We investigate a very simple model describing the evolution of protein-protein interaction networks via duplication and divergence. The model exhibits a remarkably rich behavior depending on a single parameter, the probability to retain a duplicated link during divergence. When this parameter is large, the network growth is not self-averaging and an average node degree increases algebraically. The lack of self-averaging results in a great diversity of networks grown out of the same initial condition. When less than a half of links are (on average) preserved after divergence, the growth is selfaveraging, the average degree increases very slowly or tends to a constant, and a degree distribution has a power-law tail. The predicted degree distributions are in a very good agreement with the distributions observed in real protein networks.
We demonstrate that protein–protein interaction networks in several eukaryotic organisms contain significantly more self-interacting proteins than expected if such homodimers randomly appeared in the course of the evolution. We also show that on average homodimers have twice as many interaction partners than non-self-interacting proteins. More specifically, the likelihood of a protein to physically interact with itself was found to be proportional to the total number of its binding partners. These properties of dimers are in agreement with a phenomenological model, in which individual proteins differ from each other by the degree of their ‘stickiness’ or general propensity toward interaction with other proteins including oneself. A duplication of self-interacting proteins creates a pair of paralogous proteins interacting with each other. We show that such pairs occur more frequently than could be explained by pure chance alone. Similar to homodimers, proteins involved in heterodimers with their paralogs on average have twice as many interacting partners than the rest of the network. The likelihood of a pair of paralogous proteins to interact with each other was also shown to decrease with their sequence similarity. This points to the conclusion that most of interactions between paralogs are inherited from ancestral homodimeric proteins, rather than established de novo after duplication. We finally discuss possible implications of our empirical observations from functional and evolutionary standpoints.
The mechanisms for the origin and maintenance of biological diversity are not fully understood. It is known that frequency-dependent selection, generating advantages for rare types, can maintain genetic variation and lead to speciation, but in models with simple phenotypes (that is, low-dimensional phenotype spaces), frequency dependence needs to be strong to generate diversity. However, we show that if the ecological properties of an organism are determined by multiple traits with complex interactions, the conditions needed for frequency-dependent selection to generate diversity are relaxed to the point where they are easily satisfied in high-dimensional phenotype spaces. Mathematically, this phenomenon is reflected in properties of eigenvalues of quadratic forms. Because all living organisms have at least hundreds of phenotypes, this casts the potential importance of frequency dependence for the origin and maintenance of diversity in a new light.
The possibility of complicated dynamic behavior driven by nonlinear feedbacks in dynamical systems has revolutionized science in the latter part of the last century. Yet despite examples of complicated frequency dynamics, the possibility of long-term evolutionary chaos is rarely considered. The concept of "survival of the fittest" is central to much evolutionary thinking and embodies a perspective of evolution as a directional optimization process exhibiting simple, predictable dynamics. This perspective is adequate for simple scenarios, when frequency-independent selection acts on scalar phenotypes. However, in most organisms many phenotypic properties combine in complicated ways to determine ecological interactions, and hence frequency-dependent selection. Therefore, it is natural to consider models for evolutionary dynamics generated by frequency-dependent selection acting simultaneously on many different phenotypes. Here we show that complicated, chaotic dynamics of long-term evolutionary trajectories in phenotype space is very common in a large class of such models when the dimension of phenotype space is large, and when there are selective interactions between the phenotypic components. Our results suggest that the perspective of evolution as a process with simple, predictable dynamics covers only a small fragment of long-term evolution. K E Y W O R D S :Adaptive dynamics, chaos, complex dynamics, high-dimensional phenotype space, logistic competition models.
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