The morphologic and genetic evolution of bat wing digits

SEARS, K.E.*; BEHRINGER, R.R.; NISWANDER, L.A.; University of Colorado Health Sciences Center; M.D. Anderson Cancer Center; University of Colorado Health Sciences Center: The morphologic and genetic evolution of bat wing digits

Bats suddenly appear in the fossil record about 50 million years ago. The earliest bats resemble their modern counterparts in possessing the anatomical hallmarks of powered flight (e.g., greatly elongated digits and interdigital membranes). Morphometric analyses reveal 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. The absence of transitional forms in the fossil record forces us to look elsewhere to understand the evolution of the unique morphology of the bat wing. With this in mind, we compared the embryological development of the digits of the bat wing (Carollia perspicillata) with the more generalized digits of the mouse (Mus musculus) using histological and molecular techniques. Histological results indicate that the initial cartilage condensations and segmentation patterns of bat digits are similar in size and position to those observed in mouse, suggesting that bat digit elongation is due to post-segmental developmental processes. Longitudinal growth of post-segmental digits is dependent upon the relative proliferation and differentiation of chondrocytes in the growth plate. The area in which chondrocytes undergo differentiation (hypertrophic zone) is expanded in the bat growth plate, relative to mouse. Limb culture experiments reveal that the application of BMP protein can stimulate expansion of the hypertrophic zone in both bat and mouse digits. In addition, in situ hybridization results suggest that the expression area of BMP2 is expanded in bat digits relative to mouse. Taken together, these results suggest that a change in the spatial expression of a single key genetic regulator of limb development drove the rapid evolutionary elongation of bat wing digits.

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