Comparative analysis of gene expression patterns in the arthropod labrum and the onychophoran frontal appendages, and its implications for the arthropod head problem

Ralf Janssen

doi:10.1186/s13227-016-0064-4

Abstract

The arthropod head problem has troubled scientists for more than a century. The segmental composition of the arthropod head, homology of its appendages, and especially the nature of the most anterior region of the head are still, at least partially, unclear. One morphological feature of the head that is in the center of current debate is the labrum (upper lip), a fleshy appendicular structure that covers the arthropod mouth. One hypothesis is that the labrum represents a fused pair of protocerebral limbs that likely are homologous with the frontal appendages (primary antennae) of extant onychophorans and the so-called great appendages of stem arthropods. Recently, this hypothesis obtained additional support through genetic data, showing that six3, an anterior-specific gene, is exclusively expressed in the arthropod labrum and the onychophoran frontal appendages, providing an additional line of evidence for homology. Here I present data that put this finding into perspective. The outcome of my study shows that the homologization of a morphological structure by the expression of a single genetic factor is potentially misleading.

Highlights

The arthropod head problem has troubled scientists for more than a century
The idea has been put forward that the labrum is homologous with the frontal appendages of extant onychophorans and stem-group lobopodians and the great appendages of stem-group arthropods (e.g., [27,28,29,30]), but see [3, 16, 17] for another homology hypothesis
Putting the homology test to the test: taking a look beyond six3 In their very much noticed review article Scholtz and Edgecombe [3] suggested to search for genes that are expressed in the labrum and the frontal appendages since those patterns would likely serve as direct evidence for homology: “..., if peculiarities of gene expression in the labrum, which are absent in trunk limbs of euarthropods, find their correspondence in that of onychophoran ‘antennae,’ we could have direct evidence for homology between these two structures” [3]

Summary

Introduction

The arthropod head problem has troubled scientists for more than a century. The segmental composition of the arthropod head, homology of its appendages, and especially the nature of the most anterior region of the head are still, at least partially, unclear. One hypothesis is that the labrum represents a fused pair of protocerebral limbs that likely are homologous with the frontal appendages (primary antennae) of extant onychophorans and the so-called great appendages of stem arthropods. This hypothesis obtained additional support through genetic data, showing that six, an anterior-specific gene, is exclusively expressed in the arthropod labrum and the onychophoran frontal appendages, providing an additional line of evidence for homology. The idea has been put forward that the labrum is homologous with the frontal appendages of extant onychophorans and stem-group lobopodians and the great appendages of stem-group arthropods (e.g., [27,28,29,30]), but see [3, 16, 17] for another homology hypothesis

Methods

Results

Discussion

Conclusion