The origin and evolution of animal appendages

Abstract

Animals have evolved diverse appendages adapted for locomotion, feeding and other functions. The genetics underlying appendage formation are best understood in insects and vertebrates. The expression of the Distal-less (Dll) homeoprotein during arthropod limb outgrowth and of Dll orthologs (Dlx) in fish fin and tetrapod limb buds led us to examine whether expression of this regulatory gene may be a general feature of appendage formation in protostomes and deuterostomes. We find that Dll is expressed along the proximodistal axis of developing polychaete annelid parapodia, onychophoran lobopodia, ascidian ampullae, and even echinoderm tube feet. Dll͞Dlx expression in such diverse appendages in these six coelomate phyla could be convergent, but this would have required the independent co-option of Dll͞Dlx several times in evolution. It appears more likely that ectodermal Dll͞Dlx expression along proximodistal axes originated once in a common ancestor and has been used subsequently to pattern body wall outgrowths in a variety of organisms. We suggest that this pre-Cambrian ancestor of most protostomes and the deuterostomes possessed elements of the genetic machinery for and may have even borne appendages.

The Caenorhabditis elegans Distal‐less ortholog ceh‐43 is required for development of the anterior hypodermis

“…1) expression resembles the antibody staining pattern published by Panganiban et al (1997). Therefore, both methods are likely to reflect the natural ceh-43 expression pattern.…”

“…We believe that this expression may not reflect the natural ceh-43::gfp expression, because it is not consistent with the antibody staining from Panganiban et al (1997).…”

“…Drosophila and Tribolium Distal-less mutants both lack the distal part of legs and antennae (Sato, 1984;Sunkel and Whittle, 1987;Cohen et al, 1989;Beermann et al, 2001), and ectopic Dll expression can induce ectopic outgrowth of distal legs or antennae (Gorfinkiel et al, 1997). An antibody against the butterfly Dll homeodomain reveals expression in developing appendages as different as echinoderm tube feet, Chaetopterus parapodia, ascidian ampullae, and the apical ectodermal ridge of mouse limb buds (Panganiban et al, 1997). Zebrafish Dlx genes are expressed in fin buds as well, and the human split hand/ foot syndrome as well as the chicken limbless mutant may be due to defects in Dlx genes (Akimenko et al, 1994;Ferrari et al, 1999;Merlo et al, 2000).…”

Model Organisms in the Study of Development and Disease

“…In animal systems where function of Dll genes has been determined, it has been found that Dll function is required for appendage outgrowth in many, but not all, cases. The fact that Dll is expressed at the distal tip of all body wall outgrowths, including the tube feet of starfish (Panganiban et al, 1997), suggests that this gene performed a function required to initiate such outgrowth in the bilateral ancestor of vertebrates and invertebrates (Panganiban, 2000;Zerucha and Ekker, 2000).…”

“…For example, a series of investigations showed that all bilateralia, including humans, possess a common genetic mechanism for patterning the anterior/posterior (A/P) body axis involving the Hox cluster genes (McGinnis and Krumlauf, 1992), the dorsal/ventral (D/V) body axis DeRobertis and Sasai, 1996), and the three derived axes of the appendages (A/P, D/V, and proximo/distal [P/D]) (Irvine and Vogt, 1997;Panganiban et al, 1997;Shubin et al, 1997). Many of the pathways involved in this discussion are covered in more detail in other sections of the book, but here we use them to illustrate the validity of studying model organisms.…”