Bridging disciplines to better elucidate the evolution of early Homo sapiens in southern Africa

Elucidating the history of Homo sapiens has been a passion shared by many researchers spanning several decades. There are now overwhelming lines of evidence from genetic, archaeological, palaeoanthropological and, to some extent, palaeoenvironmental research, that place Africa as the region of origin of our species. The different fields of study use diverse types of data, and methods are subject to variances introduced by mutation rates, time estimates and/or sampling biases. All of these approaches have their respective shortcomings and error ranges and are accompanied by intense debate. Yet, it is timeous to review the most recent and salient highlights that the different approaches are contributing towards explaining our deep history and ancestry. It is, after all, one history, and consequently, there ought to be several convergent patterns between data sets. Our focus is to present an updated regional synthesis from each discipline for a specific window in time within the southern African context, namely between ~160 ka and 85 ka, and to speculate about possible connections between data sets for this period. Even though our focus is specific in time and space, it is not intended to consider southern Africa in isolation from the rest of Africa or to suggest a singular ‘origins’ locale for modern Homo sapiens. We hope that this integrated approach will stimulate discussions to include broader time periods within Africa and between continents.

Another study, which examined human variation in conjunction with the spread of Helicobacter pylori strains (Gram-negative, micro-aerophilic bacteria found in the stomach), estimated that the H. pylori strain that is uniquely associated with Khoe-San populations, diverged from all other human associated H. pylori strains at ~116-88 ka. 13 By examining the co-evolution of H. pylori and humans, an independent scrutiny of deep human ancestry is provided.

Context within the MIS chronology
Using the current time estimates of ~160-88 ka from the genetic data as a proxy for the history of Homo sapiens in southern Africa, we explore possible connections with the palaeoenvironments and marine isotope stages (MISs) in which these ancestors would have lived.Most of the earliest population and lineage divergences in our species, based on existing genetic dates, involve human populations currently living in southern Africa.These divergence dates overlap with the younger part of MIS 6 (~195-130 ka) and MIS 5b-e (~130-85 ka) (Figure 3).Even though we use the MIS record as a broad, global time frame and palaeoenvironmental backdrop, we acknowledge that MIS boundaries might not account for many of Africa's climate changes, 14 or all variation in human behaviour. 15S 6 is generally seen as one of the longest, coldest glacial periods. 16ts effect on the ecosystems of southern Africa remains poorly understood. 17Comparative work, based on a range of data, shows that generalised climatic patterns derived from northern hemisphere glacial/ interglacial cycles are imprecise when applied to the African record. 14onetheless, in sub-Saharan Africa, glacial periods such as MIS 6 were often, but not exclusively, accompanied by aridity with expanding deserts and arid regions. 18,19Such regions could have hampered interand/or intra-regional movement of humans and other animals. 17Data for MIS 6 in South Africa indicate two dry phases, interspersed by a wet phase at ~140-130 ka (Figure 3). 14S 6 was followed by MIS 5e, a sub-stage during which global conditions warmed and sea levels probably rose rapidly.20 During such interglacial phases wetter climates and extended woodlands are expected, yet these remain general trends that might not apply equally to all regions or environmental niches.18,19 As a whole, MIS 5 comprises a sequence of sub-stages alternating between warmer and cooler conditions (Figure 3).21 MIS 5e was an early warm interval, and was followed by irregular, but generally cooler, conditions culminating in the glacial conditions of MIS 4 (~71/74-60 ka).Inferred climatic conditions point to a dry spell spanning the MIS 6-5 boundary and again at ~108-90 ka (Figure 3).14 Similar to current patterns, past climates varied with latitude, so that periods of relatively increased aridity or humidity were asynchronous across the northern, eastern, tropical and southern portions of Africa. 14Changes most likely occurred under different regimes of climate forcing, creating alternating opportunities for migration into adjacent areas.For continental Africa, current data suggest: (1) little relation between largescale demographic and climate change in southern Africa between ~130 ka and 30 ka, (2) strong support of hominin occupation of the Sahara during discrete humid intervals from ~135 ka to 115 ka and from ~105 to 75 ka and (3) that hominin populations in equatorial and eastern Africa may have been buffered from the extremes of climate change.14 The data Figure 3: Timeline with relevant marine isotope stage (MIS) boundaries and generalised temperature interpretations, climatic inferences 14 , current interpretations of the DNA record based on different approaches 1,4,5,9,12,13 , age estimates for the relevant dated fossil record 22 , the revised archaeological sequence 33 and potential long-sequence sites where occupations might span gaps in the directly dated record.

The palaeoanthropological record and genetic data
Fossil remains, dated close to the estimate of genetic divergence times of current southern Africans from other humans, could possibly be linked to the common ancestral H. sapiens population.For example, by ~160-80 ka some of the earliest modern H. sapiens fossil material is reported from South African contexts (Figures 1 and 3) 22 : • A phalanx and tooth from Sea Harvest mostly likely date to MIS 5b (~95-85 ka).
• Human teeth at Blombos occur in deposits with age estimates of ~100 ka.
• Human cranial fragments, jaws, teeth and post-cranial bones from Klasies River were found in archaeological contexts with age estimates of ~110 ka, ~100 ka and ~100-80 ka.
A partial femur from Blind River dates to MIS 5e (~118 ka).
• A partial cranium and mandible from Border Cave with age estimates of either >150 ka or ~91-71 ka, could be relevant to our time slice.Because the material was found in secondary context, however, the age estimates are still insecure.A partial infant skeleton found in a grave at the site is thought to date to ~90-66 ka, but its context too has been questioned.
With the exception of Klasies River that produced more than 30 specimens, the fossil sample that can be traced to this period with a measure of surety is small, and the majority of the specimens are isolated teeth.Based on morphological characteristics, the population is mainly accepted as H. sapiens, but some specimens exhibit archaic morphology. 23It seems that during this period South Africa was inhabited by populations who showed a wide range of anatomical variation, mostly morphologically similar to present-day H. sapiens.However, the process of gracilisation (reduction of prominence of facial features) was not yet completed, 22 and did not yet reflect more recent Khoe-San morphology. 24acilisation is expected to be accompanied by several morphological changes.We suggest that certain aspects of gracilisation could be the result of gene interactions under the influence of selective forces.Some evolutionary processes that might have influenced the shaping of genomic variation in humans at >100 ka have been identified in genetic studies. 9,25,26Of the five genomic regions that were found to have signatures for strong selective pressure in humans before ~100 ka, 9 three contained genes that were associated with skeletal development, and may have contributed to the process of gracilisation.Positive signals for selection were obtained in a region immediately upstream of the ROR2 gene that is involved in the regulation of bone and cartilage development and SPTLC1, a gene involved in hereditary sensory neuropathy.Other signals for selection were obtained for the region containing the SULF2 gene that regulates cartilage development, and a region containing RUNX2, which is involved in skeletal morphogenesis. 9ntatively, variations in RUNX2 have also been linked to phenotypic differences between H. sapiens and archaic humans, such as frontal bossing, clavicle morphology, a bell-shaped ribcage and regulating the closure of the fontanel [26][27][28] -the latter being critical for brain expansion.Perhaps also relevant, is that a fixed difference between the DNA of archaic and modern humans occurs in EVC2, which when mutated in modern humans, causes Ellis-van Creveld syndrome. 26Among other symptoms, this syndrome includes taurodontism, an enlargement of the dental pulp cavity and fusion of the roots.Taurodontism is a common trait in the teeth of H. neanderthalensis and other archaic humans.Although a Denisovan molar also has an enlarged pulp cavity, it lacks fused roots. 26These observations suggest that mutations in EVC2, perhaps in conjunction with mutations in other genes, might have caused a change in the dental morphology of early H. sapiens.Because gracile H. sapiens morphology appeared fairly abruptly, selection on a few morphology genes such as those mentioned above, could have been involved in the 'anatomical' emergence of our species. 9,26Morphological changes are, however, complex, and further work needs to test these suggestions.
Homo fossils in the South African record pre-dating 200 ka, and considered to perhaps represent morphological trends leading up to current anatomical characteristics, include for example (Figure 1) 22 : • A partial cranium from Florisbad dated to 259±35 ka that is ascribed to Homo helmei or late archaic H. sapiens.
• A mandible and radius from Cave of Hearths ascribed to archaic H. sapiens and/or early H. sapiens that have an age estimate of ~500-200 ka.
• A tibia and teeth (most of which show modern morphology, but are larger than the contemporary African average) from Hoedjiespunt, dated to ~300-200 ka, that are ascribed to H. heidelbergensis.
The relevant South African Homo fossil record before ~200 ka is sparse, and presently we are not aware of material that can be placed securely at ~200-120 ka, except perhaps the material from Border Cave that has a questionable age estimate of ~171-152 ka.This gap could simply reflect current sampling, preservation and/or dating deficits.On the other hand, possible morphologically intermediary fossil material is present in assemblages pre-and post-dating ~200-120 ka.The gap in the fossil record could be seen as evidence that early H. sapiens evolved elsewhere in Africa and migrated to southern Africa, but this possibility should be considered in the light of the archaeological record, some aspects of which are highlighted below.Fossil material from other African regions dating to this period is also sparse, but include remains from Omo Kibish, Ethiopia, at ~195 ka, 29 Herto, Ethiopia, at 160-154 ka, 30,31 and Singa, Sudan, at >133 ka. 32These remains have all been interpreted as either archaic (potentially ancestral to modern humans) or anatomically modern H. sapiens, and they provide direct evidence of human presence in east Africa at the time.

The archaeological record, human behaviour and the genetic record
In contrast to the fossil record, the South African archaeological record supports human occupation at several sites during ~200-120 ka (Figure 1).Even though the dating of some contexts remains controversial, examples of sites include (Figures 1 and 3) 22,33 34,35 Thus, apart from indicating human presence on the landscape, technological approaches also do not seem to point to discernible breaks, yet this interpretation could be an artefact of still coarse research resolution. 35epared core technologies, also referred to as Mode 3, provide a level of flexibility in predetermining tool shapes that is not evident in preceding knapping strategies. 34Such flexibility is expressed in the variability observed in and between stone tool assemblages. 36But it is not only knapping strategies that provide insight into human technological and associated cognitive capacity at the time.It has been suggested that hafted technologies, such as stone-tipped spears, often associated with Mode 3 artefacts, signal development towards advanced technological, behavioural and cognitive flexibility, opening the way towards a considerable expansion of, and variability in, problem solution ability. 37,38mbrose 39 argues that composite tools, such as hafted hunting weapons, place greater demands on integrating working memory with prospective memory, and ultimately constructive memory. 40These faculties are associated with the anterior frontal lobe of the human brain and Broca's area that also facilitate processes involved with grammatical language and manual hierarchical assembly. 39,41Early H. sapiens were, however, not the only hominins to produce composite tools, and thus probably shared the associated cognitive and behavioural traits with H. neanderthalensis, H. heidelbergensis and other archaic humans. 38her interesting trends that appear in the archaeological record, concurrently with genetic evidence for the divergence of the Khoe-San ancestral population and fossil evidence of early H. sapiens, include socalled symbolically mediated behaviours.For example, the use of red ochre has, arguably, been interpreted as circumstantial evidence for the painting of abstract designs on the bodies of ritual performers. 42Utilised red ochre nodules occur in South Africa associated with archaeological material at Pinnacle Point 13B by ~164 ka. 43From ~100 ka, such red pigments become a common feature at most Middle Stone Age sites.
The recent find of an ochre-processing workshop at Blombos Cave, 44 in which a liquefied ochre-rich mixture was produced and stored in two abalone (Haliotis midae) shells by ~100 ka, confirms that pigment use was firmly established at the time.Perhaps more secure evidence of symbolically mediated behaviour includes engraved ochre nodules, some with complex geometric patterns, also from contexts dating to ~100 ka at Blombos, Pinnacle Point 13B and Klasies River. 45,46But, even when evidence of symbolic thinking (i.e. the capacity to attribute specific meaning to conventional signs) is apparent, it is a trait shared with a growing number of hominins. 47Yet, it can hardly be argued that during the period under discussion we see early signals of a uniquely human way of doing and thinking in the archaeological record of southern Africa.[51][52][53] Some of these behavioural and cognitive trends can, conceivably, also be explored through genetic research.By using what is known from medical science and comparing the DNA in contemporary humans with that of archaic humans such as Neanderthals and the Denisovan specimen, researchers are finding tentative links with certain genetic variants involved in cognitive function that might be exclusive to H. sapiens. 25,26Furthermore, when compared with Neanderthals, several genes involved in cognitive development showed strong evidence for selection in early H. sapiens. 25These genes include DYRK1A that is medically associated with cognitive impairment, NRG3 medically associated with schizophrenia, and two genes, CADPS2 and AUTS2, medically associated with autism. 25Other genes linked with development and neuronal function have also been shown to be strongly selected for in early humans. 9SDCCAG8 has been medically associated with microcephaly, LRAT with Alzheimer's disease and SULF2 with distorted brain development. 54And ROR2, that was previously mentioned in relation to its role in skeletal development, is upregulated by FOXP2, 55 which is the only gene currently known to be involved with speech and language disorders that follows Mendelian inheritance. 26,56,57e above-mentioned medical associations with genes are mere pointers to some of the gene/genomic region's functions.Most of these functional associations and their evolutionary advantages are still poorly understood.With further research, particularly when linked with gene expression studies, we should learn more about the developmental processes that distinguish our species from our early ancestors.

What have we learnt from the multidisciplinary approach?
It has been suggested 58 that an appropriate theoretical framework for understanding our origins can be achieved by integrating evolutionary geography, based on spatial distributions of populations and contingent, adaptive and demographic aspects of micro-evolutionary change.
Following on previous calls for the integration of different data sets, 58,59 our cross-disciplinary approach attempts to update and contribute to the broader theoretical framework from a southern African perspective for the period between ~160 ka and 88 ka.Bottleneck scenarios are often used to explain the relative lack of genetic diversity in H. sapiens compared to other species. 58,60Two broad hypotheses have been formulated for a population bottleneck during MIS 6. 58 According to the first, humans in sub-Saharan Africa separated into a number of regional groups, some of whom survived, depending on resources and/or their respective evolutionary responses.The second hypothesis suggests that a single (founder) population survived as a result of the interaction between population size and the carrying capacity of the environment.The first scenario would imply that the palaeoanthropological diversity in Africans between ~200 ka and ~100 ka represents true ancestral diversity.On the other hand, if the second hypothesis is accurate, archaeological and Homo fossil diversity in Africa at the time does not represent ancestral diversity, but a single surviving H. sapiens ancestral group. 58ing genetic data, various possible scenarios have been explored regarding the origins of early H. sapiens or anatomically modern humans.One possible scenario is a multiregional origin of H. sapiens, where anatomically modern humans originated in several places in Africa within the same time frame as a result of similar selective pressures.Alternatively, anatomically modern H. sapiens could have originated in one place on the continent and then replaced archaic populations (groups that do not show the distinctive modern human morphology).The third scenario is an intermediate scenario in which anatomically modern H. sapiens originated in one place on the continent and then distributed and produced offspring with 'archaic' groups, resulting in the spread of 'modern' genetic material.Whereas mtDNA and Y-chromosome studies initially alluded to a single origin model, recent studies based on autosomal genetic variation in African populations do not conclusively point to one region of origin within the continent. 9enetic support, therefore, currently leans toward either a multiregional scenario or a situation in which admixture took place between early H. sapiens and human populations with archaic features.[63] Human fossil remains could potentially be used to assess bottleneck and/or population isolation scenarios, and it is suggested that expecting craniometric similarities between H. sapiens populations from different regions and genetic relationships is probably misplaced. 64 with more recent Khoe-San groups or their immediate ancestors.Rather, such features might have developed more recently as a result of isolation and local adaptation to the environment of the region. 24,64,65The seeming absence of well-contextualised human fossil specimens during a key stage in South Africa could indicate that anatomically modern H. sapiens 'originated' elsewhere on the continent, as is often hypothesised for east Africa. 66The archaeological sequence serves to expose a possible sampling and/or preservation bias in the fossil record, but is itself still plagued with shortcomings in dating resolution and sampling.However, similar to the genetic record, the current archaeological data could be seen to support a local, but not necessarily unique, origin and/or an archaic-modern admixture scenario.
The multidisciplinary approach incorporating information from diverse disciplines afforded us the opportunity to review some aspects of early human history in southern Africa.For example, the 'Cape Floral Region -South Coast Model' for the origins of early H. sapiens during the Middle Stone Age, is linked to a genetic bottleneck during which populations crashed and survived only in favourable refugia, possibly resulting in a single ancestral group. 17,67Yet, South African inland sites such as Bundu Farm, Wonderwerk Cave, Florisbad and Border Cave were also inhabited during MIS 6 (Figures 1 and 3).None of these sites are located near the Cape Floral Region, and all are in zones with very different climatic conditions.Based on the topography of South Africa, past climatic conditions, even though different from current ones, would also have been different between the Cape Floral Region and the inland sites mentioned above.From a genetic viewpoint, the current interpretation that all human mtDNA and Y-chromosome lineages coalesced ~200-300 ka, just before MIS 6, might suggest such a population bottleneck, 5,6,68 and numerical simulations on autosomal data to reproduce current genetic diversity initially supported these findings. 69Blum and Jakobsson 70 , however, suggest that although a bottleneck model at MIS 6 might be viable, a model of multiple archaic African populations surviving and giving rise to early H. sapiens is also plausible.Re-sequencing of the African data furthermore shows that a demographic model without an ancestral bottleneck during MIS 6 is the most likely scenario. 71The work of Li and Durbin 72 even indicates an increase in human population sizes during this time, or, alternatively, a scenario in which multiple populations became separated and then mixed again.[7] Based on current understanding of the different data sets and their interpretations, we predict that if a bottleneck scenario with a single surviving population is considered, it probably occurred before MIS 6, and that subsequent H. sapiens populations survived in several African landscapes.This outcome is similar to the best interpretation ventured 15 years ago. 58However, it pushes back the time frame and might explain what we see in the collective records that seem to increasingly indicate a number of regionalised early H. sapiens populations.These groups might have been impacted upon by more recent or secondary bottlenecks, such as the Mt Toba volcanic winter at ~75 ka, 60 and/or extended periods of separation before new expansions and admixtures recurred.Palaeoenvironmental data, however, remain coarse-grained.The notion of a volcanic winter in east Africa at ~75 ka and an accompanying population bottleneck is being challenged based on sediments recovered from Lake Malawi. 73The integrative theoretical framework suggested by Lahr and Foley 58 includes three key aspects: (1) the geographical relationships between parent and daughter populations, (2) the longevity of populations and their subsequent roles in sub-structuring and diversification and (3) the relationships between environmental change and behavioural innovations in relation to range expansion.This framework requires a multidisciplinary approach.However, currently we do not have the fine-grained resolution in any of the research areas and/ or their associated disciplines to produce the conclusive outline for the origins of our species.Yet, by pooling knowledge we can continue to refine our interpretations of past data sets.
Regardless of ongoing 'origins' debates and shortcomings in ages and data sets, several traits, currently considered to reflect the modern characteristics of our species (anatomically and behaviourally), had their southern African roots in MIS 6-5.And there seems to be acceleration in behavioural and cognitive trends towards complexity and higher levels of variability in the archaeological record from at least ~160 ka, subsequent to the time identified in several genetic studies associated with the establishment of a split in the common population lineage of our species.The current genetic record remains inconclusive as to where in Africa early H. sapiens first emerged, and indeed if there was only one 'origin', but it does not negate a local (southern African) scenario.
This short synthesis shows that much progress has been made regarding how we understand and interpret the presence of early H. sapiens in southern Africa, and that we can come closer to a robust history by interweaving data obtained from multiple approaches (Figure 3).Relationships between the data sets remain tentative, but we suggest they clearly provide impetus for future cross-disciplinary exploration.By collating information from the different disciplines, it seems increasingly possible that the perceived gap between early H. sapiens biology and archaeological interpretations of our behavioural and cognitive evolution will continue to shrink.

South
African Journal of Science http://www.sajs.co.zaReview Article Early Homo sapiens in southern Africa Page 2 of 8 Grey squares, fossil sites; black squares, archaeological sites; grey and black squares, archaeological sites with fossil material.

Figure 1 :
Figure 1: Map of southern Africa with the locations of population groups, fossil sites and archaeological sites mentioned in the text.

Figure 2 :
Figure 2: Rooted population tree showing the genetic relationships of some sub-Saharan African populations.
34b-Saharan Africa (Figure3).Wurz34provides a synthesis of developments in stone tool technologies in southern Africa for the period under discussion.According to her, prepared core technology with blades and points, typical of the Middle Stone Age, starts before MIS 7 (~244-195 ka) and continues into MIS 6 with inter-and intrasite variability, but without discernible technological breaks.By MIS 5, Middle Stone Age assemblages become widespread and a variety of technological strategies, perhaps representing technological trends that developed from earlier technological approaches, are evident.Early Middle Stone Age assemblages are typically >130 ka and characterised by prepared core technologies in what can be considered components of generalised toolkits.
This group of assemblages represents a parsimonious reflection of human presence at the time.Many more sites with similar Middle Stone Age archaeology are known from across the region, but dating is weak or absent.Some genetic time estimates of the first divergences within H. sapiens, derived from present-day populations in southern Africa, overlap with the archaeological record of a section of the Middle Stone Age Volume 109 | Number 11/12 November/December 2013 South African Journal of Science http://www.sajs.co.za in What is more, the palaeoanthropological data also indicate that early H. sapiens populations in South Africa did not yet have the gracile features associated 6 http://www.sajs.co.za