Pheromone emergencies and drifting moth genomes

At the heart of evolutionary biology is the endeavor to characterize how descent with modification occurs within species and how these processes can, at times, produce a novel group of individuals different enough from the others in their group that we dub them a new species. We lump the mechanisms that split these individuals (or groups thereof) into two broad categories of pre- and postmating isolation mechanisms, each of which can be further subdivided. It is within the premating class of isolation mechanisms that changes to pheromone systems occur. In general terms, pheromones are sex attractants that a species produces to attract individuals of the opposite sex of the same species. Their interest to those working in the field of evolutionary biology is intense for the aforementioned reasons, and they have an equally intense interest to those engaged in the science and practice of agriculture as amenas to monitor or possibly control pest species, such as moths. Female moths use sex pheromones to attract mates across a potentially long geographic distance. The bichemical basis of how moth female sex pheromones are synthesized has been elucidated in a number of species, and a particularly large amount of effort has been expended on the agricultural pest Ostrinia nubilalis, which is commonly known as the European corn borer (ECB). The females of this species and its close relative, the Asian corn borer (ACB; O. furnacalis), use a blend of 14-carbon acetate E/Z isomers. One of the key enzymatic steps in the biosynthesis of these blends is desaturation catalyzed by acyl-CoA desaturases that exhibit unique substrate specificities, as well as regio- and stereoselectivities (1). The enzymes that catalyze the biosynthesis of the ECB and ACB blends belong to a group known as the Z/E D11 desaturases (2). Given their importance to corn borer reproductive biology, scientists from a broad array of disciplines are interested in understanding how these enzymes have evolved and how they contribute to corn borer speciation. In PNAS, Fujii et al. (3) show that a cryptic gene catalyzes the female sex pheromone of a primitive member of the genus Ostrinia, the Far Eastern knotweed borer (FKB; O. latipennis).

Xue et al. (4) found a family of retroposon–desaturase fusion genes in the ECB and ACB, which they termed ezi desaturases. The retroposon part of these genes is derived from a long interspersed element (LINE) closely related to a LINE that they also found in the silkworm genome, which they named kaikoga (4). Despite the obvious disruption of the normal desaturase gene structure, there was no indication that ezi desaturases are pseudogenes. In fact, statistical analysis of the rate of nucleotide and amino acid substitution suggested that these fusion genes have been retained in the genus Ostrinia for several million years; however, confirmation from another member of the genus was missing. Fujii et al. (3) go a long way to help answer this question by showing that the FKB genome possesses a normal desaturase gene (which they term LATPG1) that is derived from within the ezi desaturase radiation on the basis of its phylogenetic clustering pattern (Fig. 1). This result, however, raises even more questions.

Fig. 1.

Timing of events producing the major categories of D11 and ezi desaturases in Ostrinia.

Fujii et al. (3) point out that the pheromone of FKB is not a blend but a single-component product, which is comprised entirely of (E)-11-tetradecenol, as opposed to the pheromone blends synthesized by ECB and ACB. Fujii et al. (3) conclude that it is impossible at present to infer whether the single-component pheromone of the FKB is a derived trait and the possession of a pheromone blend is a primitive feature or if the converse is true. Given that the normal state in other moth species is to produce a blend of pheromone components, it is probably safe to assume that the single-component blend of the FKB is a derived condition, despite the fact that it is a primitive member of the genus Ostrinia. However, where does the relationship to ezi desaturases come in?

Based on the facts that ezi desaturases are divided into two groups (α and β) and that LATPG1 clusters at the base of the α-ezi gene group, we have two very interesting possible inferences: (i) the ezi–desaturase fusion event occurred two times independently, or (ii) it occurred only one time, but the ezi component of the LATPG1 gene was subsequently lost. Of the two possibilities, the most parsimonious explanation is the second, although it is by no means the easiest to explain. The most likely course of events probably involved unequal cross-over that produced the intact LATPG1 gene. If so, should we observe an ezi remnant (if not a full ezi–desaturase fusion gene) in the FKB genome? For this, we will need genomic studies, which are currently lacking in this species.

More interestingly, the question remains: what are these ezi–desaturase fusion genes doing in Ostrinia genomes? One possibility is that the fusion genes have lost their functions and represent junk genes. However, Xue et al. (4) clearly showed that ezi–desaturase fusion genes have remained conserved for several million years; moreover, statistical analyses on the probability of pseudogenization revealed that the probability is extremely low that ezi desaturases have become pseudogenized. However, it is possible that these genes have taken on a role in the genomes in which they exist. In this case, it is possible that this role evolved through a process of exaptation (5) in which the ezi LINE was used for some unknown function. Indeed, the exaptation of retroposons has been documented to have occurred in primates for the vitamin D-mediated innate immune response (6) and the vertebrate neurodevelopmental gene ISL1 (7). Recently, Okada et al. (8) concluded that the exaptation of retroposons ∼250 Mya in the ancestor of modern mammals allowed for adaptation of the brain to a novel environment. Okada et al. (8) likened this to an emergency response of having to adapt to a new environment, which in this case, was brought on by a cataclysmic event. According to Okada et al. (8), an organism can use the pieces of junk DNA available in its genome to piece together a new gene or set of genes, which could be used to fill a new function.

If that is the case with Ostrinia species, what sort of emergency situation might have prompted the exaptation of the ezi element in the Ostrinia genome to produce a fusion with a sex pheromone desaturase? This argument is selectionist at heart, assuming that the drive to adaptation must be at the heart of our observations. Another possibility is that the process of genomic drift (9) is responsible for the evolution of ezi fusion genes in Ostrinia, as well as the unique single-component pheromone system of the FKB. Genomic drift is the random change in gene copy number observed in a multigene family that undergoes birth and death evolution (10). Previously, it has been shown that sex pheromone desaturases undergo birth and death evolution (1, 2, 4, 10). Therefore, the mechanism for driving these events is present. The stochastic nature of genomic drift could very well have produced a scenario in which birth and death mechanisms led to the inactivation or loss of normal D11 desaturase genes (for example, those encoding Z/E11 isomers).Through birth and death gene dynamics, the ezi–desaturase fusion event occurred. Once established, this fusion event provided a genomic scaffold on which unequal cross-over (also expected under birth and death dynamics) may have given rise to LATPG1 and the birth of the single-component pheromone system. Of course, we have no concrete proof that these events occurred, although their likelihood seems high given what we know about the genomic complement of sex pheromone desaturases in the Ostrinia species. Ultimately, we must determine whether ezi desaturase genes have any functionality at all. This important question remains to be answered.