Isolating and Quantifying the Role of Developmental Noise in Generating Phenotypic Variation

Abstract

Phenotypic variation in organisms is typically attributed to genotypic variation, environmental variation, and their interaction. Developmental noise, which arises from stochasticity in cellular and molecular processes occurring during development when genotype and environment are fixed, also contributes to phenotypic variation. The potential 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 phenotypic variation due to genotype and environment, 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 genetic and environmental variation 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, the component of variation due to genotype and environment exceeds that due to developmental noise in the studied gecko cohort. However, the effect of developmental noise on patterning is also substantial. 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, body segmentation in segmented animals. Our approach addresses one of the major goals of evolutionary biology: to define the role of stochasticity in shaping phenotypic variation.

Ecological, behavioral, and phylogenetic influences on the evolution of dorsal color pattern in geckos*

“…In contrast plain geckos transition first to stripes, and only fade to plain again from a spotted phenotype. This result mirrors the results of mathematical models of pattern formation and evo-devo results that demonstrate how, once a pigment pattern generating mechanism is operational, minor alterations to the developmental process are required to produce marked phenotypic differences (Murray and Myerscough 1991;Chang et al 2009;Allen et al 2013;Dhillon et al 2017;Kiskowski et al 2019).…”

Capturing and analyzing pattern diversity: an example using the melanistic spotted patterns of leopard geckos

“…Indeed, we can conceptualize abstract sets of possible patterns that can be attained under the same combination of environmental and genetic conditions, but with the random contribution of developmental noise. In a previous work, we have called this set a ‘phenotype cloud’ (Kiskowski et al 2019); see Figure 9 below. In our case, it is a subset of a 14-dimensional pattern space.…”

“…Since the distribution function for random noise is completely unknown, and we only have two sample points for each instance - the pairs of front legs or the pairs of back legs for each individual-, the actual shapes of these phenotype clouds are unclear. However, in the context of stochastic mathematical models of pattern formation, such model-dependent phenotype clouds can be determined computationally (Kiskowski et al 2019), which then allows us to test such model prediction against the empirical data.…”

“…This species is commonly bred in captivity to obtain distinct colors and color patterns, a major advantage when trying to unveil the mechanisms producing variation at these traits (Cieslak et al 2011). Furthermore, our previous work on color patterns on the head of this species (Kiskowski et al, 2019) suggests that developmental noise may be an important contributor to its variation.…”

“…The data capture and analysis methods presented here can also be applied to study variation in color pattern elements for developmental, ecological and evolutionary purposes in other organisms. Furthermore, our previous work used mathematical modeling of the process of skin pattern formation to elucidate the influence of developmental noise on patterning (Kiskowski et al, 2019). Many different other mathematical models for skin patterning have been proposed (e.g.…”