Social cognition and the evolution of language: constructing cognitive phylogenies

“Since Premack and Woodruff’s (Premack and Woodruff, 1978) seminal paper asked ‘‘Does the chimpanzee have a theory of mind?’’”

“Also, the discovery of mirror neurons (neurons that fire both when monkeys watch another animal perform a goal-directed action and when they perform the same action) in rhesus monkeys suggests that they possess the neural framework for the matching system of imitation (Ferrari et al., 2009; Rizzolatti and Craighero, 2…”

“Human cultural evolution also allows for accumulation of good ideas, a fact that is central to human cultural progress (Tomasello, 1999).”

“…elements of a TOM in some nonhuman primates, striking differences exist from the human system of understanding mental states and intentional agency (Csibra and Gergely, 2006, 2009; Tomasello et al., 2005), especially in their use of such understanding in communication (Seyfarth and Cheney, 2005).”

“However, research on the chameleon effect in human adults (Chartrand and Bargh, 1999; van Baaren et al., 2009) and ‘‘overcopying’’ in children (Whiten et al., 2009) suggests that, even when control is limited, imitation can have systematic and far-reaching effects on cooperative behavior and the…”

“Mirror Neurons and Language Evolution Our third example involves mirror neurons, one of the more fascinating neuroscientific findings in the last few decades (di Pellegrino et al., 1992; Rizzolatti and Craighero, 2004).”

“Social learning is a core element of the social intelligence hypothesis (Dunbar and Shultz, 2007; Humphrey, 1976), which suggests that the physical environment does not present the kind of challenges that lead to the evolution of a flexible, intelligent mind, but that the social environment does.”

“However, the discovery of macaque mirror neurons that respond to the sound of actions cast some doubt upon this conclusion (Kohler et al., 2002), as does the fact that the macaque monkeys studied have poor imitative abilities in either gestural or vocal domains (cf. Fitch, 2010).”

“Early sensitivity to ostensive-communicative cues and to the efficiency of goal-directed actions is thought to be a crucial prerequisite for such relevance-guided selective imitation (Csibra and Gergely, 2009).”

“Primates in particular may cope with others’ intentions and goals, but not with false beliefs like humans (Call and Tomasello, 2008).”

“Newborn humans are already responsive to their mothers’ visual orientation (Farroni et al., 2002), and coordination with others’ head and eye orientation to look in the same direction (gaze following) or at a specific target (joint visual attention) develops during early ontogeny (Butterworth”

“Although the capacity to understand false beliefs among humans has long been thought to emerge after age four (de Villiers and Pyers, 2002; Happé, 1995), recent findings suggest that human sensitivity to others’ perceptual and knowledge states emerge earlier in ontogeny (reviewed in Caron, 2009).”

“…cognition in birds poses a clear challenge to the primatecentered viewpoint that has dominated psychology and neuroscience for the last century; birds are currently neck-and-neck with the smartest primate in many tests of both social and physical intelligence (cf. Emery and Clayton, 2004).”

“…whether any animal species is capable of imitation of a high enough fidelity to allow such cumulative change (cf. Heyes, 2009; Huber et al., 2009; Tennie et al., 2009; Whiten et al., 2009), and while cultural variants are well documented, (e.g., birds, Lachlan, 1999; Slater and Ince, 1979; and…”

“…in the context of hand movements and visual perception, and the discovery of mirror neurons was seen by some as support for the gestural protolanguage hypothesis: the idea that hominids evolved language in the gestural domain before the evolution of spoken language (Arbib, 2005; Hewes, 1973).”

“However, the discovery of macaque mirror neurons that respond to the sound of actions cast some doubt upon this conclusion (Kohler et al., 2002), as does the fact that the macaque monkeys studied have poor imitative abilities in either gestural or vocal domains (cf. Fitch, 2010).”

“Chimpanzees can differentiate between individuals that can and cannot see food behind a barrier (Bräuer et al., 2007; Hare et al., 2000; but see Karin-D’Arcy and Povinelli, 2002), and those that have and have not seen the hiding of food in the recent past (Hare et al., 2001; Kaminski et al., 2008).”

“More recent competitive designs (Figure 2), in which subjects compete with conspecifics and/or human experimenters for access to food (Hare et al., 2000), have led to unexpectedly strong results, probably because they are ecologically more meaningful to primates (Hare, 2001).”

“One explanation may be that, during domestication, dogs have been specifically selected to attend to human communicative cues (Hare et al., 2002; Miklósi et al., 2003).”

“Highly controlled experiments have been conducted with a wide range of species, investigating what exactly is copied, and what information about the observed action the observer uses (Heyes, 1994; Whiten and Ham, 1992; Whiten et al., 2004; Zentall, 2004, 2006).”

“Although some bird species will learn a song from recordings when isolated (e.g., Marler, 1970), others will not, and young males in many species learn preferentially from a living ‘‘tutor’’ bird (Baptista and Petrinovich, 1986; Immelman, 1969; Mann and Slater, 1995).”

“…2009; Huber et al., 2009; Tennie et al., 2009; Whiten et al., 2009), and while cultural variants are well documented, (e.g., birds, Lachlan, 1999; Slater and Ince, 1979; and great apes, van Schaik et al., 2003; Whiten et al., 1999), the existence of cumulative culture remains highly contentious.”

“…orientation (Farroni et al., 2002), and coordination with others’ head and eye orientation to look in the same direction (gaze following) or at a specific target (joint visual attention) develops during early ontogeny (Butterworth and Jarrett, 1991; Johnson et al., 1998; Moll and Tomasello, 2004).”

“If they could, they ignored ineffective components, and predominantly tried effective ones instead (Horner and Whiten, 2005), suggesting that emulation is the favored strategy of chimpanzees when sufficient causal information is available.”

“…Can Be Tested Using Convergence The ‘‘social intelligence hypothesis’’ is a leading contemporary hypothesis that attempts to explain the evolution of intelligence, in general, as a result of selection for social intelligence in particular (Byrne, 1997; Dunbar, 2003; Humphrey, 1976; Jolly, 1966).”

“This observation was extended by Jürgens et al. (1982),”

“This appears to be another example of ‘‘deep homology’’ in which the development of convergent structure is mediated by homologous genes (Gehring and Ikeo, 1999; Shubin et al., 1997).”

“Today, birdsong is the best available model system for understanding the neural and genetic bases of a culturally transmitted signaling system (cf. Catchpole and Slater, 2008; Marler and Slabbekoorn, 2004).”

“However, when many children were brought together in a school for the deaf in Nicaragua, a few ‘‘generations’’ of deaf students developed their own new signed language with a rich lexicon and complex grammar (Senghas et al., 2005).”

“This appears to be another example of ‘‘deep homology’’ in which the development of convergent structure is mediated by homologous 808 Neuron 65, March 25, 2010 ª2010 Elsevier Inc. genes (Gehring and Ikeo, 1999; Shubin et al., 1997).”

“Highly controlled experiments have been conducted with a wide range of species, investigating what exactly is copied, and what information about the observed action the observer uses (Heyes, 1994; Whiten and Ham, 1992; Whiten et al., 2004; Zentall, 2004, 2006).”

“There is considerable debate about whether any animal species is capable of imitation of a high enough fidelity to allow such cumulative change (cf. Heyes, 2009; Huber et al., 2009; Tennie et al., 2009; Whiten et al., 2009), and while cultural variants are well documented, (e.”

“Why do dogs outperform primates in such tasks? One explanation may be that, during domestication, dogs have been specifically selected to attend to human communicative cues (Hare et al., 2002; Miklósi et al., 2003).”

“Many of these constraints are shared with other species, suggesting that a rich set of conceptual building blocks was already in place before language evolution began (Cheney and Seyfarth, 2007; Kaminski et al., 2004; Seyfarth and Cheney, 2005).”

“Despite this complexity (Macnamara, 1972; Quine, 1970), children typically hone in unerringly on the intended meaning of a speaker by relying on conceptual constraints on possible word meanings (Clark, 1987; Markman, 1990).”

“Although some bird species will learn a song from recordings when isolated (e.g., Marler, 1970), others will not, and young males in many species learn preferentially from a living ‘‘tutor’’ bird (Baptista and Petrinovich, 1986; Immelman, 1969; Mann and Slater, 1995).”

“…appears to have evolved convergently in three bird lineages (songbirds, parrots, and hummingbirds, Jarvis, 2004; at least four mammalian clades: humans, seals, cetaceans, and bats, Janik and Slater, 1997; Knörnschild et al., 2010; and, as suggested by recent data, elephants, Poole et al., 2005).”

“The second system is cortically driven, and is present in humans (and perhaps other species with voluntary control over complex, learned vocalizations), but not other primates (cf. Deacon, 1992; Jürgens, 1998; Jürgens et al., 1982; Myers, 1976).”

“For years, tests based on cooperative paradigms, in which subjects must rely on help from knowledgeable human experimenters, provided little evidence of TOM in chimpanzees (Povinelli and Eddy, 1996; Povinelli et al., 1990; Premack and Woodruff, 1978).”

“The ‘‘Large Carcass’’ Niche: Parallels between Hominids and Ravens In the course of hominid evolution, the proportion of meat in the diet increased, reflecting an increased importance of scavenging and hunting (Blumenschine and Selvaggio, 1988; Bunn and Kroll, 1986).”

“These observations suggest that other vocal learning species should also go through a stage of vocal play during ontogeny (Fitch, 2006).”

“…in the context of hand movements and visual perception, and the discovery of mirror neurons was seen by some as support for the gestural protolanguage hypothesis: the idea that hominids evolved language in the gestural domain before the evolution of spoken language (Arbib, 2005; Hewes, 1973).”

“In mice, successful genetic manipulations of FoxP2 provide a powerful tool to begin exploring, in detail, the role of this gene in the developing mammalian brain (Enard et al., 2009; Groszer et al., 2008; Shu et al., 2005).”

“Although Darwin knew that many songbirds must be exposed to conspecific song in order to sing properly themselves, it wasn’t until the 1960s that scientists began a detailed investigation of their vocal learning ability (Marler and Tamura, 1964).”

“tools of molecular phylogenetics (Cavalli-Sforza et al., 1992; Lieberman et al., 2007; Pagel et al., 2007).”

“A distinction is often made between ‘‘motor’’ imitation and ‘‘vocal’’ imitation, and research and debate on animal social learning has often focused solely on the former (cf. Laland and Janik, 2006).”

“Kuypers compared cortical projections to brainstem motor nuclei in humans and other mammals by combining experimental lesions with Nauta/Gygax staining of degenerating axons to map the descending connections from cortex to the brainstem and spinal cord (Kuypers, 1958a, 1958b; Kuypers, 1973).”

“This learning has been specified as learning about the operating mechanisms of objects or environment, properties of objects, relations between objects and functions, and the causal structure of the task (Byrne, 1998; Whiten et al., 2004).”

“Little agreement exists regarding whether these results can be interpreted as evidence for mental state attribution and basic TOM in nonhuman animals (cf. Povinelli and Vonk, 2003; Tomasello et al., 2003).”

“The ‘‘Large Carcass’’ Niche: Parallels between Hominids and Ravens In the course of hominid evolution, the proportion of meat in the diet increased, reflecting an increased importance of scavenging and hunting (Blumenschine and Selvaggio, 1988; Bunn and Kroll, 1986).”

“Language provides a particularly rich example of such cultural evolution via historical change, sometimes termed ‘‘glossogeny’’ (Fitch, 2008; Hurford, 1990), and linguistic elements such as words or grammatical rules can be analyzed using many of the tools of molecular phylogenetics (Cavalli-Sforza et al., 1992; Liebe…”

“…marmosets, Burkart and Heschl, 2007), rhesus macaques have been shown to discriminate between human experimenters who can and cannot see food (Flombaum and Santos, 2005), as well as individuals who can and cannot hear the removal of food (Santos et al., 2006), indicating multimodal…”

“First, a variety of surface behavioral cues potentially given by conspecifics during tests hardly affect subjects’ performance (Dally et al., 2006; Hare et al., 2000; Kaminski et al., 2008).”

“Recent research has strongly implicated the importance of the transcription factor gene FoxP2 in human speech, because clinical data show that speech production is severely disrupted when this gene suffers a missense mutation (cf. Vargha-Khadem et al., 2005).”

“In songbirds, FoxP2 is upregulated in nuclei involved in song learning (Haesler et al., 2004), and reduction of FoxP2 expression levels in song nuclei of zebra finches leads to less accurate, incomplete song learning (Haesler et al., 2007), providing direct evidence for the importance of FoxP2 in…”

“…among Vertebrates, whereas Geometric Gaze Following May Be Restricted to a Few Species For humans, monitoring others’ head and eye orientation (gaze) is a central feature of social life and communication (Brooks and Meltzoff, 2002), even influencing eye anatomy (Kobayashi and Kohshima, 2001).”

“Originally described in primates (Povinelli and Eddy, 1996a; Tomasello et al., 1998), gaze following has now been demonstrated in distantly related mammals (dogs, Miklósi et al., 1998; goats, Kaminski et al., 2005) and birds (ravens, Bugnyar et al., 2004; rooks, Schloegl et al., 2008a; and bald…”

“Although some bird species will learn a song from recordings when isolated (e.g., Marler, 1970), others will not, and young males in many species learn preferentially from a living ‘‘tutor’’ bird (Baptista and Petrinovich, 1986; Immelman, 1969; Mann and Slater, 1995).”

“Such an abrupt change was recently documented off eastern Australia, when the population adopted a novel song apparently carried by just a few males from the west coast population (Noad et al., 2000).”

“Nonhuman primates generally fail to take receiver’s knowledge into account when signaling (e.g., Cheney and Seyfarth, 1980; Rendall et al., 2000), suggesting that TOM, to the extent that it is present at all, is not employed pragmatically Neuron 65, March 25, 2010 ª2010 Elsevier Inc. 795 in…”

“The argument that mirror neurons imply a gestural protolanguage has been further weakened by the discovery of audiovocal mirror neurons in songbirds (Prather et al., 2008).”

“For years, tests based on cooperative paradigms, in which subjects must rely on help from knowledgeable human experimenters, provided little evidence of TOM in chimpanzees (Povinelli and Eddy, 1996; Povinelli et al., 1990; Premack and Woodruff, 1978).”

“…among Vertebrates, whereas Geometric Gaze Following May Be Restricted to a Few Species For humans, monitoring others’ head and eye orientation (gaze) is a central feature of social life and communication (Brooks and Meltzoff, 2002), even influencing eye anatomy (Kobayashi and Kohshima, 2001).”

“, 2004), and reduction of FoxP2 expression levels in song nuclei of zebra finches leads to less accurate, incomplete song learning (Haesler et al., 2007), providing direct evidence for the importance of FoxP2 in vocal learning across species.”

“One explanation may be that, during domestication, dogs have been specifically selected to attend to human communicative cues (Hare et al., 2002; Miklósi et al., 2003).”

“For more than a decade, evidence for this kind of intelligent social learning was restricted to chimpanzees (Tomasello et al., 1987).”

“Chimpanzees can differentiate between individuals that can and cannot see food behind a barrier (Bräuer et al., 2007; Hare et al., 2000; but see Karin-D’Arcy and Povinelli, 2002), and those that have and have not seen the hiding of food in the recent past (Hare et al., 2001; Kaminski et al., 2008).”

“Despite this complexity (Macnamara, 1972; Quine, 1970), children typically hone in unerringly on the intended meaning of a speaker by relying on conceptual constraints on possible word meanings (Clark, 1987; Markman, 1990).”

“, 1998, 2004), and although they have not been tested formally for geometrical gaze following, they seem to understand how barriers impair others’ perception (Bräuer et al., 2006).”

“Much has been discovered about the evolutionary roots of social learning and traditions through comparative studies (Fragaszy and Perry, 2003), especially in fish, birds, and nonprimate mammals (Laland and Galef, 2009), as well as insects (Leadbeater and Chittka, 2007).”

“Most other species seem to have problems in understanding the cooperative, communicative nature of the task, or they may be biased by competitive motives (Hare and Tomasello, 2004).”

“Data from tool-using birds remain far from convincing in this respect (woodpecker finches, Tebbich et al., 2002; New Caledonian crows, Hunt and Gray, 2003).”

“Monkeys show cognitive imitation by copying an expert’s use of a rule (Subiaul et al., 2004), recognize when they are being imitated (Paukner et al., 2005; Paukner et al., 2009), and imitate adult facial movements as neonates (Ferrari et al., 2006, 2009).”

“Chimpanzees can differentiate between individuals that can and cannot see food behind a barrier (Bräuer et al., 2007; Hare et al., 2000; but see Karin-D’Arcy and Povinelli, 2002), and those that have and have not seen the hiding of food in the recent past (Hare et al., 2001; Kaminski et al., 2008).”

“But investigation of observational learning in nonsocial animals, such as solitary octopuses (Fiorito and Scotto, 1992) and solitary tortoises (Wilkinson et al., 2010), suggests otherwise: the latter can learn to solve a detour task by observing the actions of a conspecific.”

“In humans at least, such inhibitory processes depend on the functioning of the same higher-order brain centers that are involved in attributing mental states to others (Brass et al., 2009).”

“Nonetheless, the best known example of a directional cultural ratchet effect in animals comes from research with zebra finches (Figure 3, Fehér et al., 2009).”

“In the case of deaf children raised in hearing families, it is common to see ‘‘home sign’’ systems develop, which support basic communicative needs but have nothing like the rich vocabulary and syntax of real signed languages (Goldin-Meadow and Mylander, 1998).”

“Outside primates, the strongest evidence of mechanisms involved in TOM comes from corvids tested with variants of the competitive food retrieval design, involving the caching and pilfering of food (Clayton et al., 2007).”

“Kuypers compared cortical projections to brainstem motor nuclei in humans and other mammals by combining experimental lesions with Nauta/Gygax staining of degenerating axons to map the descending connections from cortex to the brainstem and spinal cord (Kuypers, 1958a, 1958b; Kuypers, 1973).”

“At a given time, all of the males in a given area sing the same song, but this song typically changes gradually throughout the mating season (Payne et al., 1983) with complete song replacement in about 15 years (Payne and Payne, 1985).”

“Although this competence was previously thought to be human specific, recent experiments show an analogous capacity in dogs (Figure 6) and chimpanzees (Buttelmann et al., 2007; Range et al., 2007).”

“Simply looking for something of interest in the direction of the others’ gaze would result in subjects searching in front of the barrier, but if they reposition themselves to look behind a barrier, it suggests they appreciate the difference between their own and another’s line of sight (Povinelli and Eddy, 1996a).”

“Tract tracing studies show that cells in the final songbird motor region in the pallium (homologous to mammalian cortex) indeed send direct monosynaptic projections to the motor neurons controlling the syrinx whose cell bodies lie within the lower brainstem (Wild, 1993, 1997).”

“Meat eating had important effects on nutrition and social behavior of hominid groups, long thought to be central in understanding the evolution of human cognitive and communicative skills (Dart, 1949; Lee and De Vore, 1968; Montagu, 1976).”

“Dogs, however, are outstanding in solving these tasks instantly and reliably across a large number of variations (Agnetta et al., 2000; Miklósi et al., 1998, 2004), and although they have not been tested formally for geometrical gaze following, they seem to understand how barriers impair others’…”

“…appears to have evolved convergently in three bird lineages (songbirds, parrots, and hummingbirds, Jarvis, 2004; at least four mammalian clades: humans, seals, cetaceans, and bats, Janik and Slater, 1997; Knörnschild et al., 2010; and, as suggested by recent data, elephants, Poole et al., 2005).”

“This ability has only been demonstrated in great apes (Bräuer et al., 2005) and two corvid species (Schloegl et al.”

“A crucial property of culture is that it can give rise to a new level of evolution, cultural evolution, in which traditions diversify progressively in ways analogous to Darwinian biogenetic evolution (Darwin, 1859; Dawkins, 1976; Mesoudi et al., 2004).”

“In songbirds, FoxP2 is upregulated in nuclei involved in song learning (Haesler et al., 2004), and reduction of FoxP2 expression levels in song nuclei of zebra finches leads to less accurate, incomplete song learning (Haesler et al., 2007), providing direct evidence for the importance of FoxP2 in…”

“But when the model performed the task without the blanket (or without the ball) (‘‘free’’ condition), the majority of a second group of observers opted to copy the model’s head (or paw) movements, as if deciding that if the model did it, then it must be a better approach (Gergely et al., 2002; Range et al., 2007).”

“Indeed, ravens are outstanding at deceptively withholding information (Bugnyar and Heinrich, 2006; Bugnyar and Kotrschal, 2002), potentially creating the selective force favoring judging others’ perspectives (Bugnyar et al., 2004) and knowledge states (Bugnyar and Heinrich, 2005).”

“Language provides a particularly rich example of such cultural evolution via historical change, sometimes termed ‘‘glossogeny’’ (Fitch, 2008; Hurford, 1990), and linguistic elements such as words or grammatical rules can be analyzed using many of the tools of molecular phylogenetics (Cavalli-Sforza et al., 1992; Liebe…”

“Recent studies with common marmosets have provided evidence of very precise copying of new movements (Figure 4), challenging current theories of imitation in terms of associative learning, human-specific adaptations, and mirror neurons (Voelkl and Huber, 2000, 2007).”

“Similarly, the existence of trichromatic color vision in Old World monkeys, apes, and humans indicates that trichromacy evolved in the LCA of all cercopithecids (Jacobs, 1996).”

“Dogs, however, are outstanding in solving these tasks instantly and reliably across a large number of variations (Agnetta et al., 2000; Miklósi et al., 1998, 2004), and although they have not been tested formally for geometrical gaze following, they seem to understand how barriers impair others’ perception (Bräuer et…”

“Many of these constraints are shared with other species, suggesting that a rich set of conceptual building blocks was already in place before language evolution began (Cheney and Seyfarth, 2007; Kaminski et al., 2004; Seyfarth and Cheney, 2005).”

“In contrast, lesions to motor cortex have no effect on vocalization in nonhuman primates (Aitken, 1981; Sutton et al., 1974), leading many researchers to posit two distinguishable neural control systems involved in vertebrate vocalization.”

“These findings jibe with results from geometrical gaze following (Bugnyar et al., 2004; Tomasello et al., 1999) and support the hypothesis that the poor performance of nonhuman primates on cooperative tasks may better reflect their competitive motivation than their cognitive abilities per se…”

“Although some bird species will learn a song from recordings when isolated (e.g., Marler, 1970), others will not, and young males in many species learn preferentially from a living ‘‘tutor’’ bird (Baptista and Petrinovich, 1986; Immelman, 1969; Mann and Slater, 1995).”

“However, research on the chameleon effect in human adults (Chartrand and Bargh, 1999; van Baaren et al., 2009) and ‘‘overcopying’’ in children (Whiten et al., 2009) suggests that, even when control is limited, imitation can have systematic and far-reaching effects on cooperative behavior and the…”

“…(Povinelli and Eddy, 1996a; Tomasello et al., 1998), gaze following has now been demonstrated in distantly related mammals (dogs, Miklósi et al., 1998; goats, Kaminski et al., 2005) and birds (ravens, Bugnyar et al., 2004; rooks, Schloegl et al., 2008a; and bald ibises, Loretto et al., 2010).”

“But investigation of observational learning in nonsocial animals, such as solitary octopuses (Fiorito and Scotto, 1992) and solitary tortoises (Wilkinson et al., 2010), suggests otherwise: the latter can learn to solve a detour task by observing the actions of a conspecific.”

“Highly controlled experiments have been conducted with a wide range of species, investigating what exactly is copied, and what information about the observed action the observer uses (Heyes, 1994; Whiten and Ham, 1992; Whiten et al., 2004; Zentall, 2004, 2006).”

“More recent competitive designs (Figure 2), in which subjects compete with conspecifics and/or human experimenters for access to food (Hare et al., 2000), have led to unexpectedly strong results, probably because they are ecologically more meaningful to primates (Hare, 2001).”

“Both scrub jays and ravens differentiate between competitors that have or have not seen food cached in particular locations, selectively recovered food whose caching was observed (Bugnyar and Heinrich, 2005; Emery and Clayton, 2001), altered their cache protection strategies (Dally et al.”

“Younger birds ( 5 years of age) give specific calls, ‘‘yells’’ (Heinrich, 1988) or ‘‘haa’’ calls (Bugnyar et al., 2001), when they encounter food that is difficult to access and/or feared.”

“Monkeys show cognitive imitation by copying an expert’s use of a rule (Subiaul et al., 2004), recognize when they are being imitated (Paukner et al., 2005; Paukner et al., 2009), and imitate adult facial movements as neonates (Ferrari et al., 2006, 2009).”

“, 2002, 2003; common marmosets, Burkart and Heschl, 2007), rhesus macaques have been shown to discriminate between human experimenters who can and cannot see food (Flombaum and Santos, 2005), as well as individuals who can and cannot hear the removal of food (Santos et al., 2006), indicating multimodal sensitivity to…”

“There is considerable debate about whether any animal species is capable of imitation of a high enough fidelity to allow such cumulative change (cf. Heyes, 2009; Huber et al., 2009; Tennie et al., 2009; Whiten et al., 2009), and while cultural variants are well documented, (e.”

“Chimpanzees can differentiate between individuals that can and cannot see food behind a barrier (Bräuer et al., 2007; Hare et al., 2000; but see Karin-D’Arcy and Povinelli, 2002), and those that have and have not seen the hiding of food in the recent past (Hare et al., 2001; Kaminski et al., 2008).”

“Meat eating had important effects on nutrition and social behavior of hominid groups, long thought to be central in understanding the evolution of human cognitive and communicative skills (Dart, 1949; Lee and De Vore, 1968; Montagu, 1976).”

“Monkeys show cognitive imitation by copying an expert’s use of a rule (Subiaul et al., 2004), recognize when they are being imitated (Paukner et al., 2005; Paukner et al., 2009), and imitate adult facial movements as neonates (Ferrari et al., 2006, 2009).”

“NEURON information centers (Marzluff et al., 1996; Wright et al., 2003) and attracting others via food calls (Bugnyar et al.”

“The discovery that this open-ended learning results from neurogenesis in the song nuclei of adult canaries prompted the rediscovery of mammalian neurogenesis, leading to the explosion of research on this topic today (Nottebohm, 2006).”

“Most nonhuman species, including apes, monkeys, and ravens, find it surprisingly difficult to use the gaze direction of a human experimenter, or a conspecific, as a cue to find hidden food (Anderson et al., 1996; Call et al., 2000; Schloegl et al., 2008b).”

“The second system is cortically driven, and is present in humans (and perhaps other species with voluntary control over complex, learned vocalizations), but not other primates (cf. Deacon, 1992; Jürgens, 1998; Jürgens et al., 1982; Myers, 1976).”

“…locations, selectively recovered food whose caching was observed (Bugnyar and Heinrich, 2005; Emery and Clayton, 2001), altered their cache protection strategies (Dally et al., 2005, 2006) and, when tested as bystanders, adjusted their pilfering strategies (Bugnyar and Heinrich, 2005, 2006).”

“The most stringent test of whether animals can learn a new movement by observation involves the demonstration of at least one action that is unlikely to be performed, unless the subject had the opportunity to witness its performance (Bugnyar and Huber, 1997).”

“However, when many children were brought together in a school for the deaf in Nicaragua, a few ‘‘generations’’ of deaf students developed their own new signed language with a rich lexicon and complex grammar (Senghas et al., 2005).”

“Long underestimated, the importance of gaze for nonhuman animals is receiving increased interest (reviewed in Gómez, 2005).”

“The argument that mirror neurons imply a gestural protolanguage has been further weakened by the discovery of audiovocal mirror neurons in songbirds (Prather et al., 2008).”

“Nonhuman primates generally fail to take receiver’s knowledge into account when signaling (e.g., Cheney and Seyfarth, 1980; Rendall et al., 2000), suggesting that TOM, to the extent that it is present at all, is not employed pragmatically”

“Crowd-foraging ravens hardly share but carry off consecutive loads of food, which they scatter hoard at a moderate distance from the feeding site (Heinrich and Pepper, 1998).”

“Although little is known, at present, about the function of FoxP2 in the bat brain, the recent discovery of complex vocal learning in a bat (Knörnschild et al., 2010) suggests that bats may also have much to teach us about the function of this gene in mammalian vocal control.”

“Such subordinate birds cope with this challenge by teaming up (Heinrich, 1988; Marzluff and Heinrich, 1991).”

“…2009; Huber et al., 2009; Tennie et al., 2009; Whiten et al., 2009), and while cultural variants are well documented, (e.g., birds, Lachlan, 1999; Slater and Ince, 1979; and great apes, van Schaik et al., 2003; Whiten et al., 1999), the existence of cumulative culture remains highly contentious.”

“…debate about whether any animal species is capable of imitation of a high enough fidelity to allow such cumulative change (cf. Heyes, 2009; Huber et al., 2009; Tennie et al., 2009; Whiten et al., 2009), and while cultural variants are well documented, (e.g., birds, Lachlan, 1999; Slater…”

“Most nonhuman species, including apes, monkeys, and ravens, find it surprisingly difficult to use the gaze direction of a human experimenter, or a conspecific, as a cue to find hidden food (Anderson et al., 1996; Call et al., 2000; Schloegl et al., 2008b).”

“These calls develop from juvenile begging calls and are affected by hunger level (Heinrich and Marzluff, 1991) as well as the quality and quantity of a food source (Bugnyar et al.”

“In contrast, lesions to motor cortex have no effect on vocalization in nonhuman primates (Aitken, 1981; Sutton et al., 1974), leading many researchers to posit two distinguishable neural control systems involved in vertebrate vocalization.”

“These calls are not specific to the occurrence of food but are primarily given during food-related interactions (Bugnyar et al., 2001).”

“…elements of a TOM in some nonhuman primates, striking differences exist from the human system of understanding mental states and intentional agency (Csibra and Gergely, 2006, 2009; Tomasello et al., 2005), especially in their use of such understanding in communication (Seyfarth and Cheney, 2005).”

“…debate about whether any animal species is capable of imitation of a high enough fidelity to allow such cumulative change (cf. Heyes, 2009; Huber et al., 2009; Tennie et al., 2009; Whiten et al., 2009), and while cultural variants are well documented, (e.g., birds, Lachlan, 1999; Slater…”

“Geometrical gaze following is thought to rest on a cognitively more sophisticated mechanism; developmental data from ravens indicate that geometrical gaze following develops later and shows a different habituation pattern than gaze following into space (Schloegl et al., 2007).”

“NEURON information centers (Marzluff et al., 1996; Wright et al., 2003) and attracting others via food calls (Bugnyar et al.”

“Although mixed results have been reported for some monkeys (brown capuchins, Hare et al., 2003; Kuroshima et al., 2002, 2003; common marmosets, Burkart and Heschl, 2007), rhesus macaques have been shown to discriminate between human experimenters who can and cannot see food (Flombaum and Santos,…”

“Furthermore, capuchin monkeys repeatedly fail to learn how to use an object as a tool by observation (reviewed in Fragaszy and Visalberghi, 2004).”

“Finally, social cognition must be intact to appropriately decode verbal languag”

“The social intelligence hypothesis proposes that increased social complexity (frequently indexed by social group size) was the major selective pressure in primate cognitive evolution (6, 44, 48, 50, 87, 115, 120, 125 – 141).”

“Humansarenot theonly species inwhichcommunicative learning is affected by social interaction (see Fitch et al., 2010, for review).”

“, emotional state), humans can use language to basically communicate about any concept (131).”

“Based on these findings, many investigators hypothesized that the evolution of spoken language in humans was associated with the formation of a direct projection from LMC to nucleus ambiguus in humans (Kuypers, 1958a; Kirzinger and Jurgens, 1982; Iwatsubo et al., 1990; Jurgens, 2002; Khedr and Aref, 2002; Jarvis, 2004…”

“One human trait poorly back-translatable into animals is fully syntactical, recursive and abstract language (Fitch et al., 2010; Poeppel, 2012), of which a loss of fluent production (alogia) characterises NS (Table 1) (Foussias et al.”

“Even in the case of human language, which is much richer in its content, the meaning behind a word or sentence is often highly contextual (Dunbar, 2003; Fitch et al., 2010).”

“This evidence opens up the possibility that voice areas may have a longer evolutionary history than previously proposed [10], dating back to the common ancestor of dogs and humans some 100 million years ago [4], although convergent evolution cannot be excluded [37].”

“Over the last two decades the diversity of species under study has grown further and has generated renewed interest in testing hypotheses regarding how cognitive differences across species might have evolved (Shettleworth 2009, 2010; Fitch et al. 2010).”

“This is no different in language than in, for example, vision (Hubel, 1988; Marr, 1982), music (Peretz & Coltheart, 2003), aesthetics (Leder, Belke, Oeberst, & Augustin, 2004), or social cognition (Fitch et al., 2010).”

“Given the central importance of learning referential words in language, a key question is whether this is a uniquely human trait [6, 7].”

“…2011; Arriaga et al., 2012; Hammerschmidt et al., 2012; Portfors and Perkel, 2014) and this is thought to be attributed to the absence or very sparse presence of a forebrain pathway that in vocal learners, like songbirds and humans, is well-developed (Fitch et al., 2010; Arriaga and Jarvis, 2013).”

“…as one of the key neural transformations in the evolution of spoken-language and learned song (Deacon, 2007; Fischer & Hammerschmidt, 2010; Fitch et al., 2010; Jarvis, 2004; Jürgens et al., 1982; Kirzinger & Jürgens, 1982; Okanoya, 2004; Simonyan & Horwitz, 2011; Simonyan & Jürgens, 2003).”

“Outside of primates, however, skillful vocal control can be learned in a limited group of species including songbirds, parrots, cetaceans, bats, and elephants (Janik and Slater, 1997; Jarvis, 2004; Fitch et al., 2010).”

“The laryngeal motor cortex: the hypothesis The absence of laryngeal representation in the primary motor cortex and of direct (monosynaptic) motor cortical connections with brainstem laryngeal motoneurons in non-human primates has been puzzling for several years [2 ,52–55].”

“These are known as phylogenetic comparative methods and they have already been utilized to test possible scenarios regarding the evolution of inhibitory control [11], language [16] and general intelligence [17] within the primate clade.”

“The direct projection to the brainstem vocal MN is considered critical for the evolution of vocal learning and spoken language, as it is either absent or very sparse in vocal non-learners [2,42,87–92].”

“If, on the other hand, 41 similarities are found between humans and more distantly related species, these features represent 42 analogs and hence do not give any information on the phylogenetic origins of the feature, but can 43 help elucidate the environmental or social conditions favourable to its convergent evoluti…”

“…dogs and humans went through convergent evolution, researchers have suggested that dogs might be an additional, and in some respect, more informative model when investigating the evolution of human social behavior and cognition (Miklósi et al., 2004; Hare and Tomasello, 2005; Fitch et al., 2010).”

“Language can be considered a system that permits the expression of thoughts as signals and the reverse, the interpretation of such signals as thoughts (Fitch et al., 2010).”

“…understand beliefs of others is argued to have underpinned the evolution of complex social cognition phenomena in humans, including language, which relies on a set of communally shared symbols with arbitrary assigned meanings (Tomasello et al. 2005; Tomasello and Carpenter 2007; Fitch et al. 2010).”

“As social animals, we constantly move in an environment where we actively perceive others’ movements as a form of meaningful behavior (Blakemore and Decety, 2001; Gallese et al., 2007; Fitch et al., 2010).”

“A better understanding of the mechanisms contributing to vocal learning in birds as well as investigations of vocal learning in other mammalian species such as seals (Fitch et al., 2010) will be important to investigate such a scenario.”

“Gaze following into distant space seems common in the animal kingdom and has been shown in five taxa of mammals, in three taxa of birds and a tortoise (see [32,33] for review).”

“When this approach is taken with cognitive traits it can be termed “cognitive phylogenetics” (Fitch et al. 2010).”

“Although gaze following seems to be elicited in a reflexive manner and exists in many vertebrates (review in Fitch et al. 2010), including solitary reptiles (Wilkinson et al. 2010), the following of others’ gaze direction into distant space or around barriers seems to be a less common and more…”

“More precisely, Fong et al. (2003) listed some “human-like” behavioral and cognitive features that such socially interactive robots should possess.”

“Partly in recognition of this, some current research focuses on the extent to which great ape communication shares the same social-cognitive basis as linguistic communication (Fitch, Huber, and Bugnyar 2010; Tomasello 2008).”

“For review of the importance of gaze and visual cueing in the evolution of cognition and language see (Fitch et al., 2010).”

“…that article, researchers in the fields of comparative cognition, animal psychology, cognitive archaeology, and cognitive biology (Shettleworth 2009; Fitch et al. 2010) have made considerable advances in tackling different cognitive and behavioral elements that form the layered system of cognition.”

“The second and third authors contributed equally to this article.”

“On the basis of current evidence, it now seems unlikely that our ability to assess others’ psychological states evolved entirely de novo after humans split from other apes (Call & Tomasello 2008, Fitch et al. 2010, Rosati et al. 2010).”

“Although both views predict laterality for faces in humans (Fitch et al., 2010), the fundamental premise that differs between these hypotheses is that according to the former theory a similar degree of laterality is expected when the same non-linguistic face stimuli are presented to monkeys or humans.”

“In the context of vocal learning, the most pressing question is whether elephants possess direct connections between telencephalic neurons and the primary vocal motor neurons in the brainstem controlling the vocal apparatus (following the Kuypers/Jürgens hypothesis) [5–9].”

“Integrating approaches to research and examining cognition and communication as interrelated traits will provide a more comprehensive understanding of how the social environment may shape specializations of behavior and the brain to support social living (Dunbar 2003; Connor 2007; Tomasello 2008; Fitch et al. 2010; Pi…”

“The Kuypers-Jurgens hypothesis proposes that the direct connection between the LMC and laryngeal motor neurons is required for vocal learning [94].”

“Whether ravens have indeed mastered displacement, and if so how they accomplish it, is currently under investigation [59].”

“Thus, just as sociality is proposed to drive the evolution of intelligence and cognitive specialization (Byrne & Whiten, 1989; Jolly, 1966), it may also contribute to the origin and maintenance of vocal learning abilities (Dunbar, 2003; Fitch et al., 2010; McComb & Semple, 2005; Pinker, 2010).”

“The study of similarities and differences in their cognition can inform about homologies and analogies of cognitive mechanisms across the amniotes [5].”

“This bottom-up approach, seeking to establish ‘‘cognitive phylogenies’’ (Fitch et al. 2010), focuses on the fundamental capacities underlying larger cognitive phenomena and is more in line with the Darwinian logic of descent (Hauser et al.”

“…or spoken-language pathway (blue arrows in Figure 3b,d) (Friederici et al. 2017) and (ii) a direct projection from the vocal motor cortex to brainstem vocal motor neurons that control the muscles to produce song and speech (green arrows in Figure 3a,b) (Fitch et al. 2010, Petkov & Jarvis 2012).”

“But other differences, for example in the social cognition involved in semantics and pragmatics [22] and vocal learning [23] also needed to evolve after hominins diverged from our last common ancestor with chimpanzees around six million years ago.”

“Verbal communication affects social behavior [16].”

“…of descent-with-modification (De Waal & Ferrari, 2010; Hauser et al., 2002), which opens up the possibility of constructing ‘cognitive phylogenies’ (Fitch et al., 2010); 3) A reduction of the theoretical machinery needed to account for the fundamental properties of grammar within linguistics— a…”

“Only humans code and decode knowledge about the (social) world by means of symbolic language systems (Fitch et al., 2010).”

“This connection is similar to humans, where the face motor cortex makes a direct projection to the mammalian analog of brainstem vocal motor neurons, nucleus ambiguus (Amb) [2,6,7,8,11,12].”

“By examining the distribution of these mechanisms, researchers can determine which are shared and which are unique, and begin to piece together a putative history of cognitive evolution (Fitch et al. 2010).”

“We, furthermore, embrace the idea that feelings may have evolved convergently in multiple lineages and that the comparative study of these taxa will help us shed light on the selection pressures that may have shaped the evolution of both emotions and feelings (Fitch et al., 2010; Massen, 2020).”

“Earlier comparative data have also suggested that the skill is present across mammals (Fitch et al. 2010).”

“Language communication from an early life stage is an essential tool for bidirectional information transmission (Fitch et al., 2010; Kuhl, 2011), and is clearly delayed in certain ASD subtypes.”

“Studies have demonstrated the capacity of f0 modulation [28,30] through vocal imitation in some species (elephants: [31,32]; bats: [33]).”

“The answer to these questions is related to the animal mindreading debate.”