Ubx Regulates Differential Enlargement and Diversification of Insect Hind Legs

Abstract

Differential enlargement of hind (T3) legs represents one of the hallmarks of insect evolution. However, the actual mechanism(s) responsible are yet to be determined. To address this issue, we have now studied the molecular basis of T3 leg enlargement in Oncopeltus fasciatus (milkweed bug) and Acheta domesticus (house cricket). In Oncopeltus, the T3 tibia displays a moderate increase in size, whereas in Acheta, the T3 femur, tibia, and tarsus are all greatly enlarged. Here, we show that the hox gene Ultrabithorax (Ubx) is expressed in the enlarged segments of hind legs. Furthermore, we demonstrate that depletion of Ubx during embryogenesis has a primary effect in T3 legs and causes shortening of leg segments that are enlarged in a wild type. This result shows that Ubx is regulating the differential growth and enlargement of T3 legs in both Oncopeltus and Acheta. The emerging view suggests that Ubx was co-opted for a novel role in regulating leg growth and that the transcriptional modification of its expression may be a universal mechanism for the evolutionary diversification of insect hind legs.

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

“…The interplay of the Hox proteins and the upstream and downstream factors that influence their action has been termed the Hox gene pathway (13). Changes at multiple levels of this pathway are linked to morphological diversity: Changes in the expression of Ubx have been implicated in mouthpart diversity in crustaceans (14-16), evolution of femur shape in Drosophila (17,18), or the evolution of novel appendage morphologies in grasshoppers (19) and waterstriders (20). Changes can also take place in the targets of a Hox gene, as has been suggested for Ubx as the cause for the differences in insect hindwing morphology (21,22), or for Sex combs reduced (Scr) as the cause for the evolution of the dorsal helmet in treehoppers (23).…”

Evolving expression patterns of the homeotic gene Scr in insects

“…The results obtained identified key changes in expression patterns of Ubx that directly correlated with changes in arthropod body plans Angelini and Kaufman, 2005;Averof and Patel, 1997;Castelli-Gair and Akam, 1995;Damen et al, 1998;Mahfooz et al, 2004;Peterson et al, 1999;Stern, 1998;Telford and Thomas, 1998;Zheng et al, 1999). In insects, Ubx expression has also been linked to the differential enlargement of insect hind (T3) legs, which were subsequently confirmed by functional studies (Mahfooz et al, 2007;Mahfooz et al, 2004). As illustrated by these findings, the availability of cross-reacting antibodies are critical in that they provide better phylogenetic sampling by circumventing the laborious process of cloning and characterizing orthologous genes.…”

“…Numerous studies have shown that changes in the expression and function of homeotic (hox) genes were pivotal in the evolution of the insect bauplan (Beeman et al, 1993;Beeman et al, 1989;Carroll et al, 2001;Hughes and Kaufman, 2000;Hughes and Kaufman, 2002;Mahfooz et al, 2007;Mahfooz et al, 2004;Rogers et al, 1997;Rogers et al, 2002;Struhl, 1982;Tomoyasu et al, 2005). This insight was primarily based on mRNA expression patterns, however, data on protein accumulation are much more limited.…”

Annelids in evolutionary developmental biology and comparative genomics

“…Changes in the expression of these genes can have a role in morphological evolution (e.g. Averof & Patel, 1997;Cohn & Tickle, 1999;Mahfooz et al, 2007), and the expression of Hox genes is conventionally thought to be linked to their organisation in ordered clusters (Duboule & Morata, 1994). The relationship between cluster organisation and gene expression has been most clearly demonstrated in the mouse (Kmita & Duboule, 2003).…”