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Home , Ardi, Aurignacian, Australopithecus sediba, Behavioral modernity, Blombos Cave, Bruniquel Cave

doi 10.4436/jass.97001 JASs Invited Reviews Journal of Anthropological Sciences Vol. 97 (2019), pp. 45-68

Mosaic in hominin phylogeny: meanings, implications, and explanations

Andrea Parravicini1 & Telmo Pievani2 1) Department of Philosophy, State University of Milan and Department of , University of Padua, e-mail: [email protected] 2) Department of Biology, University of Padua, Italy e-mail: [email protected]

Summary - In paleoanthropological literature, the use of the term “mosaic” (, mosaic trait, mosaic , and so on) is becoming more and more frequent. In order to promote a clarification of the use of the concept in literature, we propose here a classification in three different meanings of the notion of mosaic in evolution: 1) morphological (inter-specific and intra-specific) instability in a certain phase of a branched phylogeny; 2) multiple trajectories and versions of the same adaptive trait in a branched phylogeny; 3) the trait itself as a complex mosaic of sub-traits with different phylogenetic stories (as is the case in ). We argue that the relevance of such mosaic patterns needs a macro-evolutionary interpretation, which takes into consideration the interaction between general selective pressures (promoting different versions of the same ) and a cladogenetic approach in which played a crucial role, due to ecological instability, habitat fragmentation, and geographical dispersals in .

Keywords - Mosaic evolution, Macro-evolutionary approach, , Encephalization, , Stone-, Human language evolution.

The term “mosaic” in human old linear anagenetic model of human phylog- evolution eny with the cladogenetic Darwinian model of a knotty and irregularly branched tree. However, The leading perspective on human evolu- the more new data and findings are available, the tion has been largely modified, due to a num- more the general picture of hominin phylogeny ber of different factors: the paleontological and seems puzzling and problematic, which raises archaeological record has been widely expanded; new research questions. new dating methods and tools of integrated Despite the fact many efforts have been made analysis are available; the possibility to integrate to put in order and explain the tangled puzzle a great amount of new convergent evidence com- of and evolutionary trajectories, the pic- ing from different fields – such as , ture of the hominin tree remains full of question , paleo-, paleo- marks and blind spots, especially following dis- ecology, social studies – is increasing more and coveries in recent . ramidus has more. All these changes and the dramatic expan- weakened the dominant framework of the 20th sion of the empirical basis have made it clear that century that used living African , especially the linear model of a single anagenetic evolution , as proxies for the immediate ances- is today hardly tenable (despite its recent resur- tors of the human . Referring to a “missing- gence for restricted periods of human evolution: link” between and such alleged apelike see Lordkipanizde et al., 2013 and Rightmire et ancestors, after “”, no longer makes sense al., 2017, about an alleged single polymorphic (White et al., 2015). A stone has species of early ). Today, the scientific com- been found at the 3 site, West Turkana munity is generally unanimous in replacing the (), at 3.3 Mya, predating the by

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700.000 years, and conjecturally not in associa- Mosaic 1: hominin tion with a Homo species (Harmand et al., 2015). morphological instability A jawbone from Hadar and Ledi-Geraru formations in Afar was recently dated to ca. 2.8– Mosaic evolution is a pervasive pattern that 2.75 Mya, pushing back the origin of the has characterized, in general, the evolutionary Homo by 400,000 years (Villmoare et al., 2015). patterns of several groups of organisms through- The amazing number of remains from the Rising out ’s (Hopkins & Lidgard, 2012). , South , have been associated De Beer (1954, p. 163) firstly coined the term of to the new species , which dates to mosaic evolution with reference to the urvogel 315-236 Kya (Dirks et al., 2017). This bizarre , indicating the presence of a mixture human species had a very small (560 cc in of ancestral and derived traits. Today, it has been males) and an -like body in a largely proven that some can evolve combination with modern human-like derived with different timing and stages within a single traits, such as suited to handling tools and lineage so that a given organism shows a mosaic precision grip. Surprisingly, it lived in the African of ancestral and evolving descendant characters at the same of the , in respect to its own ancestors. Mosaic evolution which were evolving in , and maybe of results from multiple influences molding morpho- the early Homo sapiens, which were emerging logical traits and implies the hierarchical organi- in the African continent. Fossil remains from zation of organismal traits into semiautonomous , , have been dated to ca subsets, or modules, which reflect differential 315 Kya and associated to hominin forms which genetic and developmental origins. The degree were endowed with teeth, and faces indis- of independence of the modules can be quanti- tinguishable from anatomically modern humans, fied using statistical tests providing in this way a but also with elongated and non-globular strong evidence of the presence of mosaic evolu- (Hublin et al., 2017). tion in a or in a lineage (beyond the seminal According to several authors, hominin phy- work by Olson & Miller 1958, see in particular logeny seems to proceed through so-called Adams, 2015; Clarke & Middleton, 2008; Felice “mosaic-like patterns”, with several coeval species & Goswami, 2018; Goswami & Polly 2010; evolving along different trajectories, and show- Klingenberg, 2008, 2009; Klingenberg & Lobón, ing combinations of derived and retained traits. 2013; Londe et al., 2015). Despite the fact the use of the term “mosaic” in Mosaic-like patterns play a major role in the human evolution field is widespread today human evolution field. In The of Human among specialized scholars, the meaning of this Evolution, John Langdon (2016, pp. 129-131) seems yet to be univocally defined. The argues that “When paleontologists compare a growing importance of the term “mosaic” in ref- single ancestral species with a known descendant, erence to the characterization of hominins key there is an expectation that a fossil intermediate features and the current lack of precision in the in time will be similarly intermediate in all ana- use of this term in literature might be an indica- tomical features. However, these different species tion that we need novel conceptual tools to better of hominin do not a simple linear story. Each focus on the new paleo-anthropological picture. body part has its own history and has evolved at The goal of the present review is, on the one a different pace and sometimes a different direc- , to examine the main uses of the notion of tion in each species to produce unique combina- “mosaic” in the literature related to the human tions of ”. This is what paleoanthropolo- research field. Furthermore, the essay aims to gists generally call “mosaic evolution”: a differen- investigate the possible patterns and processes tiated evolution and a “potential independence which undergo such mosaic-like changes in bio- of traits” (Gould, 1977b, p. 58), combined in logical and cultural human evolution. different ways from species to species. The term A. Parravicini & T. Pievani 47

“mosaic” refers here to the description of what The team leader of the Malapa enterprise, we call “hominin morphological instability”, Lee Berger, refers to “The mosaic of which means specific morphological assemblages sediba” (Berger, 2013) in his or modules evolving independently from each introduction to the 2013 Science’s special issue. other, in a non-harmonious way and at different In the final part of the text, Berger writes that rates when compared with other related species. “This examination of a large number of associ- As S.J.Gould wrote, “The concept of ‘mosaic ated, often complete and undistorted elements evolution’ […] refuted the notion of harmonious gives us a glimpse of a hominin species that development by affirming that individual organs appears to be mosaic in its anatomy and that pre- could have independent phyletic , sents a suite of functional complexes that are dif- despite the evident correlation of parts within ferent from both those predicted for other aus- any organism” (Gould, 1977a, p. 234). tralopiths and those of early Homo”; concluding The six articles of the 2013 special issue that that “Such clear insight into the anatomy of an Science dedicated to the anatomy of Au. sediba early hominin species will clearly have implica- (ca.1,98 Mya) are good examples of what the tions for interpreting the evolutionary processes term “mosaic” concretely means. These studies, that affected the mode and tempo of hominin along with other research published in the previ- evolution and the interpretation of the anatomy ous three years, provide a comprehensive exami- of less preserved species”. nation of the anatomy of the new species which Another paradigmatic example which can was found in 2008 in Malapa, . Au. illustrate this sense of “mosaic evolution” is the sediba appears phylogenetically distinct from anatomy of Homo naledi. Recently dated to 236- Au. afarensis, but close to Au. africanus for what 335 Kya (Dirks et al., 2017), the species was dis- regards the highly heritable nonmetric dental covered in the Rising Star complex, South traits and it also shares derived traits with the Africa, which is today the largest assemblage of a genus Homo (Irish et al., 2013). Some mandibu- single hominin species yet found in the African lar materials and other features of the cranium continent. H. naledi shows a similar body mass and skeleton share similarities with those of and stature to small-bodied human populations, other , but differ from Au. afri- but it also has a small endocranial volume, rang- canus both in size and shape, as well as in their ing from 465 cm3 to 560 cm3 (Schroeder et al., ontogenetic growth trajectory (De Ruiter et al., 2017), which is analogous to australopithecine 2013). The upper limbs are largely “primitive” species. The dentition is small and simple in in their , well suited for arboreal occlusal morphology but still primitive (Berger climbing and possibly suspension, and therefore et al., 2015). Cranial morphology is unique, similar to other australopithecines (Churchill et nevertheless sharing traits (i.e., aspects of cra- al., 2013). However, Au. sediba’s hand presents nial form, facial morphology, and mandibular a suite of derived Homo-like features, such as a anatomy) with species across the genus Homo, long and short fingers associated with such as H. habilis, H. rudolfensis, H. erectus and precision gripping (Kivell et al., 2013). Even the Middle Homo (Laird et al., 2017). H. morphology reveals a mosaic combina- naledi’s hand possesses a combination of primi- tion of retained and derived traits (Schmid et al., tive and derived features never seen in any other 2013) and many features of the hominin, with strongly curved proximate and are largely derived, with the highly flexible spine intermediate phalanges, but also with a , showing a configuration which is quite similar to thumb and palm that suggests enhanced the Nariokotome H. erectus skeleton (Williams et manipulation ability (Berger et al., 2015; Kivell al., 2013). Finally, the morphologies of the heel, et al., 2016). The same mosaic assemblage can midfoot, , hip, and back are unique and be found in the morphology and inferred func- peculiar (De Silva et al., 2013). tion of the , which is predominantly modern

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human-like, well adapted for striding bipedal- mosaics of H. sapiens’ anatomical traits in dif- ism, but still different from modern humans in ferent parts of the African continent (and not having more curved proximal pedal phalanges only in ), as also recently suggested by (Harcourt-Smith et al., 2016, p. 1). All these Schlebusch et al. (2017). unique or derived features are still combined in Further examples of mosaic morphological a marked mosaic with more “primitive” patterns could be the anatomy of H. floresien- australopith-like trunk, upper- and shoul- sis, showing its “unique mosaic morphology” der, and proximal (Fuerriegel et (Aiello, 2015, p. 2289), and the recent discovery al., 2017; Marchi et al., 2017; Williams et al., of two crania from Lingjing, Xuchang (), 2017). As Lee Berger et al. (2015, p. 23) insight- dated to 105-125 Kya, which exhibit a peculiar fully observe, “In of this evidence from morphological mosaic of traits, namely differ- complete skeletal samples, we must abandon ences and similarities compared to their probable the expectation that any small fragment of the ancestor, i.e. H. heidelbergensis, and their western anatomy can provide singular insight about the contemporaries, namely Neanderthals and mod- evolutionary relationships of fossil hominins”. ern humans (Li et al., 2017). Although a number Thus, the phylogenetic interpretation becomes of scholars have associated these caps to the harder and harder. still quite elusive , this hypothesis is Recent new evidence shows that even our still awaiting genetic confirmation. species may have evolved through a mosaic- In all the above-mentioned cases, the term like pattern, as shown by the anatomy of the “mosaic” is used as a descriptive notion related to -like forms found in Jebel- morphological instability. The mosaic describes Irhoud, Morocco, which date to ca. 315-334 Kya specific anatomic module-like assemblages in (Hublin et al., 2017; Stringer & Galway-Witham, which different traits have evolved at different 2017). These remains are associated to a possible rates and through some degrees of independence early “pre-modern” phase in H. sapiens evolution when compared with other related species. In and point to a surprising mosaic assemblage of other , it refers to anatomical forms which features, including facial, dental and mandibular show evolutionary changes in some derived or morphology that aligns with recent anatomically unique features, combined with other retained modern humans and more primitive endocranial parts where there are no marks of apparent evo- and neurocranial morphology. In particular, the lutionary . These macro-evolutionary facial shape of Jebel Irhoud shows simi- mosaic transitions in hominin phylogeny are larities to the structure of H. sapiens’ face, but usually connected to phases of ecological insta- the shape of the braincase is retained in its form, bility (Parravicini & Pievani, 2016a). with an elongated shape that is less globular than The same term may describe in literature anatomically modern H. sapiens. Jebel Irhoud’s also a situation of instability within a single spe- fossils could document another case of mosaic- cies – seemingly in the case of H. heidelbergensis, like evolutionary transition. This new discovery with its regional variants in Africa, Europe and does not necessarily contradict the fact that the , each one showing peculiar mosaic pat- first true H. sapiens actually emerged in Ethiopia terns in their morphologies (see, e.g., Arsuaga at ca. 200 Kya, as a strong of molecu- et al., 2014) - or even within a single popula- lar and paleontological data attests, but it could tion. The latter case is well represented by the indeed mean that the of modern hominin remains from , . The humans’ anatomical traits was preceded by a long five ancient skulls associated to H. georgicus are and still little-known transitional phase (between highly different from each other, but still belong- 350 Kya and 260 Kya), during which different ing to the same single, variable population human populations (proto-sapiens or late forms (Lordkipanidze et al., 2013). For this , of H. heidelbergensis) were evolving differentiated H. georgicus could be defined as a “surprising A. Parravicini & T. Pievani 49

mosaic” (Lordkipanidze et al., 2007, p. 305) rise to a complex behavioral trait (locomotion) even at population level. which is unique when compared to the same The anatomical assemblages in hominin spe- functional trait shown by other (hominin) spe- cies or populations, which show a combination cies. As De Silva et al. (2013, p. 1) argue, “these of different traits, suggest the occurrence of dif- bipedal mechanics are different from those often ferent rates of disjointed changes. This is what reconstructed for other australopiths and suggest we mean when we define here “mosaic type 1”. that there may have been several forms of bipe- As Langdon (2016, p. 131) pointed out, “the dalism during the Plio-Pleistocene”. So, many most important lesson” that such a pervasive pat- forms of bipedalism. H. naledi shows another tern of mosaic evolution “has to tell us is that “unique locomotor repertoire” (Harcourt-Smith human evolution is not linear, but the hominin et al., 2016), namely a combination of primitive lineage has produced a confusing array of side (shared with australopithecines), derived (shared branches. There is not a single main trunk except with Homo species), and unique traits, “func- in retrospect”. tionally indicative of a bipedal hominin adapted for long distance walking and possibly running” (Marchi et al., 2017, p. 174). Mosaic type 2: multiple phylogenetic These cases indicate different ways of trajectories for the same trait being bipeds. If we further expand the focus by encompassing the whole hominin phyloge- The mosaic evolution of bipedal locomotion netic tree during a given period of time (e.g., Mosaic type 1 is the most used meaning of around 1,5–2 Mya), we can see that multiple the term “mosaic” in human evolution literature forms of bipedalism were adopted by different (see how the term is employed in teaching manu- coeval hominin species, often living in different als, e.g. in Lewis et al., 2013). Nevertheless, the environmental contexts (open clearings, forest term “mosaic” appears also with a slightly differ- coverings, etc.). While H. ergaster and H. erectus ent meaning. Sometimes, it describes the differ- showed advanced (or obligate) forms of bipedal ent ways in which a single trait evolves in multiple locomotion, other coeval species, such as austra- coeval species living in different environmental lopithecines or species, exhibited contexts. The meaning of “mosaic” in this second more flexible and mixed styles of locomotion, sense used in literature, which we will call “mosaic such as facultative bipedalism with residual type 2”, appears to express a more explicative and adaptations for arboreal and climbing (see predictive meaning than “mosaic type 1”. Figure 1). It is clear, as Lee Berger et al. (2010, The evolution of bipedalism provides a good p. 204) stated, that “the evolutionary transition example of mosaic type 2 pattern. We may again from a small-bodied and perhaps more arboreal- consider the mosaic anatomy of Au. sediba. The adapted hominin (such as Au. africanus) to a foot, in particular, shows an anatomical mosaic larger bodied, possibly full-striding terrestrial of traits (sensu mosaic-1) which is not present in biped (such as H. erectus) occurred in a mosaic either Au. afarensis or Au. africanus and the heel, fashion”. However, the meaning of the term midfoot, knee, hip, and back are also unique when “mosaic” here appears to be something different compared to the same traits of other hominin than “mosaic type 1”, because in this case the species. This peculiar combination of anatomi- term implies different variants of the same type cal parts of the feet and the lower limbs config- of trait (e.g., bipedalism) across a number of ures a unique adaptive solution for locomotion. coeval species living in different environments. In fact, this anatomical ensemble is consistent In S.J.Gould’s words, “the concept of mosaic for a biped walking with a hyper pronating . evolution dictates that organs will evolve in dif- In other words, a mosaic combination of differ- ferent ways to meet varying selective pressures” ent features (such as lower limbs and feet) gives (Gould, 1977b, p. 66).

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Fig. 1- From Harcourt-Smith W.E.H., 2015. Origin of bipedal locomotion. In W. Henke & I. Tattersall (eds): Handbook of , 2nd edition, p. 1940. Springer, Verlag-Berlin-Heidelberg (adapted from Wood, 2002). Temporal ranges of known hominin taxa. Solid shading refers to taxa that were unequivocally obligate bipeds; cross-hatching relates to taxa where they are mosaic, or there is disagreement over the degree to which they are bipedal; no shading indicates taxa where there is insufficient evidence.

The encephalization trend and the evolution of the supposed, but it surprisingly dates to ca. 236-335 first industries Kya. In other words, H. naledi was contemporary The evolution of hominin bipedalism clearly to other human species that possessed a three contradicts the long-held view of a linear and larger brain, such as the earliest anatomi- anagenetic transition from a quadrupedal apelike cally modern humans and Neanderthals (Dirks hominin ancestor to a fully bipedal human. In a et al., 2017). skeletal remains similar fashion, even the so-called encephaliza- were found during the 2001-2004 excavations tion trend in the genus Homo could no longer be at (, ) and have been depicted as a linear trend from a small-brained recently re-dated to between about 100 and 60 hominin to the large-brained Neanderthals and Kya (Sutikna et al., 2016). This bizarre human anatomically modern humans. form was about one tall and was endowed H. naledi had an approximately 500 cm3 with an endocranial volume of 417 cm3 (Falk et brain. However, it didn’t live 2 Mya, as previously al., 2005). A. Parravicini & T. Pievani 51

H. naledi and H. floresiensis are two examples such as . The earliest known (probably an evolutionary relict or a spe- Oldowan stone tools appeared in localities in cies the former, a geographic speciation by insular the Gona region of the Afar depression, north- dwarfism the latter) which disprove the alleged east Ethiopia (Semaw et al., 2003). By 2.4–2.3 encephalization trend, as they are two very small- Mya, this appears at sites in other brained species of the genus Homo which lived at regions of Ethiopia and Kenya and by 2.1–1.9 the same recent times of early H. sapiens and H. Mya it had spread throughout the Rift Valley neanderthalensis. Furthermore, even the corre- of and basins in North and Central spondence of a large brain with complex techno- Africa, and afterwards all over the Ancient World logical abilities seems to be ill-founded. While H. (in particular, Europe, the , South naledi has yet to be associated neither with Asia). We cannot tell exactly who made these tool production nor with intentional use of fire, Oldowan tools, because several species of homi- H. floresiensis has been connected with the - nins (belonging to at least three different genera, duction of a complex lithic industry, involving i.e., Australopithecus, Paranthropus, and Homo) both pebble-based cores and small-flake based are known to have originated from East Africa cores and spanning at least several hundred mil- between 2.5 and 1 million years ago. lennia (Moore & Brumm, 2009; Moore et al., The appearance of the industry 2009). The new findings consisting of a man- dates back to approximately 1.7 Mya in East dible and teeth at (Flores), which Africa (Beyene et al., 2013; Diez-Martin et al., have been attributed to direct ancestors of H. 2015; Lepre et al., 2011) and it spread to Europe floresiensis and dated back to 700 Kya (van den and Asia perhaps as early as about 1 Mya (Pappu Bergh et al., 2016), have strengthened the idea of et al., 2011; Scott & Gibert, 2009). Although long-persistent technological abilities in associa- the origin of the Acheulean is thought to have tion with this isolated hominin species. closely coincided with major changes in human In a more general picture, both the evolution brain evolution, the actual evidence from the fos- of and the evolution of technological sil record does not support this assumption. The skills seem to proceed through differentiated transition from Oldowan tools to Acheulean tech- paces and mosaic type 2 patterns. The tool- nology is attributed to H. ergaster. The passage to making and tool-use abilities appear not to be mode 2 technology (or Acheulean) at about 1.6 an exclusive behavioral trait of the genus Homo, Mya appears to have not been characterized by whose first emergence has been recently dated any proven morphological change. Furthermore, back to 2.8 Mya (Villmoare, 2015). Beyond the the stable and unchanged presence of mode 1 putative stone-tool-assisted consumption of ani- lithic industry, which is thought to have lasted for mal tissues which was found at Dikika (Ethiopia) more than 1 million years, is generally associated and dates to 3.39 Mya (Dominguez-Rodrigo et with large-brained species, such as the Asiatic H. al., 2010; McPherron et al., 2010), significant erectus, with an endocranial volume of 1150 ml findings have been recently unearthed at the in the most recent specimens. The absence of Lomekwi-3 site, Kenya. They consist of a 3.3 mode 2 tools in and almost in the Mya complete lithic industry, which includes totality of the other eastern Asian sites is rather 83 cores, 35 flakes, some passive elements or peculiar, including sites, where the latest potential anvils, cobbles and further artefacts presence of H. erectus is attested almost until the (Harmand et al., 2015). end of the Middle Pleistocene (i.e., 130 Kya). The well-known Oldowan lithic tools Even though “the absence of evidence is not evi- emerged 700,000 years after the Lomekwian – dence of absence”, one might intriguingly think i.e., 2.6 Mya – in East Africa and consisted of that the eastern Asian technological traditions stone industries containing simple cores and could have followed an autonomous trajectory, flaked pieces, along with some battered artifacts maybe due to isolation from the other human

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populations which were distributed in Africa, in are exclusively associated with Neanderthals. At Europe or in other parts of Asia, as a consequence Attirampakkam, , luminescence dating has of the dispersal patterns that occurred during the recently shown that processes signifying the end first out of Africa (see below). of the Acheulian and the emergence of Therefore, mode 1 industries coexisted for a Middle culture occurred about 385 several hundred thousand years with the mode 2 Kya, i.e. much earlier than conventionally pre- industries. The latter lasted from approximately sumed for (Akhilesh et al., 2018). 1.7 Mya to 250 Kya and the earlier Acheulean is Late Paleolithic stone industries (ca. 40-10 associated with the above-mentioned H. ergaster Kya), consisting of more complex technolo- /erectus, while the later Acheulean (by ca. 500 gies such as blades transformed into a variety of Kya), which shows more complexity, more crafts- tool forms – including end scrapers, burins, and manship in its realization, and higher symmetry backed –, and elongated flakes that are and aesthetic sense than the earlier ones, is asso- produced by soft or indirect percussion, ciated with the larger-brained H. heidelbergensis. are almost always associated with anatomically Such handaxe/ industries are contempo- modern humans. However, some early Upper raneous and sometimes regionally co-occurring Paleolithic sites in Europe are also contempora- with the simpler Oldowan-like . neous with the last populations that Acheulean and contemporaneous mode 1 indus- lived there (Harvati, 2015). tries are found throughout Africa and , While in Europe, there is doubtless a dif- but classic handaxe and cleaver assemblages are ference between Middle and especially characteristic of Africa, the , assemblages, many forms typically associated the Indian subcontinent, and Western Europe. with the Upper Paleolithic appear in earlier peri- Elsewhere, the simpler mode 1 technologies are ods. Many regions in Europe (Conard & Fischer, found, especially in Eastern Europe and most of 2000) and Africa (McBrearty & Brooks, 2000) eastern Asia (Toth & Schick, 2015). show different patterns of cultural development. The industries of Europe, Also in the Near East, the later Middle Paleolithic the Near East, , sub-Saharan Africa is characterized by Levalloisian assemblages that are usually characterized by prepared core tech- were made by both Neanderthals and anatomi- nologies (e.g., Levallois cores, flakes, and points), cally modern humans (Shea, 2003), which also side scrapers, denticulates, and retouched points show how tenuous the link is between anatomi- and are found between approximately 250 and cal and . 30 Kya. During such a time span, hominins This overview evidences that the emergence extended their ranges to most of the different and the evolution of the lithic assemblages also environmental zones of Africa and Eurasia. Mode show heterogeneous evolutionary trajectories 3 industry is found in tropical, subtropical, tem- and mosaic type 2 patterns of development and perate, and even periglacial climatic regimes. It transmission and do not provide clues for pre- is associated, in Africa, with larger-brained pre- dicting when modern patterns of human behav- sapiens hominins (sometimes assigned to Homo ior emerged. Rather, scattered development of helmei) and early anatomically modern humans. both new and older technologies can be observed Recent findings document that Acheulean through heterogeneous regional patterns, often technology of Basin in Kenya was associated with different coeval hominin species. entirely replaced by Middle technol- ogy already by ca. 320 Kya, i.e. tens of thou- Mosaic evolution of symbolic behaviours? sands of years earlier than previously thought The emergence and consolidation of modern (Deino et al., 2018). In the Near East, mode 3 behavior accelerated its evolutionary pace in the tools are associated with Neanderthals and ana- middle of the . Culturally mod- tomically modern humans, while in Europe they ern behavior is attested in many parts of Africa, A. Parravicini & T. Pievani 53

Europe, Asia, and between 30 and 45 provided particularly abundant evidence for the Kya through several bursts of local . use of ground during the Middle Stone An increasing amount of archeological and fossil Age and studies at Blombos have also docu- proof supports the hypothesis of mosaic polycen- mented toolkits for making and storing tric bursts of symbolic intelligence, not only (d’Errico & Stringer, 2011). Furthermore, a quan- restricted to Homo sapiens as has been traditionally tity of very recent evidence that surprisingly date thought. An asynchronous appearance and disap- to before 300 Kya from the pearance of key cultural innovations is attested not sites from the Olorgesailie basin (southern Kenya) only in the African Middle Stone Age, but also has shown that hominins at these sites exploited in the Eurasian Middle Paleolithic (300-40 Kya) -rich rocks to obtain red (Brooks before becoming fully consolidated in the cogni- et al., 2018). In the Levant and Europe, strong tive modern humans (Conard, 2015; D’Errico & data for the use of ochre are attested at Middle Banks, 2013; D’Errico & Stringer, 2011). Paleolithic sites, including Qafzeh (Hovers et The Asian and Java H. erectus are commonly al., 2003). Several European sites suggest that associated with the stable use of the simple Neanderthals regularly used pigments in Middle Oldowan technology. However, at least one puta- Paleolithic contexts, including - tive burst of symbolic behavior has been recently Belvédére (Roebroeks et al., 2012), Pech de l’Azé attributed to H. erectus in , Java, with the (d’Errico & Soressi, 2002), Cueva de los Aviones, first possible abstract patterns engraved on a and Cueva Antón (Zilhão et al., 2010). freshwater shell. This is the earliest known trace Several Middle Stone Age incised objects tes- of symbolic intelligence, which amazingly dates tify the presence of symbolic behavior. Important back to 540-430 Kya (Joordens et al., 2015). examples include engraved abstract patterns on A number of sporadic expressions of symbolic pieces of ochre dating to approximately 75 Kya behaviors has been associated to Neanderthals. (Henshilwood et al., 2002) and a cross-hatched , use of pigments, complex lithic and pattern drawn with an ochre crayon on a ground technologies, and personal ornamenta- silcrete flake recovered from approximately 73 tion (and not only at the end of the Neanderthal Kya, both from Still Bay deposits at evolutionary trajectory) are among the elements (Henshilwood et al., 2018). Furthermore, incised that definitely challenge the idea that behavio- pieces of ochre were found, e.g., in Peers Cave, ral modernity is unique to our species (Hovers Klein Kliphuis (Mackay & Welz, 2008), and & Belfer-Cohen, 2006; Langley et al., 2008; Klasies River Cave 1 (d’Errico et al., 2012), not to Nowell, 2010; Zilhão, 2007). mention fragments of decorated ostrich eggshells A wealth of Middle Paleolithic human skele- from (Texier et al., 2010). The tons appear to have been buried deliberately, both density of many of these finds in southern Africa associated to anatomically modern humans and has been interpreted as an indication of the defin- also to Neanderthals, like those in the Shanidar itive emergence of cultural modernity with fully Cave (, 35-65 Kya) (Solecki, 1971; Trinkaus, developed modern cognitive abilities, including 1983), in La Chapelle-aux-Saints (35-70 Kya) language (d’Errico et al., 2003; Henshilwood et (Rendu et al., 2013) or in , Dordogne al., 2002; Texier et al., 2010). () (Zilhão, 2012). Such sporadic signals Early evidence for the use of marine shells preceded the unambiguous Upper Paleolithic evi- as ornaments come from (100 dence of burials, many of which preserved opu- Kya) (Bar-Yosef & Vandermeersch, 1993) and lent , such as for example, ’, from Skhūl Cave in (Vanhaeran et al., Dolní Vĕstonice, and the Grimaldi Caves. 2006), and from Grotte des Pigeons in Morocco Pigments were used in a lot of Middle Stone (Bouzouggara et al., 2007). Perforated marine Age and Middle Paleolithic settings of the Late shell ornaments are attested in Still Bay deposits Pleistocene (Watts, 2002). Southern Africa has at Blombos Cave (75 Kya) (Henshilwood et al.,

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2011) and Middle Stone Age contexts at Sibudu regular geometry of stalagmite circles that appear (d’Errico et al., 2008). Starting from 40 Kya, to have been deliberately moved and placed in personal ornaments have been attested in several their current locations (Jaubert et al., 2016). parts of the Old World from multiple regions of Figurative is universally accepted as an Africa, Eurasia, and Australia. indication of and a hall- Normally, the perforated shells have been mark of symbolic behavior. For this reason, interpreted as having been made and used by Europe has always been thought as the privileged anatomically modern humans. However, the place where symbolic intelligence emerged for late Middle Paleolithic sites of Cueva de los the first time. Several sites have provided evi- Aviones and Cueva Antón in are signifi- dence of figurative representation between 30 cant exceptions (Zilhão et al., 2010). Recent and 40 Kya. The earliest includes dating of the flowstone capping in the Cueva the figurines and other ivory de los Aviones deposit shows, in particular, that figurines and isolated representations in the symbolic finds made therein are 115 to 120 and stone from the Swabian caves () Kya, thus predating the earliest known compa- (Conard, 2003, 2009), together with the earliest rable evidence associated with modern humans examples of musical instruments (Conard et al., by 20,000-40,000 years (Hoffmann et al., 2018). 2009). The earliest spectacular from Furthermore, Neanderthals apparently produced Grotte Chauvet in the Ardèche region of south- a wide range of perforated and incised ornaments ern France date to between 37-33.5 Kya (Quiles and symbolic artefacts in Châtelperronian con- et al., 2016). Other important sites include texts, such as at Arcy-sur-Cure Stratzing (), Abri Cellier, La Ferrassie, (Baffier, 1999). Here, a pioneering study has con- Abri Blanchard, and Abri Castanet (France), firmed that the link between Neanderthals and Peştera Coliboaia (), which date to the artifacts is real (Welker et al., 2016). Further between 30-34 Kya. evidence of artefacts with clear symbolic rele- But the perspective was likely biased. All these vance have been found in other Châtelperronian traces of symbolic behavior of the early Upper sites in Europe, dating from 41 to 45 Kya, Paleolithic were presumably made by modern such as the Quinçay shelter in France, the humans. However, Neanderthals still occupied Ilsenhöhle in Germany, the Trou parts of Europe at that time, roughly 40 Kya. Magrite (Pontà-Lesse) site in , Fumane In fact, an abstract pattern from Gorham’s Cave rockshelter in Italy and others (Zilhão, 2012). in , which was found to be older than The levels of Grotta di Fumane 39 Kya, was probably engraved by Neanderthal (44 Kya) have revealed evidence of intentional populations living there (Rodríguez-Vidal et al., removal of large by Neanderthals for 2014). Furthermore, hand and disks non-utilitarian use (Peresani et al., 2011), and a onto the wall in the El Castillo cave (Spain) bone fragment of a raven (Corvus corax) date back to at least 40,800 years, meaning that from Zaskalnaya VI rock shelter, Crimea (38- such paintings could have been done by the last 41 Kya) bearing seven notches, perhaps a nee- Neanderthals that had inhabited the Iberian dle, suggests advanced technological abilities in peninsula for more than 200,000 years and up Neanderthals (Majkić et al., 2017). to 42 Kya (Pike et al., 2012). The hypothesis of Annular constructions of broken stalagmites sporadic Neanderthal art has been recently con- have been found in the in south- firmed by Hoffmann et al. in Science, who discov- west France. Dating to 176.5 Kya, this enigmatic ered paintings and engravings in three Spanish structure is among the oldest known well-dated caves occupied by Neanderthal groups 65 Kya, constructions made by humans living in that area, when no modern humans (as far as we know) had i.e., early Neanderthals, and could represent some yet arrived in Europe (Hoffmann et al., 2018). kind of symbolic or behavior, as it shows a Due to all this and further evidence, imaginative A. Parravicini & T. Pievani 55

and symbolic intelligence appear to have evolved cultural behaviours and symbolic communica- independently among Neanderthals, and not as tion across the Old World (Conard, 2015). the result of contact with modern humans. It In conclusion, mosaic type 2 describes appro- seems that they did not systematically practice it, priately the way in which crucial traits in human but were however capable of it. The alternative evolution appear to have evolved. Looking from hypothesis is to substantially predate the arrival the broadest perspective, the above-described of anatomically and cognitively modern humans major transitional phases of hominin evolu- in Europe. tion (related to locomotion, foraging and diet, In any case, the European figurative depic- encephalization, technological and symbolic tions appear not to be the oldest known world- behaviours) reveal a series of mosaic type 2 pat- wide, as has been presumed to date. terns which occur at a different and higher level traditions on the Indonesian island of than the mosaic type 1 patterns. According to have been recently found at least compatible in Robert A. Foley, 2016, each of the identified age with the oldest European ones and include transition patterns should be considered as a twelve human hand stencils and two figurative different element composing the much broader depictions from seven cave sites. The ear- mosaic picture which configures the human evo- liest dated image from Maros in Sulawesi lution taken as a whole. shows a minimum age of 39.9 Kya, being now the oldest known hand associated to Homo sapiens in the world (25,000 years after the Mosaic type 3: when the trait itself Neanderthal rock paintings in Spain). In addi- is a mosaic tion, a of a babirusa (‘pig-’) made at least 35.4 Kya ago is among the earliest dated The most recent literature regarding the evo- figurative depictions in Homo sapiens world- lution of human language has also described the wide (Aubert et al., 2014). Further evidence emergence of this faculty through the notion of for symbolic activity at Leang Bulu Bettue has mosaic. However, the use of the term seems to reveal been recently dated to 30-22 Kya (Brumm et al., a slightly different, and possibly third, meaning. 2017). More recently, uranium-series analysis of Since ’s time, the origin of deposits that overlie a large human language has been investigated by several reddish-orange figurative painting of an animal at scholars, who have always considered this faculty Lubang Jeriji Saléh, Indonesian Borneo, yielded as a single monolithic trait. Hauser et al. (2002) a minimum date of 40 Kya. This is currently the proposed to distinguish a “faculty of language in oldest date for figurative artwork in the world. In a broad sense” (FLB) and a “faculty of language the same site, two reddish-orange-coloured hand in a narrow sense” (FLN). According to this pro- stencils yielded a minimum uranium-series date posal, FLB includes the sensory-motor system of 37.2 Kya and a third hand stencil has a maxi- (i.e., ), the conceptual-intentional system mum date of 51.8 Kya (Aubert et al., 2018). (i.e., semantic) and the faculty of language narrow The emergence of behavioral modernity sense itself. FLN consists of the abstract linguis- does not appear to reflect a quantum leap from tic computational system alone (i.e., ), and archaic to modern patterns of behavior. It may involves the computational mechanisms for recur- not have been a revolution, but rather a mosaic sion and the ability to produce a potentially infi- transition. Especially, it seems to shape a mosaic nite range of expressions from a finite set of ele- type 2 picture in which advanced technologies ments. The authors claim that it is likely that only and symbolic behaviours follow regionally and the possesses FLN, which has to be temporally different trajectories, at least in two considered as a derived trait of H. sapiens, evolved human species. In short, these patterns config- for certain evolutionary and then coopted ure a patchy and mosaic evolution of complex for different functions (a case of exaptation). On

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the other hand, the other FLB components are that innovations indicative of modern cogni- thought to have evolved gradually, and to be tion are not actually restricted to Homo sapiens. shared with other non-human species. Asynchronous appearance and disappearance of The interesting issue in this proposal, beyond key cultural innovations have been witnessed not whether it works or not when compared with only in the African Middle Stone Age, but also the empirical data, is that language is no longer in the Eurasian Middle Paleolithic (300-40 Kya) treated as a single trait, but as a mosaic of different before becoming fully consolidated. Several of elements with distinct functions that intertwine these mosaic expressions of symbolic behaviors in a complex way. This idea is still awaiting to be are also today associated to Neanderthals, and in seriously tested, but it has already led to a series one case even to H. erectus. Therefore, sporadic of fruitful hypotheses (see Fitch, 2012; Hurford, expressions of linguistic behaviors – for consoli- 2003; Okanoya, 2007, Pievani, 2014, 2016; dated reasons linked with symbolic and imagina- Suman & Pievani, 2015). tive intelligence – could have predated the more According to this literature, the traits com- complex and systematic behaviors of the anatom- posing the faculty of language could have ically and cognitively modern humans. In other evolved by following different trajectories. Some words, a plurality of hominin populations and of them could have evolved through functional species could have followed multiple and non- direct adaptations, some others through exaptive linear trajectories of cultural and cognitive evolu- processes, while others as by-products of struc- tion across the different branches of the recent tural or developmental constraints. In this “tree human phylogeny (D’Errico & Banks, 2013). thinking” approach to language, we see different This third concept of mosaic concerns a given evolutionary histories and different combina- behaviour or structure, previously supposed to tions of subsystems involved in language. Some be a single trait, which is then found to be the of them may be very old and come before the result of the convergence of multiple traits char- genus Homo, and then functionally coopted in acterized by different evolutionary trajectories in new ecological niches (for example, the lower- hominin branched phylogeny. The mosaic type ing of the – Fitch, 2012). Others could 1 concept applies to any individual or species be more recent and even typical of our species, as showing a mixture of derived and retained traits. is supposedly the case for the syntactic aspects of Similarly, the mosaic type 3 notion may apply to language. Some traits have homologues or ana- any complex trait that is found to be a combi- logues in other extant species and could be stud- nation of derived and retained sub-components ied comparatively, while some others are likely to evolving through different rates. Some sub-com- be unique to our species. ponents could be derived traits, which evolved in The language faculty is therefore composed a punctuational fashion, while some others may of multiple interacting subsystems, which involve be retained traits, which evolved gradually and phonetic, semantic, symbolic and pragmatic was shared with different species, so stepping capacities. All these different elements com- beyond the old-fashioned debate between the bine together and form a single complex trait. gradualist and the punctuational view of human We propose here to connect this idea with the language evolution (Parravicini & Pievani, recent evidence concerning the bushy hominin 2016b). Furthermore, mosaic type 3 involves a evolutionary tree. The hypothesis of language as phylogenetic notion related to the evolution of a a mosaic of traits works very well when matched single trait, thus sharing the same logic as mosaic with the extant paleoanthropological data. As we type 2. In this respect, for example, further traits described above in the paragraph Mosaic evo- beyond language could be linked with mosaic lution of symbolic behaviors?" about symbolic type 3 pattern, such as the above-mentioned case behavior, an increasing amount of archeologi- of bipedalism (see The mosaic evolution of bipedal cal and fossil findings supports the conjecture locomotion) where it has been hypothesized to be A. Parravicini & T. Pievani 57

Tab. 1 - The table summarizes three different types of mosaic notions, with their most widespread meaning, which emerged from the analyses conducted in the literature. The table also provides a list of some paradigmatic case-studies that exemplify each of the mosaic type.

TYPE OF MEANING IN LITERATURE PARADIGMATIC CASE STUDIES MOSAIC

Mosaic type 1 Strong variability of the morphological • Au. sediba, H. naledi, H. floresiensis, assemblages evolving in hominin species with their very peculiar morphological independently from each other, at different assemblages. rates when compared with other related • The early phase of Homo sapiens evolution. species. The same pattern can be observed • The regional variants of H. heidelbergensis within a single species or a single population. and the population of H.georgicus in Dmanisi.

Mosaic type 2 Traits following regionally and temporally • Multiple forms of bipedalism. different trajectories and evolving in • Encephalization proceeding through multiple coeval species that live in different differentiated pace within multiple coeval environmental contexts. Usually, this pattern species. ends with the macro-evolutionary consolidation • The evolution of lithic assemblages and of the trait itself. symbolic behaviours.

Mosaic type 3 Behaviour or structure, previously supposed • Human language, no longer treated as a to be a single trait, which is then found to single trait, but as a mosaic of different be the result of the convergence of multiple elements and combinations of subsystems traits characterized by different evolutionary with distinct functions that intertwine in a trajectories in hominin branched phylogeny. complex way.

the result of a mosaic-combination of sub-traits Explaining mosaic evolution through (like lower limbs and feet) that follow different a macro-evolutionary approach evolutionary trajectories across the hominin phy- logenetic tree (see Table 1 for a brief conceptual If the clarification of the three possible mean- summary about the three mosaic types). ings of “mosaic evolution” is useful, we still lack The three mosaic types described so far aim at an explanation for the somehow odd evidence clarifying some conceptual differences in the use associated with such mosaic traits belonging to of the term “mosaic” that are largely unseen in different species. The processes of natural selec- literature. The identification of different mosaic tion and occurring at the micro- types intends to provide a conceptual distinction levels of organisms and populations seem insuf- for an unclear use of the term, but it says noth- ficient to fully explain the macro-evolutionary ing about the biological processes at the base of patterns which have broadly affected the homi- the terminological differentiation. Such a mosaic nin evolution (i.e., episodes of adaptive radia- approach calls therefore for new hypotheses con- tions, mosaic evolution of traits in several coeval cerning the underlying mechanisms. A plurality species, serial dispersals out of Africa and so on). of patterns seems to be required to account for The macro-evolutionary patterns emerging from such a mosaic evolution of traits, because they the field currently point to the need for an ecolog- are not “modeled” by a single selective agent for ical extension of the evolutionary theory, namely a single function, but could be the result of dif- when applied to human evolution, which is able ferent processes, such as exaptations, multi-level to account for the complex interactions among factors, processes, phenotypic ecological and genealogical factors and between plasticity dynamics, in the light of an extended the micro-evolutionary levels of the organisms neo-Darwinian research program (Pievani, 2014; and populations, and the macro-level of spe- 2016; Suman & Pievani, 2015). cies and higher taxa in a broader geo-physical

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scenario (Parravicini & Pievani, 2016a; Eldredge modulated by periods of strong variabil- et al., 2016). ity alternating with relative stability. The pro- According to the paleontological data, mosaic gressive rifting and tectonic uplift of East Africa evolution implies both a diversification of puta- blocked the warm and wet air streams from the tive species or sub-species, each one bearer of , and these climate and environ- a different combination of sub-traits, and the mental changes transformed eastern and south- achievement of a final version (among the pos- ern Africa from a flat and homogenous region sible others) which is more successful than oth- full of tropical mixed forest, to a heterogeneous ers (as for bipedalism, expanded brain, modern region, with high mountains and a mix of habi- behaviours, etc.). The overall effect is a major tats ranging from cloud forest and woodlands to evolutionary transition, but realized through and deserts (Bobe, 2006; Cerling et al., multiple morphological and behavioural trajec- 2011; deMenocal, 2011). Thus, the importance tories. Therefore, the most parsimonious expla- of climatic and environmental factors already nation for this phenomenon seems to be the appears in this first phase of hominin evolution. interaction between general selective pressures Mosaic type 1 and type 2 patterns prevail in in human evolution (promoting different ver- a strongly changing and fluctuating ecological sions of the same adaptation; in other words, scenario. The populations of apes isolated in the several adaptive peaks) and a highly branched eastern and southern African regions were forced phylogeny – due to ecological instability, habitat to adapt to an unprecedented mix of fragmented fragmentation, and geographical dispersals – in ecological niches characterized by an ever-chang- which speciation played a crucial role. ing climate (Pickford, 2006; White et al., 2009). We can test this hypothesis with the paleon- The effects of such an unstable and fluctuating tological data. At the beginning of our phylog- context of life could be closely associated with eny, four species of early hominins belong to bursts of novel adaptations – which possibly three different putative genera between 7 and include different forms of bipedalism and - 4.4 Mya: tchadensis (6-7 Mya), ther innovations like the diminution of the tugenensis (6-5.7 Mya), Ardipithecus canine premolar honing complex, the advent of kadabba (5.8-5.2 Mya) and Ardipithecus ramidus megadontia, and so on – for the earliest putative (4.4 Mya). These forms show a combination of hominin species. Therefore, selective pressures retained and derived features (mosaic type 1), connected to an increasing extension of open suggesting different hybrid forms of locomotion, habitats could have favored the emergence of which could alternate quadrupedalism and bipe- episodic and heterogeneous forms of bipedalism. dalism, or even “forest bipedalism” as is suppos- Whichever hypothesis might be advanced for the edly the case for Ar. ramidus (Lovejoy et al., 2009; emergence of bipedalism (see Niemitz, 2010, White et al., 2009; for a comment see Cerling for a review), a patchy distribution of different et al., 2010). The mosaic type 1 of unstable environments closely interrelates with a these putative earliest hominin forms suggest the mosaic type 2 transition of forms capable of dif- occurrence of multiple postural “adaptive experi- ferent locomotor adaptations, to be intended as ments” at about the time of divergence between multiple strategies of facultative bipedalism. hominin lineage and lineage. Fossil remains associated with Au. anamensis The biogeographic area where these homi- (Kenya) establish the first appearance of the genus nins lived covered the System Australopithecus at 4-4.2 Mya, which was highly and South Africa, apart from S. tchadensis which diversified (with about 7-8 different species) and has been surprisingly found 2,500 km west of the very long-lived (spanning from ca. 4.2 Mya to Rift Valley, maybe because of an early geographi- 1.8 Mya). Compared to the genus Ardipithecus, cal dispersion. The entire region was affected by which was more adapted to a woody environ- a long term aridity trend during the , ment rich in forests and punctuated by clearings, A. Parravicini & T. Pievani 59

australopithecines were adapted to more arid and also the macro-evolutionary reasons behind the open habitats, covered by grasslands alternating explosion of diversification and branching of with forests and woodlands (White et al., 2009). hominin species and consequent mosaic patterns Again, each of these australopithecines reveals of evolution that occurred, e.g., between 3 and 2 a unique assemblage of anatomic features with Mya, with multiple phenomena of and several innovations (mainly related to dentition evolution of unprecedented hominin species and and posture) which align with typical features of maybe even genera. the genus Homo, combined with retained traits Afterwards, the plethora of species which (related to facial shape, low cranial capacity, the diversified after the two first out of Africa pro- length of thoracic limbs, toes and fingers). Such cesses (resulting from at 2 Mya heterogeneous combinations of traits compose and from at 800-600 Kya) unique original mosaic type 1 morphologies. show marked mosaic type 1 combinations of In particular, limb anatomy points to advanced traits, probably due to the different geographi- bipedalism and mixed styles of locomotion, with cal trajectories followed by the human popula- residual adaptations for arboreal life and climb- tions. The high fragmentation of habitats due to ing, which was well suited to a changing niche the harsh climatic conditions of the Old World, and unstable climate (Senut, 2006). combined with the planetary dispersion of the In this range of adaptive strategies, some were genus Homo, could explain this adaptive radia- characterized by a greater ecological flexibility (in tion. The conformation of these areas, strongly locomotion or diet) while others, as in the case of diversified, full of geographic barriers, in a situ- Paranthropus, by an increase in specialization of ation of intense climatic and ecological instabil- dietary habits. ity, is highly compatible with a mosaic type 1 After the emergence of the genus Homo, at and mosaic type 2 patterns related to multiple around 2.8 Mya (Villmoare et al., 2015), bipedal geographic speciation processes, as shown by locomotion became first prevalent and then obli- the fossil record. Even the patterns of dispersal gate. Once again, the evolutionary transition in and migration of the human species across the locomotion came about in parallel in a plural- Eurasian continent could be closely related to ity of separated morphologically unstable spe- macro-evolutionary factors, linked to climate cies (mosaic type 2), each one showing a mix of fluctuations and habitat instability, as argued by specific sets of traits (mosaic type 1). Mosaic type Mark Maslin and colleagues in their “pulsed cli- 2 patterns could be considered as a macro-evolu- mate variability hypothesis” (cf. Maslin, 2017). tionary “laboratory” of mosaic-like experimenta- The encephalization trend in the genus Homo tion which is carried out by a number of different seems no longer to follow the old-fashioned related forms in multiple ways, usually ending model of a stable, gradual, and linear evolution. with the macro-evolutionary consolidation of the On the contrary, it appears to follow a mosaic type trait itself (seemingly by a sorting process among 2 evolution, as we above (see The encephali- species or populations with differential ). zation trend and the evolution of the first stone tool In the case of bipedalism, the mosaic type 2 pat- industries). Recent evidence shows that the Homo tern ends with the consolidation of a stable form species with large , such as H. sapiens and of obligate bipedal behavior. This trend, however, Neanderthals, evolved at the very same time of is not so definitive as to exclude further residual other Homo species endowed with relatively small mosaic experiments (see for example the still brains, like H. naledi and H. floresiensis. elusive exception of H. naledi’s locomotion, The We can base our understanding of the mosaic mosaic evolution of bipedal locomotion). Therefore, evolution of human brain on the idea that most the turbulent climatic and environmental scenario of the evolutionary changes are concentrated in that characterized most of the transition phases of rapid (geologically speaking) events of speciation human evolution may help us to better understand in peripheral isolates, which undergo different

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processes (selection, drift, migration) triggering (included geographically local stasis), undergo a the cladogenetic pattern in allopatry that our process of differential success of some hominin phylogeny (like many others) shows (Eldredge & species or populations compared to other homi- Lieberman, 2014). In this view, speciation could nin species or populations. The success of one be the driver of major morphological and behav- version of the complex trait as the final stage of ioural changes, which occur mainly during the the mosaic type 2 evolution across a number of early stage in which a new species emerges, fol- different species appears to be the outcome of a lowed by a period of apparent stasis. process of sorting, at the end of which only one Keeping this perspective in , the fog species actually survived, i.e. H. sapiens, after a surrounding the cases of H. naledi and H. flo- demographic competition with other coeval resiensis seems to thin. Some archaic traits shown human species (mainly Homo neanderthalensis by H. floresiensis, including the skull size, suggest and Denisovans). that its ancestors were small-bodied and closely This hypothesis goes in the same direction of related to the early-Homo species, such as H. recent research authored by Bernard Wood and habilis and H. rudolfensis (Argue et al., 2017), colleagues, according to which hominin brain apart from the adaptations due to the insular size to different extents at different times could dwarfism. Similarly, H. naledi, which dates to be influenced by both micro- and macroevo- around 236-335 Kya, shows a mosaic combi- lutionary changes, with a major role played by nation of traits, some of which are also typical large-scale climate and environmental changes, of the early-Homo species or even of the latest habitat fragmentation and vicariance, interspe- australopithecines living between 2 and 2,5 Mya cific interactions and so on. In particular, they (such as the small brain, the basin, the curved also argue, “if species with larger ECVs (endocra- fingers and so on – see Mosaic type 1: hominin nial volumes) are found to have higher diversifi- morphological instability). While some African cation rates (origination minus extinction rates), H. heidelbergensis were evolving into H. sapi- this may suggest that species sorting also caused ens, groups of H. naledi with brains three times clade-level ECV to increase. […] If species sort- smaller and still adapted to an arboreal life wan- ing is borne out, it would suggest that all three dered in southern Africa. At the same time, H. mechanisms known to influence phenotypic floresiensis was living in Indonesia, with its small evolution within a clade (i.e. , direc- brain and, nonetheless, its technologies. This is tional speciation and species sorting) were acting highly surprising from a gradualistic and anage- in concert at multiple taxonomic scales to pro- netic perspective, but not so much if we assume duce the directional ECV trend observed at the a pluralistic approach to evolution, which takes hominin clade level” (Du et al., 2018, p. 6). into consideration the possibility of punctua- According to the ’s tional and mosaic patterns in genus Homo evo- Human Origins Program Team, directed by Rick lution. In such a perspective, it is possible that Potts, well-proven stages of climate change, eco- Homo naledi and Homo floresiensis are something logical instability and habitat variability, which like evolutionary “wrecks” that survived locally occurred repeatedly at (geologically) short inter- for a long period of time, showing a very per- vals, favored inter-specific processes of adapt- sisting and resilient morphological stasis in their ability selection, i.e. a selection of pools respective mosaic of traits. that favored greater versatility in adaptation and According to this view, the so called greater ecological flexibility. These processes may encephalization trend, similar to other mosaic have triggered behavioral innovations in homi- type 2 patterns, could be a paradigmatic exam- nin species, such as the spread of technological ple of a species sorting mechanism (cf. Vrba & abilities, as a strategy to successfully buffer the Gould, 1986), where a multiplicity of coeval spe- deleterious effects deriving from unstable eco- cies, following different evolutionary trajectories logical conditions (Potts & Faith, 2015). A. Parravicini & T. Pievani 61

The patchy spread of lithic industries through- proceeded through a scattered and mosaic-like out Africa and Eurasia, which occurred in a period fashion, with punctuated bursts of innovation of major climatic change, with several cold/warm and long periods of apparent cultural stasis. and dry/humid oscillations, appears to confirm African chronological reconstructions of Still Potts’ “variability selection hypothesis”. The above- Bay and Howieson’s Poort industries (from about mentioned case of Olorgesailie basin in Kenya (see 75 Kya to 60 Kya) represent, to date, the earli- above, The encephalization trend and the evolution est traces of behavioral modernity: they show the of the first stone tool industries and Mosaic evolu- occurrence of ephemeral and punctuated bursts of tion of symbolic behaviours?), where evidence of technological and behavioral innovations, linked advanced technology, complex social behavior and to climate changes and demographic fluctuations symbolic intelligence were found before 300 Kya, in southern Africa. Local environmental changes is paradigmatic. According to Potts et al. 2018, in southern Africa during the Middle Stone Age an increased pace of environmental changes, well triggered a number of demographic expansions documented in the Olorgesailie sequence, with and contractions in Homo sapiens populations, prolonged wet-dry climate oscillation, more pro- and they consequently affected social networks nounced erosion-deposition cycles, tectonic activ- and bursts of cultural innovations (Jacobs & ity, with consequent impressive faunal turnover, Roberts, 2009; Jacob et al., 2008). were crucial in order to account for that develop- Also the data related to the evolution of sym- ment of Middle Stone Age technological, social, bolic behavior and language (Mosaic evolution of and cognitive innovations in . symbolic behaviours? and Mosaic type 3: when “Foraging unpredictability, with increased poten- the trait itself is a mosaic) do not show a strictly tial for resource scarcity, describes the conditions linear model, but rather patterns of mosaic type 2 in which human hunter-gatherers broaden the spa- and type 3 evolution, with scattered bursts of cul- tial scale of the landscape they encounter through tural innovations, preceding the consolidation of a combination of wider mobility, information and the so-called behavioral modernity in cognitively resource sharing, and the maintenance of resource modern humans. Different hominin populations exchange networks. […] We thus hypothesize and species (from H. erectus and Neanderthals to that the emergence of the MSA and its wholesale H. sapiens) seem to have followed different trajec- replacement of the Acheulean in the Kenya rift by tories of cultural evolution among the branches ~320 kya ago represents an evolutionary response of human phylogeny (D’Errico & Banks, 2013; to resource landscapes that were less predictable Parravicini & Pievani, 2016a). in time (as a result of amplified climate variabil- As D’Errico & Stringer (2011, p. 1061) ity throughout eastern Africa) and were also more argued, the cognitive prerequisites of modern heterogeneous in space (as a result of local tectonic human behavior may have been already “largely activity)” (Potts et al., 2018, p. 89). in place among the ancestors of Neanderthals and The ecological scenario, which is highly modern humans”, and “social and demographic fragmented and unstable due to climate oscilla- factors, arguably triggered by climate change”, tion, fits very well, in general, with the proved may account for “the asynchronous emergence, presence of a plurality of hominin species, and disappearance and re-emergence of modern cul- for the same reason, it is an ideal context to bet- tural traits among both African ‘modern’ and ter understand the series of attested different Eurasian ‘archaic’ populations”. bursts of early technological innovation. From High climatic and environment instability the first lithic , such as the Lomekwian might be an important factor which contrib- tools dated 3.3 Mya (Harmand et al., 2015) to uted to triggering the final wave of the cogni- the more recent artifacts typical of the first cog- tively modern humans, and maybe the series of nitively modern humans, the so-called “cumu- further migratory waves outside Africa which lative culture” of genus Homo appears to have preceded it, as attested by recent high-resolution

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genetic studies on a wide scale (Pagani et al., anatomical and cognitive traits that, 100,000 2016; for the “final wave” model, Pievani, 2012). years later, made it particularly flexible, mobile, Therefore, the so-called “Paleolithic Revolution” creative, invasive and talkative. Now we are the could be due not only to cultural diffusion but only representative of the genus Homo, a late also to demic diffusion, that is, a diffusion that and contingent exception, which likely emerged was brought about by the arrival of new groups from a mosaic process of species sorting within a of hunters-gatherers which left Africa. It was, highly fluctuating ecological scenario. in fact, a complex transition that was preceded by many failed attempts and was probably not exclusive to H. sapiens. The other human spe- Author contributions cies, before extinction also due to the contact with groups of Homo sapiens, were exploring the Andrea Parravicini wrote the sections: “The potentialities of symbolic intelligence in their term “mosaic” in human evolution”, “The mosaic own way, through mosaic type 2 and mosaic type evolution of bipedal locomotion”, “Mosaic evo- 3 patterns of diversifications occurring at species lution of symbolic behaviours?”, “Explaining and population levels. mosaic evolution through a macro-evolutionary approach”. Telmo Pievani wrote the sections: “Mosaic Conclusion type 1: hominin morphological instability”, “The encephalization trend and the evolution of the Summing up, the three patterns of mosaic first stone tool industries”, “Mosaic type 3: when evolution here presented suggest that human the trait itself is a mosaic”, “Conclusion”. Both evolution has been much more similar to a mul- authors revised and approved the final manuscript. tiple exploration of adaptive possibilities than to a linear process of achievements, with several species showing faster pace in the evolution of References some heterogeneous traits and slower pace in others, each carrying a mosaic combination Adams D.C. 2016. Evaluating in of traits, each of them being closely connected morphometric data: challenges with the RV co- to the local environmental contingencies. The efficient and a new test measure. Methods Ecol. result of such complex and diversified mosaic Evol., 7: 565-572. evolution is that the key transitions that shaped Aiello L.C. 2015. Homo floresiensis. In W. Henke humanity as we know it (bipedalism, social com- & I. Tattersall (eds): Handbook of paleoanthro- plexity, lithic technologies, use of fire, articulated pology, 2nd edition, pp. 2281-2297. Springer, language, symbolic intelligence) do not seem to Verlag-Berlin-Heidelberg. have been developed in unison by one dominant Akhilesh K., Pappu S., Rajapara H.M. et al. 2018. species at a time, but may have been developed Early Middle Palaeolithic culture in India by several species at a time, in scattered and around 385–172 ka reframes Out of Africa punctuated ways and rates. Macro-evolutionary models. Nature, 554: 97-101. processes - like climate changes, environmental Argue D., Groves C., Lee M.S.Y. et al. 2017. The instability, ecological unpredictability - seem to affinities of Homo floresiensis based on phyloge- be crucial in order to better understand such netic analyses of cranial, dental, and postcranial mosaic patterns that characterized hominin evo- characters. J. Hum. Evol., 107: 107-133. lution. Mosaic evolution could also shed light Arsuaga J.L., Martinez I., Arnold L.J. et al. 2014. on the emergence of H. sapiens, a species among roots: Cranial and chronological ev- many, which appeared around 200 Kya in Africa, idence from Sima de los Huesos. Science, 344 : and which carried an unprecedented mosaic of 1358-1363. A. Parravicini & T. Pievani 63

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