Abstract

Diversity is widely known to fuel adaptation and evolutionary processes and increase robustness at the population, species and ecosystem levels. The Neo-Darwinian paradigm proposes that the diversity of biological entities is the consequence of genetic changes arising spontaneously and randomly, without regard for their usefulness. However, a growing body of evidence demonstrates that the evolutionary process has shaped mechanisms, such as horizontal gene transfer mechanisms, meiosis and the adaptive immune system, which has resulted in the regulated generation of diversity among populations. Though their origins are unrelated, these diversity generator (DG) mechanisms share common functional properties. They (i) contribute to the great unpredictability of the composition and/or behavior of biological systems, (ii) favor robustness and collectivism among populations and (iii) operate mainly by manipulating the systems that control the interaction of living beings with their environment. The definition proposed here for DGs is based on these properties and can be used to identify them according to function. Interestingly, prokaryotic DGs appear to be mainly reactive, as they generate diversity in response to environmental stress. They are involved in the widely described Red Queen/arms race/Cairnsian dynamic. The emergence of multicellular organisms harboring K selection traits (longer reproductive life cycle and smaller population size) has led to the acquisition of a new class of DGs that act anticipatively to stress pressures and generate a distinct dynamic called the “White Queen” here. The existence of DGs leads to the view of evolution as a more “intelligent” and Lamarckian-like process. Their repeated selection during evolution could be a neglected example of convergent evolution and suggests that some parts of the evolutionary process are tightly constrained by ecological factors, such as the population size, the generation time and the intensity of selective pressure. The ubiquity of DGs also suggests that regulated auto-generation of diversity is a fundamental property of life.

Highlights

  • Reviewed by: Ye Deng, Research Center for Eco-Environmental Sciences (CAS), China Jomar Fajardo Rabajante, University of the Philippines Los

  • A growing body of evidence demonstrates that the evolutionary process has shaped mechanisms, such as horizontal gene transfer mechanisms, meiosis and the adaptive immune system, which has resulted in the regulated generation of diversity among populations

  • In keeping with this assumption, numerous examples of tightly regulated mechanisms generating individual genetic and phenotypic diversity have been described among prokaryotes, parasites and complex multicellular organisms. These mechanisms seem to play a key role in the evolution of biological systems as well as in the dynamics of the host–pathogen relationship. Their ubiquity suggests that they are indispensable to adaptation to environmental stress, and that regulated autogeneration of diversity must be considered as a fundamental trait of biological systems

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Summary

Eric Muraille*

Laboratoire de Parasitologie, Faculté de Médecine, Université Libre de Bruxelles, Brussels, Belgium. A growing body of evidence demonstrates that the evolutionary process has shaped mechanisms, such as horizontal gene transfer mechanisms, meiosis and the adaptive immune system, which has resulted in the regulated generation of diversity among populations. Though their origins are unrelated, these diversity generator (DG) mechanisms share common functional properties. Prokaryotic DGs appear to be mainly reactive, as they generate diversity in response to environmental stress They are involved in the widely described Red Queen/arms race/Cairnsian dynamic.

THE FUNDAMENTAL QUESTION OF HOW AND WHY DIVERSITY IS GENERATED
THE IMMEASURABLE DIVERSITY OF LIVING ENTITIES
GENERATION OF GENETIC DIVERSITY AMONG PROKARYOTES
MULTICELLULAR EUKARYOTES ACQUIRED INHERITABLE PHENOTYPIC DIVERSITY GENERATORS
THE TWO QUEEN HYPOTHESIS
COMMON CHARACTERISTICS OF DIVERSITY GENERATORS
THE ISSUE OF THE SELECTION OF DIVERSITY GENERATORS DURING EVOLUTION
OVERALL CONCLUSION
THEORETICAL PREDICTIONS
Constitutive Constitutive Constitutive Constitutive Anticipative
Findings
SOCIETAL IMPLICATIONS
Full Text
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