Modulations in Hox expression patterns within fields that contribute to insect diversity

Homologous insect appendages have become diversified in the context of a highly conserved pattern of Hox gene expression along the main body axis. Nevertheless, some important differences exist in Hox deployment within the homologous limb fields of different insects.

We return to the subject of insect abdominal limbs to discuss an apparent evolutionary atavism—that is, reversion to a more ancestral state. Recall that, in general, adult insects do not have abdominal limbs. However, butterfly caterpillars (and some other insect larvae) do have abdominal limb-like structures called prolegs, which are used in locomotion. These stubby prolegs are not jointed like thoracic limbs, but their development is marked by Dll expression in embryos. How does this Dll expression escape repression by Ubx and abd-A in the abdomen?

In early stages of larval development, there is uniform expression of Ubx and abd-A and no sign of Dll expression or proleg outgrowth in the butterfly abdomen. Later, however, the expression of Ubx and abd-A is turned off within small clusters of cells in the A3-A6 abdominal segments, just before proleg development begins. These cells then begin to express Dll and to grow out from the body wall (Fig. 5.15). Thus the apparent evolutionary reversal that allows larval prolegs to develop in lepidopterans appears to be a segment-specific modification of abdominal Hox gene expression. Interestingly, sawfly (Hymenoptera) larvae, which also possess abdominal prolegs, circumvent Hox-mediated limb repression differently than caterpillars, by initiating proleg formation independent of Dll expression.

A second example of an evolutionary modification of insect limb patterning that is correlated with changes in Hox expression within the limb field has been identified in several Drosophila species. Subtle differences have been noted in the pattern of tiny leg hairs (trichomes) on the second thoracic legs of Drosophila melanogaster, Drosophila simulans, and Drosophila virilis (Fig. 5.16). In D. melanogaster, trichomes do not form in a certain region of the posterior femur of the T2 leg, resulting in a small "naked valley" of smooth epidermal cuticle. This "naked valley" is associated with high levels of Ubx expression, and indeed Ubx acts to repress trichome development. D. simulans has a larger "naked valley" and high levels of Ubx expression over an expanded region of the T2 femur. The more distantly related

Figure 5.15

Changes in Ubx and Abd-A expression correlate with the development of abdominal limbs in butterfly larvae

Butterfly larvae have abdominal limbs (prolegs) that form on segments A3-A6 (a). Dll protein is expressed in all developing larval limbs, including the abdominal prolegs (b), suggesting that Hox repression of abdominal Dll expression has been released during butterfly development. This release from repression is correlated with the disappearance of Ubx and Abd-A proteins from the cells that express Dll and form prolegs in the abdomen (c). Abdominal proleg development occurs because of the loss of Ubx and abd-A expression, rather than because Hox repression of Dll changes.

Sources: Part b from Panganiban G, Nagy L, Carroll SB. The role of Distal-less in the development and evolution of insect limbs. Curr Biol 1994; 4: 671-675; part c from Warren R, Nagy L, Selegue J, et al. Nature 1994; 372: 458-461.

Drosophila virilis lacks a "naked valley" in the T2 trichome array and exhibits only low levels of Ubx expression.

Careful genetic dissection of the differences in trichome patterning between D. melano-gaster and D. simulans has indicated that evolutionary differences in the level and extent of Ubx expression map genetically to the Ubx locus. This finding indicates that the source of evolutionary divergence in trichome patterning between D. melanogaster and D. simulans lies within these fruit flies' respective Ubx cis-regulatory control regions. Since the time of the last common ancestor of these species, sequence changes must have evolved in Ubx cis-regulatory elements that led to a relative increase in Ubx expression in the T2 femur of D. simulans. In this way, regulatory evolution at the Ubx locus contributed to a quantitative change in T2 leg morphology between Drosophila species.

This example demonstrates a potential link between the larger shifts in Hox expression seen among distantly related arthropods and the generally similar patterns of Hox expression between insects. That is, if even slight differences can evolve in domains of Hox gene expression between fairly closely related species, then one can begin to conceive of how larger shifts might arise over greater periods of evolutionary time.

Drosophila Melanogaster Hox

Figure 5.16

Evolutionary changes in Ubx expression regulates morphological differences between related Drosophila species

Trichomes (small leg hairs) cover much of the femur of the T2 legs of different Drosophila species. A "naked valley" devoid of trichomes (area between arrowheads) appears on the posterior T2 femur of Drosophila melanogaster (a) and D. similans (b), but not D. virilis (c). The level of Ubx protein expression in this region controls the size of this "naked valley" in D. melanogaster and D. similans during pupation. High levels of Ubx (dark red) repress trichome formation; lower levels do not (orange-yellow). The evolutionary differences in leg morphology and Ubx expression between these species reflect changes in the cis-regulation of Ubx. Source: Modified from Stern DL. Nature 1998; 396: 463-466. Copyright (1998), reprinted with permission from Nature.

Figure 5.16

Evolutionary changes in Ubx expression regulates morphological differences between related Drosophila species

Trichomes (small leg hairs) cover much of the femur of the T2 legs of different Drosophila species. A "naked valley" devoid of trichomes (area between arrowheads) appears on the posterior T2 femur of Drosophila melanogaster (a) and D. similans (b), but not D. virilis (c). The level of Ubx protein expression in this region controls the size of this "naked valley" in D. melanogaster and D. similans during pupation. High levels of Ubx (dark red) repress trichome formation; lower levels do not (orange-yellow). The evolutionary differences in leg morphology and Ubx expression between these species reflect changes in the cis-regulation of Ubx. Source: Modified from Stern DL. Nature 1998; 396: 463-466. Copyright (1998), reprinted with permission from Nature.

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