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written by: Ben Burgunder Many of us are fascinated by insects and their stories. We are amazed by the transformation of the earth-bound caterpillar to the glorious butterfly. But before a caterpillar can become a butterfly, it first must hatch from the egg. How much do we know about the building blocks that allow a tiny egg to become a caterpillar in the first place? A largely unexplored world of genetic machinery tirelessly works to form the developing embryo beneath the egg’s shell. With advanced genetic tools, researchers can tinker with the embryological building blocks that shape caterpillars and begin to reveal this hidden world.  Figure 1 The painted lady butterfly (Vanessa cardui) is a common but stunning sight in North American gardens and natural spaces. Photo: John Deitsch Dr. Ximena Gutiérrez Ramos, a postdoctoral associate in the Pick Lab at the University of Maryland, is one of these researchers expanding our understanding of embryonic genetics. Dr. Gutiérrez Ramos researches the embryos of painted lady butterflies (Vanessa cardui). These striking orange, black, and white butterflies (Figure 1) are a familiar sight across North America and are even commonly sold as pets for budding scientists to raise and release. One study estimates that US consumers spend 20 million dollars on this species every year (Losey et al., 2022). The ease of raising this species also attracted Dr. Gutiérrez Ramos, who needed a butterfly that could be easily manipulated in the lab. Despite the great diversity of adult insects, many insect embryos look similar (Figure 2). While some would assume that this similarity would extend to the genes kickstarting embryogenesis, Dr. Gutiérrez Ramos’s research challenges this assumption by investigating the differences in the pair-rule genes between species. Pair-rule genes establish the alternate segment primordia in insect embryos.  Figure 2 Insects can look very similar as embryos but totally different as adults; Figure: Dr. Ramos While certain pair-rule genes may be found in multiple insects, these genes may serve very different purposes depending on the species. Previous Pick Lab research had determined that paired (prd), which is required for alternate segment formation in the fruit fly Drosophila melanogaster, is lost in the mosquito Anopheles stephensi. This challenged the belief that prd determined developmental segmentation in all insects. A different gene, gooseberry (gsb), has taken over its function instead (Cheatle Jarvela et al. 2024).  Figure 3 Loss of gsb causes mosquito larvae to lose the alternate segments (d) when compared to control mosquitoes (c). Figure: Cheatle Jarvela et al. 2020 Following Cheatle Jarvela et al. 2020, Lepidoptera, the insect order containing butterflies and moths, was the only major order of insects unexplored for the presence and function of prd.
Dr. Gutiérrez Ramos built a phylogenetic tree using sequenced genomes of 20 lepidopterans spread across the order’s gigantic family tree and determined that prd was lost. Without prd, would gsb play a similar role in painted ladies as it does in mosquitoes? The first step was to check if, where, and when gsb was expressed in the developing embryos using in-situ hybridization, which binds dye to probes that bind to copies of the target mRNA within the embryo. She found that gsb was expressed in stripes throughout the butterfly embryo starting roughly eight hours after the egg was laid. Since prd is similarly distributed in alternating segments in Drosophila, Dr. Gutiérrez Ramos wondered whether has similar functions as in the formation of alternate segments. To find out gsb’s purpose in the embryo, Dr. Gutiérrez Ramos decreased the expression of the gene and watched what unfolded. To accomplish this, Dr. Gutiérrez Ramos used embryonic RNA interference (eRNAi), in which the developing embryo is tricked into thinking the messenger RNA (mRNA) of a target gene is an invading virus and destroys all copies (Agrawal et al. 2003). Without any gsb mRNA, painted lady embryos are forced to develop without the gene’s influence. Dr. Gutiérrez Ramos painstakingly injected hundreds of butterflies’ eggs to silence the gene and determine its role in development. That effort paid off when Dr. Gutiérrez Ramos discovered that without gsb, caterpillars did not hatch, and after dissection of the unhatched embryos, she observed caterpillars that were only heads, heads with one set of prolegs (leg-like appendage in the abdominal segments), or as odd, strange donut-shaped caterpillars with laterally fused segments. While reducing gsb expression majorly affected painted lady development, the appearance of caterpillars caused by its knockdown did not resemble the changes caused by removing a typical pair-rule gene. While prd has been lost in moths, butterflies, and mosquitoes, unlike in mosquitoes, lepidopteran gsb does not act as a pair-rule gene. With this discovery, Dr. Gutiérrez Ramos plans to further explore the diversity and function of pair-rule genes in painted ladies and is working on investigating how some pest lepidopteran embryos develop. Her work on painted lady embryology demonstrates that even though insect embryogenesis may appear superficially similar, there are different genetic pathways that converge on the same pattern of segmentation. She has begun to chip away at the unknown depths of the genetic embryology iceberg, but there is still so much more to discover! Author Ben Burgunder is a third-year master’s student in the Fritz Lab. He is interested in whether mosquito vector community composition and West Nile virus prevalence can help explain patterns of human West Nile virus cases in Chicago. He can be reached at [email protected]. Literature Cited:
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