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Cite this article
* Kubo Daisuke,
* Kono Reiko T. and
* Kaifu Yousuke

2013Brain size of Homo floresiensis and its evolutionary implicationsProc. R.
Soc. B.2802013033820130338http://doi.org/10.1098/rspb.2013.0338

SECTION

* Abstract
* 1. Introduction
* 2. Background and research design
* 3. Material and methods
* 4. Results
* 5. Discussion and conclusions
* Acknowledgements
* Footnotes

Supplemental Material
You have accessResearch articles

BRAIN SIZE OF HOMO FLORESIENSIS AND ITS EVOLUTIONARY IMPLICATIONS

Daisuke Kubo

Department of Biological Sciences, The University of Tokyo, 7-3-1 Hongo,
Bunkyo-ku, Tokyo 113-0033, Japan

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,
Reiko T. Kono

Reiko T. Kono

Department of Anthropology, National Museum of Nature and Science, 4-1-1
Amakubo, Tsukuba-shi, Ibaraki 305-0005, Japan

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and
Yousuke Kaifu

Yousuke Kaifu

Department of Biological Sciences, The University of Tokyo, 7-3-1 Hongo,
Bunkyo-ku, Tokyo 113-0033, Japan

Department of Anthropology, National Museum of Nature and Science, 4-1-1
Amakubo, Tsukuba-shi, Ibaraki 305-0005, Japan

kaifu@kahaku.go.jp

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Daisuke Kubo

Department of Biological Sciences, The University of Tokyo, 7-3-1 Hongo,
Bunkyo-ku, Tokyo 113-0033, Japan

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,
Reiko T. Kono

Reiko T. Kono

Department of Anthropology, National Museum of Nature and Science, 4-1-1
Amakubo, Tsukuba-shi, Ibaraki 305-0005, Japan

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Yousuke Kaifu

Yousuke Kaifu

Department of Biological Sciences, The University of Tokyo, 7-3-1 Hongo,
Bunkyo-ku, Tokyo 113-0033, Japan

Department of Anthropology, National Museum of Nature and Science, 4-1-1
Amakubo, Tsukuba-shi, Ibaraki 305-0005, Japan

kaifu@kahaku.go.jp

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Published:07 June 2013https://doi.org/10.1098/rspb.2013.0338

ABSTRACT

The extremely small endocranial volume (ECV) of LB1, the type specimen of Homo
floresiensis, poses a challenge in our understanding of human brain evolution.
Some researchers hypothesize dramatic dwarfing of relative brain size from Homo
erectus presumably without significant decrease in intellectual function,
whereas others expect a lesser degree of brain diminution from a more primitive,
small-brained form of hominin currently undocumented in eastern Asia. However,
inconsistency in the published ECVs for LB1 (380–430 cc), unclear human
intraspecific brain–body size scaling and other uncertainties have hampered
elaborative modelling of its brain size reduction. In this study, we accurately
determine the ECV of LB1 using high-resolution micro-CT scan. The ECV of LB1
thus measured, 426 cc, is larger than the commonly cited figure in previous
studies (400 cc). Coupled with brain–body size correlation in Homo sapiens
calculated based on a sample from 20 worldwide modern human populations, we
construct new models of the brain size reduction in the evolution of H.
floresiensis. The results show a more significant contribution of scaling effect
than previously claimed.

1. INTRODUCTION

Homo floresiensis is a diminutive, extinct hominin species from the Late
Pleistocene of the Flores Island, eastern Indonesia. Since its initial
publication [1,2], the extremely small endocranial volume (ECV) for the type
specimen, LB1 (approx. 400 cc), which is comparable to Australopithecus, has
been a point of intensive debate [1–14]. Two major explanatory hypotheses
discussed are (i) H. floresiensis experienced dramatic brain size reduction from
the condition of Homo erectus (approx. 1000 cc) on an isolated insular setting,
and (ii) the species was derived directly from a more primitive and
smaller-brained form such as Homo habilis (approx. 600 cc) or even
Australopithecus (approx. 400 cc). Either possibility has major implication. The
former implies that insular brain dwarfing to an unparalleled degree has been a
significant factor in the hominin evolution on Flores, whereas the latter
demands a revision of the current Out of Africa 1 hypothesis, which supposes H.
erectus as the first hominin dispersed deep into Eurasia. Some researchers
suspect that the LB1 cranium is from a microcephalic modern human, but so far
such claims have failed to show a case of modern human patient with overall
skeletal characteristics similar to LB1 (reviewed in [15], but see [16]).
Although the possibility that LB1 was an archaic hominin individual with
microcephaly may not be entirely rejected at the present stage of the research,
the robust limb bones, phalanges with osteophytes and signs of healed trauma on
the cranial vault and tibia point to an active life rather than a disabled
condition in this individual [17].

In order to investigate the actual amount of brain size reduction in H.
floresiensis and its evolutionary causes, we first need to know the ECV and body
size in H. floresiensis as well as those of its ancestor candidates. Then, we
will be able to evaluate proportions of the brain size decrease explained by
intraspecific allometric scaling with body size and other factors such as
insular dwarfism of the relative brain size. However, presently, there remain
several issues to be resolved to discuss this question: (i) inconsistency in the
published ECVs for LB1 (380–430 cc: [1,3,6,18]); (ii) uncertain intraspecific
brain–body scaling in the extant Homo species, Homo sapiens [19]; (iii)
difficulty in estimating brain and body size in fossil hominins, and (iv) lack
of our knowledge about possible degree of brain size reduction in insular
primate and hominin species. The purposes of this study are to improve the
situations of (i) and (ii) for more accurate modelling of possible brain
reduction in the evolution of H. floresiensis. Although not only brain size but
also neural arrangement and connectivity are important in understanding brain
evolution of this species, we here focus on the former as a palaeontologically
measureable element.

2. BACKGROUND AND RESEARCH DESIGN

(A) CT-BASED ENDOCRANIAL VOLUME MEASUREMENT

Using traditional seed displacement methods, the ECV of LB1 was initially
measured as 380 cc [1], whereas Jacob et al. [6] obtained 430 cc after removing
some ‘breccia’ from the endocranial surface. Another report is 417 cc which is
based on a virtual endocast from CT data taken by a medical CT scanner, with
interpolation of missing areas and adjustment of slight taphonomic distortion
[3]. Holloway et al. [18] independently examined the medical CT scan. They also
found some distortion in the endocranial form, and suggested that the original
undistorted endocast was somewhat smaller than 417 cc.

Advances in X-ray CT and computer imaging technology now allow us more accurate
measurement of ECV from a fossil skull than has been possible. Still, a CT-based
ECV measurement is affected by various types of error. Some are related to the
nature of the cranial specimen (missing parts, damages, distortions, sedimentary
matrix or adhesive left in the endocranial cavity, etc.), and others owing to
calibration of the CT-scan system, scan resolution, artefacts such as beam
hardening and methods of segmentation of the endocranium [20–22]. In this study,
we attempt to minimize these errors.

We use a new, high-resolution/quality micro-CT scan of the LB1 cranium [23] to
measure its ECV. Fortunately, the LB1 cranium is nearly complete with no
substantial post-mortem deformation [1,23]. However, there are numerous cracking
and small damages to be filled; small patches of sediments are still attached on
the endocranial surfaces and these must be removed. The accuracy of ECV
measurement in LB1 rests primarily on the accuracy of locating such damages and
sediments, as well as that of reconstructing these damages. In order to
facilitate such works, we prepared physical replicas (three-dimensional prints)
of the virtually sectioned cranium, which enabled us three-dimensional ‘direct’
observation of the endocranial surface topography (figure 1).

Figure 1. Physical replicas (three-dimensional prints) of horizontally sectioned
cranium of LB1 (a) before and (b) after cleaning and clay-based reconstruction.
(Online version in colour.)

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(B) INTRASPECIFIC BRAIN–BODY SIZE SCALING FOR HOMO SAPIENS

Martin et al. [7,8] cited values of 0.03–0.17 as intraspecific scaling exponents
for H. sapiens when they claimed that the brain of LB1 is far too small to be
attributed to intraspecific dwarfism in H. erectus. These figures are from a
study on a modern Danish sample [24], and may not be appropriate for this
polymorphic and geographically widely distributed species. Brain–body size
correlation is normally weak within each regional group of H. sapiens, but
becomes higher among the groups [19]. Because we are here dealing with evolution
to a new species, we investigate not within- but between-regional group,
species-wide trend of H. sapiens by analysing data from various regional
samples.

Researchers are debating whether H. floresiensis originated from H. erectus or
more primitive forms of African Homo or even Australopithecus (reviewed in
[15]). Some studies support the latter view [25,26], although currently we have
no evidence for the presence of such primitive hominins in eastern Asia (see
additional discussion about this issue in [23]). Recent craniological studies
strongly suggest that H. floresiensis evolved from early Indonesian H. erectus
from the Early Pleistocene of Java (ECV: approx. 800–1000 cc) [23,27], not from
a generalized condition of H. erectus sensu lato represented by the mean of its
global sample (ECV: approx. 991 cc) [7–11]. Importantly, this view is compatible
with a recent finding that archaic hominins reached Flores by 1.0 Ma [28]. The
early Indonesian H. erectus fossil assemblage can be further divided into
stratigraphically upper and lower groups, which show significant morphological
differences from each other [29,30]. Because the former likely postdate 1.0 Ma
[31], the latter, which currently represents the oldest H. erectus assemblage
from Java, is a likely ancestor candidate for H. floresiensis.

In this study, we construct models of brain size decrease from H. habilis and
early Indonesian H. erectus. We pay particular attention to the latter not only
because we believe it plausible, but also because this, the one supposing a
dramatic relative brain size reduction, is the most challenging hypothesis in
terms of human brain evolution.

3. MATERIAL AND METHODS

(A) ENDOCRANIAL VOLUME CALCULATION

(I) CT SCAN AND THREE-DIMENSIONAL PRINTS

ECV measurement was performed based on the serial CT data reconstructed as a 512
× 512 × 593 matrix of isotropic voxels of 0.260 mm size, which was obtained in
2009 by a microfocal X-ray CT system TX225-ACTIS (Tesco Co.), at the University
Museum, University of Tokyo [23]. Prior to the scan of the LB1 cranium, the
system was calibrated with known size phantoms; linear measurement error in a
horizontal plane was less than 0.1 per cent [20], and the error along the
vertical axis, which mostly depends on machine accuracy of the specimen stage,
was less than 10 μm.

In order to directly observe the endocranial surfaces, we created
three-dimensional prints of horizontally sectioned neurocranium (figure 1a),
based on the micro-CT scan and using a three-dimensional printer system (EDEN
260, Objet Geometries, MA, USA). Half maximum height (HMH) thresholding between
the CT values of air and bone was used for segmentation. Polygon surface models
were extracted from the volume data, using the marching cube routine in Analyze
v. 8.1 (Mayo Clinic, MN, USA) to generate the three-dimensional prints.

(II) PREPARATION, PRESERVATION AND PATHOLOGICAL ALTERATION

The states of endocranial preservation and morphology were inspected based on
the CT imagery, original specimen (from the anatomical foramina and holes caused
by damages) and the horizontally sectioned three-dimensional prints (see the
electronic supplementary material, figure S1 and text S1). On the endocranial
surfaces of LB1, relatively large pieces of the bone are missing at the
endobregma, left orbital surface, much of the sphenoid lesser wings including
the anterior clinoid processes, right sphenosquamous suture, dorsum sellae, the
anterior tip of right petrous and right sigmoid sinus. Otherwise, the
endocranial surfaces of LB1 are well preserved, with some regions still covered
by minute lumps or thin patches of sediments. The reconstructed alignment of the
bones is also good [1,23]. Some parts of the bones are slightly dislocated
inward owing to minor cracking inside the bone, but their effects on the ECV
appear to be negligible. One small but noticeable distortion lies in the right
petrous bone, but we left this distortion uncorrected because it would not
significantly affect the ECV (see the electronic supplementary material, figure
S1d).

Pathological alteration of endocranial bones, if present, may affect the ECV as
a measure of the brain volume. Vannucci et al. [16] suggested that the LB1 brain
was pathological showing (i) ‘very prominent gyri recti of the frontal lobes,
suggestive of microgyria’, (ii) ‘asymmetry of the temporal lobes, the left
appearing abnormally small on the lateral surface’ and (iii) ‘a keel-like dorsal
expansion of the lower brain-stem’. Falk et al. [3,5] view the character (i) as
a non-pathological, derived feature in H. floresiensis. The character (ii) may
be ascribed to deformational plagiocephaly [17,32], and (iii) are not evident in
our virtual endocast. In either case, these reflect aspects of the brain
substance that should be included in ECV measurement.

Along the sagittal suture and around the vertex of the LB1 cranium, a relatively
large area of the inner parietal bone surface (40 mm anteroposteriorly and 25 mm
transversely) is depressed approximately 3 mm superiorly (evident in figure 2).
No signs of bone fracture are evident, and the three-layer structure of the
cranial bone (inner and outer tables, and diploe) appears to remain undisturbed
in the CT sections, indicating that the depression was present when this
individual was alive. Because depressions similar to this were also observed in
a few modern human skulls, we decided to include the space for the endocranial
depression (approx. 1.7 cc) in our ECV measurement.

Figure 2. Virtual endocast of LB1 showing reconstructed areas. Anterior,
posterior, right lateral, left lateral, basal and superior views (clockwise).
Grey, intact original bone surface (untreated); light blue, clay reconstruction
of relatively simple surfaces; blue, clay reconstruction of relatively complex
structures (with minute digital correction when necessary); orange, anatomical
foramina, and cracks and other damages treated digitally. See text for
methodological details.

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(III) RECONSTRUCTION OF THE ENDOCAST AND ITS ERROR ESTIMATION

We used Analyze v. 8.1 (Mayo Clinic), Amira v. 5.3 (Visage Imaging, Inc., CA,
USA) and Rapidform v. 2006 (INUS Technology, Inc., Seoul) to conduct the
following works. By observing the original specimen and the CT sections, we
first virtually removed sedimentary matrix attached to the endocranial surfaces
(see the electronic supplementary material, figure S2), and we again made
horizontally sectioned three-dimensional prints based on this ‘virtually cleaned
CT imagery’. Upon these replicas, we reconstructed the missing/damaged
endocranial bones by putting and moulding modelling clay with reference to
endocranial morphology of modern humans (figure 1b). Fortunately, sufficient
endocranial bones remain intact for LB1, and clay reconstructions can be
reasonably executed by extending preserved bone surfaces and/or mirror imaging
the intact other side (see the electronic supplementary material, text S1).
After these clay reconstructions, the upper and lower braincase replicas were
physically joined together for another CT scan to create the ‘replica CT imagery
with clay reconstructions’.

Then, we digitally superimposed this ‘replica CT imagery with clay
reconstructions’ on the ‘virtually cleaned CT imagery’, so that the replica
parts of the former are replaced by the original CT scan of the cranial bones in
the latter. Small gaps untreated by clay and parts of the clay reconstructions,
when found to be inappropriate, were then further corrected in this integrated
imagery to ensure smooth continuity of the endocranial surfaces (see the
electronic supplementary material, figure S3). Based on this final imagery
(virtually cleaned endocranial surface + clay reconstructions of the damaged
parts with additional digital corrections), we segmented the endocranial region
using the bone–air or clay–air HMH threshold values. Small anatomical foramina
and minute cracking untreated by clay were then virtually sealed at the level of
the endocranial opening. The foramen magnum was sealed by bridging between its
anterior and posterior margins (horizontally most protruding points) in each
sagittal section (figure 2). Finally, we calculated the total volume of voxels
assigned to the endocranial region.

We also estimated the magnitudes of the following three types of error involved
in our ECV measurement. First, in order to examine error related to delimitation
of the endocranial cavity, we experimentally changed bone–air threshold value
and observe variation in the resultant ECVs. Second, we estimated possible
errors stemming from our clay reconstructions of the damaged bones.
Reconstruction errors at smoothly curved endocranial surfaces should be
negligible, but those parts with complex morphology (figure 2) may significantly
affect our ECV measurement. We calculate a total surface area of such complex
parts to approximate the effects of their inflation or deflation. Third, we
evaluated error in size calibration of our CT scanning. In addition, in order to
evaluate the effect from differences in plugging method of the foramen magnum,
we tried another method to see associated volume change.

(B) BRAIN–BODY SIZE SCALING IN HOMO SAPIENS

We compared ECV with femoral head diameter (FHD), the most commonly used proxies
for brain and body mass, respectively [33–35]. Various equations have been
developed to estimate body mass from the FHD, but here, we do not attempt such
conversion to avoid complicated effects of the choice of these equations [36].
Vertical head diameter (Martin's no. 18) was preferred as the FHD but transverse
(Martin's no. 19) or maximum diameters, both of which are nearly equal to the
former, were used when the former was not available.

We collected ECV and FHD data for 20 chrono-regional groups of Holocene H.
sapiens worldwide from literature and our own data (table 1). The data and their
sources are available from the electronic supplementary material, table S1.
These include small- and large-bodied (group means of FHD: 37.7–48.6 mm for
males, 35.5–42.5 mm for females) and small- and large-brained (group means of
ECV: 1244–1543 cc for males, 1100–1368 cc for females) populations. We excluded
ECV estimates based on linear cranial measurements. The samples consist of adult
and a small number of adult-equivalent individuals. Although adult brain size is
attained by juvenile in modern humans [37], for the sake of safety, we excluded
juvenile individuals except for the Egypt sample that may include a small number
of juveniles. In some cases, the measurements were taken by different authors
based on different samples from the same population, and this is a potential
source of (presumably minor) error.

TABLE 1.

Samples of modern humans.

View inlineView popup

Table 1.Samples of modern humans.

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Asia Andamanese, Philippine Negrito, Neolithic Japan (Jomon), Bronze Age Japan
(Tanegashima Islanders), modern Japanese, Southern Chinese Australia Australian
Aborigines (Murray Valley) Polynesia Easter Island North America Aleut, Alaska
Eskimo, Old Zuni (Hawikuh), Pecos Pueblo Europe Sami (Lapp), Neolithic Denmark,
England (Spitalfields) Africa Predynastic Egypt, Zulu, Western Pygmies, Eastern
Pygmies, Khoisan

Males and females were analysed separately due to the sexual differences in
human body and brain sizes. Intraspecific scaling exponents were estimated based
on natural logarithms of the sex-specific group mean data and the following four
line fitting methods: two types of ordinary least-square regressions (OLSs), ECV
on FHD (‘inverse calibration’, OLS-IC) and FHD on ECV (‘classical calibration’,
OLS-CC), major axis (MA) and reduced major axis (RMA) [38]. Because we are
aiming to predict the condition in a dwarfed hominin, we need to obtain a
general slope to extrapolate conditions outside (particularly downside) the
range of the reference sample (H. sapiens) distribution. Some researchers
suggest that OLS-CC works better for extrapolation [38], but it remains
uncertain if this is always the case [39]. In this paper, we mainly focus on MA
and RMA as methods best describing the bivariate scatter of X and Y, and produce
intermediate (thus ‘conservative’) results between the two OLS regressions [39].
The slopes and their 95% CIs were calculated using R software [40] and its
package lmodel2 [41].

The ECV and FHD data were also collected from the following premodern fossil
hominin samples (genera Australopithecus and Homo). These data are tabulated in
the electronic supplementary material, table S2.

(I) AUSTRALOPITHECUS AFARENSIS

The ‘small individual’ is represented by A.L. 288-1 [42,43], whereas the ‘large
individual’ is composite data from A.L. 444-2 and KSD-VP-1/1 [43,44]. The group
mean is the average of these two datasets.

(II) AUSTRALOPITHECUS AFRICANUS

Means were calculated from five cranial (MLD 37/38; Sts 5; Stw 60, 71, 505) and
six femoral (Sts 14; Stw 25, 99, 311, 392; 443) specimens [22,33].

(III) HOMO HABILIS SENSU LATO

Means calculated from three cranial (KNM-ER 1470, 1805, 1813) and two femoral
(KNM-ER 1472, 1481a) specimens [34,43]. Although some researchers suggest that
the sample includes multiple species [45], they are lumped together mainly
because of uncertain association between the cranial and postcranial specimens.

(IV) DMANISI HOMO

A femur (D4167) from a large adult individual is inferred to be associated with
a large mandible (D2600) [46]. Here, the femur is tentatively associated with a
relatively robust adult cranium, D2280 which is probably male [47].

(V) H. ERGASTER (AFRICAN H. ERECTUS)

Owing to the lack of adult femoral heads, the species is represented here by an
estimated adult condition of the large juvenile skeleton, KNM-WT 15000 [34,48].

(VI) EARLY INDONESIAN H. ERECTUS (1.2–0.8 MA)

Two chronological subsamples from the Early Pleistocene of Sangiran, Central
Java are included. The ‘Sangiran Upper’ (Bapang-AG) subsample is chronologically
younger, and represented by probable male (Sangiran 17) and female (Sangiran IX)
crania [49]. The ‘Sangiran Lower’ (Grenzbank/Sangiran) subsample is older and
currently represents the earliest Indonesian H. erectus. Relatively gracile
(Sangiran 2) and robust (Sangiran 4) crania are available for its ECV [30,31].
The FHD of the earliest Indonesian H. erectus remains unknown. That for Trinil 3
is 45 mm (Y. Kaifu 2007, personal observation), but taxonomic assignment of this
specimen to Indonesian H. erectus is questioned [50]. Because their cranial size
and shape as well as dento-mandibular morphology are broadly comparable to or
slightly more primitive than African H. ergaster [29,30], their mean FHD is
expected to have been larger than H. habilis (40–44 mm) or Dmanisi Homo (40 mm),
and lesser than the large H. ergaster individual, KNM-WT 15000, whose adult FHD
is predicted as 51 mm (95% error range: 46.8–55.2 mm; [34]). In addition, FHDs
estimated from pelvic acetabular sizes of African Homo specimens are 46.8 mm for
KNM-ER 3228 (approx. 1.9 Ma) and 47.8 mm for OH 28 (0.7 Ma), respectively [34].
In consideration of these, 45–50 mm may be reasonable estimates for the earliest
Indonesian H. erectus.

(VII) HOMO FLORESIENSIS

The FHD for LB1 used here is the mean of vertical and transverse diameters (31
mm; [51]), and is slightly smaller than the FHD reported in ([1]; 31.5 mm).

4. RESULTS

(A) ENDOCRANIAL VOLUME OF LB1

The total amount of the matrix we virtually removed endocranially was
approximately 1.5 cc, of which 0.8–1.0 cc was inside the original endocranial
cavity (i.e. inside the boundary defined by our reconstruction described
earlier). The rest of the removed matrix (0.5–0.7 cc) was distributed outside
the original endocranial cavity (mostly within the areas of the damaged bones),
and thus irrelevant to the ECV calculation.

For each of the cranial bone (inner table) and air, we measured CT values at
arbitrarily selected 132 different voxels taken from three different CT slices
to calculate their means. The median of these means was used to differentiate
the bone and air. With this HMH thresholding, the volume of the endocranial
cavity was 425.7 cc.

If we change the bone/air threshold value ±5 per cent or ±10 per cent of the
difference between the average CT values for the bone and air, this ECV shifts
by ±0.5 cc or ±1.3 cc, respectively. The total area of the endocranial surface
prepared above was approximately 352 cm2, 17 per cent of which (approx. 60 cm2)
had been reconstructed either by clay or digital plugging. If we make an
unrealistic assumption that all of these parts were erroneously delimited by one
pixel (0.26 mm) either inward or outward, then the resultant volume change would
be up to ±1.5 cc. Clay-based reconstruction of complex morphology such as the
central sphenoid, the medial part of the right petrous bone and the lower part
of the right sigmoid sulcus may include some more substantial error (blue
portions in figure 2). The total surface area of these parts was 14 cm2, which
would result in error of up to ±1.4 cc assuming inflation or deflation of all of
these parts by 1 mm either inward or outward. Finally, error owing to size
calibration of the CT scanning is no more than ±1 cc [20]. Taken together, given
that many of the above error estimates are supposed maxima, we conclude that the
original ECV of the LB1 cranium was 426 cc with only a limited degree of error,
probably within ±3 cc.

In our definition, the foramen magnum is sealed not by a flat plane but by a
folded surface constituted by lines connecting the anterior and posterior
margins of the foramen magnum defined separately in each mid/parasagittal CT
section. If we change this definition and plug the foramen with a flat,
horizontal plane passing through the line connecting endobasion and opisthion,
then the ECV decreases by 0.5 cc.

(B) ENDOCRANIAL VOLUME REDUCTION EXPLAINED BY INTRASPECIFIC SCALING

The log-transformed ECV and FHD are moderately correlated in the male and female
H. sapiens samples (r = 0.73 or 0.75, p < 0.001). As seen in table 2, the
scaling exponents for male and female H. sapiens calculated by MA (1.05, 1.27)
and RMA (1.03, 1.20) are almost identical, whereas those by OLS-IC (0.76, 0.90)
and OLS-CC (1.38, 1.60) are lesser and higher, respectively. The slopes are
slightly steeper in the female than in the male analyses. Log-transformed ECV
and FHD values are plotted in figure 3, together with RMA lines for H. sapiens.
Table 2 also shows expected ECV reductions associated with body size (FHD)
changes following different scaling models.

TABLE 2.

Slopes for the best-fit lines for H. sapiens (left columns) and expected ECV
values after simulated body size reduction from the two hypothetical ancestors
to the H. floresiensis conditions (right columns).

View inlineView popup

Table 2.Slopes for the best-fit lines for H. sapiens (left columns) and expected
ECV values after simulated body size reduction from the two hypothetical
ancestors to the H. floresiensis conditions (right columns).

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model used regression parameters

--------------------------------------------------------------------------------

H. habilis (614 cc)

--------------------------------------------------------------------------------

earliest Indonesian H. erectus (860 cc)

--------------------------------------------------------------------------------

slope 95% CI for the slope intercept expected ECV (cc) decrease to 426 cc (%)
expected ECV (cc) decrease to 426 cc (%) OLS-IC male 0.76 0.41–1.10 4.39 488 67
599–649 49–60 OLS-IC female 0.90 0.50–1.29 3.84 468 78 561–616 56–69 MA male
1.05 0.65–1.71 3.29 447 89 522–582 64–78 MA female 1.27 0.82–2.06 2.47 417 105
469–536 75–90 RMA male 1.03 0.74–1.44 3.34 449 88 525–585 63–77 RMA female 1.20
0.87–1.65 2.74 427 100 485–551 71–86 OLS-CC male 1.41 0.97–2.63 1.90 400 114
438–508 81–97 OLS-CC female 1.60 1.11–2.85 1.26 378 126 400–474 89–106

Figure 3. Relationship between the ECV and FHD. Open circle, H. sapiens (male);
filled circle, H. sapiens (female); rhombus, mean data for the fossil hominin
samples; x, individual data for Australopithecus; +, individual data for
premodern Homo. Possible range of the ECV is indicated for the small A.
afarensis individual (A.L. 288-1). Estimated ranges of the FHD for the two early
Indonesian H. erectus samples (Sangiran Upper and Lower) are indicated by thick
broken lines (3.81–3.91 in logarithmic form; see text for more details). The
diagonal lines indicate expected brain size reductions from the H. habilis and
Sangiran Lower (earliest Indonesian H. erectus) conditions following the scaling
relationship for male (dotted lines) and female (solid lines) H. sapiens based
on the RMA regressions. (Online version in colour.)

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If the body size of LB1 reduced from the average H. habilis condition (ECV = 614
cc, FHD = 42 mm) following the MA or RMA scaling models based on the male data,
then the resultant ECV would be 447–449 cc, 11–12% larger than the measured ECV
for LB1 (426 cc). If LB1 is female as suggested previously [1,51], such brain
size reduction is achieved by the body size scaling alone.

If the earliest Indonesian H. erectus, here represented by the Sangiran Lower
sample, experienced body size reduction to the state of LB1, then the MA or RMA
male models suggest that their ECV would reduce from 860 to 522–585 cc (63–78%
reduction) depending on the ancestral FHD values (45–50 mm). When the female
models are used, such expected reduction increases to 71–90%. In other words,
10–29% of the ECV reduction is to be explained by factors other than body size
if LB1 was female. More of the ECV reduction is ascribed to body size scaling if
we use the OLS-CC models, whereas such proportion becomes less in the OSL-IC
models.

5. DISCUSSION AND CONCLUSIONS

Previous studies are in agreement that the brain of H. floresiensis is too small
to have been dwarfed from H. erectus following human intraspecific body size
scaling [1–14]. Although this view is probably correct, the earlier-mentioned
re-examination shows that the proportion of the brain reduction unexplained by
body size scaling is smaller (and thus less difficult) than previously claimed.
This is because of the following reasons. First, the newly determined ECV of
LB1, approximately 426 cc, which is based on high-quality micro-CT scan and
elaborate cleaning, reconstruction and error estimations, is slightly larger
than the previous estimate (approx. 400 cc). Second, scaling exponents for H.
sapiens used previously [7,8] were based on a single regional population and
thus considerably underestimated the actual species-wide trend. Although the
exponent values cannot be compared directly owing to different scales taken
(body weight [7,8] versus FHD (this study)), between-group analyses presented
earlier and elsewhere [19] clearly indicate a relatively high level of
correlation between body and brain sizes in our species. Several population
samples used in this study are small (n = 3–5: electronic supplementary
material, table S1), but broadly similar slopes derived from the male and female
analyses (table 2) suggest that these reflect actual scaling exponent for H.
sapiens. Finally, there are reasons to suppose early Indonesian H. erectus (mean
ECV: approx. 860 cc), rather than generalized H. erectus (mean ECV: 991 cc), as
an ancestor candidate for H. floresiensis.

In the model of Martin et al. [8], decreased body size from 60 (estimated
average for generalized H. erectus) to 16 kg (smallest estimate for LB1 [1])
results in only moderate reduction of ECV from 991 to 794 cc. In our model of
ancestor (early Indonesian H. erectus) and descendant (LB1) relationships, and
RMA or MA scaling, the estimated body size decrease (changes in the FHD from
45–50 to 31 mm) would reduce the ECV from 860 to 469–585 cc (63–90% reduction)
by body size scaling alone (table 2). Even if we use the OLS-IC models that are
probably inappropriate for extrapolation [38], 49–69% of the brain size
reduction could be explained by body size. The OLS-CC models, recommended by
some researchers for extrapolation [38], predict even greater proportion,
81–100%. We cannot exactly determine which of these figures are more correct
owing to unresolvable limitations such as small fossil samples, extrapolation
and ultimately unknown scaling exponent for extinct Homo. Still, the
earlier-mentioned results, based on the best available data and various
regression methods, suggest that at least 50 per cent, probably much more, of
the brain size reduction in H. floresiensis could occur as scaling effect if
this little hominin derived from early Indonesian H. erectus. This means that
0–50% of its brain size decrease needs to be explained by other factors.

There are a few reports about relative brain size reduction in island mammals.
Weston & Lister [10] suggested that approximately 30 per cent of brain size
decrease occurred in an extinct dwarf species of Malagasy hippopotamus
(Hippopotamus lemerlei), in addition to normal intraspecific scaling effect
associated with body size decrease. Köhler & Moyà-Solà [52] examined ECV of
Myotragus, an extinct, dwarfed caprine genus endemic to the Mediterranean island
Majorca [53]. Although its Miocene continental ancestor is presently unknown,
these authors found that (i) their continental bovid sample composed of a
variety of extant and fossil taxa, including seven caprine species from three
tribes (Rupicaprini, Caprini and Ovini) show a fairly consistent brain–body
allometric scaling relationship, and (ii) the relative brain size of Myotragus
was distinctly (approx. 50%) smaller than expected from this general trend for
the mainland bovids.

Therefore, it is ‘mechanistically’ possible [10] that H. floresiensis evolved
from early H. erectus, and 0–50% of the total brain size reduction occurred
independently from the scaling effect. However, such marked relative brain size
reduction in insular mammals is generally considered to have occurred to reduce
energetic demand. Because metabolic cost of the brain tissue is expensive, in an
insular environment with limited food resources and increased intraspecific
competition under the absence of predators, it is advantageous to reduce brain
size at the cost of some neural functions such as sensory, motor, social and/or
intellectual activities [50]. If one applies a similar energetic explanation for
the brain size evolution in H. floresiensis, then we need to answer what aspects
of central nervous system were sacrificed in this little hominin [13,14] who
show no sign of retrogression at least in stone tool technology compared with
earlier hominins on Flores or elsewhere in island Southeast Asia [54,55]. The
absence of mammalian carnivores in the Pleistocene of Flores [28,56,57] may
explain the situation, despite the presence of a giant lizard (Varanus
komodoensis) and a giant marabou stork (Leptoptilos robustus); the close
relative brain sizes between H. habilis and H. floresiensis documented above may
imply that intellectual capacity comparable to the former was enough for the
latter. Otherwise, H. floresiensis may have experienced ‘neurological
reorganization’ where brain functions are largely maintained in spite of its
overall size change [5], but such proposal is unacceptable for other researchers
[9].

We conclude that evolution from early Javanese H. erectus to H. floresiensis was
possible in terms of brain size. Still, in this scenario, some amount of the
brain size reduction remains to be explained by factors other than body size
scaling, posing a challenge to our current knowledge about human brain size
evolution. If H. floresiensis descended from H. habilis-like ancestor, the need
for such relative brain size reduction is less significant, but we stress
currently we have no convincing fossil evidence to support this hypothesis
except for the brain size issue discussed here. Then which hypothesis is more
correct? The question will be answered most effectively by future discoveries of
skeletal evidence for the first hominins to colonize Flores [58].

ACKNOWLEDGEMENTS

We thank E. Wahyu Saptomo, Thomas Sutikna, Jatmiko, Mike J. Morwood, other Liang
Bua research team members and Hisao Baba for support, John de Vos, Shozo Iwanaga
and Kyoko Funahashi for access to the materials under their care, Tsuyoshi
Kaneko, Nobuhito Morota and anonymous reviewers for comments, and Gen Suwa for
CT scanning. This work was supported by grants from the JSPS (no. 24247044) and
MEXT, Japan (no. 22101006).

FOOTNOTES

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Pérez-Claros J and Palmqvist P (2022) Heterochronies and allometries in the
evolution of the hominid cranium: a morphometric approach using classical
anthropometric variables, PeerJ, 10.7717/peerj.13991, 10, (e13991)
Gingerich P (2022) Pattern and rate in the Plio-Pleistocene evolution of
modern human brain size, Scientific Reports, 10.1038/s41598-022-15481-3, 12:1
Sawafuji R, Tsutaya T and Ishida H (2022) A review of the spread and habitat
of the genus Homo:ホモ属の拡散と生息時期, Anthropological Science (Japanese Series),
10.1537/asj.220214, 130:1, (55-74), .
Eckhardt R and Henneberg M (2021) Paleospecies as cognitive construct: The
meme of “Homo floresiensis”, Anthropological Review, 10.2478/anre-2021-0023,
84:3, (317-336)
Ponce de León M, Bienvenu T, Marom A, Engel S, Tafforeau P, Alatorre Warren
J, Lordkipanidze D, Kurniawan I, Murti D, Suriyanto R, Koesbardiati T and
Zollikofer C (2021) The primitive brain of early Homo , Science,
10.1126/science.aaz0032, 372:6538, (165-171), Online publication date:
9-Apr-2021.
Püschel H, Bertrand O, O’Reilly J, Bobe R and Püschel T (2021)
Divergence-time estimates for hominins provide insight into encephalization
and body mass trends in human evolution, Nature Ecology & Evolution,
10.1038/s41559-021-01431-1, 5:6, (808-819)
Scardia G, Neves W, Tattersall I and Blumrich L (2020) What kind of hominin
first left Africa?, Evolutionary Anthropology: Issues, News, and Reviews,
10.1002/evan.21863, 30:2, (122-127), Online publication date: 1-Mar-2021.
VanSickle C, Cofran Z and Hunt D (2020) Did Neandertals have large brains?
Factors affecting endocranial volume comparisons, American Journal of
Physical Anthropology, 10.1002/ajpa.24124, 173:4, (768-775), Online
publication date: 1-Dec-2020.
Hung H (2020) History and Current Debates of Archaeology in Island Southeast
Asia Encyclopedia of Global Archaeology, 10.1007/978-3-030-30018-0_3373,
(5159-5180), .
Wall-Scheffler C, Kurki H and Auerbach B (2019) The Evolutionary Biology of
the Human Pelvis
Murphy E (2019) No Country for Oldowan Men: Emerging Factors in Language
Evolution, Frontiers in Psychology, 10.3389/fpsyg.2019.01448, 10
Poza-Rey E, Gómez-Robles A and Arsuaga J (2019) Brain size and organization
in the Middle Pleistocene hominins from Sima de los Huesos. Inferences from
endocranial variation, Journal of Human Evolution,
10.1016/j.jhevol.2019.01.006, 129, (67-90), Online publication date:
1-Apr-2019.
Diniz-Filho J, Jardim L, Mondanaro A and Raia P (2019) Multiple Components of
Phylogenetic Non-stationarity in the Evolution of Brain Size in Fossil
Hominins, Evolutionary Biology, 10.1007/s11692-019-09471-z, 46:1, (47-59),
Online publication date: 1-Mar-2019.
Hung H (2019) History and Current Debates of Archaeology in Island Southeast
Asia Encyclopedia of Global Archaeology, 10.1007/978-3-319-51726-1_3373-1,
(1-22), .
Holloway R, Hurst S, Garvin H, Schoenemann P, Vanti W, Berger L and Hawks J
(2018) Endocast morphology of Homo naledi from the Dinaledi Chamber, South
Africa , Proceedings of the National Academy of Sciences,
10.1073/pnas.1720842115, 115:22, (5738-5743), Online publication date:
29-May-2018.
Beaudet A, Dumoncel J, de Beer F, Durrleman S, Gilissen E, Oettlé A, Subsol
G, Thackeray J and Braga J (2017) The endocranial shape of Australopithecus
africanus : surface analysis of the endocasts of Sts 5 and Sts 60 , Journal
of Anatomy, 10.1111/joa.12745, 232:2, (296-303), Online publication date:
1-Feb-2018.
Lyras G (2019) Brain Changes during Phyletic Dwarfing in Elephants and
Hippos, Brain, Behavior and Evolution, 10.1159/000497268, 92:3-4, (167-181),
.
Albessard-Ball L and Balzeau A (2018) Of Tongues and Men: A Review of
Morphological Evidence for the Evolution of Language, Journal of Language
Evolution, 10.1093/jole/lzy001, 3:1, (79-89), Online publication date:
1-Jan-2018.
Belmaker M (2018) Insights from carnivore community composition on the
paleoecology of early Pleistocene Eurasian sites: Implications for the
dispersal of hominins out of Africa, Quaternary International,
10.1016/j.quaint.2017.02.017, 464, (3-17), Online publication date:
1-Jan-2018.
Kaifu Y (2017) Archaic Hominin Populations in Asia before the Arrival of
Modern Humans, Current Anthropology, 10.1086/694318, 58:S17, (S418-S433),
Online publication date: 1-Dec-2017.
Diniz-Filho J and Raia P (2017) Island Rule, quantitative genetics and
brain–body size evolution in Homo floresiensis, Proceedings of the Royal
Society B: Biological Sciences, 284:1857, Online publication date:
28-Jun-2017.
Argue D, Groves C, Lee M and Jungers W (2017) The affinities of Homo
floresiensis based on phylogenetic analyses of cranial, dental, and
postcranial characters, Journal of Human Evolution,
10.1016/j.jhevol.2017.02.006, 107, (107-133), Online publication date:
1-Jun-2017.
Hawks J, Elliott M, Schmid P, Churchill S, Ruiter D, Roberts E, Hilbert-Wolf
H, Garvin H, Williams S, Delezene L, Feuerriegel E, Randolph-Quinney P,
Kivell T, Laird M, Tawane G, DeSilva J, Bailey S, Brophy J, Meyer M, Skinner
M, Tocheri M, VanSickle C, Walker C, Campbell T, Kuhn B, Kruger A, Tucker S,
Gurtov A, Hlophe N, Hunter R, Morris H, Peixotto B, Ramalepa M, Rooyen D,
Tsikoane M, Boshoff P, Dirks P and Berger L (2017) New fossil remains of Homo
naledi from the Lesedi Chamber, South Africa, eLife, 10.7554/eLife.24232, 6
(2017) Homo erectus and Homo floresiensis First Islanders,
10.1002/9781119251583.ch3, (34-85)
Churchill S and Vansickle C (2017) Pelvic Morphology in Homo erectus and
Early Homo , The Anatomical Record, 10.1002/ar.23576, 300:5, (964-977),
Online publication date: 1-May-2017.
Schroeder L, Scott J, Garvin H, Laird M, Dembo M, Radovčić D, Berger L, de
Ruiter D and Ackermann R (2017) Skull diversity in the Homo lineage and the
relative position of Homo naledi, Journal of Human Evolution,
10.1016/j.jhevol.2016.09.014, 104, (124-135), Online publication date:
1-Mar-2017.
Laird M, Schroeder L, Garvin H, Scott J, Dembo M, Radovčić D, Musiba C,
Ackermann R, Schmid P, Hawks J, Berger L and de Ruiter D (2017) The skull of
Homo naledi, Journal of Human Evolution, 10.1016/j.jhevol.2016.09.009, 104,
(100-123), Online publication date: 1-Mar-2017.
(2017) REFERENCES 50 Great Myths of Human Evolution,
10.1002/9781119308058.refs, (258-272), Online publication date: 9-Jan-2017.
Montgomery S (2017) Evolution of Large Brain and Body Size in Mammals
Evolution of Nervous Systems, 10.1016/B978-0-12-804042-3.00034-8, (103-136),
.
Gómez-Robles A (2016) The dawn of Homo floresiensis, Nature, 10.1038/534188a,
534:7606, (188-189), Online publication date: 9-Jun-2016.
Baab K, Brown P, Falk D, Richtsmeier J, Hildebolt C, Smith K, Jungers W and
Hawks J (2016) A Critical Evaluation of the Down Syndrome Diagnosis for LB1,
Type Specimen of Homo floresiensis, PLOS ONE, 10.1371/journal.pone.0155731,
11:6, (e0155731)
Grabowski M, Voje K and Hansen T (2016) Evolutionary modeling and correcting
for observation error support a 3/5 brain-body allometry for primates,
Journal of Human Evolution, 10.1016/j.jhevol.2016.03.001, 94, (106-116),
Online publication date: 1-May-2016.
Grabowski M (2016) Bigger Brains Led to Bigger Bodies?: The Correlated
Evolution of Human Brain and Body Size, Current Anthropology, 10.1086/685655,
57:2, (174-196), Online publication date: 1-Apr-2016.
Balzeau A and Charlier P (2016) What do cranial bones of LB1 tell us about
Homo floresiensis?, Journal of Human Evolution, 10.1016/j.jhevol.2015.12.008,
93, (12-24), Online publication date: 1-Apr-2016.
Zeitoun V, Barriel V and Widianto H (2016) Phylogenetic analysis of the
calvaria of Homo floresiensis, Comptes Rendus Palevol,
10.1016/j.crpv.2015.12.002, 15:5, (555-568), Online publication date:
1-Apr-2016.
Kaifu Y, Kono R, Sutikna T, Saptomo E, Jatmiko , Due Awe R and Bae C (2015)
Unique Dental Morphology of Homo floresiensis and Its Evolutionary
Implications, PLOS ONE, 10.1371/journal.pone.0141614, 10:11, (e0141614)
Dembo M, Matzke N, Mooers A and Collard M (2015) Bayesian analysis of a
morphological supermatrix sheds light on controversial fossil hominin
relationships, Proceedings of the Royal Society B: Biological Sciences,
282:1812, Online publication date: 7-Aug-2015.
Bruner E, Grimaud-Hervé D, Wu X, de la Cuétara J and Holloway R (2015) A
paleoneurological survey of Homo erectus endocranial metrics, Quaternary
International, 10.1016/j.quaint.2014.10.007, 368, (80-87), Online publication
date: 1-May-2015.
Eckhardt R, Henneberg M, Chavanaves S, Weller A and Hsü K (2015) Reply to
Westaway et al.: Mandibular misrepresentations fail to support the invalid
species Homo floresiensis , Proceedings of the National Academy of Sciences,
10.1073/pnas.1422176112, 112:7, Online publication date: 17-Feb-2015.
KAIFU Y, KONO R, SUTIKNA T, SAPTOMO E, JATMIKO , AWE R and BABA H (2015)
Descriptions of the dental remains of Homo floresiensis, Anthropological
Science, 10.1537/ase.150501, 123:2, (129-145), .
Biesalski H (2015) Nutritive Nischen und Nischenkonstruktionen
Mikronährstoffe als Motor der Evolution, 10.1007/978-3-642-55397-4_3,
(27-60), .
Aiello L (2015) Homo floresiensis Handbook of Paleoanthropology,
10.1007/978-3-642-39979-4_78, (2281-2297), .
Menke P (2015) The Ontogeny-Phylogeny Nexus in a Nutshell: Implications for
Primatology and Paleoanthropology Handbook of Paleoanthropology,
10.1007/978-3-642-39979-4_3, (177-211), .
Macho G (2015) General Principles of Evolutionary Morphology Handbook of
Paleoanthropology, 10.1007/978-3-642-39979-4_26, (921-936), .
Holloway R (2015) Introduction: Paleoneurology, Resurgent! Human
Paleoneurology, 10.1007/978-3-319-08500-5_1, (1-10), .
Balzeau A, Gilissen E, Holloway R, Prima S and Grimaud-Hervé D (2014)
Variations in size, shape and asymmetries of the third frontal convolution in
hominids: Paleoneurological implications for hominin evolution and the origin
of language, Journal of Human Evolution, 10.1016/j.jhevol.2014.06.006, 76,
(116-128), Online publication date: 1-Nov-2014.
Stringer C (2014) Human evolution: Small remains still pose big problems,
Nature, 10.1038/514427a, 514:7523, (427-429), Online publication date:
1-Oct-2014.
Bshary R, Gingins S and Vail A (2014) Social cognition in fishes, Trends in
Cognitive Sciences, 10.1016/j.tics.2014.04.005, 18:9, (465-471), Online
publication date: 1-Sep-2014.
Henneberg M, Eckhardt R, Chavanaves S and Hsü K (2014) Evolved developmental
homeostasis disturbed in LB1 from Flores, Indonesia, denotes Down syndrome
and not diagnostic traits of the invalid species Homo floresiensis ,
Proceedings of the National Academy of Sciences, 10.1073/pnas.1407382111,
111:33, (11967-11972), Online publication date: 19-Aug-2014.
Antón S, Potts R and Aiello L (2014) Evolution of early Homo : An integrated
biological perspective , Science, 10.1126/science.1236828, 345:6192, Online
publication date: 4-Jul-2014.
Williams A and Dunbar R (2014) Big brains, meat, tuberculosis and the
nicotinamide switches: Co-evolutionary relationships with modern
repercussions on longevity and disease?, Medical Hypotheses,
10.1016/j.mehy.2014.04.003, 83:1, (79-87), Online publication date:
1-Jul-2014.
de Sousa A and Proulx M (2014) What can volumes reveal about human brain
evolution? A framework for bridging behavioral, histometric, and volumetric
perspectives, Frontiers in Neuroanatomy, 10.3389/fnana.2014.00051, 8
Buckner R and Krienen F (2013) The evolution of distributed association
networks in the human brain, Trends in Cognitive Sciences,
10.1016/j.tics.2013.09.017, 17:12, (648-665), Online publication date:
1-Dec-2013.
Haslam M (2013) ‘Captivity bias’ in animal tool use and its implications for
the evolution of hominin technology, Philosophical Transactions of the Royal
Society B: Biological Sciences, 368:1630, Online publication date:
19-Nov-2013.
(2013) 'Hobbit' brains not so small, Nature, 10.1038/496401a, 496:7446,
(401-401), Online publication date: 1-Apr-2013.
Aiello L (2013) Homo floresiensis Handbook of Paleoanthropology,
10.1007/978-3-642-27800-6_78-3, (1-16), .
Menke P (2013) The Ontogeny-Phylogeny Nexus in a Nutshell: Implications for
Primatology and Paleoanthropology Handbook of Paleoanthropology,
10.1007/978-3-642-27800-6_3-4, (1-33), .
Macho G (2013) General Principles of Evolutionary Morphology Handbook of
Paleoanthropology, 10.1007/978-3-642-27800-6_26-5, (1-15), .
*

REFERENCES

* 1
Brown P, Sutikna T, Morwood MJ, Soejono RP, Jatmiko Saptomo EW& Rokus AD.
2004 A new small-bodied hominin from the Late Pleistocene of Flores,
Indonesia. Nature 431, 1055–1061.doi:10.1038/nature02999
(doi:10.1038/nature02999). Crossref, PubMed, ISI, Google Scholar
* 2
Morwood MJ, et al.. 2005 Further evidence for small-bodied hominins from the
Late Pleistocene of Flores, Indonesia. Nature 437,
1012–1017.doi:10.1038/nature04022 (doi:10.1038/nature04022). Crossref,
PubMed, ISI, Google Scholar
* 3
Falk D, et al.. 2005 The brain of LB1, Homo floresiensis. Science 308,
242–245.doi:10.1126/science.1109727 (doi:10.1126/science.1109727). Crossref,
PubMed, ISI, Google Scholar
* 4
Falk D, et al.. 2006 Response to Martin et al.'s comment: ‘the brain of LB1,
Homo floresiensis.’. Science 312, 999.doi:10.1126/science.1124972
(doi:10.1126/science.1124972). Crossref, PubMed, ISI, Google Scholar
* 5
Falk D, Hildebolt C, Smith K, Morwood MJ, Sutikna T, Jatmiko Saptomo EW&
Prior F. 2009 LB1's virtual endocast, microcephaly, and hominin brain
evolution. J. Hum. Evol. 57, 597–607.doi:10.1016/j.jhevol.2008.10.008
(doi:10.1016/j.jhevol.2008.10.008). Crossref, PubMed, ISI, Google Scholar
* 6
Jacob T, Indriati E, Soejono RP, Hsü K, Frayer DW, Eckhardt RB, Kuperavage
AJ, Thorne A& Henneberg M. 2006 Pygmoid Australomelanesian Homo sapiens
skeletal remains from Liang Bua, Flores: population affinities and
pathological abnormalities. Proc. Natl Acad. Sci. USA 103, 13 421–13
426.doi:10.1073/pnas.0605563103 (doi:10.1073/pnas.0605563103). Crossref,
ISI, Google Scholar
* 7
Martin RD, MacLarnon AM, Phillips JL, Dussebieux L, Williams PR& Dobyns WB.
2006 Comment on ‘the Brain of LB1, Homo floresiensis.’. Science 312,
999b.doi:10.1126/science.1121144 (doi:10.1126/science.1121144). Crossref,
PubMed, ISI, Google Scholar
* 8
Martin RD, MacLarnon AM, Phillips JL& Dobyns WB. 2006 Flores hominid: new
species or microcephalic dwarf? Anat. Rec. 288A,
1123–1145.doi:10.1002/ar.a.20389 (doi:10.1002/ar.a.20389). Crossref, Google
Scholar
* 9
Martin RD. 2007 Problems with the tiny brain of the Flores hominid. Recent
advances on Southeast Asian paleoanthropology and archaeology (ed. & Indriati
E), pp. 9–23. Yogyakarta, Indonesia: Gadjah Mada University. Google Scholar
* 10
Weston EM& Lister AM. 2009 Insular dwarfism in hippos and a model for brain
size reduction in Homo floresiensis. Nature 459,
85–88.doi:10.1038/nature07922 (doi:10.1038/nature07922). Crossref, PubMed,
ISI, Google Scholar
* 11
Montgomery SH, Capellini I, Barton RA& Mundy NI. 2010 Reconstructing the ups
and downs of primate brain evolution: implications for adaptive hypotheses
and Homo floresiensis. BMC Biol. 8, 9.doi:10.1186/1741-7007-8-9
(doi:10.1186/1741-7007-8-9). Crossref, PubMed, ISI, Google Scholar
* 12
Conroy GC& Smith RJ. 2007 The size of scalable brain components in the human
evolutionary lineage: with a comment on the paradox of Homo floresiensis.
Homo 58, 1–12.doi:10.1016/j.jchb.2006.11.001
(doi:10.1016/j.jchb.2006.11.001). Crossref, PubMed, ISI, Google Scholar
* 13
Niven JE. 2007 Brains, islands and evolution: breaking all the rules. Trends
Ecol. Evol. 22, 57–59.doi:10.1016/j.tree.2006.11.009
(doi:10.1016/j.tree.2006.11.009). Crossref, PubMed, ISI, Google Scholar
* 14
Köhler M, Moyà-Solà S& Wrangham RW. 2008 Island rules cannot be broken.
Trends Ecol. Evol. 23, 6–7.doi:10.1016/j.tree.2007.10.002
(doi:10.1016/j.tree.2007.10.002). Crossref, PubMed, ISI, Google Scholar
* 15
Aiello LC. 2010 Five years of Homo floresiensis. Am. J. Phys. Anthropol. 142,
167–179.doi:10.1002/ajpa.21255 (doi:10.1002/ajpa.21255). Crossref, PubMed,
ISI, Google Scholar
* 16
Vannucci RC, Barron TF& Holloway RL. 2011 Craniometric ratios of microcephaly
and LB1, Homo floresiensis, using MRI and endocasts. Proc. Natl Acad. Sci.
USA 108, 14 043–14 048.doi:10.1073/pnas.1105585108
(doi:10.1073/pnas.1105585108). Crossref, ISI, Google Scholar
* 17
Kaifu Y, et al.. 2010 Posterior deformational plagiocephaly properly explains
the cranial asymmetries in LB1: a reply to Eckhardt and Henneberg. Am. J.
Phys. Anthropol. 143, 335–336.doi:10.1002/ajpa.21387
(doi:10.1002/ajpa.21387). Crossref, ISI, Google Scholar
* 18
Holloway R, Schoenemann T& Monge J. 2011 The LB1 endocast: un-adorned,
unsmoothed, a replication study based on the original CT scan data. Am. J.
Phys. Anthropol. S52, 165–166. Google Scholar
* 19
Peters M, Jäncke L, Staiger JF, Schlaug G, Huang Y& Steinmetz H. 1998
Unsolved problems in comparing brain sizes in Homo sapiens. Brain Cogn. 37,
254–285.doi:10.1006/brcg.1998.0983 (doi:10.1006/brcg.1998.0983). Crossref,
PubMed, ISI, Google Scholar
* 20
Kubo D, Kono RT, Saso A, Mizushima S& Suwa G. 2008 Accuracy and precision of
CT-based endocranial capacity estimations: a comparison with the conventional
millet seed method and application to the Minatogawa 1 skull. Anthropol. Sci.
116, 77–85.doi:10.1537/ase.070502 (doi:10.1537/ase.070502). Crossref,
ISI, Google Scholar
* 21
Weber GW& Bookstain FL. 2011 Virtual anthropology: a guide to a new
interdisciplinary field. Wien, Germany: Springer. Crossref, Google Scholar
* 22
Neubauer S, Gunz P, Weber GW& Hublin JJ. 2011 Endocranial volume of
Australopithecus africanus: new CT-based estimates and the effects of missing
data and small sample size. J. Hum. Evol. 62,
498–510.doi:10.1016/j.jhevol.2012.01.005 (doi:10.1016/j.jhevol.2012.01.005).
Crossref, ISI, Google Scholar
* 23
Kaifu Y, Baba H, Sutikna T, Morwood M, Kubo D, Saptomo EW, Jatmiko X, Rokus
AD& Djubiantono T. 2011 Craniofacial morphology of Homo floresiensis:
description, taxonomic affinities, and evolutionary implication. J. Hum.
Evol. 61, 644–682.doi:10.1016/j.jhevol.2011.08.008
(doi:10.1016/j.jhevol.2011.08.008). Crossref, PubMed, ISI, Google Scholar
* 24
Holloway R. 1980 Within-species brain–body weight variability: a
reexamination of the Danish data and other primate species. Am. J. Phys.
Anthropol. 53, 109–121.doi:10.1002/ajpa.1330530115
(doi:10.1002/ajpa.1330530115). Crossref, PubMed, ISI, Google Scholar
* 25
Brown P& Maeda T. 2009 Liang Bua Homo floresiensis mandibles and mandibular
teeth: a contribution to the comparative morphology of a new hominin species.
J. Hum. Evol. 57, 571–596.doi:10.1016/j.jhevol.2009.06.002
(doi:10.1016/j.jhevol.2009.06.002). Crossref, PubMed, ISI, Google Scholar
* 26
Morwood MJ& Jungers WL. 2009 Conclusions: implications of the Liang Bua
excavations for hominin evolution and biogeography. J. Hum. Evol. 57,
640–648.doi:10.1016/j.jhevol.2009.08.003 (doi:10.1016/j.jhevol.2009.08.003).
Crossref, PubMed, ISI, Google Scholar
* 27
Baab KL& McNulty KP. 2009 Size, shape, and asymmetry in fossil hominins: the
status of the LB1 cranium based on 3D morphometric analyses. J. Hum. Evol.
57, 608–622.doi:10.1016/j.jhevol.2008.08.011
(doi:10.1016/j.jhevol.2008.08.011). Crossref, PubMed, ISI, Google Scholar
* 28
Brumm A, Jensen GM, van den Berg GD, Morwood MJ, Kurniawan I, Aziz F& Storey
M. 2010 Hominins on Flores, Indonesia, by one million years ago. Nature 464,
748–752.doi:10.1038/nature08844 (doi:10.1038/nature08844). Crossref, PubMed,
ISI, Google Scholar
* 29
Kaifu Y, Baba H, Aziz F, Indriati E, Schrenk F& Jacob T. 2005 Taxonomic
affinities and evolutionary history of the Early Pleistocene hominids of
Java: dento-gnathic evidence. Am. J. Phys. Anthropol. 128,
709–726.doi:10.1002/ajpa.10425 (doi:10.1002/ajpa.10425). Crossref, PubMed,
ISI, Google Scholar
* 30
Kaifu Y, Indriati E, Aziz F, Kurniawan I, Jacob T& Baba H. 2010 Cranial
morphology and variation of the earliest Indonesian hominins. Asian
paleoanthropology: from Africa to China and beyond (eds , Norton CJ& Braun
DR), pp. 143–157. Heidelberg, Germany: Springer. Google Scholar
* 31
Hyodo M, et al.. 2011 High-resolution record of the Matuyama–Brunhes
transition constrains the age of Javanese Homo erectus in the Sangiran dome,
Indonesia. Proc. Natl Acad. Sci. USA 108, 19 563–19
568.doi:10.1073/pnas.1113106108 (doi:10.1073/pnas.1113106108). Crossref,
ISI, Google Scholar
* 32
Kaifu Y, et al.. 2009 Brief communication: ‘Pathological’ deformation in the
skull of LB1, the type specimen of Homo floresiensis. Am. J. Phys. Anthropol.
140, 177–185.doi:10.1002/ajpa.21066 (doi:10.1002/ajpa.21066). Crossref,
PubMed, ISI, Google Scholar
* 33
McHenry HM. 1992 Body size and proportions in early hominids. Am. J. Phys.
Anthropol. 87, 407–431.doi:10.1002/ajpa.1330870404
(doi:10.1002/ajpa.1330870404). Crossref, PubMed, ISI, Google Scholar
* 34
Ruff C. 2010 Body size and body shape in early hominins: implications of the
Gona Pelvis. J. Hum. Evol. 58, 166–178.doi:10.1016/j.jhevol.2009.10.003
(doi:10.1016/j.jhevol.2009.10.003). Crossref, PubMed, ISI, Google Scholar
* 35
Isler K, Kirk EC, Miller JMA, Albrecht GA, Gelvin BR& Martin RD. 2008
Endocranial volumes of primate species: scaling analyses using a
comprehensive and reliable data set. J. Hum. Evol. 55,
967–978.doi:10.1016/j.jhevol.2008.08.004 (doi:10.1016/j.jhevol.2008.08.004).
Crossref, PubMed, ISI, Google Scholar
* 36
Churchill SE, Berger LR, Hartone-Rose A& Zondo BH. 2012 Body size in African
Middle Pleistocene Homo. African genesis: perspectives on Hominin evolution
(eds , Reynolds S& Gallagher A), pp. 319–346. Cambridge, UK: Cambridge
University Press. Crossref, Google Scholar
* 37
Leigh SR. 2004 Brain growth, life history, and cognition in primate and human
evolution. Am. J. Primatol. 62, 139–164.doi:10.1002/ajp.20012
(doi:10.1002/ajp.20012). Crossref, PubMed, ISI, Google Scholar
* 38
Konigsberg LW, Hens SM, Jantz LM& Jungers WL. 1998 Stature estimation and
calibration: Baysian and maximum likelihood perspectives in physical
anthropology. Yearb. Phys. Anthropol. 41,
65–92.doi:10.1002/(SICI)1096-8644(1998)107:27%2B%3C65::AID-AJPA4%3E3.0.CO;2-6
(doi:10.1002/(SICI)1096-8644(1998)107:27+<65::AID-AJPA4>3.0.CO;2-6).
Crossref, Google Scholar
* 39
Smith RJ. 2009 Use and misuse of the reduced major axis for line-fitting. Am.
J. Phys. Anthropol. 140, 476–486.doi:10.1002/ajpa.21090
(doi:10.1002/ajpa.21090). Crossref, PubMed, ISI, Google Scholar
* 40
R Development Core Team. 2011 R: a language and environment for statistical
computing. Vienna, Austria: R Foundation for Statistical Computing. See
http://www.R-project.org. Google Scholar
* 41
Legendre P. 2011 lmodel2: model II regression. R package, version 1.7.
http://cran.r-project.org/web/packages/lmodel2/. Google Scholar
* 42
Johanson DC, Lovejoy CO, Kimbel WH, White TD, Ward SC, Bush ME, Latimer BM&
Coppens Y. 1982 Morphology of the Pliocene partial hominid skeleton (A.L.
288-1) from the Hadar formation, Ethiopia. Am. J. Phys. Anthropol. 57,
403–451.doi:10.1002/ajpa.1330570403 (doi:10.1002/ajpa.1330570403). Crossref,
ISI, Google Scholar
* 43
Holloway RL, Broadfield DC& Yuan MS. 2004 The human fossil record, vol. 3.
Brain endocasts. New York, NY: Wiley. Crossref, Google Scholar
* 44
Haile-Selassie Y, Latimer BM, Alene M, Deino AL, Gibert L, Melillo SM,
Saylorg BZ, Scott GR& Lovejoy CO. 2011 An early Australopithecus afarensis
postcranium from Woranso-Mille, Ethiopia. Proc. Natl Acad. Sci. USA 107, 12
121–12 126.doi:10.1073/pnas.1004527107 (doi:10.1073/pnas.1004527107).
Crossref, ISI, Google Scholar
* 45
Leakey MG, Spoor F, Dean MC, Feibel CS, Antón SC, Kiarie C& Leakey LN. 2012
New fossils from Koobi Fora in northern Kenya confirm taxonomic diversity in
early Homo. Nature 488, 201204.doi:10.1038/nature11322
(doi:10.1038/nature11322). Crossref, ISI, Google Scholar
* 46
Lordkipanidze D, et al.. 2007 Postcranial evidence from early Homo from
Dmanisi, Georgia. Nature 449, 305–310.doi:10.1038/nature06134
(doi:10.1038/nature06134). Crossref, PubMed, ISI, Google Scholar
* 47
Rightmire GP, Lordkipanidze D& Vekua A. 2006 Anatomical descriptions,
comparative studies and evolutionary significance of the hominin skulls from
Dmanisi, Republic of Georgia. J. Hum. Evol. 50,
115–141.doi:10.1016/j.jhevol.2005.07.009 (doi:10.1016/j.jhevol.2005.07.009).
Crossref, PubMed, ISI, Google Scholar
* 48
Begun D& Walker A. 1993 The endocast. The Nariokotome Homo erectus skeleton
(eds , Walker A& Leakey R), pp. 326–358. Cambridge, MA: Harvard University
Press. Crossref, Google Scholar
* 49
Kaifu Y, Zaim Y, Baba H, Kurniawan I, Kubo D, Rizal Y, Arif J& Aziz F. 2011
New reconstruction and morphological description of a Homo erectus cranium:
skull IX (Tjg-1993.05) from Sangiran, Central Java. J. Hum. Evol. 61,
270–294.doi:10.1016/j.jhevol.2011.04.002 (doi:10.1016/j.jhevol.2011.04.002).
Crossref, PubMed, ISI, Google Scholar
* 50
Day MH& Molleson TI. 1973 The Trinil femora. Human evolution (ed. & Day MH),
pp. 127–154. London, UK: Taylor and Francis. Google Scholar
* 51
Jungers WL, Larson SG, Harcourt-Smith W, Morwood MJ, Sutikna T, Rokus AD&
Djubiantono T. 2009 Descriptions of the lower limb skeleton of Homo
floresiensis. J. Hum. Evol. 57, 538–554.doi:10.1016/j.jhevol.2008.08.014
(doi:10.1016/j.jhevol.2008.08.014). Crossref, PubMed, ISI, Google Scholar
* 52
Köhler M& Moyà-Solà S. 2004 Reduction of brain and sense organs in the fossil
insular bovid Myotragus. Brain Behav. Evol. 63, 125–140.doi:10.1159/000076239
(doi:10.1159/000076239). Crossref, PubMed, ISI, Google Scholar
* 53
Lalueza-Fox C, Shapiro B, Bover P, Alcover JA& Bertranpetit J. 2002 Molecular
phylogeny and evolution of the extinct bovid Myotragus balearicus. Mol.
Phylogenet. Evol. 25, 501–510.doi:10.1016/s1055-7903(02)00290-7
(doi:10.1016/s1055-7903(02)00290-7). Crossref, PubMed, ISI, Google Scholar
* 54
Moore MW& Brumm A. 2007 Stone artifacts and hominins in island Southeast
Asia: new insights from Flores, eastern Indonesia. J. Hum. Evol. 52,
85–102.doi:10.1016/j.jhevol.2006.08.002 (doi:10.1016/j.jhevol.2006.08.002).
Crossref, PubMed, ISI, Google Scholar
* 55
Brumm A, Moore MW, van den Bergh GD, Kurniawan I, Morwood MJ& Aziz F. 2010
Stone technology at the Middle Pleistocene site of Mata Menge, Flores,
Indonesia. J. Archaeol. Sci. 37, 451–473.doi:10.1016/j.jas.2009.09.012
(doi:10.1016/j.jas.2009.09.012). Crossref, ISI, Google Scholar
* 56
Van den Bergh GD, et al.. 2009 The Liang Bua faunal remains: a 95 k.yr.
sequence from Flores, East Indonesia. J. Hum. Evol. 57,
527–537.doi:10.1016/j.jhevol.2008.08.015 (doi:10.1016/j.jhevol.2008.08.015).
Crossref, PubMed, ISI, Google Scholar
* 57
Meijer HJM& Rokus AD. 2010 A new species of giant marabou stork (Aves:
Ciconiiformes) from the Pleistocene of Liang Bua, Flores (Indonesia). Zool.
J. Linn. Soc. 160, 707–724.doi:10.1111/j.1096-3642.2010.00616.x
(doi:10.1111/j.1096-3642.2010.00616.x). Crossref, ISI, Google Scholar
* 58
Aziz F, Morwood MJ& van den Bergh GD (eds) 2009 Palaeontology and archaeology
of the Soa Basin, Central Flores, Indonesia. Bandung, Indonesia: Indonesian
Geological Survey Institute. Google Scholar

THIS ISSUE

07 June 2013
Volume 280Issue 1760
*

Article Information
* DOI:https://doi.org/10.1098/rspb.2013.0338
* PubMed:23595271
* Published by:Royal Society
* Online ISSN:1471-2954

History:
* Manuscript received11/02/2013
* Manuscript accepted26/03/2013
* Published online07/06/2013
* Published in print07/06/2013

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75 Total citations
10 Recent citations
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Keywords
* Homo floresiensis
* endocranial volume
* relative brain size
* brain–body scaling

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Subjects
* evolution
* neuroscience
* palaeontology

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