Mosaic physiology from developmental noise: within-organism physiological diversity as an alternative to phenotypic plasticity and phenotypic flexibility

Abstract

A key problem in organismal biology is to explain the origins of functional diversity. In the context of organismal biology, functional diversity describes the set of phenotypes, across scales of biological organization and through time, that a single genotype, or genome, or organism, can produce. Functional diversity encompasses many phenomena: differences in cell types within organisms; physiological and morphological differences among tissues and organs; differences in performance; morphological shifts in external phenotype; and changes in behavior. How can single genomes produce so many different phenotypes? Modern biology proposes two general mechanisms. The first is developmental programs, by which single cells and their single genomes diversify, via relatively deterministic processes, into the sets of cell types, tissues and organs that we see in most multicellular organisms. The second general mechanism is phenotypic modification stemming from interactions between organisms and their environments – modifications known either as phenotypic plasticity or as phenotypic flexibility, depending on the time scale of the response and the degree of reversibility. These two diversity-generating mechanisms are related because phenotypic modifications may sometimes arise as a consequence of environments influencing developmental programs. Here, I propose that functional diversity also arises via a third fundamental mechanism: stochastic developmental events giving rise to mosaics of physiological diversity within individual organisms. In biological systems, stochasticity stems from the inherently random actions of small numbers of molecules interacting with one another. Although stochastic effects occur in many biological contexts, available evidence suggests that they can be especially important in gene networks, specifically as a consequence of low transcript numbers in individual cells. I briefly review known mechanisms by which organisms control such stochasticity, and how they may use it to create adaptive functional diversity. I then fold this idea into modern thinking on phenotypic plasticity and flexibility, proposing that multicellular organisms exhibit ‘mosaic physiology’. Mosaic physiology refers to sets of diversified phenotypes, within individual organisms, that carry out related functions at the same time, but that are distributed in space. Mosaic physiology arises from stochasticity-driven differentiation of cells, early during cell diversification, which is then amplified by cell division and growth into macroscopic phenotypic modules (cells, tissues, organs) making up the physiological systems of later life stages. Mosaic physiology provides a set of standing, diversified phenotypes, within single organisms, that raise the likelihood of the organism coping well with novel environmental challenges. These diversified phenotypes can be distinct, akin to polyphenisms at the organismal level; or they can be continuously distributed, creating a kind of standing, simultaneously expressed reaction norm of physiological capacities.