Empathy, resemblance and relatedness: the anthropomorphic stimuli hypothesis

The ability to understand others’ feelings through empathy is crucial for successful social interactions between humans19,20. Our predispositions for empathy are partly determined by our genes21 and, in all likelihood, this prosociality driver has been selected during the evolution of our species, in facilitating coordination and cooperation between individuals1,13,22. The extension of our empathic sensitivity toward other living beings remains nevertheless an issue poorly explored from an evolutionary perspective.

Our results show that our ability to empathize considerably fluctuates from one species to another, and that its magnitude mostly depends on the phylogenetic distance that separates them from us. Although relatedness and resemblance (sensu overall similarity) refer to different concepts, they empirically tend to be correlated. In an anthropocentric frame of reference, it can therefore be postulated that relatedness (here expressed as the divergence time) correspond to a rough holistic approximation of the total amount of shared external traits inherited from our common ancestor (synapomorphies), as retrospectively, they are expected to decrease relatively gradually over a long period of divergence.

Based on our results, we here hypothesize that our ability, real or supposed, to connect emotionally with other organisms would mostly depend on the quantity of external features that can intuitively be perceived as homologous to those of humans. The closer a species is to us phylogenetically, the more we would perceive such signals (and treat them as anthropomorphic stimuli), and the more inclined we would be to adopt a human to human-like empathic attitude toward it. Intuitively, the correlation could have been expected but actually the assumption was not so obvious as it seemed. Indeed, in the phylogenetic thinking, overall similarity (the external features we do perceive) is not phylogenetic relatedness (ex. the coelacanth is perceived more similar to the trout than to us, whereas it is more closely related to us than to the trout). It is interesting to note that, in spite of this difficulty, overall external similarity as it generates an anthropomorphic stimuli, is still globally correlated to phylogenetic relatedness.

Consistently with the anthropomorphic stimuli hypothesis, the overall linear correlation between empathic perceptions and phylogenetic divergence time suggests differences of degree, and not differences in kinds, in the perceptions we have of the different organisms. Indeed, our data do not show any break in our empathic perceptions that would explain the customary ethical stances opposing the intrinsic values of humans versus other organisms (ex. Abrahamic religions, humanism), tetrapods vs “fishes” (ex. pesco-vegetarianism), animals vs plants (ex. antispecism, veganism) or vertebrates vs non-vertebrates (ex. various system of regulations promoting animal welfare). In such representations, values manage relationships between us and other species in terms of oppositions, while our senses perceive a gradient of shared features between us and other species. Overall, these results suggest that raters recorded what is shared in the realm of perceptions, rather than mobilizing oppositions in the realm of ethical values. Likewise, we noticed that despite the fact that some rater’s traits (such as opinions on the value of an animal’s life comparatively to those of a human) can have an effect on empathy scores, their values remain overall strongly correlated with the time of divergence.

Interestingly, the retrospective inflexion (estimated at 611.1 Mya, 95% CI: 518–703 Mya) and the stagnation of the empathic perceptions curve coincides with the transition from gnathostomes (jawed vertebrates) to non-gnathostomes (lampreys and all the others clades whose divergence from us is equal or superior to 615 Mya). Nevertheless, such an estimate is unprecise and should be considered with caution. The stagnation of our perceptions might also correspond to the prebilaterian organisms (in our dataset, all the sampled clades that have diverged from our lineage 824 Mya or earlier). Indeed, bilaterians, to which we belong, are characterized by a bilateral symmetry, with a ventrodorsal and an anteroposterior axis. Most often, they are mobile and have a head (concentration of the mouth, sense organs, and nerve ganglia at the front end). In contrast, clades having diverged from our lineage prior to bilaterians (cnidarians, fungi and plants in the present study) are lacking all these external traits and are most often sessiles. The plesiomorphic anatomical organization of these neither heads nor tails organisms can be destabilizing from a perceptual point of view: It is almost impossible to spontaneously establish structural or behavioral homologies connecting them to us, likely reducing our empathic projection ability to its minimum. Accordingly, several bilaterian organisms having secondarily lost externally visible bilateral symmetry (echinoderms) or undergone spectacular changes of their anatomical organization (tunicates and bivalves) present minimal empathic scores among bilaterians (their empathic scores are actually equivalent to those attributed to non-bilaterian organisms, what may have contributed to the shift of the inflection point of the curve toward a more recent time). Among the macroscopic organisms present in our sampling, such a low level of empathy is interpreted as the most basic anthropomorphic signal, and may correspond with the recognition of an entity as a living being. Overall these results suggest that humans are relatively indifferent to organisms that do not show obvious signs of antero-posterior and dorso-ventral differentiations.

Shift between empathy and compassion

The extension of altruistic intentions (eg. sympathic or compassionate behaviours) to other organisms remains enigmatic from an evolutionary perspective, especially if we consider the latter as potential competitors, predators or as a valuable food resource for our species23.

Our data shows that empathy and compassion scores are significantly correlated to each other, and that both decrease with divergence time. These results were relatively expected as empathy is known to promote compassionate responses, although the neuronal networks recruited by each of these mental states have been shown to be distinct19.

Nevertheless, the trends obtained in these two analyses differ in several ways (Fig. 4):

(i) the correlation with divergence time is less pronounced for compassion scores than for empathy scores, and the decrease in scores with divergence time is slower for compassion than for empathy; (ii) the retrospective inflexion and the stagnation of the compassion scores curve seems to occur more recently than for the empathy scores (564.9 Mya for compassion scores versus 611.1 Mya for empathic scores, SI Appendix, Figs. S1 and S2); (iii) recorded response times are significantly higher for the compassion test, suggesting here a greater hesitation from the raters, but the differences in response time for each type of question is remarkably steady and independent from the phylogenetic distance between two species (Fig. 3B); (iv) some features of the evaluators (e.g., diet) have a confounding effect on the probability of choosing the closest phylogenetically related species that is more pronounced for compassion scores than for empathy scores (Fig. 3A, SI Appendix, Tables S2 and S3); and finally, v) for few taxa only, the decisions made by the raters in the compassion questionnaire are strikingly dissociated from the empathic perceptions they felt (Fig. 4). Indeed, although empathic scores attributed to tick and oak tree are relatively well corresponding to those obtained for the others protostomians and plants, respectively, their compassion scores are notably disconnected from those attributed to their relatives (strikingly lower for the tick and higher for the oak). The compassion score given to the tick is actually so low (well below the plateau formed by all the other low compassion score species) that it could be tempting to consider this result as a sharp expression of antipathy rather than as a mere lack of compassion. The strong aversion to parasitic species is not surprising given the threat they represent, and might explain the observed dissociation between empathic perceptions and compassionate responses. However, this trivial interpretation is counterbalanced by the fact that another potentially threatening species, the great white shark, reached compassion score relatively high in comparison with both its empathic score and phylogenetic distance from humans. The high compassion score for the oak tree also represents an outlier difficult to interpret. The imposing size of trees, their slow growth and long lifespan, their upright shape vaguely reminiscent of a human silhouette or their symbolic weight (which might itself results from the biological properties previously mentioned) are among the possible factors explaining the strong affective bond with trees, despite the obvious difficulties of being in empathy with a plant. Interestingly, the oak and the white shark have in common to be large sizes organisms, a trait that has been shown to positively influence our taxonomic preferences within vertebrates8,9.

Overall, these results led us to consider that compassionate responses, although strongly structured by intuitive empathic perceptions, nevertheless tend to be modulated by the personal ethical inclination toward non-human organisms and by the knowledge we have acquired about each species. Therefore, the compassion score as developed in our study is likely not a strict measure of the intensity of our spontaneous compassionate impulse. Whereas the empathic questionnaire is morally and affectively neutral (impression to better understand the emotions of one of the species presented in each pair), the compassion questionnaire was designed to involve emotionally the raters as much as possible. It is dilemmatic and virtually engaging their responsibility, since choosing to save one individual of the pair indirectly implies the sacrifice of the remaining one. At the end of the test, several raters have even spontaneously informed us about the discomfort perceived during certain choices they had to make. For these reasons, it would likely be more accurate to consider the compassion score as a complex expression of spontaneous emotional responses (the death of which of these two individuals would affect me the most?) mitigated by ethical considerations (which one deserves the most to survive?). Nevertheless, despite the probable intervention of reason in this rebalancing, it is remarkable to note that compassion scores remain closely linked to our spontaneous empathic perceptions and our phylogenetic proximity with a given organism.

Sympathy beyond the confines of man

Phylogenetic distance separating us from a given organism is a key parameter to explain our predisposition to connect emotionally with the different life forms. This finding supports the hypothesis of a significant biological component at the origin of our taxonomic preferences, although additional studies involving non-occidental raters (ex. hunter-gatherer or pastoral societies) would be necessary to ensure this trend can be generalized to the whole humankind. The fluctuations of our affective preferences are likely corresponding to the amount of traits shared with humans, gradually acquired over the long term evolution of the lineage leading to us, and that are involved in the intraspecific recognition of our fellow human beings. To some extent, such anthropomorphic stimuli induced by other organisms could therefore mobilize a cognitive circuitry that is usually at work in human relationships. The emotional reactions and prosocial behaviors they may promote would therefore be all the stronger as the species is close to us, as it shares with us more of these traits.

This phenomenon evokes similarities with the interspecific behavioral diversions episodically reported in other vertebrates providing parental care. Incidental cases of interspecific adoption - most often between relatively closely related species - are well documented in mammals and birds24,25. Some birds, such as the cuckoos (Cucculus sp.) have even turned these behavioral flaws at their advantage, through a successful brood parasitic way of life, in forcing the adoption of their offspring by parents from another species26. However, it may be reductive to consider the derivation of human prosocial traits from the sole perspective of a selective disadvantage. Our interactions with other organisms are highly diversified and little is known about the real impact our emotions toward them may have had on the human evolution. Our empathic skills may have for instance offered to early hominids the advantage to better anticipate the reactions of wild mammals, either to facilitate their hunt or to assess instantaneously and individually their mood and the danger they may represent. Likewise, our compassionate impulses may have pushed our ancestors to rescue injured or hungry animals, or to adopt young orphaned animals. To what extent could such altruistic interactions between humans and animals have preceded and contributed to the emergence and the long-run development of the multiple domestication episodes remains unknown. What do we know, for instance, about the cognitive predispositions and the motivations that may have allowed humans to make the dog – proverbially presented as our best friend – the very first of the domesticated species?