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Evolution and development of shape: integrating quantitative approaches

Key Points

  • Quantitative approaches are used increasingly in evolutionary developmental biology ('evo-devo').

  • In particular, geometric morphometrics is widely used to quantify the shape of organisms or their parts. A wide range of tools is available to address specific questions and interpret results in their anatomical context.

  • Genetic studies of shape variation have shown that inheritance tends to be polygenic, with many loci of mostly small effects. Because developmental processes integrate variation from diverse sources, interactions of genes with each other and with environmental factors seem to be important.

  • Shape variation tends to be integrated and often has a modular structure; there is usually strong integration within morphological modules but relatively weak integration among modules.

  • Strong integration can act as an evolutionary constraint by hindering the independent evolution of different traits. Identifying constraints and their evolutionary effects is an active area of current research.

  • Functional considerations are increasingly important in evo-devo and provide explicit links between the genetic and developmental basis of variation and its adaptive significance for evolving populations.

  • Large-scale comparative analyses of shape with an explicit phylogenetic basis provide a means of examining the long-term evolutionary consequences of the processes observed in contemporary populations.

  • Overall, integration of quantitative approaches into evo-devo promises to unify developmental and adaptive factors of morphological evolution.

Abstract

Morphological traits have long been a focus of evolutionary developmental biology ('evo-devo'), but new methods for quantifying shape variation are opening unprecedented possibilities for investigating the developmental basis of evolutionary change. Morphometric analyses are revealing that development mediates complex interactions between genetic and environmental factors affecting shape. Evolution results from changes in those interactions, as natural selection favours shapes that more effectively perform some fitness-related functions. Quantitative studies of shape can characterize developmental and genetic effects and discover their relative importance. They integrate evo-devo and related disciplines into a coherent understanding of evolutionary processes from populations to large-scale evolutionary radiations.

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Figure 1: Relative and absolute constraints.

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Acknowledgements

I thank J. M. Gómez, A. Drake, B. Sidlauskas and M. Sabaj Perez for providing the images in Box 1, and C. Allen and B. Sidlauskas for providing the graphs in Figure 1 and Box 6, respectively. I greatly appreciate the thoughtful comments of three anonymous referees on earlier versions of this article.

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Glossary

Shape

The shape of an object encompasses all of its geometric properties except its size, position and orientation.

Morphological integration

The covariation of morphological structures in an organism or of parts in a structure, which may reflect developmental or functional interactions among traits.

Allometry

The dependence of shape on size, often characterized by a regression of shape on size.

Vital staining

Staining of live organisms to follow developmental processes (for example, calcium-binding stains, such as Alizarin Red and Calcein, label bone tissue and, if administered at different times, can indicate bone growth).

Shape space

A special type of morphospace in which each point represents a shape and the distances between points correspond to the amount of shape change between the respective shapes.

Principal component analysis

A multivariate analysis that provides a new coordinate system whose axes, the principal components, successively account for the maximum amount of variance and are uncorrelated with each other.

Canonical variate analysis

A multivariate analysis that finds new shape variables that maximize the separation between groups (such as species or genotypes) relative to the variation within groups.

Multivariate regression

A type of analysis in which variation in one set of variables, the dependent variables, is predicted or explained by variation in one or more other variables, the independent variables.

Partial least squares analysis

A multivariate analysis that aims to find the optimal variables for showing patterns of covariation (for example, in studies of integration). The analysis looks for new variables that maximize covariation between two sets of variables (for example, between the shapes of two anatomical structures).

Constraint

The tendency for evolutionary change to occur in some directions of a morphospace more than in other directions.

Quantitative trait loci

Genes or small genomic regions that affect a phenotypic trait of interest.

Fluctuating asymmetry

Subtle deviations between paired structures on the left and right body sides due to random perturbations of developmental processes.

Modules

Parts of biological systems tend to be organized into clusters, or modules, which consist of parts that are integrated tightly by many or strong interactions and which are relatively independent from other modules because there are fewer or weaker interactions between them.

Squared-change parsimony

A method for inferring ancestral phenotypic values in a phylogeny by minimizing the sum of squared phenotypic changes over all branches of the phylogeny.

Independent contrasts

A method that addresses the interdependence in comparative data due to shared ancestry among species by focusing on differences between contrasts of phenotypic values between sister nodes in a phylogeny.

Morphospace

A multidimensional space in which forms of organisms are represented by points, and distances between points correspond to the morphological similarity between forms.

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Klingenberg, C. Evolution and development of shape: integrating quantitative approaches. Nat Rev Genet 11, 623–635 (2010). https://doi.org/10.1038/nrg2829

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