Isolating and quantifying the role of developmental noise in generating phenotypic variation

Maria Kiskowski, Tilmann Glimm, Nickolas Moreno, Tony Gamble and Ylenia Chiari

PLOS Computational Biology, 2019, vol. 15, issue 4, 1-31

Abstract: Genotypic variation, environmental variation, and their interaction may produce variation in the developmental process and cause phenotypic differences among individuals. Developmental noise, which arises during development from stochasticity in cellular and molecular processes when genotype and environment are fixed, also contributes to phenotypic variation. While evolutionary biology has long focused on teasing apart the relative contribution of genes and environment to phenotypic variation, our understanding of the role of developmental noise has lagged due to technical difficulties in directly measuring the contribution of developmental noise. The influence of developmental noise is likely underestimated in studies of phenotypic variation due to intrinsic mechanisms within organisms that stabilize phenotypes and decrease variation. Since we are just beginning to appreciate the extent to which phenotypic variation due to stochasticity is potentially adaptive, the contribution of developmental noise to phenotypic variation must be separated and measured to fully understand its role in evolution. Here, we show that variation in the component of the developmental process corresponding to environmental and genetic factors (here treated together as a unit called the LALI-type) versus the contribution of developmental noise, can be distinguished for leopard gecko (Eublepharis macularius) head color patterns using mathematical simulations that model the role of random variation (corresponding to developmental noise) in patterning. Specifically, we modified the parameters of simulations corresponding to variation in the LALI-type to generate the full range of phenotypic variation in color pattern seen on the heads of eight leopard geckos. We observed that over the range of these parameters, variation in color pattern due to LALI-type variation exceeds that due to developmental noise in the studied gecko cohort. However, the effect of developmental noise on patterning is also substantial. Our approach addresses one of the major goals of evolutionary biology: to quantify the role of stochasticity in shaping phenotypic variation.Author summary: The observable characteristics of an organism make up its phenotype. Variation among phenotypes is due to genetic differences, environmental factors and developmental noise (effects due to inherent stochasticity) during development. We used mathematical models to investigate the contributions of variation of the developmental process due to genetic and environmental factors (treated in this work as a single unit) versus developmental noise (unavoidable variation within the developmental program) to the development of pigment patterns on gecko heads. We found that for our cohort, the proportion of phenotypic variation due to variation in the unit composed of genotypic and environmental variation is larger than that due to developmental noise. Furthermore, by allowing the parameters of the mathematical model to vary, we generated the full extent of potential phenotypic pattern variation that could occur on the head of geckos. This serves to further study the influence of the buffering mechanisms (canalization, selection, and developmental stability) limiting phenotypic variation. This approach can be applied to any regular morphological trait that results from self-organized processes such as reaction-diffusion mechanisms, including the frequently found striped and spotted patterns of animal pigmentation patterning, patterning of bones in vertebrate limbs, and body segmentation in segmented animals.

Date: 2019
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Persistent link: https://EconPapers.repec.org/RePEc:plo:pcbi00:1006943

DOI: 10.1371/journal.pcbi.1006943

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