Author
Listed:
- Maria Kiskowski
- Tilmann Glimm
- Nickolas Moreno
- Tony Gamble
- Ylenia Chiari
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.
Suggested Citation
Maria Kiskowski & Tilmann Glimm & Nickolas Moreno & Tony Gamble & Ylenia Chiari, 2019.
"Isolating and quantifying the role of developmental noise in generating phenotypic variation,"
PLOS Computational Biology, Public Library of Science, vol. 15(4), pages 1-31, April.
Handle:
RePEc:plo:pcbi00:1006943
DOI: 10.1371/journal.pcbi.1006943
Download full text from publisher
References listed on IDEAS
- Liana Manukyan & Sophie A. Montandon & Anamarija Fofonjka & Stanislav Smirnov & Michel C. Milinkovitch, 2017.
"A living mesoscopic cellular automaton made of skin scales,"
Nature, Nature, vol. 544(7649), pages 173-179, April.
- William L. Allen & Roland Baddeley & Nicholas E. Scott-Samuel & Innes C. Cuthill, 2013.
"The evolution and function of pattern diversity in snakes,"
Behavioral Ecology, International Society for Behavioral Ecology, vol. 24(5), pages 1237-1250.
Full references (including those not matched with items on IDEAS)
Most related items
These are the items that most often cite the same works as this one and are cited by the same works as this one.
- Gopal Murali & Ullasa Kodandaramaiah & John FitzpatrickHandling editor, 2018.
"Body size and evolution of motion dazzle coloration in lizards,"
Behavioral Ecology, International Society for Behavioral Ecology, vol. 29(1), pages 79-86.
- Elizabeth G Postema & Mia K Lippey & Tiernan Armstrong-Ingram, 2023.
"Color under pressure: how multiple factors shape defensive coloration,"
Behavioral Ecology, International Society for Behavioral Ecology, vol. 34(1), pages 1-13.
- Lazzari, Paolo & Seriani, Nicola, 2024.
"Two-dimensional cellular automata—Deterministic models of growth,"
Chaos, Solitons & Fractals, Elsevier, vol. 185(C).
- Guangjie Cui & Yunbo Liu & Di Zu & Xintao Zhao & Zhijia Zhang & Do Young Kim & Pramith Senaratne & Aaron Fox & David Sept & Younggeun Park & Somin Eunice Lee, 2023.
"Phase intensity nanoscope (PINE) opens long-time investigation windows of living matter,"
Nature Communications, Nature, vol. 14(1), pages 1-10, December.
Corrections
All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pcbi00:1006943. See general information about how to correct material in RePEc.
If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.
If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .
If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.
For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: ploscompbiol (email available below). General contact details of provider: https://journals.plos.org/ploscompbiol/ .
Please note that corrections may take a couple of weeks to filter through
the various RePEc services.