A Developmental Analysis of an Evolutionary Trend: Digital Reduction in Amphibians

Abstract

In this study, we integrate information from phylogeny, comparative ontogeny, and experimental embryology in an attempt to elucidate the mechanisms controlling evolutionary trends towards digital reduction and loss observed in amphibians. Frogs and salamanders that have lost phalanges and even whole toes have done so in a very ordered manner, i.e., certain skeletal elements are lost prior to others. This pattern of morphological diversity is described and trends elucidated. It is concluded that the process is characterized by striking intraordinal convergences coupled with substantial differences between the trends observed in frogs as compared to urodeles. We argue that this pattern is essentially a reflection of the differences in the ontogenies of the two orders. Similarly, the convergences within urodeles and within anurans can be explained as the result of regulation of developmental parameters in a resilient developmental program. We further explore this hypothesis by experimentally perturbing the number of cells in the embryonic limb primordium to show that reduction in the number of mesenchymal cells secondarily affects the developmental process of pattern formation causing a rearrangement of the skeletal morphology of the foot. The same experimental manipulation has different effects in frogs as compared to salamanders. However, in both cases, the experimentally generated morphologies tend to parallel the phenotypes and trends observed in nature. Our conclusion is that most of the patterns of diversity in the digital morphology of amphibians can be explained as a reflection of developmental properties. In general, we present a methodology that attempts to empirically address the issue of identifying developmental constraint in morphological evolution.

From genes to phenotype: dynamical systems and evolvability

“…In all of the instances the forms have converged in the loss of the fifth toe; --(B) Identical treatment of an embryonic limb bud with a mitotic inhibitor with reversible effects results in the loss of pre-axial digits in frogs while salamanders lose post-axial elements. These differences in experimentally generated forms parallel observed evolutionary trends (from Alberch & Gale, 1985).…”

“…6, see Alberch & Gale, 1985) is probably an empirical example of the theoretical diagram in Figure 5.…”

EvoDevo as a Motley Aggregation: Local Integration and Conflicting Views of Genes During the 1980s

“…This argument is similar to that ofAlberch and Gale (1985) on frogs and salamanders, although Hall cited research on whales with hind limbs, wingless chicks, and legless lizards.…”

“…This idea conflicted with the developmental-genetic perspective of morphogenesis supported by Raff and Kaufman (1983). Alberch emphasized the role of developmental constraints for evolutionary changes (Alberch 1980(Alberch , 1982Alberch and Gale 1985). Both in natural populations and experimental conditions, some kinds of morphological changes were more likely to occur than others, e.g., the consistent differences in digit loss between frog and salamander lineages.…”

“…7 Integration of the Results or Approaches from Different Fields: Comparative Morphology and Experimental Embryology A shared characteristic of the studies of Alberch, Hall, and Müller was integration of the results or approaches from comparative morphology and experimental embryology. For instance, based on the approach of comparative morphology (i.e., comparing morphologies between lineages to reveal their evolutionary history), Alberch and Gale (1985) compared the degeneration of digits in frogs and salamanders and showed that the patterns of digital loss were different among lineages. Frogs tended to lose their first digits, while salamanders tended to lose their fifth and fourth digits.…”