Invisible Designers: Brain Evolution Through the Lens of Parasite Manipulation

Abstract

keywords behavior, brain evolution, hormones, neurobiology, parasite-host interactions, parasite manipulation abstract The ability of parasites to manipulate host behavior to their advantage has been studied extensively, but the impact of parasite manipulation on the evolution of neural and endocrine mechanisms has remained virtually unexplored. If selection for countermeasures has shaped the evolution of nervous systems, many aspects of neural functioning are likely to remain poorly understood until parasites-the brain's invisible designers-are included in the picture. This article offers the first systematic discussion of brain evolution in light of parasite manipulation. After reviewing the strategies and mechanisms employed by parasites, the paper presents a taxonomy of host countermeasures with four main categories, namely: restrict access to the brain; increase the costs of manipulation; increase the complexity of signals; and increase robustness. For each category, possible examples of countermeasures are explored, and the likely evolutionary responses by parasites are considered. The article then discusses the metabolic, computational, and ecological constraints that limit the evolution of countermeasures. The final sections offer suggestions for future research and consider some implications for basic neuroscience and psychopharmacology. The paper aims to present a novel perspective on brain evolution, chart a provisional way forward, and stimulate research across the relevant disciplines.

Toxoplasma gondii and Psychopathology: Latent Infection Is Associated with Interpersonal Sensitivity, Psychoticism, and Higher Testosterone Levels in Men, but Not in Women

“…The ability of parasites to hijack the nervous system of host organisms in a way that enhances parasite fitness whilst compromising host fitness is a topic of significant interest in evolutionary biology (Dawkins 1982;Geffre et al 2017;Del Giudice 2019). The importance of this study lies in providing an evolutionarily informed analysis on the endocrine mechanisms by which T. gondii influences the nervous system of its human hosts, including the development of psychopathological symptoms.…”

“…In this regard, previous literature has hypothesized that higher testosterone levels and the development of mental disorders could be an accidental by-product of chronic T. gondii infection (e.g., Flegr 2007;Brüne 2019). However, it seems that many symptoms associated with psychopathology could represent transmission-related benefits for T. gondii (Brüne 2019;Del Giudice 2019). For example, T. gondii infection blocks the innate aversion of rats for cat urine, increasing the likelihood of a cat predating a rat (Berdoy et al 2000).…”

“…Moreover, in recent years, latent toxoplasmosis has also been associated with the development of some mental disorders such as schizophrenia, obsessive-compulsive disorder, and suicidal tendencies (Torrey et al 2006;Flegr and Horáček 2019;Torrey and Yolken 2019), and there is evidence that testosterone feedback regulation could also be modulated by T. gondii (Flegr et al 2008;Del Giudice 2019). For example, T. gondii invades testes in male rodents and increases testosterone production (Del Giudice 2019).…”

Origin of Mutualism Between Termites and Flagellated Gut Protists: Transition From Horizontal to Vertical Transmission

“…Although there are numerous examples of parasites driving changes in host behavior, these are predominantly in parasites with complex life cycles (i.e., those that require more than one host species to complete their life cycle) (Combes, 1991;Perrot-Minnot and Cézilly, 2009), not the basic twostage life cycle of the flagellates in Cryptocercus. Selection may furthermore limit the evolution of host manipulation by any one microbial taxon in the gut microbiome, because of the large number of species and strains that compete with one another for space and resources (Johnson and Foster, 2018;Giudice, 2019).…”

Cell-Autonomous Immunity and The Pathogen-Mediated Evolution of Humans: Or How Our Prokaryotic and Single-Celled Origins Affect The Human Evolutionary Story

“…Since cell-autonomous defenses are hardwired into each cell, and each cell interacts with pathogens known and unknown, every physiological system bears the mark of direct past pathogen interactions. For decades, it has been understood that microorganisms and cell-autonomous immune responses to them alter human behavior and vice versa (Dantzer and Kelley 1989;Chiu et al 2013;Liu et al 2014;Stock et al 2017;Del Giudice 2019). Incorporation of the same biological relationships between pathogens, cell-autonomous defenses, and body system X extended to other physiological systems or traits at the center of the classic questions of human evolutionary biology (e.g., why does skin color vary in humans, why do primate placentae vary in shape and size, how did human bipedal locomotion evolve, how does primate bone and dental microstructure vary) can enrich and improve our understanding of why such features evolved (Robbins and Bakardjiev 2012).…”