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

Abstract

Developmentally regulated programmed cell death sculpts the limbs and other embryonic organs in vertebrates. One intriguing example of species-specific differences in apoptotic extent is observed in the tissue between the digits. In chicks and mice, bone morphogenetic proteins (Bmps) trigger apoptosis of the interdigital mesenchyme, leading to freed digits, whereas in ducks, Bmp antagonists inhibit the apoptotic program, resulting in webbed feet. Here, we show that the phyllostomid bat Carollia perspicillata utilizes a distinct mechanism for maintaining interdigit tissue. We find that bat forelimb and hindlimb interdigital tissues express Bmp signaling components but that only bat hindlimbs undergo interdigital apoptosis. Strikingly, the retention of interdigital webbing in the bat forelimb is correlated with a unique pattern of Fgf8 expression in addition to the Bmp inhibitor Gremlin . By using a functional assay, we show that maintenance of interdigit tissue in the bat wing depends on the combined effects of high levels of Fgf signaling and inhibition of Bmp signaling. Our data also indicate that although there is not a conserved mechanism for maintaining interdigit tissue across amniotes, the expression in the bat forelimb interdigits of Gremlin and Fgf8 suggests that these key molecular changes contributed to the evolution of the bat wing.