Extent With Modification: Leg Patterning in the BeetleTribolium castaneumand the Evolution of Serial Homologs

Abstract

Serial homologs are similar structures that develop at different positions within a body plan. These structures share some, but not all, aspects of developmental patterning, and their evolution is thought to be constrained by shared, pleiotropic gene functions. Here we describe the functions of 17 developmental genes during metamorphic development of the legs in the red flour beetle, Tribolium castaneum. This study provides informative comparisons between appendage development in Drosophila melanogaster and T. castaneum, between embryonic and adult development in T. castaneum, and between the development of serially homologous appendages. The leg gap genes Distal-less and dachshund are conserved in function. Notch signaling, the zinc-finger transcription factors related to odd-skipped, and bric-à-brac have conserved functions in promoting joint development. homothorax knockdown alters the identity of proximal leg segments but does not reduce growth. Lim1 is required for intermediate leg development but not distal tarsus and pretarsus development as in D. melanogaster. Development of the tarsus requires decapentaplegic, rotund, spineless, abrupt, and bric-à-brac and the EGF ligand encoded by Keren. Metathoracic legs of T. castaneum have four tarsomeres, whereas other legs have five. Patterns of gene activity in the tarsus suggest that patterning in the middle of the tarsal region, not the proximal- or distal-most areas, is responsible for this difference in segment number. Through comparisons with other recent studies of T. castaneum appendage development, we test hypotheses for the modularity or interdependence of development during evolution of serial homologs.

Patterning of the Adult Mandibulate Mouthparts in the Red Flour Beetle, Tribolium castaneum

“…The molar and incisor regions of Krn-depleted mandibles were both reduced, with the distal incisor area more severely affected. This distal bias is consistent with the Krn RNAi phenotypes of other appendages, including the legs (Angelini et al 2012). …”

“…Phenotypic penetrance varied across appendage types; Table 3 details the penetrance of dsRNA treatments in each mouthpart. The effects of these genes on metamorphic development of antennae, genitalia, and legs in T. castaneum appear elsewhere (Angelini et al 2009(Angelini et al , 2012Aspiras et al 2011). Other genes were also targeted for RNAi in those studies, and while they produced defects in other appendages, informative phenotypes were not produced in the mouthparts.…”

“…Depletion of hth caused dramatic shape changes in the proximal palps, stipes, cardo, prementum, and mentum, suggestive of partial homeotic transformations (Figure 4, B and C). Proximalto-distal homeotic transformations were observed in the legs of T. castaneum (Angelini et al 2012).…”

“…homothorax: homothorax is a homeodomain transcription factor required for normal development of proximal leg segments in T. castaneum (Angelini et al 2012), D. melanogaster (Abu-Shaar and Mann 1998; Wu and Cohen 1999;Yao et al 1999), and other insects (Angelini and Kaufman 2004;Ronco et al 2008). It is one of the leg gap genes (Rauskolb 2001).…”

“…First, we test the hypothesis that the main axis of the adult maxillary and labial appendages is patterned using genes also required in the leg development network. Key aspects of this network are conserved in the legs of numerous arthropods, suggesting that they were likely components of the leg patterning network of ancestral arthropods (e.g., Palopoli and Patel 1998;Abzhanov and Kaufman 2000;Jockusch et al 2000;Beermann et al 2001;Schoppmeier and Damen 2001;Inoue et al 2002;Rogers et al 2002;Angelini and Kaufman 2005b;Prpic and Damen 2009;Angelini et al 2012). Second, we test several hypotheses about the mechanism that governs branching of the PD axis to give rise to endites.…”