Evolutionary thanatology

Abstract

Societies, including those of humans, have evolved multiple ways of dealing with death across changing circumstances and pressures. Despite many studies focusing on specialized topics, for example necrophoresis in eusocial insects, mortuary activities in early human societies, or grief and mourning in bereavement, there has been little attempt to consider these disparate research endeavours from a broader evolutionary perspective. Evolutionary thanatology does this by adopting an explicit evolutionary stance for studies of death and dying within the sociological, psychological and biological disciplines. The collection of papers in this themed issue demonstrates the value of this approach by describing what is known about how various nonhuman species detect and respond to death in conspecifics, how problems of disposing of the dead have evolved in human societies across evolutionary time and also within much shorter time frames, how human adults' understanding of death develops, and how it is ultimately reflected in death-related language. The psychological significance and impact of death is clearly seen in some species' grief-like reactions to the loss of attachment figures, and perhaps uniquely in humans, the existence of certain psychological processes that may lead to suicide. Several research questions are proposed as starting points for building a more comprehensive picture of the ontogeny and phylogeny of how organisms deal with death.

This article is part of the theme issue ‘Evolutionary thanatology: impacts of the dead on the living in humans and other animals’.

Death could not be more profound a subject for the biological sciences. The treatment of the corpse, and the effect of an organism's death on its surviving conspecifics, are core research topics for biological and social scientists, clinical practitioners, and philosophers, for myriad reasons including death's universality, inevitability, irreversibility, and its social and behavioural consequences. Many of us fear death—or at least dying in pain—and as we shall see, even our languages reveal how deep-rooted our concern with it is; the moral standing of the dead can be profound and exert considerable agency among the living, and self-induced death remains a considerably controversial moral and social issue. Despite this, however, as several of the contributors to this themed issue note, social and cultural trends over the last century have distanced most of us from the direct experience of death, and have often fostered a concern to shield children from exposure to it. The result has been the replacement of direct experience and explicit reference by a complex system of culturally varied euphemisms that are usually aimed at masking death or denying its terminal effects [1].

Studying the antecedents, causes and sequelae of death in the animal kingdom and over the long term should, we suggest, form one of the most profound scientific endeavours. Many disciplines have contributed specific perspectives on these, in species ranging from bacteria to insects, birds to aquatic and terrestrial mammals, and anthropoid primates including humans. The literature in these disparate fields, comprising observational, experimental, clinical and sociological studies, is already voluminous; however, thanatology—the academic study of death and dying—has largely lacked a broad evolutionary perspective that could draw these fields together.

We formally propose here the field of evolutionary thanatology. We believe that now is a highly appropriate time to do so, developing a more explicit evolutionary consideration of all aspects of studies of death and dying across the biological and sociological fields. Many volumes have been published that are devoted to bereavement, grief, and to the development of ‘funerary’ activities in both early and modern humans (e.g. [2–5]), but little attention has been paid to the evolutionary roots and development of many of the death-related activities that have been observed in ancient, recent and modern human societies, and to their psychological foundations and significance. Major changes in human funerary activities can be traced not only over thousands of years [6], but also within much shorter time frames [1]; examples include an increasing distance from the experience of death and funerary treatment of the corpse, by way, for example, of the increasing outsourcing of funeral services, smaller funeral gatherings, and new ways of disposing of corpses as a result of increasing urbanization and industrialization [7]. The use of online social media has played an increasing role in the dissemination of death notices and expressions of condolences and commemoration, essentially a digitalization of funerary activity, and in the USA some drive-through funeral parlours are even tailored to allow mourners to pay their respects without leaving their car. Funerals and memorial events for dead nonhuman animals (not only pets) are becoming increasingly popular in various countries [8], and in Japan this extends to defunct (‘dead’) robotic dogs, whose parts (‘organs’) may be removed and donated to other defective robots [9] (figure 1). Clearly, such rapid and profound changes in how we treat the dead, and indeed even in what our concept of ‘dead’ might mean, reflect cultural developments that fall within the scope—if at one extreme—of evolutionary thanatology.

Figure 1.

A funerary ceremony for robots, Chiba Prefecture, Japan, April 2018. Photo credit: Kei Oumawatari/28Lab.

But where to start? As we shall see, the recognition of death, and responses to the corpse, can have chemical, emotional, rational and cultural bases. The evolutionary perspective we advocate requires a comparative approach, not just within but also across biological taxa. Our aims should be ambitious. What, then, do observations of insects, birds and nonhuman mammals contribute to modern human thanatology? Is it justifiable to seek links between complex modern beliefs and practices and the chemically determined responses of insects or emotionally variable responses of mammals? Can one distinguish discrete packages of responses, perhaps correlated with distinct animal classes, orders, families, and genera? If so, are certain categories or ‘levels’ of thanatological behaviour predictable under given biological and social circumstances? Under what circumstances do taxa come under selection for evolution of their treatment of the dead? How do the dead impact on the living in various species, and how important is this to the expression of behaviour towards the corpse? A coherent collection of papers that address such issues will be an important first step on the road to setting out an agenda for the emerging field of evolutionary thanatology, and we outline a more specific set of research questions at the end of this paper.

Currently, most thanatology-related reports comprise isolated publications in specialist journals (e.g. in archaeology, primatology, zoology, psychology, sociology or human thanatology). Although it is increasingly rich and nuanced, and despite some broader accounts aimed at a general audience (e.g. [10]), this literature provides us with mostly unconnected glimpses of ‘crow funerals’, ‘elephant graveyards’ and ‘Neanderthal burials’, with no rigorous investigation of their intra- or interspecific significance or examination of the evolutionary connections between them. Although, as we shall see from several contributions, current thanatological understanding is for most taxa incomplete and even poor, the available literature does provide a valuable set of studies on which to base preliminary hypotheses for an explicit evolutionary thanatological perspective with which to address these lacunae. From our own research on responses to dead individuals in chimpanzees and early humans [6,11,12] the three of us have become increasingly aware that a cross-field fertilization is critical for this new thanatology. Hence, to provide comprehensive and balanced coverage, this themed issue presents a broad survey of non-human responses to the dead, including corpse avoidance and disposal mechanisms in social insects, exploratory interactions with deceased companions in corvids, and caretaking responses to dying and dead individuals in mammals including cetaceans and primates. Contributions also address the evolution of funerary activities in ancestral humans, cultural variations in funerary practices in prehistoric to modern humans, and related phenomena including suicide, infanticide, ‘cannibalism’, developments in the treatment of grief, cognition, and linguistic and philosophical underpinnings of humans' perception of and activities towards the dead, which take us from the chemical to the cultural realm.

An obvious point of departure is the mechanisms by which animals detect that death has occurred, and at what stage they are cognizant of it. Drawing on evolutionary thanatology's broad taxonomic comparison of non-human animals' responses to death and the deceased, Goncalves & Biro [13] explore the cognitive and sensory bases for detecting life and death in others across invertebrate and vertebrate taxa, seeking phylogenetically ancient as well as more derived mechanisms behind the responses exhibited. When vertebrate taxa encounter dead conspecifics they are confronted by conflicting data; the brain's imperfect agency system will retain notions of the animacy of the deceased, albeit in the absence of any signs of animacy. The authors suggest that the resulting ‘animacy detection malfunction’ is the mechanism that unites the drivers of responses to the dead in the vertebrate taxa examined. They argue for the integration of approaches from a variety of disciplines—including those as diverse as cognitive science and robotics—as a way of advancing the field of evolutionary thanatology.

The eusocial insects present a remarkable array of ways in which the living deal actively and efficiently with corpses. Sun et al. [14] emphasize the risks of disease from dead individuals in densely populated, enclosed colonies of ants, termites and bees; and describe the often sophisticated and complex ways in which these risks are managed, largely based on olfactory cues. It is apparent from their review that variable causes of death will affect the specific ways in which the corpse is treated, introducing a number of behaviours that must, therefore, have deep evolutionary roots, notably necrophobia (avoiding the corpse), necrophoresis (removal of the corpse from the colony), intraspecific necrophagy (cannibalism) and entombment (burial, elsewhere referred to as necroclaustralisation). In an evolutionary sense the eusocial insects, therefore, provide a remarkably variable core set of basic responses to the dead, from which further elaboration is possible over a number of trajectories.

Swift & Marzluff [15] study the drivers of tactile and other interactions with the dead, through controlled experiments with wild American crows. By presenting live crows with taxidermy-prepared specimens in various postures, they find that tactile contacts are rare and typically take the form of aggressive or sexual interactions, while the more frequent alarm calling response suggests correct identification of the specimens as being dead. The extreme manifestations of aggressive and sexual responses to the corpse, which in the case of crows may derive from an inability to mediate between conflicting stimuli, can also be traced among primates and early humans, perhaps providing an evolutionary basis for expression of the common conflicting emotions of anger and sorrow as human responses to death.

These interactions with the corpse are not restricted to the terrestrial realm. Reggente and colleagues [16] provide a compendium of more than 100 reported cases of responses to conspecific death events among aquatic mammals—most of which comprise behaviour towards deceased young—and perform a comprehensive quantitative treatment to seek individual and social variables that predict the type of response exhibited. Cetaceans and non-cetaceans both react to death, but in distinct ways; whereas the latter protect their dead from attack, cetaceans carry the corpse, a difference that may relate to the relative maternity investment (short in non-cetaceans), and is reminiscent of the effects of the parent–offspring bond on corpse management observable among primates. Reggente et al. identify characteristics such as levels of alloparental care and calf dependence as variables that shape behaviour towards the dead in different species, for example by increasing the length and intensity of caretaking directed at deceased young.

The parent–offspring bond takes centre stage again in Watson & Matsuzawa's [17] discussion of the phylogeny of maternal responses towards dead infants among non-human primates. In their review they identify varied responses among apes and monkeys including grooming, protection of the corpse, and filial cannibalism. As in crows, the wide range of these responses is notable. They argue that to elucidate proximate and ultimate drivers of these varied responses the detailed reporting of data from a diverse range of species will be needed. To facilitate the development of evolutionary thanatology they propose explanatory hypotheses for these behaviours, and provide a systematic framework for testing alternative hypotheses through the quantitative coding of post-mortem behaviour.

Anderson [18] focuses specifically on chimpanzees, reviewing the literature and describing the various ways in which they can learn about death in conspecifics and other species. As in Sun et al.'s analysis of eusocial insects, his review of causes of death raises the question of to what extent cause is reflected in the behaviour towards the corpse. Based on chimpanzees' known cognitive and empathic abilities, Anderson notes that they are likely to be aware that death is characterized by a cessation of function, and that it is irreversible, traits that, as we shall see, modern human children possess by the age of 10. Anderson suggests that with sufficient personal experience of dangerous situations, and through witnessing injurious or fatal events in others, these great apes may construct a concept of death that shares several of the components of adult humans' death concept, a notion picked up by Pettitt (see below). As with other contributors, Anderson notes a desire for researchers to pay more attention to cultural (i.e. inter-group) variations in practice.

Several contributors take us into the complexities of the modern world. Shimane [7] is interested in how modernization over the last century has impacted on funerary practices. His quantitative analysis of contemporary practices in five east and southeast Asian countries reveals that in the context of relentless population migration and rise of average age at death, death-related services have become increasingly commoditized and outsourced over a very short period of time, alongside a growing disengagement of local communities from their own funerary ceremonies. Thus, he documents how the evolution of human funerary practices, which began with simple necrophoresis, is undergoing rapid and significant change in the industrialized world.

This rapid pace of change in modern, industrialized societies has altered children's exposure to death, with changes in multiple direct and indirect factors variably affecting their acquisition of death concepts. In their discussion of the changing weight of these factors, Longbottom & Slaughter [19] highlight the importance of direct experience (including the deaths of animals), parental communication, and media portrayals in children's developing concept of death. They conclude with recommendations for enhancing children's understanding and readiness to cope with bereavement. Harris [20] takes a developmental psychologist's perspective on children's concepts of death. By the age of 10 children know that it is inevitable for all living creatures, and irreversible. Harris argues in particular that children adopt two parallel concepts of death: one from a biological viewpoint in which the dead are corpses, and another in which they are thought of as continuing in another existence, despite being deceased in this one. Such continuing ties to the dead manifest, among other things, in burials. Given their proximity to the living, he argues, these may ratchet up the accumulation of memories about the dead, and hence deepen awareness of antecedent generations.

In an agenda for how Palaeolithic archaeology may contribute to wider evolutionary thanatology, Pettitt [21] shares the interest in the origins of burial, reading the earliest burials of Neanderthals and Homo sapiens in the context of a developing sense of persistent social space. Picking up from observations such as Anderson's, he argues that a core set of mortuary activities occurring face-to-face—similar to those documented for modern primates in this volume—began to extend into the landscape as early human group size and social complexity grew to the extent that peripersonal mortuary behaviours were no longer sustainable. He sets out a number of research questions for Palaeolithic thanatology. Chronologically, Orschiedt [22] follows on, reviewing the burial practices of the European Final Upper Palaeolithic and Mesolithic, the stable but diverse practices of Europe's last prehistoric hunter-gatherers. He observes geographical variation in whether burial was practised or not, and differences in extreme states of corpse processing (disarticulation, as opposed to burial). Most importantly, he identifies the appearance of ‘cemetery-like’ clusters of relatively large numbers of burials, a pattern that one can also see in North Africa and the Near East. He sees considerable continuity between the first cemeteries of the last few thousand years of the Pleistocene and the Mesolithic communities of early and mid-Holocene Europe, while recognizing an increasing diversity of practice among the latter. Matsumoto [23] takes us even further into the cultural evolution of burials, reviewing the relationship between the living and the dead in Japanese prehistory. The dead seem to have continued to play a central role in the social systems of the living among Jomon hunter-gatherers, evidenced, she argues, by funerary practices that changed significantly alongside major demographic thresholds. With the first population increase in the Middle Jomon period, the first cemeteries were created, as a response to increased sedentism. Following a population disruption, subsequent practices focused on burials placed centrally in circular planned settlements; after these, in turn, collective secondary burials were emplaced in newly established settlements. All of these are clear examples of the centrality of the dead to kinship systems, and the effects of population movement and disruption on the latter.

Not just our actions but also the ways we speak about death can inform us about how we think about it. In a powerful linguistic analysis, Husband [24] examines death-related verbs, which are remarkably prevalent in any language, to argue that death has a special significance in human cognition. Death-verbs are shown to exhibit different grammatical constraints compared to other verbs, and to do so consistently across different languages, suggesting that language surrounding death can reveal aspects of the evolution of mental representations of thanatological phenomena in humans. Perhaps the most profound indication that most societies believe—if unconsciously—in some kind of continued agency of the dead, is their persistence in the moral systems of the living. Luper [25] provides a philosophical treatment of the moral issues surrounding our treatment of the dead, asking if the dead have moral standing. By demonstrating that events that happen after an individual's death can indeed be good or bad for them (despite the fact that they are dead)—and thus by affecting their prudential interests it is possible for us to benefit or harm them posthumously—the dead can be argued to have moral standing.

Given that death constitutes the mental and physical cessation of an individual in the world, and as at some point in evolution individuals have come to know that they can choose when to end their existence within it, death has come to be imbued with considerable moral responsibility. Two papers focus on suicide. Noting that suicide constitutes a remarkable 1.4% of deaths worldwide—it is the leading cause of violent death—Humphrey [26] explores some of the psychological particularities of humans that might make the purposeful killing of oneself a uniquely human phenomenon. He contrasts ‘altruistic’ and ‘egoistic’ suicide, and explores how these puzzling behaviours have evolved. The suicide meme is highly infectious, and most suicides are egoistic—deriving from a desire to remove one's own mind from the world, a concern with personal escape, often with no concern for its effects on others. But how could this be adaptive, and how might attempts to deter it create cultural beliefs about death? O'Connor & Kirtley [27] note that, despite some 800 000 suicides globally per year, we are still unable to predict its imminence; it is a major public health concern. Commencing from the heuristic that suicide is a behaviour, built on precedents of ideation and intention, they present the ‘integrated motivational-volitional model’ of suicide, to explain how suicidal ideation can progress to completion of the act. The model focuses on interactions between negative feelings such as defeat or entrapment and other personal and environmental factors such as impulsivity, access to means, and exposure to suicide, with implications for preventive intervention.

Grief—and its emotional precursors—forms a central concern of thanatology, and although humans experience it as a natural response to bereavement, in many cases it may become pathological: it can persist, with little sign of the sufferer returning to normal functioning. Nakajima [28] provides a study of extreme cases of grief, through examples of persisting grief with high levels of acute symptoms. She traces developments in the understanding of normal and ‘complicated grief’, the latter of which can have profound mental health implications and act as one stimulus for suicide. Agreement on criteria for the identification of complicated grief is still lacking, hence research is required for its diagnosis and treatment.

The contributions to this themed issue understandably present a disparate set of behaviours, although there are surprisingly repeated themes that are shared by most and they provide fruitful opportunities for cross-disciplinary research. Studies across modern animal taxa will provide the spatial perspective; the long-term perspectives offered by archaeology will provide the time; and perspectives on the modern urban and industrial world will provide the extreme complexity. What do these disparate studies reveal? Certainly a surprising variability of responses to death and to the corpse in both terrestrial and aquatic realms, whereby responses vary with the relationship of the deceased to the living, the cause of death and condition of the corpse, and involving chemical, visual and tactile information gathering. We outlined some broad aims for evolutionary thanatology above; now, some more specific research questions for evolutionary thanatology emerge:

• — Is it feasible to construct a phylogeny of responses to death; what traits are phylogenetically ancient, and what ones derived?

• — Does the evolutionary diversification of responses to death/the corpse always follow an elaboration from chemical through emotional to cultural stimuli?

• — To what extent do cues in various sensory modalities elicit thanatological responses (including motoric and affective or emotional) in different taxa?

• — How variable can behaviours such as necrophobia, necrophoresis, necrophagy and necroclaustralisation be within a specific taxon? Are they applied to all of the deceased? If not, under what conditions are they applied?

• — Exactly how does social structure of the living—and the position of the deceased within this—determine the specific responses to death/the corpse? At what classificatory level/s can one identify this?

• — Can specific responses to death/corpses in a particular taxon be related to the specific nature of the death event? At what biological classificatory level/s can one identify this?

• — How are mechanisms for detecting, dealing with or denying the effects of death determined by evolving social environments?

• — As Humphrey eloquently puts it, how has natural selection got to grips with not being? At what point in evolution can one identify a specifically moral concern with suicide (and, we would add, murder)?

These questions are merely a sample; others, along with new ideas and methods for advancing knowledge of the evolution of responses to death will emerge from both ontogenetic and phylogenetic perspectives. Field workers have often been reluctant to report single case studies of death-related responses in animal societies given the perceived problem that they may be unique and hence unrepresentative of any ‘norms’. Why not? We must start somewhere, and uniqueness in a thanatological sense may be as important to document as norms. The accumulation and critical assimilation of such accounts, along with results of experimental studies such as those conducted in social insects and birds, will be of immense importance for organizing and assessing a holistic picture of the impacts of the dead on the living across evolutionary history. It is our hope that this volume will provide a valuable starting point in this endeavour, and we thank all contributors for taking this in the spirit intended.

Data accessibility

This article has no additional data.

Competing interests

We declare we have no competing interests.

Funding

We gratefully acknowledge support from The Daiwa Anglo-Japanese Foundation and a Durham University International Engagement grant (to P.P.), and Kyoto University Faculty of Primatology and Wildlife Science (to J.R.A.), for supporting the First Kyoto Workshop on Evolutionary Thanatology, Kyoto, March 2017 from which this themed issue grew.