The macroevolutionary consequences of phenotypic integration: from development to deep time

Abstract

Phenotypic integration is a pervasive characteristic of organisms. Numerous analyses have demonstrated that patterns of phenotypic integration are conserved across large clades, but that significant variation also exists. For example, heterochronic shifts related to different mammalian reproductive strategies are reflected in postcranial skeletal integration and in coordination of bone ossification. Phenotypic integration and modularity have been hypothesized to shape morphological evolution, and we extended simulations to confirm that trait integration can influence both the trajectory and magnitude of response to selection. We further demonstrate that phenotypic integration can produce both more and less disparate organisms than would be expected under random walk models by repartitioning variance in preferred directions. This effect can also be expected to favour homoplasy and convergent evolution. New empirical analyses of the carnivoran cranium show that rates of evolution, in contrast, are not strongly influenced by phenotypic integration and show little relationship to morphological disparity, suggesting that phenotypic integration may shape the direction of evolutionary change, but not necessarily the speed of it. Nonetheless, phenotypic integration is problematic for morphological clocks and should be incorporated more widely into models that seek to accurately reconstruct both trait and organismal evolution.

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.…”

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

“…Over time, the effect of phenotypic integration will produce taxa that are both more divergent and less divergent in morphology than would be otherwise expected (Fig. 2C) (63).…”

“…Analyses of morphological disparity and integration have compared trait variances in strongly and weakly integrated traits across a few clades of mammals, suggesting that strong integration may constrain trait variation across taxa although its effect is relatively weak (64). Interestingly, this weak effect on disparity may not translate simply to evolutionary rates because some of the most strongly integrated cranial traits showed limited disparity but high rates of evolution in an analysis across carnivorans (63). These results present one possible hypothesis: Phenotypic integration may constrain morphological variation to certain "preferred" directions but has little influence on the speed of changes within the allowed space, a pattern that reflects previous studies finding that evolution is more bounded by constraints than predicted (65).…”

“…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).…”

Analyzing Fluctuating Asymmetry with Geometric Morphometrics: Concepts, Methods, and Applications

“…Some authors have argued that modularity facilitates evolutionary change [418][419][420][421], a hypothesis that has been investigated with the methods of geometric morphometrics [172,[422][423][424]. Also, some authors have hypothesized that the patterns of genetic and developmental modularity should evolve to match the patterns of functional modularity [399,419,[425][426][427].…”