Lassitude: The emotion of being sick

https://doi.org/10.1016/j.evolhumbehav.2019.09.002Get rights and content

Abstract

Our long co-evolutionary history with infectious agents likely began soon after the rise of the first single-celled organisms. This ongoing evolutionary arms race has generated complex host adaptations, many highly conserved, for resisting infection (e.g., innate and acquired immune systems, infection-sensitive developmental programs, sexual reproduction). A large body of evidence suggests that, in humans, pathogen-avoidance disgust is an emotion that motivates avoidance of cues associated with pathogens, thereby reducing infection. However, the question of whether there is an emotion that coordinates resistance to active infection has received less attention. We propose that lassitude is such an emotion. It is triggered by cues of active infection and coordinates the fight against infection by: (a) reducing energetically expensive movement to make more energy available to the immune system, (b) reducing exposure to additional infections and injuries that would compound the immune system's workload, (c) promoting thermoregulatory behaviors that facilitate immunity, (d) regulating food consumption to be beneficial for the host but detrimental to pathogens, and (e) deploying strategies that elicit caregiving behavior from social allies. Lassitude exhibits the core features of an emotion – it is triggered by cues of an adaptive problem (i.e., infection), generates a characteristic facial expression (e.g., slack facial muscles, drooping eyelids, slightly parted lips), and has distinct qualia (e.g., profound tiredness, reduced appetite, feelings of vulnerability, altered temperature perception, increased pain sensitivity). We outline the information-processing structure of lassitude, review existing evidence, suggest directions for future research, and discuss implications of lassitude for models of human evolution.

Introduction

The evolutionary arms race between infectious agents and their hosts probably began soon after the rise of the first living organisms. Even single-celled prokaryotes (i.e., bacteria and archaea) are perpetually co-evolving with the viruses that infect them (Jalasvuori & Bamford, 2008; Koskella & Brockhurst, 2014; Weitz, Hartman, & Levin, 2005). Infection-related selection pressures have generated and maintained multiple adaptations in complex multicellular organisms to reduce the fitness costs of infectious disease, including generalized immune mechanisms that are effective against multiple infection types (Akira, Uematsu, & Takeuchi, 2006; Lochmiller & Deerenberg, 2000), immune mechanisms that adjust to specific pathogenic organisms (Cooper & Alder, 2006; McDade, 2005), infection-sensitive developmental programs (Georgiev, Kuzawa, & McDade, 2016; Urlacher et al., 2018), and, arguably, sexual reproduction, cellular differentiation, and patterns of parent-offspring association (Liow, Van Valen, & Stenseth, 2011; Tooby, 1982). In the human lineage, evidence indicates a long co-evolutionary history with a variety of infectious organisms, including various kinds of bacteria, viruses, parasitic worms, and protozoans (Brinkworth & Pechenkina, 2013; Deschamps et al., 2016; Houldcroft & Underdown, 2016; Hurtado, Frey, Hurtado, Hill, & Baker, 2008). Infectious disease remains a major cause of morbidity and mortality for humans in contemporary subsistence and industrialized populations (Hill, Hurtado, & Walker, 2007; Holmes et al., 2017; Sugiyama & Chacon, 2000).

The threat of infectious disease poses two major sets of adaptive problems for host organisms: (1) how to prevent infection, and (2) how to fight infection when it occurs. Substantial evidence indicates that, in humans, pathogen-avoidance disgust provides a key solution to the first problem – it appears to limit infection by reducing contact with pathogen-associated substrates, individuals, and situations (Curtis, de Barra, & Aunger, 2011; Murray, Prokosch, & Airington, 2019; Oaten, Stevenson, & Case, 2009; Schaller, 2015; Tybur, Lieberman, Kurzban, & DeScioli, 2012). The innate and acquired immune systems are critical solutions to the second set of problems (Akira et al., 2006; Cooper & Alder, 2006), but the fight against infection poses additional adaptive problems that cannot be solved by innate and acquired immune responses alone.

We propose that the emotion lassitude (see Box 1) is triggered by cues of infection and coordinates the fight against infection by: (a) reducing engagement in energetically expensive movement in order to make more energy available for the immune system, (b) reducing exposure to additional pathologies that would compound the immune system's workload (e.g., injuries, poisoning, additional infections), (c) modulating thermoregulatory behaviors in ways that are conducive to effective immune function (e.g., promoting warmth-seeking behavior), (d) regulating food consumption in ways that are beneficial to the host but detrimental to pathogens, and (e) deploying strategies to elicit caregiving behavior from social allies (e.g., preferential contact, signaling of vulnerability). We hypothesize that lassitude is an evolutionarily conserved adaptation but also has derived features that evolved in the human lineage, due to distinctive aspects of our life history, sociality, and diet.

We recognize that non-infectious pathologies (e.g., injury, chronic disease, poisoning) probably also activate lassitude (or at least an overlapping suite of mechanisms). These non-infectious somatic insults pose many of the same adaptive problems as infectious disease, and they frequently activate some of the mechanistic pathways that trigger lassitude during infectious disease (Del Giudice & Gangestad, 2018; McCusker & Kelley, 2013). However, for the sake of brevity and clarity, we focus our discussion in this paper on lassitude triggered by infection with pathogenic organisms (e.g., bacteria, viruses, parasitic worms, protozoans).

Section snippets

Infectious disease poses a suite of adaptive problems

Infectious disease is a ubiquitous feature of life for most animals (Hart, 1990; Knoll & Carroll, 1999; Zuk, 1992). Humans are no exception. Infectious disease is a major driver of mortality among extant and ethnographically known human hunter-gatherers, causing between 20% and 85% of deaths in populations for which data are available (Blurton Jones, Hawkes, & O'Connell, 2002; Early & Headland, 1998; Hill et al., 2007; Hill & Hurtado, 1996; Howell, 1979; Jones, Smith, O'Connell, Hawkes, &

Lassitude: a coordinating mechanism to fight infection

We propose that lassitude is triggered by cues of active infection and coordinates the fight against infection by initiating a set of strategic regulatory changes that typically include: (a) reducing energetically expensive movement in order to make more energy available to the immune system, (b) reducing the risk of exposure to additional pathologies (infection, injury, poisoning) that would compound the immune system's workload, (c) promoting thermoregulatory behaviors that facilitate

Cues of infection

For the lassitude program to coordinate the fight against infection, it must be able to detect reliable cues of the threat level posed by current levels of pathogen load (see Fig. 1). These cues fall into two major categories: internal cues (e.g., pathogen-associated molecular patterns, activation of the immune system) and external cues (e.g., signs of infection in social conspecifics, the presence of pathogen-associated substrates).

Lassitude: a new emotion?

Our approach to characterizing lassitude is informed by Tooby and Cosmides' framework: “[the emotions] are the neurocomputational adaptations that have evolved in response to the adaptive problem of matching arrays of mechanism activation to the specific adaptive demands imposed by alternative situations” (Tooby & Cosmides, 2008, p. 117). Lassitude satisfies this definition of an emotion. It is a coordinating system that functions to orchestrate various mechanisms to solve the adaptive problem

Social support and immunity

Humans provide care to social allies during illness and injury (see section 2.2.5). This is an important buffer against the opportunity costs of reducing movement when sick. A compelling hypothesis to explain the placebo effect is that one function of visible illness symptoms is to elicit care from others (Steinkopf, 2015). When others provide care, the signaling function of the symptoms is fulfilled and the symptoms become less severe (ibid). We predict that cues of social support (or a lack

Conclusions

In this paper, we develop a theoretical account of lassitude as an emotion that coordinates the fight against infection. We review evidence suggesting that a signal detection system monitors cues of infection and integrates this information to estimate the threat level posed by current levels of pathogen load. When threat levels are high, the system sends a signal to various motivational systems, configuring them in ways that facilitate effective immunity and pathogen clearance. Each

Declarations of Competing Interest

None.

Funding

There were no specific grants that supported this research.

Acknowledgements

We thank Dr. Debra Lieberman for her insightful comments and suggestions on earlier versions of this paper. We are grateful to the reviewers for their thoughtful and detailed reviews.

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