Digit Loss in Extent Archosaurs and Evolutionary Implications

Digit loss in archosaur evolution and the interplay between selection and constraints

Authors:

1. Merijn A. G. de Bakker (a)
2. Donald A. Fowler (a)
3. Kelly den Oude (a)
4. Esther M. Dondorp (a)
5. M. Carmen Garrido Navas (a)
6. Jaroslaw O. Horbanczuk (b)
7. Jean-Yves Sire (c)
8. Danuta Szczerbińska (d)
9. Michael K. Richardson (a)

Affiliations:

a. Department of Integrative Zoology, Institute of Biology, Leiden University, Sylvius Laboratory, Sylviusweg 72, 2333BE Leiden, the Netherlands

b. Institute of Genetics and Animal Breeding, Polish Academy of Sciences, 05-552 Jastrzębiec, Poland

c. Evolution & Développement du squelette, UMR 7138, Université Pierre et Marie Curie, 7 Quai Saint-Bernard, Bat A2, Case 5, 75005 Paris, France

d. Department of Poultry and Ornamental Bird Breeding, Western Pomeranian University of Technology, 20 Judyma Street, 71-466 Szczecin, Poland

Abstract:

Evolution involves interplay between natural selection and developmental constraints. This is seen, for example, when digits are lost from the limbs during evolution. Extant archosaurs (crocodiles and birds) show several instances of digit loss under different selective regimes, and show limbs with one, two, three, four or the ancestral number of five digits. The ‘lost’ digits sometimes persist for millions of years as developmental vestiges. Here we examine digit loss in the Nile crocodile and five birds, using markers of three successive stages of digit development. In two independent lineages under different selection, wing digit I and all its markers disappear. In contrast, hindlimb digit V persists in all species sampled, both as cartilage, and as Sox9- expressing precartilage domains, 250 million years after the adult digit disappeared. There is therefore a mismatch between evolution of the embryonic and adult phenotypes. All limbs, regardless of digit number, showed similar expression of sonic hedgehog (Shh). Even in the one-fingered emu wing, expression of posterior genes Hoxd11 and Hoxd12 was conserved, whereas expression of anterior genes Gli3 and Alx4 was not. We suggest that the persistence of digit V in the embryo may reflect constraints, particularly the conserved posterior gene networks associated with the zone of polarizing activity (ZPA). The more rapid and complete disappearance of digit I may reflect its ZPA-independent specification, and hence, weaker developmental constraints. Interacting with these constraints are selection pressures for limb functions such as flying and perching. This model may help to explain the diverse patterns of digit loss in tetrapods. Our study may also help to understand how selection on adults leads to changes in development.