New study asks if non-migratory monarchs can still become migratory - answer: maybe, but...
A very interesting and timely new study of monarchs just came out and I'm going to cover it for this blog entry. It relates to an issue of ongoing discussion about monarchs and the conservation of the North American migratory population.
First, here is a link to the paper, which I believe is accessible to everyone - https://academic.oup.com/biolinnean/article/123/2/265/4769831. I encourage everyone to check it out before going too much further here. The paper is a hefty read, but don't let that stop you, because I'm certainly not going to provide all of the details here. The title was " Non-migratory monarch butterflies, Danaus plexippus (L.), retain developmental plasticity and a navigational mechanism associated with migration." The study was conducted by some familiar faces around monarch circles, and a few folks less-familiar: Micah Freedman was the lead author (which usually means this person conducted the bulk of the work), who is from the University of California at Davis, where he (a guy) is listed as a graduate student. Also included were Myron Zalucki, a monarch scientist from the University of Queensland (Australia), Hugh Dingle (also from Davis), a well-known expert on insect migration, and Louie Yang, a young professor at Davis who is becoming more and more involved in monarch research. So all in all, a very talented group of researchers.
As my blog title indicates, the goal of this paper was to examine non-migratory monarchs and to try to figure out how they differ from migratory ones. As most people know, here in North America the eastern monarch population migrates each fall to Mexico, and the western population migrates to California. But there are also scattered populations throughout the world that do not migrate at all - like in Hawaii, the Caribbean, in New Zealand, and there are even monarchs now in Spain - there are others, but the point is that these populations exist, and they don't migrate. They simply remain at these locations and breed year-round. These populations are less-well studied, but we think that a lot of them were introduced. In fact, the current genetic work on this shows that the eastern N. American population is the ancestral population, which gave rise to all others. In other words, it looks like all monarchs of the world originally came from this one migratory population, and when they arrived at these new locations, they (or at least the new population) eventually adapted to a non-migratory lifestyle. Intuitively, this is probably because there is no need to migrate at these locations, especially if the weather is mild year-round and there is plenty of milkweed. The fact that these monarchs came from the North American migrant population is very interesting, because it points to the fact that monarchs that were once 'programmed' to migrate each year can give rise to monarchs that are 'programmed' to not migrate. This raises a million-dollar question, which is what was addressed in this paper, can the reverse be true? So can resident, non-migrant, monarchs become migratory? Or at least, do they have the capacity to do so?
Before going further, let me give you a brief lesson on diapause, because it's important to the story here. When migratory monarchs migrate, most of them are in reproductive diapause, which is a fancy term that means their internal reproductive tissues are not well-developed. Years ago, a researcher in Minnesota (William Herman) conducted extensive experiments on this process, and he described this process as being a key element in the migration. When the last summer generation is developing as larvae, they somehow sense the changing seasons, so that when they metamorphose, their reproductive tissue does not fully develop. Herman said this is because the migratory generation does not need this, and that it would be too much weight to carry during the long flight. So, the migrant generation simply postpones the reproductive development until the spring. This bit of biology actually makes it convenient for scientists to conduct experiments on the migratory ability of monarchs. We can simply raise monarchs in artificial conditions (like in incubators) that mimic the late-summer environment, and presto - they become adults that are in reproductive diapause. Since this is the precursor to migration, we refer to these as 'migrant' monarchs. Then we can compare these to those reared under summer conditions, which have all of their reproductive tissues. This is essentially what the authors of this study did, as I'll explain next.
The researchers initially collected a set of reproductively active female monarchs from sites in Australia. Apparently these were locations where monarchs are permanent residents and breed year-round, and the females were collected during the winter (they were still breeding). As I understand it, there is an introduced milkweed species there, Gomphocarpus fruticosis, which is native to South Africa, but is now the main food source of the Australian monarchs (which are also introduced!), and apparently, this plant grows year-round. The researchers then took these females to their lab, and allowed them to lay eggs for the experiment. They then split the eggs into two batches - one batch was reared under conditions mimicking summer, the other under conditions mimicking early fall (i.e. time-to-migrate-conditions). The larvae were reared to adulthood, then the researchers examined the, ahem... private parts, of the adult females. They wanted to see if the females reared under fall conditions showed evidence of reproductive diapause, and sure enough, they did. Their reproductive tissue development was less (not a lot though) than what they should have showed if they were breeding. Meanwhile, the adults from the other batch were all reproductive, as expected. This was very cool - here was direct evidence that non-resident monarchs can become migratory, at least, physiologically speaking. Below is a figure from their paper, which shows the difference between the two groups - they labelled them "Constant" and "Decreasing", which refers to the lighting conditions of the breeding and fall conditions, respectively. Both graphs show that when raised in the fall conditions, adult females had fewer oocytes (eggs before fertilization), which means reduced reproductive development.
There was another experiment done in this paper, on the genetics of resident and migrant monarchs, which I am less-knowledgeable about. The researchers collected resident adult monarchs from Guam, and reared their offspring under summer conditions. They then collected migrant adults from California, and reared them under summer-breeding conditions (though I'm not sure why). When all of these larvae became adults they did some very fancy genetic analyses of their antennae (!), which is apparently where there are some key genes that are responsible for the migratory navigational ability of monarchs. I hope I got this part right. I believe they were looking to see if these migration genes worked just as well in the permanent residents. I'll skip to the result here - they found that yes, the Guam monarch genes did not differ from those of the California monarchs. All of this seems to indicate that the year-round breeding monarchs appear to have the genetic ability to become migratory. This result is consistent with the previous one regarding reproductive diapause.
So in the end the researchers concluded that non-migrant, permanent-resident monarchs still retain some of the physiological traits of their migrant ancestors. Based on their experiments and results (which appeared sound), I'd agree with this conclusion.
Now, let's talk about what this means, because it has some interesting implications for monarch conservation. As most folks know, the monarch in the United States is being considered for listing under the endangered species act, as a "Threatened" species. I've blogged about this in the past (see here). During this process, the US Fish and Wildlife dept. got all of the monarch scientists together (me included) for a series of discussions about this. In my group, we had an in-depth discussion about what would happen if we completely lost the eastern migratory population at some point in the future. Some researchers (not me) are concerned that this is a possibility in the future, because of the many threats it's facing. Since this is the population with the longest, most famous, migration, if that happened we would be left with a bunch of these non-migrant populations around the world. So everyone at this meeting was asking, could the migrant population somehow be 're-seeded' with non-migrant monarchs from elsewhere? In other words, could you theoretically take a collection of non-migrant monarchs from say, Guam, and turn them loose in Minnesota, and hope they create a new migrant population? Based on the research here, this may not be so far-fetched. But - and this is a big but - there are some other things to consider, which I'll explain.
One thing to consider about these non-migrant populations, is that they tend to be heavily infected with OE. For example, the non-migrant population in South Florida has OE rates of 80-100%. And, even in this study by Freedman et al, the authors stated that the original, winter-breeding females they collected in Australia were all infected with OE (100%). Apparently, when they allowed the females to lay eggs in their lab, the researchers had to painstakingly removed each OE spore from the eggs, before rearing began! From all of the research done on OE, it is clear that it reduces lifespan, wing size and flight ability of monarchs, and a lot of other bad stuff. So how can these year-round breeding populations get away with being so infected? Why don't they just disappear from the monarchs dying? Good question. We think these locations with year-round breeding tend to have high rates of OE because the monarchs can get away with being infected and dying sooner - they don't need to fly very far to find the next milkweed patch and they don't need to live very long. In other words, OE is still having an effect on the monarchs, but the population can compensate with over-breeding. Back to the original thought then, what would happen if you took an infected monarch from one of these locations and brought it to an area where it wasn't as warm and sunny all day, and where there wasn't milkweed around every corner? I think you can guess the answer.
The other thing about the non-migrant monarchs is that they are all small. Over hundreds of generations of non-migration, the monarchs eventually become adapted to this resident lifestyle, and their wing and body sizes also adapt - to become smaller. I blogged about this too a couple of times. Having large wings is a crucial element to successful migration. In fact, the migration weeds out the small-winged monarchs every year, which is what works to ensure that all eastern North American monarchs are really, really big. So we couldn't just take small monarchs and expect them to migrate, at least successfully.
There is one more thing to add to this discussion. In the eastern and western North American monarch range, there is a growing phenomenon of year-round monarch breeding occurring in areas where it doesn't freeze in the winter and where the non-native tropical milkweed has been planted. At these locations, OE infection levels are typically sky-high - see a previous blog entry on this. We don't know if these monarchs have completely lost the ability to migrate or not, or if these sites are composed of a mix of migrants and year-round breeders, etc. There is a lot we need to study about this growing phenomenon. Anyway, I have heard some folks raise the possibility that these locations could someday serve as a refuge, or reserve, in case the migration breaks down and we lose all of the migratory monarchs. I'm not sure where this thought came from (perhaps some psychological desire to demonstrate these sites are valuable, which would justify planting tropical milkweed?), but it did come to my mind when I read this paper. Based on the research here, it looks like these non-migratory monarchs here in the US may still have the physiological capacity to become migratory, but would they be successful? Probably not.
OK, I think I've covered most of this study by now, and my thoughts on what this means. I applaud the authors on such a well-written paper and thorough investigation, and I hope that we will see more research like this - work that gets at these questions and issues that have such conservation implications.
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