The Evolution of Modularity in the Mammalian Skull II: Evolutionary Consequences

Abstract

Changes in patterns and magnitudes of integration may influence the ability of a species to respond to selection. Consequently, modularity has often been linked to the concept of evolvability, but their relationship has rarely been tested empirically. One possible explanation is the lack of analytical tools to compare patterns and magnitudes of integration among diverse groups that explicitly relate these aspects to the quantitative genetics framework. We apply such framework here using the multivariate response to selection equation to simulate the evolutionary behavior of several mammalian orders in terms of their flexibility, evolvability and constraints in the skull. We interpreted these simulation results in light of the integration patterns and magnitudes of the same mammalian groups, described in a companion paper. We found that larger magnitudes of integration were associated with a blur of the modules in the skull and to larger portions of the total variation explained by size variation, which in turn can exert a strong evolutionary constraint, thus decreasing the evolutionary flexibility. Conversely, lower overall magnitudes of integration were associated with distinct modules in the skull, to smaller fraction of the total variation associated with size and, consequently, to weaker constraints and more evolutionary flexibility. Flexibility and constraints are, therefore, two sides of the same coin and we found them to be quite variable among mammals. Neither the overall magnitude of morphological integration, the modularity itself, nor its consequences in terms of constraints and flexibility, were associated with absolute size of the organisms, but were strongly associated with the proportion of the total variation in skull morphology captured by size. Therefore, the history of the mammalian skull is marked by a trade-off between modularity and evolvability. Our data provide evidence that, despite the stasis in integration patterns, the plasticity in the magnitude of integration in the skull had important consequences in terms of evolutionary flexibility of the mammalian lineages.

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

“…Allometry is known to be a major component of covariation in the mammalian cranium 7 and contributes to its integration and modularity 8 . Indeed, without integration, fundamental functions could be compromised as size changes during ontogeny and in evolution 9,10 .…”

The shapes of bird beaks are highly controlled by nondietary factors

“…The trend for the face to elongate with allometry has also been noted in mammals (17) and is postulated to be related to heterochrony, an important factor in the evolution of birds from dinosaurs (46) and a demonstrated mode of generating diversity of beak forms in Darwin's finches (6,9). In mammals, it has been shown that integration constrains evolution along paths of least evolutionary resistance, meaning that heterochronic or allometric changes offer a simple mechanism by which evolution can act to produce high disparity (47,48). The fact that two nonsister clades of accipitrid vultures achieve a vulturine morphology solely by increasing skull size provides a new, nonmammalian example of this phenomenon.…”

“…A consequence of this mechanism is that skull morphology is highly constrained. Interestingly, animals that demonstrate high levels of integration are less able to respond to shifting selective pressures because they are locked in to a particular dimension of variation (47,49): in this case, size. Consequently, raptors may be particularly vulnerable if changing environmental conditions result in an adaptive peak that they cannot reach by simply sliding along their allometric trajectory.…”

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

“…Combining simulations with empirical data has shown that phenotypic integration does influence the direction of interspecific variation (50). For example, simulations using empirically derived covariance matrices from mammal crania have also shown that high integration is associated with lower ability to respond to selection (62), with both the magnitude and direction of response to selection mediated by phenotypic integration ( Fig. 2A) (63).…”

“…Many studies have tested for correlations between developmental integration, variational integration, and overall variation across taxa to assess the influence of developmental interactions on morphological evolution (18,22,23). Others have simulated the potential effects of trait integration on the ability of populations to respond to selection (50,62). Combining simulations with empirical data has shown that phenotypic integration does influence the direction of interspecific variation (50).…”