Development of bat flight: Morphologic and molecular evolution of bat wing digits

Abstract

The earliest fossil bats resemble their modern counterparts in possessing greatly elongated digits to support the wing membrane, which is an anatomical hallmark of powered flight. To quantitatively confirm these similarities, we performed a morphometric analysis of wing bones from fossil and modern bats. We found that the lengths of the third, fourth, and fifth digits (the primary supportive elements of the wing) have remained constant relative to body size over the last 50 million years. This absence of transitional forms in the fossil record led us to look elsewhere to understand bat wing evolution. Investigating embryonic development, we found that the digits in bats (Carollia perspicillata) are initially similar in size to those of mice (Mus musculus) but that, subsequently, bat digits greatly lengthen. The developmental timing of the change in wing digit length points to a change in longitudinal cartilage growth, a process that depends on the relative proliferation and differentiation of chondrocytes. We found that bat forelimb digits exhibit relatively high rates of chondrocyte proliferation and differentiation. We show that bone morphogenetic protein 2 (Bmp2) can stimulate cartilage proliferation and differentiation and increase digit length in the bat embryonic forelimb. Also, we show that Bmp2 expression and Bmp signaling are increased in bat forelimb embryonic digits relative to mouse or bat hind limb digits. Together, our results suggest that an up-regulation of the Bmp pathway is one of the major factors in the developmental elongation of bat forelimb digits, and it is potentially a key mechanism in their evolutionary elongation as well.