Limbs in whales and limblessness in other vertebrates: mechanisms of evolutionary and developmental transformation and loss.




This paper addresses the developmental and evolutionary mechanisms underlying fore and hind limb development, progressive hind limb reduction and skeletal loss in whales, and evaluates whether the genetic, developmental and evolutionary mechanisms thought to be responsible for limb loss in snakes "explain" loss of the hind limbs in whales. Limb loss and concurrent morphological and physiological changes associated with the transition from land to water are discussed within the context of the current whale phylogeny. Emphasis is placed on fore and hind limb development, how the fore limbs transformed into flippers, and how the hind limbs regressed, leaving either no elements or vestigial skeletal elements. Hind limbs likely began to regress only after the ancestors of whales entered the aquatic environment: hind-limb function was co-opted by the undulatory vertical axial locomotion made possible by the newly evolved caudal flukes. Loss of the hind limbs was associated with elongation of the body during the transition from land to water. Limblessness in most snakes is also associated with adoption of a new (burrowing) life style and was driven by developmental changes associated with elongation of the body. Parallels between adaptation to burrowing or to the aquatic environment reflect structural and functional changes associated with the switch to axial locomotion. Because they are more fully studied, and to determine whether hind-limb loss in lineages that are not closely related could result from similar genetically controlled developmental pathways, we discuss developmental (cellular and genetic) processes that may have driven limb loss in snakes and legless lizards and compare these processes to the loss of hind limbs in whales. In neither group does ontogenetic or phylogenetic limb reduction result from failure to initiate limb development. In both groups. limb loss results from arrested development at the limb-bud stage, as a result of inability to maintain necessary inductive tissue interactions and enhanced cell death over that seen in limbed tetrapods. An evolutionary change in Hox gene expression as occurs in snakes or in Hox gene regulation as occurs in some limbless mutants is unlikely to have initiated loss of the hind limbs in cetaceans. Selective pressures acting on a wide range of developmental processes and adult traits other than the limbs are likely to have driven the loss of hind limbs in whales.