The abundance and patterns of life on Earth depend on the origin of new species, and thus the process of speciation has become one of the most intriguing problems in biology. Species are thought to arise as populations become genetically distinct and individuals change in physical appearance, physiology, or behavior. Crucially for the origin and maintenance of new species in nature, some character changes limit interbreeding and prevent populations from fusing by gene exchange. Studying barriers to reproduction therefore provides a powerful approach to understand speciation.

One of the best ways of investigating speciation is to focus on currently evolving barriers to reproduction. The European corn borer (ECB) moth is an exciting organism for study because multiple barriers combine to influence reproductive patterns. Each barrier to reproduction allows for some interbreeding, but the two strongest involve behavior and ecology. In Europe and North America, females release, and males preferentially respond to different sex pheromones. Mating choice differences lead to a partial behavioral barrier to reproduction between “E” and “Z” pheromone strain populations. At locations in the Northeastern U.S., pheromone strains also differ in the physiological timing of overwintering diapause. This leads to an ecological barrier to reproduction because mating occurs during different times of the growing season. Z-strain adults mate mid-season in late July and have only a single generation of offspring. E-strain adults mate earlier in June and their offspring then produce a second generation at the end of the season in mid-August. At still other locations in the U.S., moth populations share mate preferences and are Z strain, but differ in seasonal timing. Therefore, co-occurring populations of ECB moth can vary in mating choice, mating time, or both. 

While it has long been appreciated that speciation typically involves multiple barriers to reproduction, there has been limited study of differences in mating time and interacting barriers to reproduction, leading to an incomplete perspective of the origin of new species. By studying barriers in ECB moths, we gained insight into how the evolution of interacting barriers influence the speciation process. 

Our results provide a complete gene-to-trait link for the evolution of insect diapause. We show that genetic changes on the sex chromosome responsible for diapause and mating time also control circadian rhythm. Functional ties between circadian and seasonal rhythm have long been a source of speculation, but thus far there has been limited evidence that regulation of “clock” genes also control insect life cycles. Along with earlier results showing that the sex chromosome also determines mating choice, our findings support accumulating evidence arguing for a major influence of the sex chromosome during speciation. 

We further developed insight into the causes of evolution. Although the precise environmental drivers of change in diapause still remain unknown, we found a connection between broad climatic gradients and genetic change at a clock gene underlying diapause. Genetic changes in this and other clock genes associate with geographic variation in the number of generations per year, providing the first clear evidence of genetic control over this important aspect of insect population growth. 

Finally, we studied the relative importance of behavior and ecology as populations become genetically distinct. We established that patterns of interbreeding and genetic exchange between populations depend on both ecological differences in mating time and behavioral differences in pheromone preference. Evidence suggests that mating time and mating choice are both weak barriers to reproduction when acting alone. However, there is limited genetic exchange in parts of the genome when ecology interacts with behavior, and specifically along a sex chromosome region where genes have an inverted order. Thus, changes in genome organization along with accumulating barriers to reproduction appear to be important for the maintenance of genetically distinct populations in nature. While the role of inverted chromosomes during speciation is widely appreciated, relevant barriers to reproduction are unknown for most organisms and therefore our studies helped fill an important knowledge gap about the factors influencing the origin of new species in nature.

Our work also had a number of broader impacts. We implemented an outreach program providing a unique opportunity to involve undergraduate students and urban youth in active research, education, and community service on local farms. Because the ECB moth is an invasive pest, studies of behavior and ecology are relevant for sustainability and a critical management step is determining local abundance. Our program used insect traps to provide this key information to local farms and to Massachusetts Cooperative Extension so that they could make farming recommendations in newsletters. Trapped moths provided valuable research specimens and enabled student participation in field-based scientific research aimed at solving real-world problems in evolutionary ecology and agriculture. The project supported the research and education of 5 PhD and 2 Master’s students, 1 postdoctoral researcher, 7 undergraduate students, and over 50 middle-school children living in the Boston, MA area. 

Last Modified: 08/17/2018
Modified by: Erik Dopman