Self domestication and the evolution of language

The learning of new signals

For structure to emerge through cultural evolution, it is necessary that the system be learned from others. However, the communication systems of most species are not transmitted in this way. The pattern across mammals, at least as far as vocal communication is concerned, is that most species have a limited repertoire of signals which are present in their adult form from birth (Seyfarth and Cheney 2010). We should be clear here, however, about what we mean by ‘learning’. When we talk about learning we are specifically talking about production learning (Seyfarth and Cheney 2010), where an existing signal is modified or a new signal is acquired. This stands in contrast to comprehension learning, which refers to the ability to extract a new meaning or inference from a signal; and usage learning, where the usage of a signal is modified based on the current situation or context (Janik and Slater 2000; Seyfarth and Cheney 2010).

There are, of course, examples of production learning found in nature. Among mammals, known vocal learners include some species of whales and dolphins (Reiss and McCowan 1993; Rendell and Whitehead 2001), bats (Boughman 1998), seals (Ralls et al. 1985), and elephants (Poole et al. 2005). We have no doubt that many further examples of mammalian vocal learning will be discovered in the future. Among birds, production learning is found in both parrots (Pepperberg 2010) and hummingbirds (Baptista and Schuchmann 1990). Of course, the most unequivocal evidence of vocal production learning is found in songbirds (Nottebohm and Liu 2010), many species of which require exposure to other singers during development in order to develop species-typical song (Beecher et al. 2010). The importance and widespread nature of learning in songbirds makes them a particularly good ‘natural laboratory’ for the question of how and why a central role for learning might have emerged in relation to language.

While communication through vocal signals is widespread in nature, communication through gesture—that is, through “manual communication without touching another individual or a substrate”—is found almost exclusively in apes and humans (Pollick and de Waal 2007: 8184). The gestural communication of apes is significantly more flexible and less tied to emotional reactions or specific contexts than either their vocal or facial expressions (Pollick and de Waal 2007). The comprehension and usage of ape gestures in the wild is known to shift between contexts (Hobaiter and Byrne 2011), and the emergence of new, non species-typical gestures has been observed in captivity (Leavens et al. 2005). Of course, gesture, although learned, is not the predominant modality of language as we know it today. This, amongst other things, has lead some to suggest that language may have originated in the gestural modality, only later becoming primarily vocal (e.g. Corballis 2002). In contrast, others have suggested that it is not so much that language itself switched modality, but that the same underlying cognitive capabilities that permit the flexibility of learned gesture in apes may have been extended to the vocal domain (e.g. Tomasello 2008).

Communicative inference: linking signals to meanings

However, vocal production learning is not itself enough. What is required for language is the production learning of new signal-meaning associations. There seems little evidence that any of the vocal production learners discussed above are learning new signal-meaning associations, or even that their signals have any semantic content at all (Fitch 2005). Even in one of the clearest examples of vocal production learning, that of the songbirds, there appears to be no evidence that there is any semanticity to the learned song, or that song elements can be rearranged to yield changes in meaning (Berwick et al. 2011). There are, however, some instances of signal-meaning associations being learned in apes. Learning of this kind can be seen in the process of ontogenetic ritualisation (Tomasello 1996), in which signal-meaning associations are constructed through repeated interactions. It can also be seen in ape language research (Savage-Rumbaugh et al. 1986, 1998, 2005; Lyn 2007), in the form of learned lexigrams and gestures.

Language is unusual, however, because it is both learned and symbolic (Deacon 1997). As such, the link between signals and their meanings is neither innately specified nor inherent in the form of the signal (Oliphant 2002). This greatly complicates the task of acquiring new signal-meaning pairs, because it requires not just associative learning between items, but also some way of figuring out what words actually mean. To learn a new signal-meaning pair in a language-like system, then, requires the capacity to infer what a communicator intended the signal to mean.

In language, the inferential acquisition of new signal-meaning pairs is most clearly exemplified by word learning. Many different processes are likely involved in word learning (Markman 1994; Samuelson and Smith 1998; Saffran 2003; Smith et al. 2011). However, it is the social-pragmatic account (e.g. Tomasello 2000) that has the most to say about the problem of meaning inference. This account is rooted in our awareness of others as intentional agents (Tomasello 1999), and our capacity to engage in joint-attentional activities (Tomasello et al. 2005), against a background of mutually shared knowledge, expectations and goals. This background, often referred to as ‘common ground’ (Clark 1996) or in terms of a ‘mutual cognitive environment’ (Sperber and Wilson 1995), creates a situation in which the range of potential referents for a given utterance is drastically reduced. In summary, then, our second precursor is not simply the production learning of new signal-meaning associations, but the ability to acquire these associations through an inference of communicative intent.

However, there is an even more basic form of this precursor, which stands as a requirement for any account of learned symbols to be possible in the first place. This concerns the recognition that an action or behaviour was meant communicatively at all (Scott-Phillips et al. 2009). In contrast to inferring the meaning of a particular signal, we might call this a general sensitivity to communicative intent: an awareness, that is, that a particular signal or action was made in order to communicate. Given that the full suite of capacities underpinning joint-attentional situations and the inference of communicative intent are likely unique to humans, we think it more promising to focus on this more basic form of the precursor.

The Bengalese finch and the learning of signals

The Bengalese finch is a domesticated strain of the white-rumped munia (Okanoya 2002), a bird native to tropical continental Asia and some of the surrounding islands. For the last 250 years the Bengalese finch has been bred in Japan for its white plumage (Okanoya 2004; Svanberg 2008). Importantly, the Bengalese finch has not been bred for its song. Despite this, the song of the Bengalese finch has changed remarkably over the course of its domestication. It is the nature of these changes, together with the reasons why domestication had this kind of effect on its song, that makes this bird significant for those interested in the cultural evolution of language.

The role played by learning in songbirds differs along a number of dimensions (Beecher and Burt 2004; Beecher and Brenowitz 2005; Beecher et al. 2010; Soma 2011). As such, the changes to the Bengalese song brought about through domestication are best appreciated against a backdrop of the similarities between the Bengalese finch and its wild ancestor. Firstly, both the wild and domesticated species are closed learners (Okanoya and Yamaguchi 1997; Soma et al. 2006), meaning they can only acquire their species-typical song during a developmental ‘sensitive period’. Secondly, both species require exposure to conspecific song during development (Bao et al. 2003; Peng et al. 2012). Species-typical song will not develop if they are reared in isolation, as it can in some species (e.g. Kroodsma et al. 1997; Leitner et al. 2002). Finally, both the wild and domesticated strains are ‘social learners’, who learn better from conspecifics than from prerecorded ‘tape tutors’ (Eales 1989; Soma 2011).

Both species, then, are vocal learners. Domestication has not turned a non-learner into a vocal learner. What has changed, however, is the role and importance of learning—specifically, learning from others—to the transmission of the song between generations. This can be seen in three further dimensions along which the wild and domesticated strains differ. Firstly, the domesticated Bengalese now sings a much more complex and syntactically rich song, with greater levels of unpredictability in the patterns of transition between notes and note groups than is seen in the wild munia (Okanoya 2002, 2012). Secondly, cross-fostering experiments (Takahasi and Okanoya 2010) have shown that Bengalese chicks exhibit much lower copying fidelity in what they learn from tutor birds. Whereas munia chicks copy tutors with a high level of fidelity, Bengalese chicks combine the tutor’s song with their own improvisations and variations. Finally, and most importantly, Bengalese finches are much less constrained in what they are able to learn. Song learning in the white-rumped munia is highly canalized, such that munia chicks are only able to acquire a narrow range of species-specific song. In contrast, Bengalese chicks are much less constrained in what they are able to learn (Takahasi and Okanoya 2010).

Three important points follow from these differences. The first is that the reduction in learning constraints seen in the Bengalese finch means that the specifics of experience during development (e.g. particular tutor used as model) have a much greater influence on the structure of the resulting song. The second is that the reduction in high-fidelity copying combined with the broader range of what Bengalese chicks will copy has resulted in a much greater variation in song between different finches than is seen in their munia ancestors. Finally, all three of these differences combined have meant that many Bengalese finches have come to sing songs of much greater complexity than seen in white-rumped munias.

In the wild-living white-rumped munia, we have an example of a stereotypic, highly canalized communication system in which learning plays a minimal role. In its domesticated descendent, the Bengalese finch, song learning is less canalized, the songs themselves are less stereotypic and the influence of traditional transmission on song structure has increased. We see in this example, then, a parallel with the first of the preconditions identified above: an increase in the role of learning and cultural transmission. This change occurred in the context of domestication. Recall, however, that despite this context it cannot be attributed to artificial selection for more complex song. Why, then, might domestication have changed this bird’s song in this way?

One of the major characteristics of domestication is the buffered nature of the environment (Zohary et al. 1998; Price 1999, 2002; Deacon 2010), in which organisms are no longer subject to many of the selective pressures typically found in the wild, such as predation, unpredictable variation in food supply, and climatic variation. Deacon (2003, 2009, 2010) has proposed that domestication operated to relax various selection pressures on munia song that had kept it simple and stereotypical in the wild, allowing the song to become more complex under domestication (see also, Ritchie and Kirby 2007). This relaxation of selective pressure, argues Deacon, resulted in a breakdown of the learning biases and other factors that had kept the song simple in the wild and served to restrict the potential role for learning in shaping song characteristics. In turn, this opened up the possibility for learning and other aspects of early experience to influence song structure much more greatly under domestication. It is important to note that this is not the relaxation of selective pressure, per se, such that no selection occurs, but of specific pressures that served to restrict the potential contribution of learning and individual experience to the resulting song.

One such pressure concerns the need for accurate species recognition. Kagawa et al. (2012) compared the songs of three wild populations of white-rumped munia on the island of Taiwan. The syntactic complexity of munia song was found to vary in relation to the number of sympatric, closely related species. One of the key functions of song is species recognition, which is important in order to avoid the infertile hybrids that often result from cross-species matings. This is best achieved through the use of simple, stereotypic songs that exhibit little variation. In locations with fewer sympatric close relations, however, the selective pressure on species recognition is relaxed. The greater song complexity found in areas with fewer sympatric species could well be another example of song complexification following a relaxation of selective pressure. Kagawa et al. have, then, identified a key selection pressure that is both relaxed under domestication and found to be related to song complexity in the wild.

The second strand of evidence relates to the differing levels of stress hormones found in white-rumped munia and Bengalese finches. Suzuki et al. (2012) report measurements of fecal corticosterone, a hormone known to be directly involved in the development of the song system (Suzuki et al. 2011). Bengalese finches were found to have lower levels of corticosterone than white-rumped munia, regardless of whether the munia had been wild-caught or captive raised, indicating that it is domestication of the lineage that matters and not simply the conditions in which an individual bird was raised. Indeed, changes in hormonal regulation are known to commonly follow from domestication more generally (Price 2002; Trut et al. 2009). A range of work shows that higher levels of corticosterone negatively affect the development of the song system and can reduce the complexity of the resulting song (Spencer et al. 2003; Buchanan et al. 2004). If this is the case, then the finding that domestication can reduce levels of corticosterone in finches—perhaps through consistently reduced levels of stress in a buffered environment—might well provide a physical mechanism whereby the relaxation of selection following domestication could induce song complexification.

Finally, it is also clear that both female Bengalese finches and female munias have a preference for more complex song (Okanoya 2002). The potential role of sexual selection is somewhat attenuated by the fact that Bengalese breeding has long been under human control, although there is still scope for sexual selection to influence song structure through the higher ‘breeding efficiency’ of bird pairs in which the male sings a more complex song (Okanoya 2004). The precise nature of the interplay between relaxed selection and female preference remains unclear. It may be as simple as the two factors acting to reinforce one another. Of course, we can ask why such female preference for complexity should be satisfied through complexity that is learned, rather than, say, the impressive improvisation seen in some other species (e.g. Leitner et al. 2002), either of which would fit equally well with the major selective theory of song complexity in birds, the developmental stress theory (Nowicki et al. 1998; Buchanan et al. 2004; Ritchie et al. 2008). One possibility is that the environment of domestication, having already relaxed selection on song simplicity, and thus facilitated a greater role for learning in song transmission, set up just the conditions for a demonstration of fitness through learning rather than through improvisation or other means (Thomas 2013).

The domestic dog and communicative inference

Starting in the late 1990s a number of studies appeared describing how domestic dogs were particularly adept at using human communicative cues, such as pointing (Hare et al. 1998; Soproni et al. 2001), gaze (Hare et al. 2002), location markers (Agnetta et al. 2000), and even 3D replicas and photographs (Kaminski et al. 2009). Of particular interest was the fact that dogs seemed to outperform chimpanzees and other apes (Hare et al. 2002; Hare and Tomasello 2005; Gómez 2005; Miklósi 2007), and indeed seemed more similar to human children in this respect, although the true capacity of apes in this is a matter of debate (see Mulcahy and Call 2009; Mulcahy and Hedge 2012; Kirchhofer et al. 2012). Furthermore, these abilities are found across a wide range of different breeds (Wobber et al. 2009), including breeds that had been bred as working dogs like retrievers, companion dogs like toy poodles, and even once-domestic but now-feral breeds like the Australian dingo (Smith and Litchfield 2010).

These studies all utilised a variant of the object choice task (see Miklósi and Soproni 2006). In this procedure, a piece of food or other desirable item is placed in one of two or more locations. The location of the food is then indicated to the subject through pointing or some other cue, and the subject is then allowed to choose between the locations. The question of interest is whether the subject can use the cue to select the correct location. More specifically, however, what matters is not the ability to respond to the cues per se, but the extent to which a comprehension of the communicative nature of the cues is necessary for success on the task. It is quite possible, for example, to be successful with some cues, such as location tapping or sustained, close-in pointing, purely as a result of stimulus enhancement. Other cues, however, such as iconic representations and brief points from more distant locations, are much less salient in this regard. Finally, such comprehension is even more strongly confirmed if responses are modified based on the ostensive content of those cues. For example, by responding differently to intentionally given communications than to very similar physical actions produced ‘by accident’.

Studies with wolves and young puppies suggest that this ability in dogs is neither a simple inheritance from the canid line more generally, nor dependent on exposure to humans during development. Miklósi et al. (2003) compared dogs and wolves that had been socialised with humans to a comparable level. They found that dogs significantly outperformed wolves on the object choice task. Virányi et al. (2008) conducted a longitudinal study with sets of hand-reared wolves and dogs. When tested at a young age, the dogs significantly outperformed the wolves despite similar levels of exposure to humans. They then went on to re-test the wolves at regular intervals. The wolves performance steadily increased with each re-testing, such that eventually the best subset of these highly trained wolves reached a comparable level of performance with naive dogs, who had not previously been tested. Echoing Virányi et al’s findings, Riedel et al. (2008) found a similar level of performance across dogs of all ages, including puppies as young as 6 weeks old.

We should note, however, that others have disputed the claims of dogs’ superiority to wolves and the presence of the capacity in young dogs (Udell et al. 2008; Wynne et al. 2008). This has lead to the suggestion of the so-called ‘two-stage hypothesis’, which suggests that dogs’ abilities stem from a combination of an initial exposure to humans during their early socialisation period, followed by extended reinforcement learning over the course of life (Udell et al. 2010). This, then, is something of a domain-general account of how these abilities emerged, in contrast to the more domain-specific account rooted in domestication. However, a range of further evidence suggests that the abilities found in dogs go well beyond what could reasonably be accounted for through a domain-general effect of reinforcement learning.

The most significant of these further findings concerns a number of parallels between dogs and human infants in their response to communicative cues. Firstly, like human infants, but unlike other apes (Hare and Tomasello 2004; Herrmann et al. 2006), dogs appear to show a particular sensitivity to cues in co-operative contexts (Pettersson et al. 2011), rather than in competitive situations. Secondly, dogs, again like human infants, show a particular sensitivity to the ostensive content of signals and cues (Kaminski et al. 2012). Dogs respond differently to intentionally given cues, than to similar actions produced ‘accidentally’, and show sensitivity to a range of ostensive cues, such as establishing eye contact and calling their name. Finally, dogs even exhibit some similar errors to those seen in human infants in interpreting communicative cues (Topál et al. 2008, 2009), including the so-called A-not-B error related to object permanence.

We should pause here to note that these abilities have been investigated in a number of species other than dogs, including dolphins (Pack and Herman 2004, 2006, 2007), seals (Shapiro et al. 2003; Scheumann and Call 2004), horses (Proops et al. 2010), and goats (Kaminski et al. 2005). Studies have also been conducted with a number of bird species including parrots (Giret et al. 2009), and numerous kinds of corvids (e.g. Schloegl et al. 2008; Tornick et al. 2011). In many cases the results can be explained in terms of stimulus enhancement, with levels of correct response correlating to the saliency of the cue used. However, in some cases, particularly dolphins and seals, there does indeed seem to be some genuine understanding of the communicative nature of the cues. However, much like with socialised wolves, these more impressive cases typically involve individuals who have had intensive, long-term contact with humans, often participating in research programs, demonstrations or shows for many years. In addition, there have been a number of studies of other domesticated species, including cats, horses and goats (see Miklósi and Soproni 2006; Thomas 2013 for reviews), which have returned somewhat inconclusive results.

Having an evolutionary history of domestication is not, then, a necessary condition for the sophisticated utilisation of human communicative cues. However, there may be multiple routes, each comprised of different proportions of phylogenetic and ontogenetic contributions, that can lead to similar phenotypic outcomes (Miklósi and Topál 2011). Broadly speaking, the ontogenetic route, taken by dolphins, seals and intensively socialised wolves, consists of long-term exposure to humans. In contrast, the phylogenetic route, seemingly taken by the dog over the course of domestication, means it requires little or no exposure to humans for comparable capacities to become manifest (Miklósi and Topál 2011). We are left, then, with much the same question as followed from the case of the Bengalese finch: what is it about the process of domestication that caused this change in dogs? Fortunately, however, there is a long-running experiment, expressly designed to investigate the domestication of the dog.

The farm fox experiment (Belyaev 1979; Trut 1999; Trut et al 2009) was started in 1959 by the Russian geneticist Dmitry K. Belyaev. The experiment took the Siberian silver fox—a regional variant of the more familiar red fox—as its model animal, and began a selective breeding program, still running today, to recreate the domestication of the dog, and to investigate the origins of the physical and behavioural characteristics typical of domesticated species. At the core of the experiment is the breeding of three lines of foxes, tame, aggressive, and a control group. For reasons of clarity and space we will focus on the tame-line foxes.

Selection in the tame-line foxes was solely based on their temperament, as assessed through their reactions to humans (Kukekova et al. 2006, 2008, 2012). Foxes were then classified into groups based on their overall aggressive behaviour, with the tamest, least aggressive foxes known as the ‘domesticated elite’. The selective pressure applied to the tame line of foxes was very strong, with only the top 10% of most tame individuals being allowed to breed (Trut et al. 2009). Unsurprisingly, this rapidly increased the percentage of foxes classified as ‘domesticated elite’, from 1 to 2% at the beginning of the experiment to almost the entire population after fifty or so generations (Trut et al 2009).

The most striking thing about this list is how many of these changes are typically found in domesticated species (Price 1999), forming part of the domestic phenotype. One remarkable finding of the farm fox experiment, then, is that many of these typical outcomes of domestication can be produced simply as a by-product of selection against aggression. For present purposes, however, the most important change that occurred in the tame line of foxes was that, like domestic dogs, they also came to exhibit a sensitivity to communicative intent.

Hare et al. (2005) conducted an object-choice task, similar to those described above, comparing the abilities of dog pups, tame-line domesticated fox kits and control fox kits. The three groups were tested on their ability to use a point-and-gaze cue to select the correct location of some hidden food. The two major findings were that tame-line fox kits performed as well as dog puppies, and that the tame-line kits outperformed kits of the control population. There was also no evidence of learning during the experiment, as the tame-line kits performed as well in the initial trials as in later ones.

Temperament is the only criteria on which these foxes were selected. The fact that the sensitivity to communicative intent has emerged in the tame fox line lends support, therefore, to the emotional reactivity hypothesis (Hare et al. 2005; Hare and Tomasello 2005; Melis et al. 2006). This is the view that cognitive changes, particularly those involving co-operative behaviour, may not always requires direct selection, but can appear as a by-product of selection acting on systems of emotion or aggression that had previously prevented the use of preexisting skills in these kinds of co-operative contexts. This speaks directly to the question of why and how domestication might have resulted in this ability emerging in dogs. The answer arising from the farm-fox experiment is that such capacities are likely to have emerged as a by-product of selection targeting defensive and aggressive behaviours.

What is domestication and why is it relevant to humans?

Why we should even consider the possibility of domestication having played a role in human evolution? After all, does not domestication require that there be a domesticator—an outside agency selectively breeding the species? In this section we contrast two conceptions of domestication (see Thomas 2013). (1) The conditions view, in which domestication is characterised in terms of being under the control of another species. (2) The outcomes view, in which domestication is characterised by the typical traits that are shared by many domesticated species, known as the domestic phenotype.

The domestic phenotype in humans

The idea that humans are a ‘self-domesticated’ species has deep intellectual roots, tracing back at least to classical antiquity (Leach 2007). Over the centuries this view has picked up a number of unpleasant political associations (Brüne 2007). However, from a scientific perspective the main driver of the idea has been the observation that humans, too, share many aspects of the domestic phenotype. This observation can be seen in the writings of Charles Darwin (1871), the anthropologist Franz Boas (1938), and any number of more recent scholars who have compared aspects of human evolution to the outcomes of domestication (e.g. Ashley Montagu 1955; Gould 1977; Leach 2003, 2007; Hare and Tomasello 2005; Deacon 2009, 2010; Bednarik 2012). Unlike most domesticated species, modern humans have no living ‘wild’ ancestor against which their phenotypic traits can be compared. As such, most of these observations compare the modern human phenotype with trends over the course of human evolution, as seen in the fossilised remains of human ancestors, or, where this is not possible, with their closest living relatives, the great apes.

Modern humans have shown a marked decrease in skeletal and cranial robusticity over the last 100,000 years (Ruff et al. 1993; Lahr and Wright 1996; Leach 2003; Bednarik 2012). They have also seen a significant reduction in teeth size (Brace et al. 1987), and in the occurrence of tooth-crowding and malocclusion (Larsson et al. 2005; Leach 2003). Compared both to extant great apes and to ancestral human species, modern humans exhibit a significant retention of juvenile characteristics into adulthood (Gould 1977; Shea 1989; Zollikofer and Ponce de León 2010). In recent years the evidence of neoteny in modern humans has expanded to include aspects of gene expression in the brain (Somel et al. 2009, 2012; Liu et al. 2012), and the timing of synaptogensis (Bufill et al. 2011). Modern humans also exhibit very low levels of sexual dimorphism compared both to other apes (Plavcan 2012) and ancestral species of hominids (Harmon 2006; Gordon et al. 2008; Kimbel and Delezene 2009). Unlike other great ape species, human females do not have distinct ‘breeding seasons’, and thus exhibit a form of ‘extended sexuality’ (Rodrı́guez-Gironés and Enquist 2001), notwithstanding differences in fertility and preferences across the oestrus cycle (Gangestad and Thornhill 2008). There are also early signs that humans may differ in temperament to the other great apes, in ways similar to domesticated species (Herrmann et al. 2011). Finally, it seems that this suite of changes is linked, representing the systemic impact of an underlying mechanism (Trut et al. 2009; Bidau 2009; Wilkins et al. 2014). Evidence is now emerging for a similar links between features such as cranial robusticity, temperament, and neoteny in humans (e.g. Cieri et al. 2014).

Documenting the full range of these parallels, together with the nuances of the arguments over the validity of each one, is beyond the scope of what we can manage here, and the interested reader is referred to the references cited above, particularly Leach (2003, 2007), together with the much fuller version of this discussion in Thomas (2013). We should also mention the one aspect of the domestic phenotype which humans certainly do not parallel: a reduction in brain size. Rather than see brain size reducing, the direction of human evolution has been towards an increase in brain size (Rightmire 2004), with any trends in the opposite direction linked to a concomitant reduction in body size (Ruff et al. 1993). It may be that this is one trait where the difference between domestication and self-domestication is actually important, with humans, as both constructors and inhabitants of their environment, not subject to the same reduction in stimulation and opportunities for sensory exploration (Price 2002) experienced by other species living in that environment (Leach 2003).

The selective environment of domestication

As discussed above, many aspects of the domestic phenotype are linked to ongoing natural selection in the human-made environment, with the dramatic changes in living space, food availability and type, microclimate, elemental shelter, etc. that such an environment introduces. What is less commonly recognised, however, is that it is humans themselves, as nature’s quintessential niche constructors (Odling-Smee et al. 2003), who have likely been affected most by this environment, given that they have lived in it longest of all. Indeed, as Leach (2003) notes, many of the explanations for the domestication-typical changes seen in human beings, particularly in the last 50,000 years or so, point to aspects of this human-made environment, such as increasing sedentism and associated reductions in activity (Ruff et al. 1993), changes in climate and microclimate (Pearson 2000), and dietary shifts (Cohen and Armelagos 1984; Lieberman 1996). Similar changes in response to the human-made environment have also been observed in commensals—species who live with us but are not controlled by us—such as the house mouse (Tchernov 1984), and in the ‘inadvertent domestication’ observed in captive breeding programs for endangered species (O’Regan and Kitchener 2005). Once it is recognised that many aspects of the domestic phenotype are associated with the adaptation to a human-made environment, the idea that humans might share those ‘domesticated’ traits comes to be much easier to understand.

The second key factor is the role played by selection against aggression. One of the most important contributions of the farm fox experiment to our understanding of domestication is the extent to which the domestic phenotype can emerge through a ‘correlated cascade’ of changes following selection on temperament. One question that arises from this is whether there are any examples of a similar set of changes following natural selection in the wild. Hare et al. (2012) present a range of evidence suggesting that the bonobo is just such a case. Bonobos differ from chimpanzees along a number of physical (Cramer 1977; Zihlman and Cramer 1978; Pilbrow 2006), behavioural and temperamental (Hare et al. 2007; Hare and Kwetuenda 2010) dimensions that closely parallel the differences between wild and domesticated species. Hare et al. (2012) argue that these differences are ultimately rooted in aspects of the bonobo’s feeding ecology, which have had profound implications for the structuring of bonobo society, especially the favouring of greater co-operation and reduced levels of aggression. The bonobo, then, may be a wild analogue to the proof-of-concept findings of the farm-fox experiment. Furthermore, it may also serve as something of a template for how selection against aggression could be linked to the domestic phenotype in humans. In particular, a growing body of work is now citing changes in human feeding ecology, primarily our shifting to a cooked and processed diet (Wrangham et al. 1999; Wrangham and Conklin-Brittain 2003; Wrangham 2009), as a potential source of similar selective pressure in favour of co-operation and reduced aggression. This possibility is clearly more speculative than the impact of the human-made environment. However, in the farm-fox experiment we have confirmation that this kind of selective regime can result in the domestic phenotype, and in the bonobo we have a close relative, for which there is good evidence that a similar process, this time of natural selection, has had a similar phenotypic outcome.

The physical mechanisms underpinning domestication

We now turn to the mechanisms underpinning the domestic phenotype. However, before our brief review of work in this area, it is worth saying something about the criteria such a mechanism has to meet. The domestic phenotype has two key features: the range of species in which it has been observed, and the seemingly disparate set of traits of which it is comprised. To account for the domestic phenotype, therefore, any proposed mechanism must be both highly conserved across species and capable of explaining how such an apparently unconnected set of traits so frequently occur together. Follow-up studies on the mechanisms at work in the farm fox experiment has identified changes in the domesticated foxes’ neuroendocrine system as being of fundamental importance (Trut et al. 2009). In particular, a reduction in the production of glucocorticoids and other stress hormones, together with changes in the levels of neurotransmitters such as serotonin. The importance of the role played by the neuroendocrine system is also supported by work with the Bengalese finch (Suzuki et al. 2011, 2012), bonobos (Surbeck et al. 2012a, b), and domesticated species more broadly (Price 2002).

This neuroendocrinal mechanism meets one of the two criteria: the systems involved are highly conserved across species (Bidau 2009). However, as others have noted (e.g. Wilkins et al. 2014), it does less well against the second criteria: it is unclear how such neuroendocrinal changes account for the diverse range of traits that comprise the domestic phenotype. Wilkins et al. (2014) argue that this diverse set of traits, including the neuroendocrinal changes, are linked by shifts in the development, migration, and interaction of Neural Crest Cells (NCC), a vertebrate-specific class of the developmentally important stem cells. They review a wide range of clinical and experimental work which shows similarities between aspects of the domestic phenotype and the effects of genetic disorders, so-called neurocristopathies, that affect the generation and function of NCC. Importantly, Wilkins et al. distinguish between NCC as the shared developmental basis linking the various traits of the domestic phenotype and their emergence over ontogeny, and the polygenic nature of the underlying genetic explanation. This allows them to present a unified account of the diverse traits of the domestic phenotype without needing to talk in overly simplistic terms of ‘domestication genes’.

More recently it has been suggested that changes in the development and regulation of NCC are linked not just to the domestic phenotype but also to the structural ‘language readiness’ of the human brain (Benítez-Burraco et al. 2016). In particular, Benı́tez-Burraco et al. argue for a link between changes to the NCC and the development of the human-typical ‘globular’ brain shape. This builds on previous work in which they have argued that the distinctive globular shape of the human brain is linked to key features of its modern-day patterns of neural connectivity (Boeckx and Benítez-Burraco 2014a, b), which in turn facilitate what they term ‘cross-modular’ thinking. In linguistic terms, this is exemplified by something like the syntax-semantics interface. In more general terms, it relates to the capacity to make links across cognitive domains, something which may be core to the uniqueness of modern human cognition (e.g. Mithen 1996; Hauser 2009). This work is obviously in its very early stages, but is particularly intriguing regarding the parallels it offers with our work on the mechanism and necessary biological foundations for the cultural evolution of language.

Why has domestication had this effect on humans and not other species?

If domestication set the stage for the cultural evolution of language, it is quite reasonable to ask why language itself is not part of the domestic phenotype. Why is something ‘language like’ not seen in other domesticated species? Focusing just on our two central case studies, why do we only see one of the two precursor traits in each instance, and yet humans exhibit both together? These are difficult questions, for which we do not pretend to have definitive answers. However, we think the following points are worth taking into consideration.

Much as we have focused on their similarities, there is also a need to acknowledge the differences between domesticated species. One important way in which they differ is the ‘pathway’ they take towards domestication. Some species, like cattle and sheep, are former prey animals that have been slowly corralled into our system of agriculture. Others, like dogs, began the process as freely associating commensals. In the human case, the process of domestication was one of self-domestication. We have already discussed the potential consequence of this fact in terms of human brain size increasing, rather than the typical domesticated pattern of reducing brain size. We are highly sceptical of any attempt to draw direct links between brain size and particular capabilities. However, it is at least plausible that this increase in brain size is one contributing factor to the emergence of language (see MacWhinney 2005).

Another way in which domesticated species differ is in terms of their evolutionary history prior to domestication. The evolutionary histories of many lineages have rendered them unamenable to domestication at all (Diamond 1997). Furthermore, if there is a key commonality between the Bengalese finch and the domestic dog, it is that domestication has acted to unleash ‘potentials’ that were already there in the ancestral population. The white-rumped munia is a vocal learner, but freed from selection to keep songs simple and canalized, the role of vocal learning expanded. The grey wolf exhibits sophisticated social cognition, and can reach dog-like levels of performance given extensive contact with humans and repeated exposure to the object-choice task, but does not seem to learn new signals. In the human case, might the combination of primate social cognition with, at least in the gestural realm, the capacity of primates to learn new signals, explain why both precursors emerged together?

We recognise that these brief thoughts can barely begin to address this question. However, we think there are ways in which experimental work could be done in this area. For example, as noted above, many of the more particular impacts of domestication take the form of unleashed potentials. More precisely, potentials that have thus-far been limited by aspects of temperament. It should be possible to identify what these might be in particular instances. For example, Melis et al. (2006) found that chimpanzees who were seemingly unable to solve a co-operative dyadic task could do so if dyad-pairing was manipulated such that individuals with mutually high tolerance were paired together. The poor performance of chimpanzees, relative to dogs, on tasks of co-operative communication stands, then, as something that might be remedied through a change in chimpanzee temperament.

Summary

We have not attempted to present a comprehensive overview of human self-domestication. Instead, we have focused on the more modest task of trying to close the perceived ‘gap’ between the two sets of data that form the core of this paper: the preconditions required for a structure-creating process of cultural transmission, and the two case studies of domestication in which parallels to those preconditions can be seen emerging. We hope we have helped close it somewhat in the following three ways. First, in focusing on the domestic phenotype we aim to root the idea of humans as domesticates in a concrete, coherent, and falsifiable framework. The focus on a particular set of traits, the domestic phenotype, and the evolutionary explanations for those traits allows us to move beyond metaphorical formulations of what it means to be ‘self-domesticated’. Second, we have identified two evolutionary circumstances—adaptation to the human-made environment and selection on temperament—that are known to contribute to the emergence of the domestic phenotype in other species. The first of these has definitely been a major factor in human evolution; the role of the second, while more speculative, is supported by a range of comparative and archaeological evidence. Finally, we have reviewed a range of work on the biological mechanisms underpinning domestication. These mechanisms are highly conserved—and thus present in a wide range of species, including humans—and can account for the diverse traits of the domestic phenotype. We also touched on some recent work suggestive of a link between the mechanisms mediating the domestic phenotype and language itself.