Divergent role of the Hox gene Antennapedia in spiders is responsible for the convergent evolution of abdominal limb repression

Abstract

Evolution often results in morphologically similar solutions in different organisms, a phenomenon known as convergence. However, there is little knowledge of the processes that lead to convergence at the genetic level. The genes of the Hox cluster control morphology in animals. They may also be central to the convergence of morphological traits, but whether morphological similarities also require similar changes in Hox gene function is disputed. In arthropods, body subdivision into a region with locomotory appendages (“thorax”) and a region with reduced appendages (“abdomen”) has evolved convergently in several groups, e.g., spiders and insects. In insects, legs develop in the expression domain of the Hox gene Antennapedia ( Antp ), whereas the Hox genes Ultrabithorax ( Ubx ) and abdominal-A mediate leg repression in the abdomen. Here, we show that, unlike Antp in insects, the Antp gene in the spider Achaearanea tepidariorum represses legs in the first segment of the abdomen (opisthosoma), and that Antp and Ubx are redundant in the following segment. The down-regulation of Antp in A. tepidariorum leads to a striking 10-legged phenotype. We present evidence from ectopic expression of the spider Antp gene in Drosophila embryos and imaginal tissue that this unique function of Antp is not due to changes in the Antp protein, but likely due to divergent evolution of cofactors, Hox collaborators or target genes in spiders and flies. Our results illustrate an interesting example of convergent evolution of abdominal leg repression in arthropods by altering the role of distinct Hox genes at different levels of their action.

Antennapedia is involved in the development of thoracic legs and segmentation in the silkworm, Bombyx mori

“…In insects, the Antp gene is highly conserved in its morphological homeotic function, specifying segment identity. In a non-insect arthropod, the spider A. tepidariorum, the Antp gene represses the development of legs in the first segment of the abdomen (Khadjeh et al, 2012). Our data showed that homozygous mutation in BmAntp produced the fused thorax and antennae-like appendages between the head and the thorax (Figure 1).…”

“…Ectopic expression of the Antp gene leads to distinct phenotypes, such as the transformation of antennae into second legs and eye reduction (Schneuwly et al, 1987;Plaza et al, 2008;Prince et al, 2008). Moreover, in the spider Achaearanea tepidariorum, a non-insect arthropod, the Antp gene represses the growth of legs in the first segment of the abdomen (Khadjeh et al, 2012). There are reports of extensive studies, but further exploration of the particular role of the Antp gene underlying the development of the thorax and thoracic appendages is needed.…”

A conserved genetic mechanism specifies deutocerebral appendage identity in insects and arachnids

“…Concordantly, functional data have demonstrated that the spider Antp orthologue represses limb development in the opisthosoma of Parasteatoda tepidariorum [30]. By contrast, expression dynamics of hth are more comparable to insect counterparts.…”

“…Indeed, Hth and Exd are bona fide Hox cofactors in D. melanogaster [22,44 -46]. However, functional data for chelicerate Hox genes are limited to analysis of Antp, and thus the interaction of hth and anterior Hox genes is unknown for chelicerates [30]. In addition, Antp in the spider P. tepidariorum appears to have a function that is convergent upon the role of Ultrabithorax in insects (i.e.…”

Regressive evolution of the arthropod tritocerebral segment linked to functional divergence of the Hox genelabial

“…Because targeted misexpression is not yet available in P. tepidariorum, we achieved activation of lab-1 in the L1 segment by interfering with the function of the Hox gene Dfd. Dfd is expressed in all four walking leg segments and thus posteriorly adjacent to the pedipalpal segment [21]. RNAi with Dfd leads to the ectopic expression of lab-1 (figure 3d,e), but not of lab-2 (figure 3f ), in the L1 segment.…”