge Taxa, grades and clades. Journal of Anatomy, 212, 354–376. University Press. Wynn, T., & McGrew, W. C. (1989). An ape’s view of the Tocheri, M. W., Orr, C. M., Jacofsky, M. C., & Marzke, M. W. Oldowan. Man, 24, 383–398. (2008). The evolutionary history of the hominin hand since Yantis, S., Schwarzbach, J., Serences, J. T., Carlson, R. L., the last common ancestor of Pan and Homo. Journal of Steinmetz, M. A., Pekar, J. J., et al. (2002). Transient neural Anatomy, 212, 544–562. activity in human parietal cortex during spatial attention Toth, N. (1985). Archaeological evidence for preferential shifts. Nature Neuroscience, 5, 995–1002. right-handedness in the Lower and Middle Pleistocene, Zilhão, J. (2006). Neandertals and moderns mixed, and it and its possible implications. Journal of Human Evolution, matters. Evolutionary Anthropology, 15, 183–195. 14, 607–614. Zilhão, J. (2007). The emergence of ornaments and art: An Toth, N., & Schick, K. (2009). The Oldowan: The tool making archaeological perspective on the origins of “behavioral of early hominins and chimpanzees compared. Annual modernity” Journal of Archaeological Research, 15,1–54. Review of Anthropology, 38, 289–305. Zilhão, J., Angelucci, D. E., Badal-Garcia, E., D’Errico, F., Toth, N., Schick, K. D., Savage-Rumbaugh, E. S., Daniel, F., Dayet, L., et al. (2010). Symbolic use of marine Sevcik, R. A., & Rumbaugh, D. M. (1993). Pan the tool- shells and mineral pigments by Iberian Neandertals. Pro- maker: Investigations into the stone tool-making and tool- ceedings of the National Academy of Sciences of the United using capabilities of a bonobo (Pan paniscus). Journal of States of America, 107(3), 1023–1028. Archaeological Science, 20,81–91. Zilles, K., Armstrong, E., Moser, K. H., Schleicher, A., & Uomini, N. T. (2009). The prehistory of handedness: Archaeo- Stephan, H. (1989). Gyrification in the cerebral cortex of logical data and comparative ethology. Journal of Human primates. Brain, Behavior and Evolution, 34, 143–150. Evolution, 57, 411–419. Zilles, K., Armstrong, E., Schleicher, A., & Kretschmann, H. J. Vanhaereny, M., D’Errico, F., Stringer, C., James, S. L., (1988). The human pattern of gyrification in the cerebral Todd, J. A., & Mienis, H. K. (2006). Middle Paleolithic shell cortex. Anatomy and Embryology, 179, 173–179. beads in Israel and Algeria. Science, 312, 1785–1788. Zollikofer, C. P. E., Ponce de Leon, M. S., Lieberman, D. E., Weaver, A. G. H. (2001). The cerebellum and cognitive evolu- Guy, F., Pilbeam, D., Likius, A., et al. (2005). Virtual cranial tion in Pliocene and Pleistocene hominids. The University of reconstruction of Sahelanthropus tchadensis. Nature, 434, New Mexico: Unpublished doctoral dissertation. 755–759.