The Diversity Paradox: How Nature Resolves an Evolutionary Dilemma

James M. Whitacre, Sergei P. Atamas

Adaptation to changing environments is a hallmark of biological systems. Diversity in traits is necessary for adaptation and can influence the survival of a population faced with novelty. In habitats that remain stable over many generations, stabilizing selection reduces trait differences within populations, thereby appearing to remove the diversity needed for heritable adaptive responses in new environments. Paradoxically, field studies have documented numerous populations under long periods of stabilizing selection and evolutionary stasis that have rapidly evolved under changed environmental conditions. In this article, we review how cryptic genetic variation (CGV) resolves this diversity paradox by allowing populations in a stable environment to gradually accumulate hidden genetic diversity that is revealed as trait differences when environments change. Instead of being in conflict, environmental stasis supports CGV accumulation and thus appears to facilitate rapid adaptation in new environments as suggested by recent CGV studies. Similarly, degeneracy has been found to support both genetic and non-genetic adaptation at many levels of biological organization. Degenerate, as opposed to diverse or redundant, ensembles appear functionally redundant in certain environmental contexts but functionally diverse in others. CGV and degeneracy paradigms for adaptation are integrated in this review, revealing a common set of principles that support adaptation at multiple levels of biological organization. Though a discussion of simulation studies, molecular-based experimental systems, principles from population genetics, and field experiments, we demonstrate that CGV and degeneracy reflect complementary top-down and bottom-up, respectively, conceptualizations of the same basic phenomenon and arguably capture a universal feature of biological adaptive processes.

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