Deciphering the Palimpsest: Studying the Relationship Between Morphological Integration and Phenotypic Covariation

Abstract

Organisms represent a complex arrangement of anatomical structures and individuated parts that must maintain functional associations through development. This integration of variation between functionally related body parts and the modular organization of development are fundamental determinants of their evolvability. This is because integration results in the expression of coordinated variation that can create preferred directions for evolutionary change, while modularity enables variation in a group of traits or regions to accumulate without deleterious effects on other aspects of the organism. Using our own work on both model systems (e.g., lab mice, avians) and natural populations of rodents and primates, we explore in this paper the relationship between patterns of phenotypic covariation and the developmental determinants of integration that those patterns are assumed to reflect. We show that integration cannot be reliably studied through phenotypic covariance patterns alone and argue that the relationship between phenotypic covariation and integration is obscured in two ways. One is the superimposition of multiple determinants of covariance in complex systems and the other is the dependence of covariation structure on variances in covariance-generating processes. As a consequence, we argue that the direct study of the developmental determinants of integration in model systems is necessary to fully interpret patterns of covariation in natural populations, to link covariation patterns to the processes that generate them, and to understand their significance for evolutionary explanation.

Studying morphological integration and modularity at multiple levels: concepts and analysis

“…Because processes acting at various stages of development can have different patterns of integration and modularity, involving differing sets of traits, that overlie each other in various manners, the cumulative effects of all these processes may not have a clear modular structure even if all individual processes are strictly modular. Hallgrímsson et al [38] used the metaphor of a 'palimpsest' for this situation, where processes at later stages partly overwrite the patterns of integration laid down by earlier processes, without completely extinguishing the earlier patterns. The total effect of these partly incongruent modular covariance structures, overlaid on each other, may produce the impression of a mainly integrated system where no individual hypothesis of modularity holds, even though all contributing processes may act in a clearly modular manner.…”

“…A different approach to genetic integration is to search for patterns of integration and modularity in the estimated effects of quantitative trait loci affecting the shape of a structure [62,76] or in the effects of mutations that affect the development of the structure under study [38,[77][78][79][80][81]. To quantify the effects of naturally occurring mutations, it is possible to use mutation accumulation lines and to analyse the patterns of covariation among lines [82].…”

Modularity and intra-floral integration in metameric organisms: plants are more than the sum of their parts

“…Although typically assessed through analyses of patterns of covariation among mature traits, integration is understood to reflect coregulation of the developmental processes that generate those traits ( [29], ch. 7; [28,30]). Modularity and integration Table 1.…”

Shared rules of development predict patterns of evolution in vertebrate segmentation

“…For example, while vertebrae vary in size across regions and frequently alternate in size, evidence from growth in a number of species suggests this results from later differential growth 27,28 , consistent with earlier constraints on somite-size patterning and proportions. We therefore hypothesize that an IC mechanism provides the initial pattern of proportional variation during segment formation, serving as a 'foundation' on which later variation may add or subtract 29 . That said, while later developmental processes such as differential growth may remodel proportions, the signal of the earlier segmentation event is not obliterated.…”