Evolvability, limb morphology, and primate origins

The diversification of locomotor and postural behaviors among mammals has brought about striking changes in the ancestral pattern of the pentadactyl limb. These evolutionary changes frequently involve modification of either the most marginal digits (e.g., reduction of digits one or five; Morses law) or the most distal limb segments (e.g., phalangeal elongation or reduction; Shubin et al., 1997). Goslow (1989) and Hinchliffe (1989) suggested that evolutionary change in the proximal elements of the vertebrate limb has been relatively conservative, whereas more marked changes have occurred in the distal limb (autopod) elements. A number of comparative studies demonstrate that the autopod of mammals is quite variable interspecifically, supporting the "proximal stabilization" model. Examples include variability in bat wing phalanx length related to functional variation in the aerodynamics of flight (Norberg, 1994; Norberg and Rayner, 1987), variability in apical pad and terminal phalanx morphology related to variation in arboreal foraging preferences among neotropical primates and marsupials (Hamrick, 1998, 2001a,b, 2003), and variability in claw shape related to the diversification of foot postures in climbing, perching, and ground-dwelling birds (Feduccia, 1993). Quantitative studies have also revealed an intraspecific trend of increasing variation from the proximal to distal elements of bird and bat wings (Bader and Hall, 1960; Engels, 1938). Vertebrate limbs consist of hierarchical structural units, undergo temporal transformations in form, and exhibit varying degrees of connectivity with other modules (Raff, 1996). Limbs are therefore important units, or fields, of ontogenetic and phylogenetic change (Gilbert et al., 1996). Recent studies of limb development provide new support for Hinchliffes model of proximal stabilization and distal variability in limb evolution. These include evidence that the autopodium is developmentally autonomous from the proximal limb, involving different molecular pathways during chondrogenesis and a distinctive third phase of HoxD gene expression regulated by a single "global" enhancer (Chiu and Hamrick, 2002; Hérault et al., 1998). Loss-of-function mutations also reveal that redundancy exists among many of the patterning genes expressed during limb development so that knockout mutants often show alterations in phenotype that are either relatively minor or absent altogether. These experiments demonstrate that developmental perturbations such as changes in cell number and arrangement result in new, but nonlethal, skeletal morphologies. This chapter has two objectives. First, to present evidence from limb development supporting Hinchliffes model of evolvability in distal limb structures. Evolvability refers here to a species capacity to generate heritable phenotypic variation (Kirschner and Gerhart, 1998). Data from experimental genetics indicate that the mammalian distal limb (autopod) fulfills many of the theoretical criteria for "evolvability, " suggesting that the origin and radiation of mammalian clades would be expected to include early and rapid changes in autopod morphology. The second objective of this chapter is to present comparative evidence from hindfoot morphology showing that mammalian adaptive radiations frequently involve diversification of digit proportions associated with the evolution of new postural behaviors. These data establish diversification in digit proportions as a repeated pattern in tetrapod evolution, and data are provided documenting the evolution of derived digit proportions in early primates. The fossil evidence for skeletal evolution in early primates and other mammals is therefore consistent with Hinchliffes (1989, 1991) hypothesis, revealing that the evolution of new digit proportions was a critical first step in the origin and adaptive radiation of the order Primates.