Solving the grand challenge of phenotypic integration: allometry across scales

Abstract

Phenotypic integration is a concept related to the cascade of trait relationships from the lowest organizational levels, i.e. genes, to the highest, i.e. whole-organism traits. However, the cause-and-effect linkages between traits are notoriously difficult to determine. In particular, we still lack a mathematical framework to model the relationships involved in the integration of phenotypic traits. Here, we argue that allometric models developed in ecology offer testable mathematical equations of trait relationships across scales. We first show that allometric relationships are pervasive in biology at different organizational scales and in different taxa. We then present mechanistic models that explain the origin of allometric relationships. In addition, we emphasized that recent studies showed that natural variation does exist for allometric parameters, suggesting a role for genetic variability, selection and evolution. Consequently, we advocate that it is time to examine the genetic determinism of allometries, as well as to question in more detail the role of genome size in subsequent scaling relationships. More broadly, a possible-but so far neglected-solution to understand phenotypic integration is to examine allometric relationships at different organizational levels (cell, tissue, organ, organism) and in contrasted species.

Keywords: Allometry; Genome size; Metabolic scaling; Phenotypic integration; Trait relationships.

Fig. 1

Arnold’s view of phenotypic integration. The pyramidal cascade of trait relationships from genes to organism’s fitness is represented. Here, the trait-trait relationships between two successive organizational levels are hypothetical

Fig. 2

Examples of allometric relationships between scales. A Relationship between leaf mass (M_L) and stem mass (M_S) (Price et al. 2010). B Relationship between cell area (A_C) and genome size (S) (Beaulieu et al. 2008). C Relationship between plant mass (M) and plant density (N) (Enquist et al. 1998). D Relationship between organism’s basal metabolic rate (B) and body mass (M) (West et al. 2002). E Relationship between the number of 16S/18S ribosomal genes per cell (R_C) and cell volume (V_C) (Gonzalez-de-Salceda and Garcia-Pichel 2021). F Relationship between xylem flux (F) and plant mass (M) (Enquist and Niklas 2001). G Relationship between flatworm body volume (V) and genome size (S) (Gregory et al. 2000)