Joint morphology in the insect leg: evolutionary history inferred from Notch loss-of-function phenotypes in Drosophila

Abstract

Joints permit efficient locomotion, especially among animals with a rigid skeleton. Joint morphologies vary in the body of individual animals, and the shapes of homologous joints often differ across species. The diverse locomotive behaviors of animals are based, in part, on the developmental and evolutionary history of joint morphogenesis. We showed previously that strictly coordinated cell-differentiation and cell-movement events within the epidermis sculpt the interlocking ball-and-socket joints in the adult Drosophila tarsus (distal leg). Here, we show that the tarsal joints of various insect species can be classified into three types: ball-and-socket, side-by-side and uniform. The last two probably result from joint formation without the cell-differentiation step, the cell-movement step, or both. Similar morphological variations were observed in Drosophila legs when Notch function was temporarily blocked during joint formation, implying that the independent acquisition of cell differentiation and cell movement underlay the elaboration of tarsal joint morphologies during insect evolution. These results provide a framework for understanding how the seemingly complex morphology of the interlocking joint could have developed during evolution by the addition of simple developmental modules: cell differentiation and cell movement.

RhoGAP68F controls transport of adhesion proteins in Rab4 endosomes to modulate epithelial morphogenesis of Drosophila leg discs

“…During the early stages of pupal development (2–6h APF) cells in the epithelium of the Drosophila leg imaginal disc change shape (Condic et al, 1991; Greenberg and Hatini, 2011; Mirth and Akam, 2002; Tajiri et al, 2011), and rearrange contacts with their neighbors (Taylor and Adler, 2008), to narrow and so elongate and the future appendage (von Kalm et al, 1995). To examine the rearrangements of the epithelium along the apicobasal axis, we labeled nuclei with Dapi and the lateral membrane domain with Fas3 (Fig.…”

Ancestral reconstruction of tick lineages

“…The majority of arthropods have side-by-side or uniform flexible articulation joints (Tajiri et al 2011), as found in all argasids and ixodids. Of interest is that N.…”

“…Development of ball and socket joints in the Neoptera has been linked to Notch signalling and consequent cell differentiation and movement (Tajiri et al 2011(Tajiri et al , 2010.…”

Hexapoda: Comparative Aspects of Later Embryogenesis and Metamorphosis

“…In Drosophila , all joint formation is delayed until metamorphosis. Joint morphogenesis has been described in Drosophila (Mirth and Akam 2002 ), and a detailed evolutionary scenario accounting for different joint morphologies has been proposed (Tajiri et al 2011 ). In Drosophila , the gene regulatory networks patterning the primary and tarsal joints are distinct, but share core components ( Fig.…”