Origin of biomolecular games: deception and molecular evolution

Abstract

<jats:p>Biological macromolecules encode information: some of it to endow the molecule with structural flexibility, some of it to enable molecular actions as a catalyst or a substrate, but a residual part can be used to communicate with other macromolecules. Thus, macromolecules do not need to possess information only to survive in an environment, but also to strategically interact with others by sending signals to a receiving macromolecule that can properly interpret the signal and act suitably. These sender–receiver signalling games are sustained by the information asymmetry that exists among the macromolecules. In both biochemistry and molecular evolution, the important role of information asymmetry remains largely unaddressed. Here, we provide a new unifying perspective on the impact of information symmetry between macromolecules on molecular evolutionary processes, while focusing on molecular deception. Biomolecular games arise from the ability of biological macromolecules to exert precise recognition, and their role as units of selection, meaning that they are subject to competition and cooperation with other macromolecules. Thus, signalling game theory can be used to better understand fundamental features of living systems such as molecular recognition, molecular mimicry, selfish elements and ‘junk’ DNA. We show how deceptive behaviour at the molecular level indicates a conflict of interest, and so provides evidence of genetic conflict. This model proposes that molecular deception is diagnostic of selfish behaviour, helping to explain the evasive behaviour of transposable elements in ‘junk’ DNA, for example. Additionally, in this broad review, a range of major evolutionary transitions are shown to be associated with the establishment of signalling conventions, many of which are susceptible to molecular deception. These perspectives allow us to assign rudimentary behaviour to macromolecules, and show how participation in signalling games differentiates biochemistry from abiotic chemistry.</jats:p>

Distributed physiology and the molecular basis of social life in eusocial insects

“…The elaborate honey bee dance language for example, is a system of many signals coordinating the activities of two castes of bees based on completely honest communication. There are complex signaling games in other systems, in the context of sexual signaling for example, but in these cases a mixture of honest and dishonest signaling is present 81,82 .…”

Invisible Designers: Brain Evolution Through the Lens of Parasite Manipulation

“…Using psychoactive drugs to treat psychiatric symptoms is an attempt to alter behavior by pharmacological means. This is also what manipulative parasites do-even though, in the case of psychiatric treatment, the goal is to benefit the patient (Massey and Mishra 2018). If the human brain contains evolved countermeasures to manipulation, the implications for psychopharmacology could be profound.…”

“…To prevent parasites from infecting their cells, hosts can evolve decoy surface molecules-molecules that mimic those exploited by parasites, but fail to perform the same function or even trigger a defensive response when bound. This is one of the many forms of "molecular deception" that may take place between parasites and hosts (Massey and Mishra 2018). A well-studied example of decoy molecules in humans is carcinoembryonic antigen-related cell adhesion 3 (CEACAM3), which mimics the cell adhesion molecule and immune inhibitory receptor CEACAM1 (Zimmermann 2019).…”

“…Negative feedback is a basic building block of robust systems; it is also a general purpose strategy with little functional specificity. More sophisticated forms of reactive robustness can be implemented by specialized mechanisms designed to detect manipulation attempts and respond in flexible, strategic ways (see Weinersmith and Earley 2016;Massey and Mishra 2018). The first question to ask is: How can the brain detect a manipulation attempt?…”

“…If comparative molecular data are available for both the host and the parasite, it may be possible to reconstruct the coevolutionary process, and explore the temporal links between the evolution of putative host countermeasures and that of parasite strategies and responses (Table 1). Also, patterns of molecular diversity can provide indirect cues to the existence of host-parasite conflicts and arms races (Summers et al 2003; see also Massey and Mishra 2018).…”