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

doi:10.1073/pnas.0509716103

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

*Howard Hughes Medical Institute, Department of Pediatrics, Section of Developmental Biology, University of Colorado at Denver and Health Sciences Center, 12800 East 19th Avenue, Aurora, CO 80045;
^†Department of Molecular Genetics, University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Boulevard, Houston, TX 77030; and
^‡Department of Obstetrics and Gynecology, State University of New York Downstate Medical Center, Brooklyn, NY 11203

Edited by Cliff Tabin, Harvard Medical School, Boston, MA, and accepted by the Editorial Board March 14, 2006 (received for review November 8, 2005)

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.

Footnotes

^§To whom correspondence should be addressed. E-mail: lee.niswander{at}uchsc.edu
Author contributions: K.E.S. and L.A.N. designed research; K.E.S. and R.R.B. performed research; K.E.S., R.R.B., and J.J.R. contributed new reagents/analytic tools; K.E.S. analyzed data; and K.E.S. wrote the paper.
Conflict of interest statement: No conflicts declared.
This paper was submitted directly (Track II) to the PNAS office. C.T. is a guest editor invited by the Editorial Board.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. DQ279782– DQ279785).
Abbreviations:

Abbreviations:

Bmp,

bone morphogenetic protein;

En,

embryonic day n;

PC,

principal component.