Enormous expansion of the chemosensory gene repertoire in the omnivorous German cockroach Blattella germanica

Abstract

The acquisition of genome sequences from a wide range of insects and other arthropods has revealed a broad positive correlation between the complexity of their chemical ecology and the size of their chemosensory gene repertoire. The German cockroach Blattella germanica is an extreme omnivore and has the largest chemosensory gene repertoire known for an arthropod, exceeding even the highly polyphagous spider mite Tetranychus urticae. While the Odorant Receptor family is not particularly large, with 123 genes potentially encoding 134 receptors (105 intact), the Gustatory Receptor family is greatly expanded to 431 genes potentially encoding 545 receptors (483 intact), the largest known for insects and second only to the spider mite. The Ionotropic Receptor family of olfactory and gustatory receptors is vastly expanded to at least 897 genes (604 intact), the largest size known in arthropods, far surpassing the 150 known from the dampwood termite Zootermopsis nevadensis. Commensurately, the Odorant Binding Protein family is expanded to the largest known for insects at 109 genes (all intact). Comparison with the far more specialized, but phylogenetically related termite, within the Dictyoptera, reveals considerable gene losses from the termite, and massive species‐specific gene expansions in the cockroach. The cockroach has lost function of 11%–41% of these three chemoreceptor gene families to pseudogenization, and most of these are young events, implying rapid turnover of genes along with these major expansions, presumably in response to changes in its chemical ecology.