Moths that pass in the night: Reproductive isolation due to pickiness, or just bad timing?

On a summer night in a Florida corn field, a female armyworm moth emerges from her underground cocoon and spreads her wings to dry in the humid air. Over the next few weeks, she will fly miles away in search of a mate, and a likely-looking patch of host plants on which to lay her eggs.

Her brief adult life will be shaped in many ways by the life she led as a larva, feeding on domestic corn. She could easily find other grasses to feed her offspring, but she'll probably seek out another cornfield. She may encounter armyworm males who were raised on many other grasses, but the odds are that the males she accepts as mates will also have grown up eating corn. This is so likely to be the case that it has left a mark on the genetics of her species [PDF].

At night in a cornfield, moths mate nonrandomly. Photo by K e v i n.

Yet it isn't clear how much of this isolation between armyworms from corn (the "corn strain") and armyworms from other grasses (called the "rice strain") arises because moths from the different host plants actively prefer mates from their own larval food plant, or because they just don't encounter moths from the other food plants as frequently. Like many moths, armyworms of both sexes deploy pheromones to attract and woo mates—so maybe armyworms from the same food plant smell better to each other. On the other hand, corn-strain armyworms do more of their mate searching early in the evening (although they'll keep hunting all night), while rice-strain armyworms wait to search till the last few hours of nighttime.

Disentangling which of these two sources of isolation—preference versus timing—maintains the genetic differences between host plant strains of the armyworm takes some careful experimental work. As in many biological questions, the answer might well be not one or the other, but a little of both [$a].

In a study published in the latest issue of The American Naturalist, a team of entomologists at the Max Planck Institute for Chemical Ecology took on the question of what keeps the armyworm host strains separated. They performed two mating experiments with laboratory-reared moths of both sexes from both strains.

Fall armyworm adult. Photo via Wikimedia Commons.

First was a "no-choice" experiment in which moths were kept in a chamber with a single member of the opposite sex from their own strain, or the other strain. The test was repeated over three nights in a row. On the first night, females from the corn strain were less likely to mate with males of the rice strain than males of their own, and when they did accept rice-strain males, it wasn't till later in the night. The second and third nights, though, corn-strain females mated about equally with males of both strains. Rice-strain females mated with males of both strains at about equal frequency all three nights, although they did so late in the night.

In the second round of experiments, moths were introduced into flight cages with one member of the opposite sex from each of the two host strains, so they could choose between them. To control for the differences in timing of mate searching between the two strains, the team repeated the experiment twice—in one version, the choosing moth had the entire length of the night to pick a mate, and in the other, the moths were only put into the same cage for the last four hours of the night, when the grass strain prefers to mate.

Fall armyworm larva. Photo by agrilifetoday.

In the all-night experiment, corn-strain males and females were both more likely to choose a mate from their own strain than the other. Rice-strain moths of both sexes mated with moths of both strains about equally—but rice-strain females were less likely to choose any mate at all. On the other hand, when the research team waited till the end of the night to introduce the test moths to their possible mates, rice-strain moths of both sexes mated much more frequently overall, and rice-strain females strongly preferred rice-strain males. Corn-strain males were basically indiscriminate in the late-night experiment, and corn-strain females were also less choosy.

In short, when mating during their usual activity periods, females of both strains were choosy about their mates; but when offered mates at the wrong time, they didn't discriminate as much. The authors suggest that these mistimed matings were less discriminating because they were more likely to be initiated by the males, who showed relatively weak preferences even during their own usual mating times.

So the genetic differentiation between armyworm host strains is probably due to both timing and mate choice, and the two isolating factors affect males and females differently. Females, particularly rice-strain females, are quite picky about mating with a male of their own strain. Males, on the other hand, seem mainly to be prevented from pursuing females of the other strain by the fact that their respective schedules don't line up. As the study's authors conclude, all these individual rejections and missed connections, added up across entire armyworm populations, bring these moths a little bit closer to speciation.

References

Prowell, D., McMichael, M., & Silvain, J. (2004). Multilocus genetic analysis of host use, introgression, and speciation in host strains of fall armyworm (Lepidoptera: Noctuidae). Annals Entomol. Soc. America, 97 (5), 1034-44 DOI: 10.1603/0013-8746(2004)097[1034:MGAOHU]2.0.CO;2

Schöfl, G., Dill, A., Heckel, D., & Groot, A. (2011). Allochronic separation versus mate choice: Nonrandom patterns of mating between fall armyworm host strains. The American Naturalist, 177 (4), 470-85 DOI: 10.1086/658904