Attraction gone wrong: butterfly mating and habitat choice

Leptidea sinapis and L. juvernica, two similar-looking species of Wood White butterfly, coexist across much of Northern Europe. Oddly enough, though, the two switch between being habitat specialists and generalists throughout their range. In some places, L. juvernica is a specialist which can only live in meadows while L. sinapis can move freely between meadows and forests; in other areas, the opposite is the case — L. sinapis is the specialist and L. juvernica the generalist. Specialist populations of each species aren't more closely related to each other than to generalist populations, so the switch probably results from local factors rather than genetics. Obvious factors like which host plants they prefer for food or egg-laying have also been ruled out. So what makes these two species switch specialist and generalist roles?

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Magne Friberg and his colleagues at Stockholm University suspected that the switch might result from the combined effects of population density and the butterflies' courtship behaviour. The two species look very similar, so males often court females of the wrong species. A male Wood White courts a female by following her until she lands on a plant, at which point he sets down where she can see him and waves his proboscis. The females have no choice but to put up with it. They can try to fly away, but males can easily pursue them and keep trying. Simply giving in isn't a good choice either, since mating usually takes an hour (but can last up to ten hours!), which is longer than the typical courtship. In other words, female Wood Whites have to endure serious demands on their time from eager males — often of the wrong species! For animals that only live about a week, this can be a serious issue.

How does the plight of these females affect whether a population is a habitat specialist or generalist? Population density might be the linking factor. If one species is less common in a given area, females of that species will have to put up with lots of attention from males of the wrong species. Not only does this take up their time, it also keeps them from mating with males of their own species. Simply as a result of being less common, this species will have a hard time reproducing; the females will be busy fending off males of the wrong species while the males which should be courting them are busy chasing females of the wrong species.

The majority species won't face this problem, since they're more likely to be mating with an individual of their own species. The minority species, swamped by futile mating attempts, will struggle to compete. One way out of this bind is to specialize on a particular habitat niche. This will concentrate the minority species within that niche, evening out the numbers and making individuals more likely to find a mate. In cases like this, habitat specialization could be a strategy for members of the less common species to maximize their chance of reproduction.

To test this idea, the researchers captured butterflies of both species and carried out mating experiments. On sunny summer days in 2008 and 2009, they released the butterflies into outdoor flight cages and counted how many mated over the next five hours, after which they were re-captured and dissected to catch any matings the scientists might have missed. By varying the proportion of the two species in the cage in different trials, they could directly measure how relative population density affected mating success. Their data showed that the less common a species was, the worse its chance of mating. Regardless of which species was more common, the minority species mated less often. In the most extreme case, females of the minority species ended up mating in only 8% of their encounters, while females of the majority species mated in more than half of theirs.

Friberg's findings don't directly demonstrate a link between courtship and habitat specialization, but they do show that population density and courtship behaviour can have a big impact on mating success. When courtship is long and expensive, it's important that the investment pays off. If similarity in appearance and behaviour make it easy to court a member of the wrong species, the costs of courtship can create a selective pressure on the minority species. Populations will evolve to minimize those costs — say, by specializing in a particular habitat to make same-species matings more likely. An interesting implication of this model is that the order in which species colonize an area might determine whether they become specialists or generalists. The first species to move in will probably outnumber any newcomers, allowing it to remain a habitat generalist while later colonizers become habitat specialists to escape the sink-hole of unsuccessful mating attempts. The model is also a lovely reminder of how important it is to consider the role and interaction of many different levels — from cells to populations — when thinking about ecology and evolution.

Reference
Friberg, M., Leimar, O., and Wiklund, C. (2013) Heterospecific courtship, minority effects and niche separation between cryptic butterfly species. Journal of Evolutionary Biology 26:971-979. doi: 10.1111/jeb.12106

Image credit
The Wood White butterfly image is by user böhringer friedrich at Wikimedia Commons.