Origin of evolutionary novelty: Examples from limbs

Abstract

Classic hypotheses of vertebrate morphology are being informed by new data and new methods. Long nascent issues, such as the origin of tetrapod limbs, are being explored by paleontologists, molecular biologists, and functional anatomists. Progress in this arena will ultimately come down to knowing how macroevolutionary differences between taxa emerge from the genetic and phenotypic variation that arises within populations. The assembly of limbs over developmental and evolutionary time offers examples of the major processes at work in the origin of novelties. Recent comparative developmental analyses demonstrate that many of the mechanisms used to pattern limbs are ancient. One of the major consequences of this phenomenon is parallelism in the evolution of anatomical structures. Studies of both the fossil record and intrapopulational variation of extant populations reveal regularities in the origin of variation. These examples reveal processes acting at the level of populations that directly affect the patterns of diversity observed at higher taxonomic levels.

Salamander limb development: Integrating genes, morphology, and fossils

“…Integrative approaches have previously successfully been taken to elucidate the evolutionary history of complex morphologies, e.g., the initial evolution of the tetrapod autopodium (e.g., Shubin and Alberch, 1986;Shubin et al, 1997;Shubin, 2002;Larsson, 2007;Shubin et al, 2009) or the evolution of the avian wing from a theropod autopod (e.g., Wagner and Gauthier, 1999;Larsson and Wagner, 2002;Galis et al, 2003a;Wagner, 2005). The case of salamander limb development highlights that an integration of molecular approaches, data from the fossil record, and a phylogenetic framework is essential to gain a comprehensive picture for the evolution of patterns and processes in tetrapod limb development and evolution.…”

“…This organ system exemplifies how approaches from different fields of biology can be synthesized to yield more information than any one sub-discipline could provide. Despite such a research effort, many questions surrounding the development, evolution, and morphological diversification of the tetrapod limb remain unresolved (e.g., Shubin, 2002;Shubin et al, 2009;Zeller et al, 2009;Woltering and Duboule, 2010).…”

Before programs: The physical origination of multicellular forms

“…The foregoing discussion suggests that the result of this process is not to generate new members of the molecular toolkit (with rare exceptions such as laminin; Czaker, 2000), body plans (with rare exceptions such as the Bryozoa; Valentine, 2004), or organs (with rare exceptions such as the vertebrate limb; Shubin, 2002). Our proposal that multicellular forms were originally based on the inherent physical properties of tissue masses suggests an alternative interpretation of the impact of genetic change on the evolution of development.…”

Integrating the genotype and phenotype in hominid paleontology

“…Other examples of population-based approaches and comparative cross-taxon gene expression studies are proving to be successful in the search for the genetic mechanisms underlying other types of phenotypic evolution (5,8,9,123,124). For example, when Jernvall and colleagues (9, 124) studied gene expression patterns in mouse and vole molar development, they found four genes that have spatial expression patterns that correlate with the morphological differences between these two rodents.…”

“…As contemporary genetics illuminates the relationship between genotype and phenotype, the ability of fossilized anatomies to inform us about past organisms changes and expands. This is most evident in studies of large-scale organismal evolution, such as the origins of animal body plans during the Cambrian period (1-3), the evolution of limbs (4)(5)(6), and the appearance of teeth in early fishes (7). Even within more restricted groups, such as mammals, new knowledge of dental developmental genetics has elucidated evolutionary phenomenon (8)(9)(10).…”