IN MANY CASES even large phenotypic changes can occur without much genetic change. However, occasionally a species will be placed in a situation in which its ancestor’s genes are insufficient, and if the species possesses a gene that can be co-opted into a new role, selection can favor evolution of new genes and a corresponding radiation of species. The Pieridae family of butterflies lay their eggs on plants in the Brassicaceae family, which contains mustards and cabbages. These plants have evolved to produce compounds that are harmless in undamaged leaves, but when a leaf is damaged are converted to a potent insecticide. The pierids evolved a deactivating protein that diverts the chemical reaction to produce nontoxic products. This gene evolved shortly after the plants themselves, and would have allowed these butterflies’ larvae to feed upon these plants with little competition.
This brassicacean insecticidal strategy is known as the “mustard oil bomb“. The plant produces glucosinolates, a type of thioglycoside. When plant tissue is damaged myrosinases cleave off the sugar and the molecule rearranges to produce isothiocyanates, which are insecticidal. Pierid caterpillars avoid this poison by producing an enzyme in their gut, nitrile-specifier protein (NSP), that triggers rearrangement of isothiocyanates to non-toxic nitriles. Since this plant family contains many important crop plants and one pierid butterfly has become a wide-ranging invasive species (Pieris rapae, the cabbage white butterfly), the mechanism of this resistance has been studied, and now a new article examines the evolutionary origin of this gene.
Fischer and coworkers found that the gene sequence of NSP is unique, not resembling that of any other known butterfly detoxyifying enzymes. Comparison of the gene sequence across multiple insect species revealed high sequence similarity to Cr-PII protein produced by Blatella germanica, the German cockroach. This protein is produced in the gut and passed into the environment in cockroach droppings, where it causes allergic reactions in sensitized people. The Cr-PII protein is made of multiple repeats of one domain, called the major allergen (MA) domain. Many insects screened produced proteins with multiple MA domains, but most lepidopterans produced proteins with only one MA domain, called the single-domain MA family (SDMA). The roles of MA and SDMA are unknown. The Pierinae butterflies were unique in having two additional genes with three MA domains and a signal peptide. Combining this evidence, Fischer suggests the NSP gene evolved by duplication of SDMA, then the sequential duplication of two MA domains in the SDMA duplicate to produce a three-domain ancestral gene. This duplicated again and one duplicate evolved to produce the NSP gene, while the other eventually produced the two three-domain MA genes. Alternatively, after the initial production of the three-domain ancestral gene the two MA genes may have evolved first, and then NSP may have evolved from the duplication of one of these two genes. The diagram shown illustrates both routes of evolution (copyright 2008 Molecular Biology and Evolution). The NSP and MA genes are still rapidly evolving, indicating continued selection upon these genes.
The function of MA in butterflies is unknown. It does not have any ability to influence isothiocyanate production, so this is a novel mutation that arose in NSP. Determination of the role of MA may shed light on the evolution of NSP. The authors additionally note that we have little gene information for lepidopterans, so improving the number of sequenced genomes could greatly improve our understanding of the exact route followed in NSP evolution.
Fischer, H.M., Wheat, C.W., Heckel, D.G., Vogel, H. (2008). Evolutionary Origins of a Novel Host Plant Detoxification Gene in Butterflies. Molecular Biology and Evolution, 25(5), 809-820. DOI: 10.1093/molbev/msn014