The fossil record of phenotypic integration and modularity: A deep-time perspective on developmental and evolutionary dynamics

Abstract

Variation is the raw material for natural selection, but the factors shaping variation are still poorly understood. Genetic and developmental interactions can direct variation, but there has been little synthesis of these effects with the extrinsic factors that can shape biodiversity over large scales. The study of phenotypic integration and modularity has the capacity to unify these aspects of evolutionary study by estimating genetic and developmental interactions through the quantitative analysis of morphology, allowing for combined assessment of intrinsic and extrinsic effects. Data from the fossil record in particular are central to our understanding of phenotypic integration and modularity because they provide the only information on deep-time developmental and evolutionary dynamics, including trends in trait relationships and their role in shaping organismal diversity. Here, we demonstrate the important perspective on phenotypic integration provided by the fossil record with a study of Smilodon fatalis (saber-toothed cats) and Canis dirus (dire wolves). We quantified temporal trends in size, variance, phenotypic integration, and direct developmental integration (fluctuating asymmetry) through 27,000 y of Late Pleistocene climate change. Both S. fatalis and C. dirus showed a gradual decrease in magnitude of phenotypic integration and an increase in variance and the correlation between fluctuating asymmetry and overall integration through time, suggesting that developmental integration mediated morphological response to environmental change in the later populations of these species. These results are consistent with experimental studies and represent, to our knowledge, the first deep-time validation of the importance of developmental integration in stabilizing morphological evolution through periods of environmental change.

Keywords: Late Pleistocene; carnivorans; macroevolution; modularity; phenotypic integration.

Fig. 1.

Genetic pleiotropy and developmental interactions contribute to the integration of phenotypic traits, which are often observed to form distinct modules, sets of highly integrated traits with strong correlations (solid lines) within modules and relatively weaker (thin solid lines and dotted lines) and/or fewer correlations between modules. It is hypothesized that fragmentation of integrated traits through time leads to the evolution of modular phenotypes. Modified from refs. and .

Fig. 2.

Phenotypic integration shapes morphological variation. (A) Greater integration of traits constrains the response to selection to a direction that is concordant with that of maximum variation, shown here for simulations based on empirical data from mammalian crania. Constraint is measured as the vector correlation between the response vector and the first principal component of each matrix. Integration is measured as the relative eigenvalue standard deviation (SD) of each matrix. (B) Integrated structures (black dots) repartition variance along preferred directions of change, such that, over time, they will explore fewer directions of morphospace than unintegrated structures (red dots), but will achieve a great range of shapes in those preferred directions. (C) This bias in direction of evolutionary change will ultimately produce both more and less divergent morphologies in an integrated structure (black lineages) than expected from an unintegrated one (red lineages). Modified from ref. .

Fig. 3.

Temporal patterns in log centroid size, interindividual variance, FA, phenotypic integration, and the correlation between fluctuating asymmetry and overall integration for S. fatalis and C. dirus from the Rancho La Brea tar pits. Variance, FA, integration, and correlation are scaled relative to their maximum values. Unscaled values in Table S1. Data on pit ages from refs. and . Delta O¹⁸ curve from ref. . Open symbols indicate S. fatalis; closed symbols indicate C. dirus. Silhouettes from phylopic.org.