Heterochrony in limb evolution: developmental mechanisms and natural selection



The tetrapod limb provides several examples of heterochrony—changes in the timing of developmental events. These include species differences in the sequence of skeletal chondrogenesis, in gene transcription in the developing limbs, and in the relative time at which forelimb and hind limb buds develop. Here, we examine (i) phylogenetic trends in limb heterochrony; (ii) changes in developmental mechanisms that may lead to heterochrony; and (iii) the possible role that heterochrony plays in generating adaptive traits. We analyze the published literature and present preliminary data on turtle (Emys orbicularis) and bat (Rousettus amplexicaudatus) limb development. Teleosts, marsupials, and some urodeles show extreme timing differences between forelimb (or pectoral fin) and hind limb (or pelvic fin) development; this heterochrony may, in some cases, be adaptive. Published data on limb chondrogenesis reveal sequence elements that are strongly conserved (possibly owing to constraints); and others that vary between higher taxa (for unknown reasons). We find little evidence that chondrogenic sequences are modified by selection for limb functional traits. There are a few examples of developmental mechanisms that may be modified under heterochrony to produce adaptive changes in the limb (e.g. some cases of hyperphalangy or limb reduction). In conclusion, numerous examples of limb heterochrony have been recorded. However, few cases are obviously adaptive. Indeed, current data and methodologies make it difficult to identify the developmental changes, or selective pressures, that may underlie limb heterochrony. More integrative studies, including studies of heterochrony within populations, are needed to assess the role of timing shifts in limb evolution. J. Exp. Zool. (Mol. Dev. Evol.) 312B:639–664, 2009. © 2009 Wiley-Liss, Inc.