Integrated phenotypes: understanding trait covariation in plants and animals

Abstract

Integration and modularity refer to the patterns and processes of trait interaction and independence. Both terms have complex histories with respect to both conceptualization and quantification, resulting in a plethora of integration indices in use. We review briefly the divergent definitions, uses and measures of integration and modularity and make conceptual links to allometry. We also discuss how integration and modularity might evolve. Although integration is generally thought to be generated and maintained by correlational selection, theoretical considerations suggest the relationship is not straightforward. We caution here against uncontrolled comparisons of indices across studies. In the absence of controls for trait number, dimensionality, homology, development and function, it is difficult, or even impossible, to compare integration indices across organisms or traits. We suggest that care be invested in relating measurement to underlying theory or hypotheses, and that summative, theory-free descriptors of integration generally be avoided. The papers that follow in this Theme Issue illustrate the diversity of approaches to studying integration and modularity, highlighting strengths and pitfalls that await researchers investigating integration in plants and animals.

Keywords: integration; modularity; phenotype; variation.

Figure 1.

Potential evolutionary routes to modularity via parcellation and via increased integration (modified from Wagner & Altenberg [13]). In the case of parcellation, pleiotropic links between modules are removed, whereas with increased integration pleiotropic links are added within the modules, so as to make them relatively more integrated than the whole.

Figure 2.

Increased floral integration, from unfused pistil and stamens (a), to adnate (structurally integrated) pistil and stamens (b). Fusion of filament and style tissues can lead to an increase or decrease in measured (statistical) phenotypic integration of pistil and stamen, depending, respectively, on whether the portions of the stamen filaments fused to the style (dotted lines) are, or are not, included in the stamen measurements. (The former analysis would depend on phylogenetic/evolutionary or developmental insights.) (Online version in colour.)

Figure 3.

Flower of Stylidium bicolor in the staminate phase. The column bearing the pollen is formed by fusion (adnation) of staminate and pistillate tissues and will bear the stigma in place of the pollen in one or two days. Here, comparing column length in the male and female phases shows that the positions of the anthers and stigmas are tightly correlated because of the structural integration. (Online version in colour.)

Figure 4.

(a,b) Loss of detectable covariance with stabilizing selection acting together with correlational selection. Although populations will evolve only along the ridge (diagonal dashed line), the variance within each population is too small relative to the width of the adaptive ridge, for any within-population covariation to be detected.