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.Chiroptera ͉ Bmp ͉ cartilage

Interdigital webbing retention in bat wings illustrates genetic changes underlying amniote limb diversification

“…It would be interesting to determine whether a similar mechanism for interdigital retention operates in flying lemurs. In bats, the length of the forelimb digits appears to be controlled by an increase in Bmp activity within the cartilage (26). It is exciting that the modulation of both of these aspects of bat wing development depends partly on changes in Bmp signaling: increased Bmp in the digits and reduced Bmp in the interdigits.…”

“…We cloned a 410-bp fragment of Carollia Bmp7 from RNA extracted from a stage-13 embryonic head by using the primers that are described in ref. 26. We used mouse riboprobes, which also recognize the bat transcripts, to test for the expression of Fgf8 (27), Bmp2 (28), Msx2 (29), and Sprouty2 (25).…”

Repeated modification of early limb morphogenesis programmes underlies the convergence of relative limb length inAnolislizards

“…Long bone development is a complex process and, as a result, limb length variation can arise through many processes, whether by changing the patterning of the early limb bud or through time-specific changes in growth rate (e.g. [34,35,37,[40][41][42][43][44]). Detailed description of our methodology is included in the electronic supplementary material, appendix S1.…”

The developmental basis of bat wing muscle

“…The earliest known fossil bat, Onychonycteris finneyi, from the early Eocene was clearly capable of powered flight, possessing a forelimb that was morphologically similar to that of extant bats 6 . This has led some authors to hypothesize that bats achieved powered flight in a relatively short period of geological time, possibly through small changes in gene regulation during organogenesis 7,8 . However, the fossil record of bats is currently quite poor 9 , so there is still a possibility that transitional fossils may be discovered in the future.…”