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

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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-016-0064-4) contains supplementary material, which is available to authorized users.

Fossils from South China redefine the ancestral euarthropod body plan

“…The presence of one or two pairs of 'antennae' in Antennacanthopodia [51] in addition to a pair of lobopods associated with the 'head' well supports the relative plasticity of protocerebral appendages in the totalgroup Onychophora [50]. It has also been argued that genetic evidence for homology between the onychophoran antennae and the arthropod labrum should be interpreted with caution in light of the complexity of genetic networks [52].…”

Sequence heterochrony led to a gain of functionality in an immature stage of the central complex: A fly–beetle insight

“…To compare CX development between 2 species, we wanted to mark a subset of homologous neurons that contribute to the CX. For this purpose, we decided to use the rx genetic neural lineage for 3 reasons: First, rx is one of the genes that is expressed almost exclusively in the anterior brain in bilaterians, indicating a highly conserved function in many animals [49][50][51][52][53][54][55][56][57]. Second, we had found projections into the CX in a Tribolium rx enhancer trap line and a small subset of CX projections in Drosophila rx VT-GAL4 lines (VDRC, # 220018, # 220016, discarded) [58,59].…”

The nervous and visual systems of onychophorans and tardigrades: learning about arthropod evolution from their closest relatives

“…Nonetheless, many researchers questioned the appendicular origin of the arthropod labrum (reviewed by Scholtz and Edgecombe 2006) as dll, for example, is not expressed solely in the segmental appendage anlagen, thus rendering this marker as rather noninformative for this purpose. A recent gene expression study shows that, although a single gene (six3) is expressed in both the arthropod labrum and the onychophoran antennae (Eriksson et al 2013a), another gene (FoxQ2) is expressed exclusively within the anlage of the labrum but not in the antennal anlagen of onychophorans (Janssen 2017). Therefore, it has been suggested that conclusions concerning labrum homology based on the expression of single genes should be considered carefully (Janssen 2017).…”

“…A recent gene expression study shows that, although a single gene (six3) is expressed in both the arthropod labrum and the onychophoran antennae (Eriksson et al 2013a), another gene (FoxQ2) is expressed exclusively within the anlage of the labrum but not in the antennal anlagen of onychophorans (Janssen 2017). Therefore, it has been suggested that conclusions concerning labrum homology based on the expression of single genes should be considered carefully (Janssen 2017). An alternative hypothesis suggests that the labrum does not have an appendicular origin, but is instead homologous to the anterior-most pair of lip papillae of onychophorans, while the onychophoran antennae, in turn, might be homologous to the frontal filaments of some crustaceans Richter 2013, 2016;Richter et al 2013).…”