How Did The Relationship Of Brain To Body Size Change From Australopithecines To Homo?

Philos Trans R Soc Lond B Biol Sci. 2012 Aug 5; 367(1599): 2130–2140.

Hominin cognitive development: identifying patterns and processes in the fossil and archaeological record

Susanne Shultz

¹Institute of Cognitive and Evolutionary Anthropology, University of Oxford, 64 Banbury Route, Oxford OX2 6PN, Great britain

²Faculty of Life Sciences, Academy of Manchester, Manchester M13 9PT, U.k.

Emma Nelson

^oneConstitute of Cognitive and Evolutionary Anthropology, Academy of Oxford, 64 Banbury Road, Oxford OX2 6PN, U.k.

Robin I. M. Dunbar

¹Institute of Cognitive and Evolutionary Anthropology, University of Oxford, 64 Banbury Road, Oxford OX2 6PN, United kingdom

Abstract

Equally only limited insight into behaviour is available from the archaeological tape, much of our agreement of historical changes in human cognition is restricted to identifying changes in brain size and architecture. Using both accented and residual brain size estimates, we prove that hominin brain development was likely to be the event of a mix of processes; punctuated changes at approximately 100 kya, 1 Mya and one.8 Mya are supplemented by gradual within-lineage changes in Homo erectus and Homo sapiens sensu lato. While brain size increment in Homo in Africa is a gradual process, migration of hominins into Eurasia is associated with stride changes at approximately 400 kya and approximately 100 kya. We then demonstrate that periods of rapid change in hominin brain size are not temporally associated with changes in environmental unpredictability or with long-term palaeoclimate trends. Thus, we argue that commonly used global sea level or Indian Sea grit palaeoclimate records provide lilliputian prove for either the variability selection or aridity hypotheses explaining changes in hominin encephalon size. Encephalon size change at approximately 100 kya is coincident with demographic change and the appearance of fully modern language. All the same, gaps remain in our understanding of the external pressures driving encephalization, which volition only exist filled by novel applications of the fossil, palaeoclimatic and archaeological records.

Keywords: hominin encephalization, variability choice, punctuated development, aeolian deposition, palaeoclimate

1. Introduction

One of the most distinct features of recent homo development is the tendency towards increasingly large brains over the Plio-Pleistocene. Early on hominin australopithecines had a cranial chapters (CC) slightly larger than that of extant apes [1]; over the subsequent three million years, average brain size trebled. Brains are extremely expensive to both grow and maintain; the increment in early on Homo brains imposed an estimated xx per cent increase in metabolic costs [2]. This cost is even higher in later hominin species; resting metabolic rate of female Human being ergaster was an estimated 1.53 times higher than that of Australopithecus afarensis and is 1.64 times higher for female Man sapiens [3]. An even more hitting estimate is that the daily energy expenditure in female Homo erectus may take been more than 80 per cent higher than female australopithecines [4]. Evolutionary reasoning demands that individuals can beget to pay hefty costs just if they are outweighed past commensurate benefits. There is little dubiety that the large man brain provides the machinery to execute complex cognitive tasks, including frontward planning, linguistic communication use, innovation and social perception. However, the search for the mechanisms driving the marked increase in man brain size over the by ii million years has been the subject of much debate. This paper volition (i) review the arguments for the pressures driving hominin encephalon expansion, (ii) quantitatively evaluate tempo changes in hominin encephalon size, and (3) exam environmentally based hypotheses for brain size change. Finally, nosotros will contextualize encephalization patterns within the archaeological bear witness for cerebral evolution.

(a) Potential drivers of hominin encephalization

Explanations for encephalization in hominins are mainly based on the evolution of behavioural flexibility and adaptability to changing or unpredictable environmental atmospheric condition. In add-on to responses to climatic weather condition, other suggestions focus on changes in diet, indirect effects of habitat use, social surround and applied science. Here, we briefly review these hypotheses.

(i) Climate

Iii different climatic processes have been implicated in driving hominin encephalization. The starting time procedure is the event of cooling, drying and the expansion of the savannah forcing individuals to move into novel habitats and alter their use of resource [5]; such a change is suggested in the Belatedly Pliocene archaeological record [6]. The second process is the outcome of an increasingly unpredictable climate, which has been labelled as the variability selection hypothesis [vii,eight], whereby farthermost fluctuations in the environment created dynamic and inconsistent habitats over fourth dimension. The third is the impact of climatic pulses causing abrupt habitat and environmental shifts [six,9]. For all processes, flexibility and innovation in habitat, resource or space use could be adaptive behavioural responses to a irresolute surroundings. For case, a broad and a flexible diet allows the exploitation of unpredictable resource across a mosaic habitat [10,xi], whereas the development and capacity to utilize tools opens upward novel adaptive zones [12]. The correlation betwixt environmental variance and hominin encephalon size over time has been argued to be the result of environmental unpredictability driving hominin brain evolution [13,xiv]. This assumes a causal human relationship wherein brain size has evolved equally a direct response to environmental variability. Rather than a elementary bivariate correlation, a better test of this hypothesis would exist to chronicle specific periods of rapid change in encephalon size to periods of increased environmental change or variability, which has nevertheless to be done.

(two) Predation

In addition to changing the resource base, moving into open up habitats increases predation adventure as refuges are less common [15]. For this reason, terrestrial primates live in much larger groups than arboreal species; this is especially true of species that are typically establish in open up habitats [16]. Shifting into open, high-risk habitats would have substantially increased the risk of predation for early on hominins. Predation clearly impacted on australopithecines; damage caused past both carnivores and raptors has been found on fossilized remains [17,18]. Nonetheless, we practice not know how much of an issue predation pressure was for early on Human being. The shifts in H. erectus/ergaster towards more open up habitats [nineteen,20] would take made them potentially more than vulnerable to large carnivores. Across mammals, large encephalon size in prey reduces predation run a risk, with predators showing biases towards, or preference for, small-brained prey [21,22]. The machinery driving this association is unknown, simply prey species with larger cognitive capacity could be expected to utilize more than diverse escape or defence strategies [22]. Thus, the predation and resources pressure level resulting from using more open environments constitutes a potential factor in encephalon size alter in early Human.

(iii) Sociality

Both the preceding hypotheses (ecology variability and predation) may also impact on cognitive evolution indirectly via changes they impose on hominin social environments. Predation is the principal driver of primate sociality [23], and primate species living on the footing and in smaller groups suffer higher predation rates than those in large groups [24]. Moving from closed into riskier open habitats is associated with larger foraging groups in birds, primates and other mammals. Maintaining bonded social groups imposes cerebral demands itself as a result of the need to solve (ecological) problems inside a coordinated social environment, rather than in a demographic vacuum [25]. In fact, the complex social environment in which anthropoid primates alive is one of the primary explanations for why they have exceptionally large brains for their body size [26,27]. The more disparate the needs of grouping members, the more than difficult the task of coordination and cooperation becomes. When conflict arises, individuals in stable groups must be able to negotiate to attain outcomes that are suitable for all group members. Of crucial importance in this respect is an individual'south ability to factor in others' interests, that may be dependent on cognitive mechanisms such as empathy, perspective taking and theory of mind [28,29].

Within anthropoid primates, there is a strong correlation between grouping size and encephalon size [30,31]; Aiello & Dunbar [32] extrapolated this relationship to predict social group size in hominin species (for revised estimates, see Dunbar [33]). To engagement, this method remains the only model bachelor to judge hominin grouping sizes. As this arroyo relies on the supposition that encephalon size and group size in hominins are intimately coupled, it is not appropriate if we wish to verify that changes in brain size/architecture are temporally linked with changes in hominin social grouping construction. Alternative avenues for estimating social group size, such every bit artefact deposition rates, hominin assemblage numbers [14], hearth/site sizes, are fraught with potential biases, which makes their employ difficult to justify especially when comparing over wide fourth dimension periods. Thus, at the present fourth dimension, there are no independent methods which can explicitly judge changes in social group size or population density in hominins over fourth dimension.

(iv) Language development

While language evolution is undoubtedly tethered to sociality, its importance as a defining characteristic in man cognitive evolution cannot be overstated. Language increases an individual's understanding of the globe because the individual is no longer express to holding only information that it directly perceives [34]. Autonomously from the power to share intentional thoughts, language also allows the substitution of information, ultimately leading to distributed noesis, and provides the neural substrate for symbolic thought [35]. As with other aspects of hominin sociality, language does not fossilize; instead we have to infer the evolutionary changes in the complexity of language ability from archaeological and fossil evidence. Language involves the integration of hierarchically organized subsystems [34], and understanding how cerebral power changed in lodge to arrange this is undoubtedly of major importance to understanding later hominin development. Thus, one argument may exist that it was the cognitive demands of language per se that drove hominin encephalon evolution. In this respect, intentionality (or mentalizing) competences seem to exist crucial, because these decide how complex language can become (e.g. the number of embedded clauses that can exist unpacked) [28]. If intentional competences are a function of brain (region) book, as they seem to be in humans [36,37], and then language complexity may reverberate changes in brain size. Thus, rather than language existence a macromutation-like all-or-none thing, it might take arisen every bit a graded process of increasing complexity over fourth dimension. This allows for a feedback process in which linguistic communication itself became a selection pressure for increases in brain size.

(v) Metabolic demands and life-history changes

The adaptive benefits associated with larger cognitive capacities are not the simply consideration when understanding processes driving brain evolution: mitigating constraints is also necessary to permit the development of larger brains. Large brain size is associated with a prolonged life history such equally extended juvenile periods and delayed reproduction [38,39]. If long dependency periods are crucial for developing large brains, then social changes involving increased parental care and provisioning are probable to coincide with encephalon size increases [twoscore,41]. Metabolic demands also exert strong constraints on encephalon size [39,42]; unless individuals can meet the increased metabolic demands of a large encephalon, they cannot develop or maintain them. High-energy diets such as meat could release metabolic constraints on encephalon size [43,44]. Apart from dietary changes, an intriguing possibility is that the utilise of fire for cooking made food more digestible [45], which became increasingly important equally hominins expanded their range into more temperate zones [46].

A central effect remains as to whether ecology pressures are ultimately the cause of changes in the other selection pressures that influence brain size. If and so, then periods of rapid encephalon size alter should be associated with corresponding periods of changes in climate or in climate envelopes.

2. Tempo and brain evolution

In order to place the causal forces driving the increase in hominin brain size over the past three 1000000 years, we must beginning understand the tempo and process of encephalon size modify. Large-scale evolutionary changes in continuous characters can result from two processes, punctuated equilibrium (a serial of steps (saltations) followed by stasis) or gradualism (whereby there is an accumulation of small incremental changes) [47]. If the tempo of evolution is curt rapid changes followed by long periods of stasis, then it is likely that there are pulses of selective pressures associated with either external drivers or the appearance of novel phenotypes. Conversely, if evolutionary change is underpinned by a gradual and continuous process, then the selective pressures are likely to be either a ratchet process or driven past long-term low-level directional selection. A number of proponents support gradualism [48,49], whereas others argue that in that location have been long periods of stasis in encephalon size followed by bursts of modify [l], or that rates of change vary over time [51,52] and infinite [53,54]. Ane likely reason for the dissimilar inferences fabricated about the procedure of hominin brain size changes is that unlike methodologies take been used. These vary from qualitative [46] to least-squares regression of brain size confronting time [55–58], to examining differences in brain size (or CC) between adjacent fourth dimension periods [49]. 1 conclusion that all methods agree upon is that brain size has increased, merely the tempo of those changes remains unresolved.

We suggest that one reason for the disagreement is that there may be a combination of processes occurring beyond hominin development, leading to different temporal signatures in encephalon size change. The methods used to date have been advisable for identifying the signatures of a gradual process, but may not place punctuational ones. For example, a to the lowest degree-squares regression will identify whether there are long-term trends in brain size over time [40]. Withal, a regression will not necessarily detect deviations from an underlying (or superimposed) linear relationship [54]. Additionally, treating hominins equally a single population is potentially problematic: multiple hominin species accept coexisted at different points in time [59], often at geographically distinct locations [60]. The appearance of a later on lineage often precedes the extinction of pre-existing ones: for example, archaic humans (Homo heidelbergensis) appear near 700 ky before the last evidence of H. erectus in the fossil record. If we evaluate all lineages together, we are likely to increase the fault in our estimates for whatever given time flow. To narrate patterns of brain evolution in hominins, analyses should ideally be done both comprehensively over all hominins and within specific lineages.

If encephalization is the result of a single gradual procedure, there should be an increasing trend (i.e. positive slope for the regression of encephalon size against time), but in that location should be no systematic difference in hateful residual CC betwixt time periods. Conversely, if encephalon size has inverse as a result of a serial of punctuated events, there should exist periods of fast growth (associated with big step changes and positive residuals) followed past periods with no size change. The latter tin can be detected by evaluating whether there is evidence of change in brain size or residuals between some adjacent time steps but non between others. If encephalization is solely the consequence of step changes associated with speciation events, so there should be little evidence of within lineage changes (i.eastward. a flat line in between speciation events). Finally, if encephalization is caused by a mixture of processes, nosotros would expect to run across large steps in conjunction with within-lineage trends.

(a) Methods

Data on hominin CC from 0.01 to 1.ix Mya were taken primarily from Bailey & Geary [14] and Ash & Gallup [thirteen] (electronic supplementary textile, tabular array S1). Data were cross-checked with additional sources, and additional data were added from the literature to include hominins up to 3.2 one thousand thousand years ago (see the electronic supplementary textile). Equally there is considerable disagreement about the phylogenetic relationships between hominin groups [61], nosotros execute the analyses at several levels. Firstly, we evaluate the temporal change over all hominins; nosotros so split up the groups into four super-species (Australopithecus spp., Homo habilis, H. erectus (including both H. erectus and H. ergaster) and H. sapiens (H. sapiens, H. heidelbergensis and Homo neanderthalensis); finally, we intermission down the H. sapiens group into anatomically modern humans (AMHs), Neanderthals and H. heidelbergensis. The reasons for this are twofold. Firstly, if multiple species with different encephalon sizes coexist, an evaluation of all hominins together will overestimate the variance at whatever bespeak in time. Secondly, we want to evaluate whether there is stasis or evidence for directional change within lineages.

The recognition of a tight positive allometric human relationship between brain and body size has led to the widespread apply of residuals for interspecific comparisons. However, recent show suggests that for closely related species (and individuals within a species), absolute brain size is arguably a amend predictor of cognitive ability than relative brain size, equally the latter introduces errors [62,63]. Additionally, the difficulty in estimating body sizes for hominins and the potential for introducing additional errors justifies the utilize of absolute brain size [50,54,64,65]. Still, we do admit that changes in body size and shape have occurred throughout hominin evolution [ane,65] and that these will exist associated with brain size changes. To avert confounds introduced past large errors in body size for the individual fossils, we have used absolute encephalon size within and betwixt hominin lineages through time.

We use several analytical approaches to evaluate changes in brain size:

—Changes in mean CC. Nosotros classified fossil specimens into detached fourth dimension periods (see electronic supplementary textile). We then estimated the mean log₁₀CC for each time block and evaluated the modify in mean log₁₀CC across adjacent time blocks.
—Rest brain size. To evaluate the underlying temporal trend in brain size, we used model II major centrality regression to evaluate modify in log₁₀CC against time. We then compared the mean residuals beyond adjacent time blocks.
—Changes over fourth dimension. To test whether there is also evidence for gradual change within lineages, we replicated the regression against time within taxa to decide whether there is evidence for stasis or continuous modify.
—Regional analyses. From most 1.6 Mya, hominins occupied both Africa and Eurasia. As the environments were very different, it is possible that there are differences in tempo changes between the ii continents.

(b) Results

We explored multiple line-fitting options; linear regression of log₁₀CC against fourth dimension ( β = −0.189, t = 35.43, p < 0.001, r ² = 0.87) provided every bit expert a fit as nonlinear models. At that place was prove for significant changes between 0–100 kya and 200–400 kya, 1–one.two Mya and 1.half-dozen–1.8 Mya and ane.viii–2.half dozen Mya (figure i a). The significant differences in the residuals mirror the differences in log₁₀CC (i.eastward. 0–100 kya; i–1.2 Mya; ane.6–1.8 Mya, figure 1 a,b; electronic supplementary material, tabular array S2). The consistent point for step changes suggests that hominin brain expansion is not a single, gradual process but is rather characterized past footstep changes. The offset two footstep changes coincide with the appearance of early on Man (H. habilis approximately 1.ix Mya and H. erectus sensu lato approximately 1.viii Mya); the final two steps occur at 200–400 kya and at less than 100 kya. Of the latter pair, the first coincides with the appearance of the AMHs approximately 195 kya, but the second does not coincide with a species appearance. Although there is no testify for temporal trends in encephalization inside the australopithecines and H. habilis, there is evidence for continued increase beyond the other species groups (table 1). Early H. erectus sensu lato is characterized by a large step increase in brain size, which may be associated with changes in body size [ane,3], but there is as well show for a gradual and continuous change inside the lineage over time (figure 2 and tabular array 1). This temporal trend inside H. erectus has been previously suggested [52,64]. Homo sapiens encephalon size increases over time within the sapiens super-species clade (effigy two and tabular array 1). As H. sapiens sensu lato is arguably a number of distinct species, we subdivided the group into H. heidelbergensis, H. neanderthalensis and Human sapiens sapiens (AMH) to make up one's mind whether changes within or betwixt these species were driving the overall temporal tendency. Homo heidelbergensis shows long-term stasis in encephalon size; in contrast, within lineage encephalization is suggested for both AMH and Neanderthals (tabular array one).

Tabular array 1.

Within lineage regressions of log_tenCC against time.

taxon	slope	F	p
gracile australopithecines	−0.03	F _1,12 = 0.27	p = 0.62
H. habilis	−0.24	F _one,7 = 0.62	p = 0.45
H. erectus	−0.101	F _1,39 = 42.35	p < 0.001
H. sapiens (sensu lato)	−0.165	F _1,105 = xl.63	p < 0.001
H. heidelbergensis	−0.01	F _1,18 = 0.04	p = 0.85
H. neanderthalensis	−0.46	F _1,25 = 7.148	p = 0.01
AMH H. sapiens	−0.20	F _ane,64 = 5.93	p = 0.01

An external file that holds a picture, illustration, etc. Object name is rstb20120115-g1.jpg

(a) Absolute hominin brain size across 100 ky blocks (significant differences between side by side fourth dimension blocks: ***p < 0.01, **p < 0.05, *p < 0.10). (b) The distribution of residuals from a regression of cranial chapters against fourth dimension (***p < 0.01, **p < 0.05, *p < 0.ten).

An external file that holds a picture, illustration, etc. Object name is rstb20120115-g2.jpg

Continental and species trends in hominin brain size. (a) Depicts brain size in European hominins and (b) depicts encephalon size alter in Africa. (Open squares, H. sapiens; filled triangles, H. neanderthalensis; open triangles, H. heidelbergensis, greyness filled circles, H. erectus/ergaster; open diamonds, H. rudolfensis, filled diamonds, H. habilis; open circles, H. georgicus; black circles, Australopithecus africanus; crosses, A. afarensis.)

Using 200 ky blocks, we finally evaluated whether there were differences in tempo between hominins in Africa and those in Eurasia, owing to limited sample sizes for dates older than 200 kya. Although there was evidence of a temporal trend towards encephalization on both continents, there were some marked differences between the two. Firstly, in Africa, the just significant differences between adjacent fourth dimension periods were between 1.half-dozen and 1.8 Mya and 1.8 Mya and earlier periods (effigy 2). In Eurasia, in contrast, there were significant differences between the near recent time flow and 100 kya, between 200 and 400 kya, and betwixt 1.6 and 1.viii Mya. Therefore, the footstep changes betwixt the two continents show some similarity, just several differences. The step changes in Eurasia are contemporary with migration events (i.east. AMH, H. heidelbergensis and H. erectus). However, within Eurasia, there was further evidence of encephalization within H. erectus ( β = −0.08, t = −4.57, p < 0.001) and H. neanderthalensis ( β = −0.46, t = −two.67, p = 0.01), but not inside H. heidelbergensis nor inside H. sapiens. Conversely, in Africa, there was no prove of encephalization within whatever species; the changes were primarily due to the appearance of new chronospecies (GLM with species as main effect: F _7,37 = 86.83, p < 0.001; figure 2). The lack of trend in African populations is likely to exist a consequence of short-lived species with fewer specimens per species; the chronospecies designation finer divides up a long-term trend of encephalization. This is farther supported by continental differences in mean CC within the H. erectus super-species (F _ane,37 = three.95 , p = 0.05) and H. sapiens (F _1,57 = iv.3 , p = 0.04) simply not inside H. heidelbergensis, with larger brains in Eurasian populations. Yet, if Neanderthals are viewed as a continuum from H. heidelbergensis [66,67], there is evidence for encephalization within this lineage, but non for a considerable period after colonizing Eurasia. These differences suggest that fundamentally dissimilar processes may have been acting on hominins in Eurasia and Africa. Speciation appears to be the key to alter in Africa, whereas step changes associated with migration followed past within lineage encephalization are more than characteristic of the Eurasian lineages.

These analyses strongly suggest that in that location is a combination of processes driving hominin brain evolution. When evaluated as a whole, in that location are apparent step changes ancillary with the advent of early Man, followed by steps at 1 Mya and 100 kya. The first step occurs at a period of high rates of hominin speciation and species turnover. However, the step at approximately 1 Mya is non apparently contemporary with species turnover. The steps in brain size at 100 kya and at 200–400 kya are clearly driven by the migration of African hominin species into Eurasia. These step changes are non mirrored within Africa, where at that place are no significant step changes following the appearance of Homo. The appearance of H. erectus and H. sapiens in Eurasia is associated with further gradual increases over time. These gradual increases in brain size in Eurasian populations may reverberate the demands that the depression-lite-level regimes at loftier latitudes impose on visual processing and the brain mechanisms that underpin this [68]. This proffer is given added force by the fact that at that place was no such change in encephalon size in contemporary tropical populations in which this trouble does not ascend.

iii. Testing ecology hypotheses

Our analyses of tempo changes in brain size suggest that we are non looking only for a single long-term force per unit area, but that at that place may be selective pulses in add-on to longer-term low-level pressures. Therefore, in order to fully support the postulated causal relationship between climate and brain size, information technology is necessary to demonstrate that these step changes are associated with pulses of large environmental modify rather than only demonstrating a long-term temporal correlation. Here, we re-evaluate the ii climatic hypotheses past assessing whether there is evidence for increased change coincident with (or shortly preceding) step changes in brain size.

(a) Methods

The specimens and cranial data used for these analyses are as described earlier (§2a). Two sources of climatic data were employed: global sea level predicted from benthic marine oxygen isotope (β ¹⁸O) records [69] and records of aeolian dust variability (terrigenous sediment) extracted from marine sediment cores off the East African coast [70]. The data sources are discussed in more detail in the electronic supplementary textile. The β ¹⁸O records provide an estimate of global climatic weather condition, whereas the dust records provide a climate record for Africa and Arabia.

To establish whether periods of rapid modify in hominin brain size were associated with periods of rapid or extreme climatic change, nosotros calculated the hateful and standard departure in body of water level and dust deposition for each 100 ky period prior to each specimen engagement as per Ash & Gallup [xiii]. We correlated these values both with hominin CC and with residual brain size (derived from a regression of CC against time), which identifies deviations from the underlying gradient of change (positive residuals associated with a more rapid modify than predicted by the linear regression and negative residuals associated with a slower change than predicted). We too performed step-wise regression with multiple palaeoclimate records over all homninins and at the species level.

(b) Results

Across all hominins, in that location were meaning correlations between overall CC and both mean sea level and body of water-level standard deviation (table ii). The same evidence has been used [xiii,xiv] to suggest a link between encephalization and climatic variability. Even so, in our more refined analysis, there was no human relationship betwixt periods of accelerated alter (i.e. large brain residuals) and increased climate variability over 100 ky fourth dimension-blocks, contrary to what would exist expected from Potts' variability selection hypothesis. Nor is there consistent evidence at the super-species level to support either the variability selection or the aridity hypotheses using sea-level indicators (table 2). Furthermore, when we use aeolian grit records, which provide a continental indicator for both aridity and variability, we do not observe consequent evidence to back up either hypothesis (tabular array ii). There were no significant models incorporating more than one climate tape for any of the taxonomic levels. The main weakness with the palaeoclimate records used in these analyses is that they are unable to explain the large step changes in brain size that have periodically occurred throughout hominin evolution. The virtually marked and unexplained increase is contemporary with the appearance of H. erectus (or H. ergaster) in Africa. The global bounding main-level palaeoclimate records have some predictive power for within species change over all hominins and inside H. erectus. As we have better resolution in the information from Eurasia, this suggests that ocean-level changes are likely to reflect environmental processes at higher latitudes, but they are unable to explain the environmental processes operating within Africa.

Tabular array two.

Correlations between accented brain size and residual encephalon size (size controlled for fourth dimension) and environmental variables, both over all hominins and within lineages. Positive correlations between mean isotope and CC residuum indicate larger brains are associated with periods of cooling; positive correlations between isotope standard deviation and encephalon residuals indicate that periods of increased environmental variability are associated with periods of increment in brain size (*p < 0.05, **p < 0.01). Assuming type highlights results consequent with environmental hypotheses.

	ocean-level mean		ocean-level s.d.		dust hateful		dust due south.d.
taxon	log_xCC	CC residual	log₁₀CC	CC residual	log₁₀CC	CC residual	log_tenCC	CC residual
all hominins	−0.77**	−0.08	0.57**	−0.18*	0.28**	0.09	0.16	0.06
australopithecines	−0.08	0.34	0.eighteen	−0.64*	0.27	−0.34	0.20	−0.22
H. habilis	0.05	0.24	−0.18	0.01	0.25	0.06	0.99	0.625
H. erectus	−0.65**	0.56**	0.65**	−0.57**	−0.25	0.62**	−0.25	0.50**
H. sapiens	−0.xiii	−0.04	−0.17	−0.04	0.33**	0.03	0.06	−0.11

4. Discussion

We revaluated patterns of hominin encephalon size change and demonstrate that, rather than beingness a monotonic increment, hominin encephalon size increment is dominated past pace changes with limited evidence for long-term gradual increases. Over time, both brain size and environmental stochasticity have increasing trends, which has led to the conclusion that it was ecology unpredictability that drove hominin brain evolution [7,xiii]. However, we have shown that brain size changes exercise not track patterns of increase in environmental variability or unpredictability. Nor practise the data support the proffer that continent-broad patterns of cooling or unpredictability fully explicate patterns of encephalization. Neither of the palaeoclimate records that we use explain the stepwise changes in brain size at approximately 1.8 Mya or 100 kya. Moreover, our analyses advise that the processes that have acted on encephalization in Eurasia differed from those in Africa. Long-term trends in Eurasia map onto global bounding main-level records, merely the changes within African hominins map onto neither Arabian Sea dust records nor global sea-level records. The geological history and climate processes operating in Eastward Africa accept been shown to be distinct from those outside this surface area [71]. Thus, we suggest that any future analyses that attempt to tie encephalization to environmental processes consider carefully the impact of local weather and the relevance of global climate records for understanding selection pressures operating across a wide ecology gradient.

Finally, we turn to consider prove from the archaeological record and enquire how it might allow united states of america to evaluate the arguments for encephalization presented earlier in the paper.

(a) Early on Homo

The advent of the genus Homo, and afterward of H. erectus (or ergaster), was historically associated with the expansion of the savannah [72]. Notwithstanding, recent reinterpretations of the palaeoclimate record have questioned this hypothesis [9,71,73]. Contempo re-evaluations of the African palaeoclimate data propose that pulsed changes may be more important than long-term trends [71,73]. Moreover, these analyses advise that the periods associated with this pace-modify in encephalization may have occurred during a wet rather than a dry period. Although there is bear witness for cultural and technological innovation gimmicky with H. ergaster, including the advent of the Acheulian stone tool industry, the material culture during the rest of H. erectus sensu lato being is broadly characterized by stasis [12]. This means that the gradual encephalization in H. erectus was not associated with increasingly sophisticated technologies.

The advent of early Human being was also associated with profound changes in life history, as well as body size and shape. Some of these adaptations could likewise be linked to the step-increase in brain size between H. habilis and H. erectus/ergaster [1,3]. Tobias [74] identified a marked difference in the demography of hominin assemblages between the late australopithecines and early Homo. The former were characterized by a big number/proportion of physically mature individuals, whereas the latter were characterized past a large number of immature individuals. He argues that this is the outcome of a high bloodshed charge per unit in subadults caused past ecology stress resulting from the changing surroundings during the Plio-Pleistocene. Increased mortality, however, could also consequence from increased predation force per unit area. Increasing immature mortality would provide a strong selective pressure to increase nativity rates and could explicate the modern human life history with 'stacking' of weaned, but immature offspring [3,75]. Having multiple immature-dependent young volition cause knock-on consequences for social group structure, foraging behaviour and range employ, and could drive the development of cooperative convenance, crèches and central place foraging. An extended juvenile menstruum allows for a protracted learning menstruum [76,77], during which sophisticated reasoning and problem-solving capabilities accept the opportunity to develop. Although the fossil record suggests an increment in reproductive rates, a fully modernistic life-history strategy does not appear until the arrival of AMH [78]. Unfortunately, we have little quantitative data that can exist used to test hypotheses about changes in social behaviours. We can, however, evaluate what neurological changes are associated with the pace changes in brain size. Early Man brain morphology is characterized by increases in the frontal and temporal lobe, both of which are heavily implicated in social tasks [36,37,79,lxxx]. Show that social grouping size changed in steps concurrently with brain size changes would more conclusively support the social brain hypothesis.

(b) Afterward changes

After the appearance of the genus Homo, the rate of encephalization is less straightforward. Within Africa, brain size increases at a roughly consistent charge per unit, whereas the introduction of migrants into Eurasia creates periodic step-wise changes. Whether it was changes in ecology conditions or competence that impelled these migratory events remains unclear. Moreover, despite an increasing brain size, there is little from the archaeological record that conclusively identifies cognitive advances. For much of the period following the appearance of H. erectus sensu lato, Acheulian technology is largely static until approximately 300 kya when it gave way to the prepared core technology in the Middle Palaeolithic/Stone Historic period [46,81]. At that place is tantalizing evidence for the first controlled use of fire together with charred seeds and woods [82] coincident with the commencement advent of H. heidelbergensis in Eurasia. It has been proposed that language and controlled utilize of fire may have co-evolved equally part of an adaptive suite that helped to socially bail groups [12]. However, it is not straightforward to identify the cognitive inferences associated with fire utilize.

Interestingly, although AMH first appeared in Africa around 200 kya, signatures of behavioural (and cognitive) modernity in the archaeological record remain uncommon for a protracted period following their arrival. From around 80–100 kya, there is increasing show of symbolic behaviour and cultural variation in tool manufacture [83]; notwithstanding, this prove remains desultory and does not become widespread until much later [84]. Additionally, technologies and innovations appear and then disappear at individual sites [83], suggesting that either cultural behaviours are lost inside populations or site occupancy is ephemeral. In contrast, this flow is followed past a veritable explosion of material and symbolic culture, increasingly sophisticated technologies and long send distances. This marked increase in archaeological testify has led to the proposition of a body of water-modify in human being behaviour called the Upper Palaeolithic revolution [84]. Although contention remains virtually when modernity first arose or whether there was an explosion, there is no denying the exponential increment in signatures of behavioural modernity over the past 30 kya. Critically, we cannot decide from the archaeological tape whether this cultural explosion is the result of a cerebral advance or a more mundane procedure.

For example, the sudden explosion of symbolic material, specialized tools and changes in material employ that characterize the Upper Palaeolithic have been linked to a demographic tipping indicate whereby population density is high enough to maintain culturally transmitted information [85]. In this scenario, demography allows a scaffolding of underlying gradual accumulated changes in engineering and cognitive power [83]. Population density increases could result from either ecological or social changes (i.e. being able to alive at higher densities). The ability to maintain larger population sizes could ultimately be a issue of increased cognitive capacity. The encephalon size bear witness suggests that the most recent period of encephalon size increment is effectually 100 kya (figure ane a,b). Thus, the commencement traces of modernity coincide with, or soon precede, the menses of a marked change in brain size. Withal, it is merely later population density reached a critical level that there is a clear indicate in the archaeological record with the emergence of the Upper Palaeolithic as AMH spread out of Africa (approx. lx kya).

(c) Early on language

One widely suggested innovation that could explain the cultural proliferation of the Upper Palaeolithic revolution menstruation post 50 kya is fully functional language. Without language, it is not possible to share symbolic ideas or to impart knowledge about events removed in infinite or time. It has controversially been proposed that the cultural complexity of the Upper Palaeolithic coincided with a brain mutation that permitted fully diddled modernity approximately 50 kya with the advent of the Upper Palaeolithic in Europe [86,87]. Nonetheless, this idea has been largely dismissed on the grounds that at that place is no evidence for any correlated brain size changes [88,89]. In dissimilarity, our reanalysis of the fossil data indicates a shift in brain size that is gimmicky with changes in cranial and song beefcake (which, it has been argued, become more than like that of contemporary humans at this fourth dimension [90,91]).

While in that location are various views on how early or how belatedly language evolved, at that place is an of import distinction between spoken language (the capacity to vocalise) and linguistic communication (in the sense of fully grammatical propositions) that needs to be borne in mind [92]. Communication competencies would have successively increased prior to the advent of fully modernistic language. Whether these arose through the transfer of gestural forms of advice to verbal ones, or what the structure and sound of early proto-language would accept been has been the subject of intense speculation [93]. The anatomical signatures that have been associated with language product (e.g. the thoracic nervus expansion [94] and, more controversially, the hypoglossal canal [95] coincide with the advent of primitive humans around 600 kya [92]) are, in fact, every bit required for not-exact forms of human being advice such as wordless singing (sensu [96,97]). If language complexity is dependent on intentional competences (or whatever relevant aspects of cognition these index) and these in turn are correlated with brain size, then tracing encephalon size might tell the states something virtually the phases of language development. The last step change in brain size that begins at approximately 100 kya may reflect this final phase shift in linguistic communication complexity. Some show to support this comes from a recent report tracing the global distribution of phoneme variation that provides strong evidence that complex language evolved in Africa and spread speedily from approximately 80 kya [98].

5. Determination

Our re-evaluation of the enduring mystery about what collection homo encephalization has non identified a smoking gun. Nosotros advise that the bear witness in support of either the variability or arditiy hypothesis is not compelling and that the relationship between encephalon size and palaeoclimate is not straightforward. In the light of this, we suggest that the drivers of hominin encephalization are manifold. Environment likely played a part, whether as a direct pressure or by forcing hominins to change their behaviour so as to exist able to use more risky and peripheral habitats, to alive in larger groups, or to employ novel resources. However, the climate variables we have used cannot explain encephalization. Nearly tantalizing and enigmatic is the role of social development in the encephalization process. There remains no direct measure of social grouping construction or complexity from archaeological testify; yet, social intelligence is fundamental to what makes us man. Show from language evolution studies, encephalon morphology and the appearance of symbolic behaviour, all advise that language evolution is a cardinal component of human being cognitive evolution and that cultural advances may have occurred in a serial of steps that mirror changes in brain size and compages.

Acknowledgements

S.S. is supported by a Majestic Guild Dorothy Hodgkin Fellowship.

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