Milkweed bugs:
Using RNAi to understand the evolution of specialized mouthparts
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Milkweed bugs: |
The milkweed bug Oncopeltus fasciatus is a bright orange and black insect about an inch long. It has no economic importance -- it doesn't destroy crops, carry disease, or invade people's homes. Instead, it sucks on milkweed plants, mates, lays eggs, carries on the circle of life and minds its own business. So why study the milkweed bug? Because true bugs, or hemipterans, have evolved something unique -- specialized piercing-sucking mouthparts. |
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The Hemiptera use specialized mouthparts to pierce into their food and suck out the juice. (Some bugs attack plants and some bugs attack animals, but all use piercing-sucking mouthparts.) Their mouthparts have two sets of skinny stylets, needle-like appendages that form a sort of straw for sucking up liquid. The third set of appendages is fused into the labium, a long wide structure that acts like a flexible sheath to protect and support the stylets. These kind of specialized mouthparts have made bugs remarkably successful at eating a variety of food --just ask any gardener! |
The ancestors of the Hemiptera had very different mouthparts, more like a cricket's. The ancestral mouthparts consisted of a set of chewing teeth (the mandibles), a set of spoon-like palps (the maxillae), and a scooping lower lip (the labium). Somehow the ancestor of the Hemiptera were able to evolve dramatic changes in these appendages to transform them into two sets of piercing stylets and a long straight labium. What gene changes might have led to the evolution of the bug mouthparts?
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In the fruit fly, three Hox genes are known to determine the indentity of the mouthparts: Deformed, proboscipedia, and Sex combs reduced. These genes are critical for telling the cells what kind of appendage to make. For instance, if proboscipedia is mutated, the labium develops into a pair of legs! |
Are the same genes controlling mouthparts in the milkweed bug? We used RNAi to knockdown the level of the milkweed bug's proboscipedia gene... and the labium developed into a pair of legs! |
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However, there was an important difference in the phenotype between flies and bugs. In flies, the gene pb is important for development of both the maxillae and the labium. But in the bugs, pb is expressed only weakly in the maxillae, and the RNAi does not cause defects in the maxillae. Bugs differ from other insects by using pb to direct development of the labium and not the maxillae. This difference in the role of proboscipedia may be part of the mechanism by which the specialized mouthparts evolved. The shift in expression of pb out of the maxillae may have helped turn the maxillary palps into a pair of maxillary stylets. |
What about the other genes, Deformed and Sex combs reduced? Using RNAi, we found that they also play important roles in mouthpart development in the bug. On the right you see the phenotype resulting from triple RNAi injection of the three mouthpart Hox genes. When all three are knocked out, the three sets of mouthparts all develop into antennae. This gives a bug with eight antennae on it's head -- affectionately known as "squid head". |
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The role of Deformed seems to be similar between flies and bugs. In both species Dfd specifies mandibular and maxillary development, but the resulting morphology of the appendages are very different. This suggests that Dfd is determining the identity of the same mouthparts, but that the set of downstream genes has changed to produce different morphological outcomes. Since pb is absent from the maxillae of bugs, the Hox code is simply "Deformed" in both the mandibles and maxillae, explaining why the two pairs of stylets are so similar. So in the evolution of bug mouthparts, we have evidence for several important genetic changes. The shift in expression of pb out of the maxillae caused a loss of that role and may have led to simplification, loss of palps and similarity to the mandibles. Changes in target genes downstream of Deformed must have been necessary to give the appendages the unique stylet morphology. |
Although these special piercing-sucking mouthparts are unique to the Hemiptera, the evolution of specialized appendages as adaptations for different lifestyles is a major evolutionary problem. The advent of RNAi as a tool for studying gene function in non-genetic model organisms has been helpful for starting to address this difficult but very interesting problem. |
There are now a number of papers studying developmental genes in milkweed bugs. Milkweed bugs are quickly becoming the "model" non-model organism! mouthparts R. Denell and T. Shippy. (2001). Comparative insect developmental genetics: phenotypes without mutants. Bioessays 23(5):379-82. [Pubmed] B.T. Rogers, M. D. Peterson, and T. C. Kaufman. (2002). The development and evolution of insect mouthparts as revealed by the expression patterns of gnathocephalic genes. Evol Dev 4(2):96-110. [Pubmed] early development P. Z. Liu and T. C. Kaufman. (2004). Kruppel is a gap gene in the intermediate germband insect Oncopeltus fasciatus and is required for development of both blastoderm and germband-derived segments. Development 131(18):4567-79. [Pubmed] appendage development
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