Cranial Modularity Shifts during Mammalian Evolution

Abstract

The mammalian skull has been studied as several separate functional components for decades, but the study of modularity is a more recent, integrative approach toward quantitative examination of independent subsets of highly correlated traits, or modules. Although most studies of modularity focus on developmental and genetic systems, phenotypic modules have been noted in many diverse morphological structures. However, few studies have provided empirical data for comparing modules across higher taxonomic levels, limiting the ability to assess the broader evolutionary significance of modularity. This study uses 18-32 three-dimensional cranial landmarks to analyze phenotypic modularity in 106 mammalian species and demonstrates that cranial modularity is generally conserved in the evolution of therian mammals (marsupials and placentals) but differs between therians and monotremes, the two extant subclasses of Mammalia. Within therians, cluster analyses identify six distinct modules, but only three modules display significant integration in all species. Monotremes display only two highly integrated modules. Specific hypotheses of functional and developmental influences on cranial bones were tested. Theoretical correlation matrices for bones were constructed on the basis of shared function, tissue origin, or mode of ossification, and all three of these models are significantly correlated with observed correlation matrices for the mammalian cranium.

Larger mammals have longer faces because of size-related constraints on skull form

“…The morphological disparity in their cranial shape is extraordinary, as every visitor to a natural history museum appreciates. Despite the scale of differences between major, and even minor, clades, the covariance structure in the mammalian skull seems to be highly conserved [2][3][4][5] . How the profound variety of skull forms was generated from such a seemingly conservative system is a fundamental and largely open evolutionary question.…”

Adaptive response to sociality and ecology drives the diversification of facial colour patterns in catarrhines

“…Modularity of the primate face is a likely advantage of these more structured facial colour patterns because it can enable higher levels of interspecific diversity 10,36,37 that would in turn be beneficial for species recognition. A modular framework characterizes the cranial morphology of many mammals, including primates [38][39][40] ; however, facial colour patterns have not been investigated in the context of modularity even though research suggests that various aspects of this system might be modular. First, work on mammal and insect colour patterns indicates that there is modular genetic control to the presence of colour patches and types of colouration 41,42 .…”

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

“…Indeed, a review of the few relevant macroevolutionary studies suggests that it is unlikely that there are simple trends toward decreased phenotypic integration, and increased modularity, through time. For example, multiple studies of phenotypic integration in the mammalian cranium have supported a common pattern in most living marsupials and placentals (11,15), and, where fossil mammals have been examined, most show similar patterns as their extant relatives (11). One interesting exception is that of extinct saber-toothed cats (Smilodon fatalis), in which patterns of cranial integration diverge from those of extant and extinct conical-toothed cats (53) by fragmentation of the anterior face into two new modules (11) (SI Text), possibly due to strong sexual selection on canine size (54) or the simple biomechanical requirements of accommodating these extreme structures.…”

“…Much recent work has focused on characterizing large-scale patterns of trait relationships through comparative studies of extant and fossil taxa (11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23), in some cases demonstrating shifts in phenotypic integration related to changes in development (24)(25)(26), function (27)(28)(29), and environment (30)(31)(32)(33). Although focused overwhelmingly on model organisms, these studies provide a foundation for understanding how phenotypic integration changes through ontogenetic and evolutionary time and how it relates to myriad factors shaping morphological evolution.…”

“…The study of these trait relationships, or their integration, and their frequent division into modules has typically focused on model organisms with detailed genealogies and ontogenies (3)(4)(5)(6)(7)(8)(9), which allows for distinguishing among different levels and sources of integration, from genetic and developmental to evolutionary integration (10) (SI Text). However, through quantitative analysis of phenotypic trait covariances, genetic and developmental changes can be reconstructed in taxa for which molecular data will never be available, such as fossils (1,11).…”