Natural and experimental reduction of the avian fibula: Developmental thresholds and evolutionary constraint

Fibula reduction is a key feature of avian limb evolution. In a combined comparative and experimental approach the present study analyses the trends of fibula reduction in extant birds and their developmental basis. The study of 55 species of birds reveals four different types of tibiotarsus-to-fibula relationships. Extremely small fibulae are associated with two types of limb modification: (1) elongations of the limb primarily affect the tibiotarsus, increasing its length more than that of the fibula; (2) miniaturizations of the limb reduce both tibiotarsus and fibula length, but are reglarly associated with structural reductions of the distal parts of the fibula. True structrual reductions are distinguished from relative size reductions. The specific features of fibula reduction are analyzed through experimental mesenchyme excisions in chick limb buds. The methodical variation of experimental parameters resolves a long-standing controversy about the effects of mesenchyme reductions on the patterns of skeletal formation. Mesenchyme excisions are shown to have unequal effects on the two zeugopod bones, affecting the fibula to a greater degree than the tibiotarsus. Several of the features seen in birds with advanced fibula reductions are paralleled by the effects of mesenchyme reductions. The consequences of this differential susceptibility of the skeletal blastemata are discussed both in terms of pattern formation in limb development and in terms of its bearing on the patterns of evolutionary limb reduction. It is concluded that thresholds of cell number and blastema size in development constrain the patterns of phenotypic variation in avian limbs. © 1992 Wiley-Liss, Inc.