Nature writer and photographer Chris Clarke is a great fan of yuccas and yucca moths—he’s working on a book about Joshua trees right now—and so he asked me to answer a few questions about the latest research on the evolutionary history of yucca moths, which was just published in the Biological Journal of the Linnean Society. Check out Clarke’s discussion of the mutualism, and our e-mailed interview, on his blog Coyote Crossing. Look for a post about the paper, with some basic explanation of the methods used in it, right here at D&T next Tuesday.
One of the most basic questions in evolutionary ecology is, “why are there more kinds of this kind of critter than that kind of critter?” As in, why are there more than twenty thousand species of orchids, but only one species of ginkgo? Why are there hundreds of thousands of species of beetles, but only four species of horseshoe crab? In a literature review just released online—and my first publication as lead author!—my coauthors and I assess the support for one hypothesis: that species multiply because of ecological opportunity.
Biologists interested in the origins of species diversity frequently focus on the phenomenon of adaptive radiation, the process by which a single species rapidly gives rise to many new species, each with different traits adapted to different lifestyles. Darwin’s finches, with their beaks shaped to suit to different foods [$a], are a classic case; the Anolis lizards of the Caribbean, which have repeatedly evolved into a handful of “ecomorphs” with different body sizes and shapes adapted to different perching locations [PDF], are another.
The two most influential theories of adaptive radiation—by G.G. Simpson and Dolph Schluter—have suggested that it results when a species encounters ecological opportunity. Ecological opportunity might be a newly-evolved trait, or a new habitat, or the extinction of a species’ competitors or predators. For instance, a butterfly might evolve a way to overcome the chemical defenses of an abundant plant species, or a plant introduced by humans to a new habitat might find that local pathogens aren’t as deadly to it as the ones in its native range. Ecological opportunities have the effect of granting access to new resources. We have pretty good evidence that this can allow individual populations to increase in number, and even evolve greater diversity—but is that enough to spur the rapid speciation that forms adaptive radiation?
Ecological opportunity ? adaptive radiation
Readers in certain demographic groups may think this sounds like an underpants gnome problem. But it isn’t, exactly. The gnomes’ business model can’t get to from step 1 (collect underpants) to step 3 (profit) because they don’t have a step 2. Evolutionary ecologists, on the other hand, already have their step 3 in the phenomenon of adaptive radiation. Ecological opportunity looks like a good prospect for step 1 precisely because it suggests some plausible options for step 2.
When a population encounters ecological opportunity, the new habitat, new trait, or extinction of antagonists provides access to new resources, and relaxes natural selection on the population. This leads to three phenomena usually grouped together under the term ecological release
- The population experiences density compensation—more individuals can live in a particular area, creating stronger competition within the population.
- Because of this stronger competition within the population, or because there isn’t much competition from other species, members of the population venture into new habitats, or use new food resources.
- The population becomes more diverse, either because of the relaxed selection, or because of competition-driven selection for using new habitat and new resources.
One or more of these three aspects of ecological release turn up whenever populations find new food resources, or escape predators and/or competitors. Density compensation has been widely observed in populations colonizing new habitats, especially islands; and experiments with sticklebacks and fruit flies [$a] suggest that the stronger competition resulting from density compensation can spur the population to become more diverse in its use of resources. Bacterial populations can even evolve different specialized forms—adaptive radiations in microcosm—when introduced to new food resources.
But where’s the speciation?
However, the evolution of bigger, more diverse populations is not the same thing as the evolution of new species—and that’s what adaptive radiation is really all about. These changes resulting from ecological opportunity might directly promote speciation if stronger competition leads to disruptive natural selection. Similarly, the competition-driven incentive to colonize new habitats or exploit new food sources could expose some parts of the population to different forms of natural selection, eventually causing them to evolve into specialists on the new resources. Finally, even if speciation only happens when natural barriers cut off migration, maybe larger, more variable populations provide more diversity for vicariance events to divvy up.
This is all pretty speculative, though. We still don’t know how often—or how rarely—divergent natural selection contributes to making new species. One way to deal with this is to approach the question from the other direction: look backward at the history of existing species, rather than following what happens to populations immediately after ecological release.
A backward-looking approach might use statistical analyses of the evolutionary relationships between living things to identify points in time when species formed unusually fast, and try to identify the cause. Some of my coauthors from the review paper recently published an analysis of the evolutionary tree connecting all vertebrates, and found that speciation rates increased around the origins of the largest group of birds, a large portion of the lizards and snakes, and non-marsupial mammals, among others.
This is very much a starting point, but maybe by complementing similar studies with research on populations currently evolving in response to ecological opportunity, biologists can work our way closer to understanding the origins of the endless and beautiful forms of life on Earth.
Alfaro, M., Santini, F., Brock, C., Alamillo, H., Dornburg, A., Rabosky, D., Carnevale, G., & Harmon, L. (2009). Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc. Nat. Acad. Sci. USA, 106 (32), 13410-4 DOI: 10.1073/pnas.0811087106
Bolnick, D. (2001). Intraspecific competition favours niche width expansion in Drosophila melanogaster. Nature, 410 (6827), 463-6 DOI: 10.1038/35068555
Blumenthal, D., Mitchell, C., Pysek, P., & Jarosik, V. (2009). Synergy between pathogen release and resource availability in plant invasion. Proc. Nat. Acad. Sci. USA, 106 (19), 7899-904 DOI: 10.1073/pnas.0812607106
Grant, B., & Grant, P. (1989). Natural selection in a population of Darwin’s finches. The American Naturalist, 133 (3), 377-93 DOI: 10.1086/284924
Kassen, R. (2009). Toward a general theory of adaptive radiation: Insights from microbial experimental evolution. Annals New York Acad. Sci., 1168 (1), 3-22 DOI: 10.1111/j.1749-6632.2009.04574.x
Losos, J. (1990). Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: An evolutionary analysis. Ecological Monographs, 60 (3), 369-88 DOI: 10.2307/1943062
Schluter, D. 2000. The Ecology of Adaptive Radiation. Oxford University Press. Google Books.
Simpson, G.G. 1949. Tempo and Mode in Evolution. Columbia University Press. Google Books
Svanbäck, R., & Bolnick, D. (2007). Intraspecific competition drives increased resource use diversity within a natural population. Proc. Royal Soc. B, 274 (1611), 839-44 DOI: 10.1098/rspb.2006.0198
Wheat, C., Vogel, H., Wittstock, U., Braby, M., Underwood, D., & Mitchell-Olds, T. (2007). The genetic basis of a plant insect coevolutionary key innovation. Proc. Nat. Acad. Sci. USA, 104 (51), 20427-31 DOI: 10.1073/pnas.0706229104
Yoder, J.B., Des Roches, S., Eastman, J.M., Gentry, L., Godsoe, W.K.W., Hagey, T., Jochimsen, D., Oswald, B.P., Robertson, J., Sarver, B.A.J., Schenk, J.J., Spear, S.F., & Harmon, L.J. (2010). Ecological opportunity and the origin of adaptive radiations. Journal of Evolutionary Biology DOI: 10.1111/j.1420-9101.2010.02029.x
Things that happened while I was in the middle of the Nevada desert harassing Joshua trees:
- I had two of my first-author manuscripts accepted for publication. One, reconstructing the characteristics of yucca moths before they became yucca moths [PDF], will appear in the Biological Journal of the Linnean Society; the other, a review of what we know (and don’t know) about how ecological processes create adaptive radiation [PDF], will be in the Journal of Evolutionary Biology. Needless to say, I’m very pleased. I’ll discuss each paper in more detail when they’re posted to the respective journal websites.
- The 2010 Research Blogging Award winners were announced—congrats to Ed Yong at Not Exactly Rocket Science, who took Best Blog, Best Post, and Best Lay-Level Blog; and to Bora Zivkovic at A Blog Around the Clock, who took Best Biology Blog and Research Twitterer of the Year.
- The Daily Monthly blew through its second topic, world population, and is now well into a third, fitness. Andrew Sullivan is calling for the Pope to resign. Slacktivist is almost forty pages deeper into Tribulation Force. I’ve got a lot of catch-up online reading, in other words.
- Apparently the revolution finally came, and we are now living in a socialist worker’s paradise in which pre-existing conditions are illegal and 26-year-olds can use their parents’ health insurance. I, for one, am totally excited to get my new Mao jacket.
Yeah, it was worth it. Photo by jby.
Joshua trees are about to bloom. Which means I’m off to the desert until mid-April first to tour Joshua Tree National Park with my parents for a week, then to spend a month or more at a field site in central Nevada, extending studies of co-divergence in Joshua tree and its pollinator moths.
All of which is to say, posting to D&T is about to drop to near-zero for the foreseeable future. I’ll take lots of photos, and put them online when I get to an Internet connection, but really that’s all I can promise. After all, what good is fieldwork if not as an Internet detox?
Photo by jby.
In a paper just released online at Molecuar Ecology ahead of publication, genetic tests on moth larvae provide the latest piece to the puzzle of why there are two kinds of Joshua tree — because the tree’s pollinators need to match its flowers [PDF].
I’ve written extensively about the interaction between Joshua tree and its pollinators. Like all yuccas, Joshua tree is pollinated only by yucca moths. Female yucca moths collect pollen in special mouthparts and deliberately apply it to a yucca flower after laying eggs inside it. When the eggs hatch, the moth larvae eat some of the seeds inside the developing fruit. Yuccas prevent their pollinators from laying too many eggs by selectively killing flowers too badly damaged by egg-laying [$-a].
TOP: The two forms of Joshua tree (western type on left, eastern on right). BOTTOM: Scaled comparison of moth body sizes and tree pistils. To lay eggs in a flower, moths must drill from near the top of the pistil to the positions marked by dotted lines. Photo by jby, Illustration from Smith et al.(2010), figure 1.
This last element of the interaction may have had significant consequences for Joshua trees’ evolutionary history. Joshua trees are pollinated by two different species of moths, which occur in different parts of the tree’s range: the larger Tegeticula synthetica in the west, and the smaller T. antithetica in the east. Joshua trees pollinated by the two different moth species are themselves different, both in their overall shape, and in the shape of their flowers’ pistils — specifically, the length of the route that a moth must drill to lay her eggs [PDF].
How does this difference in flower shape affect Joshua tree pollination? If a larger moth attempts to lay eggs in a smaller flower, it may be do more damage to the flower than the “native” pollinator would, triggering the tree to kill the flower. On the other hand, smaller T. antithetica might be able to lay eggs in a larger western-type flower without this risk. If this is the case, moths probably can’t pollinate western trees with eastern pollen, but they might be able to do the reverse.
Such one-way pollen transfer between the two Joshua tree types could produce a population genetic pattern called “chloroplast capture.” Joshua tree pollen doesn’t contain the full genetic code of the tree that produces it — it lacks the genes contained in the chloroplast, the cellular structure that conducts photosynthesis, because pollen grains typically don’t have chloroplasts. The DNA in the cellular nuclei of newly-formed seeds is a mixture of nuclear DNA (nucDNA) from a pollen grain and from one of their “maternal” parent’s ovules, but they get all their chloroplasts, and chloroplast DNA (cpDNA), from the ovule. If moths carry pollen from eastern trees to western trees, then the seeds produced would contain western cpDNA, but also some eastern nucDNA.
Asymmetric pollen transfer can lead to eastern-type trees with western-type chloroplasts. Figure 2 from Smith et al.(2010).
This is what we’ve found in Joshua tree populations near the region where the two tree types and their pollinators come into contact. At these sites, trees look like the eastern type (meaning they likely have eastern nucDNA, though we haven’t tested that yet) but have cpDNA that matches nearby populations of western-type trees [PDF].
The genetic pattern is only suggestive of one-way pollen transfer between the two Joshua tree types, though. We haven’t yet tracked the movement of moths directly, or estimated whether they actually are less successful when laying eggs on the wrong tree type. The newly-published study provides exactly these data. My colleague Chris Smith placed glue traps on Joshua tree flowers at the contact zone to estimate how often adult moths of each pollinator species visited each type of tree in the mixed population. Adult moths were more likely to be trapped on their “native” trees, though they did show up on the other type sometimes.
A yucca moth larva emerges from a Joshua tree fruit in the lab. Photo by jby.
Chris and I then collected fresh fruit from trees in the contact zone, and caught yucca moth larvae as they chewed their way out. Chris and another coauthor, Chris Drummond, then identified the species of each larva based on their genetics (the two pollinators look very similar at that stage) — and in our sample, the pattern of specificity was even stronger than that in the adults. The larger moth species, T. synthetica, never emerged from fruits of the small-flowered eastern trees. The vast majority of larvae of the smaller T. antithetica were also found inside their “native” tree’s fruit — but a handful did emerge from large-flowered western trees.
This mechanism could create the genetic pattern we see in Joshua tree populations. Larger T. synthetica doesn’t seem to lay eggs in (or pollinate) small-flowered eastern trees, but smaller T. antithetica can occasionally lay eggs in (and pollinate) large-flowered western trees. This should create asymmetric gene flow, with pollen moving from eastern trees to western trees, but not the reverse. The two Joshua tree types may not yet be reproductively isolated, separate species — but we won’t know for sure without looking at the plants’ nuclear DNA. As it happens, I’m working on that right now.
Godsoe, W.K.W., Yoder, J.B., Smith, C.I., & Pellmyr, O. (2008). Coevolution and divergence in the Joshua tree/yucca moth mutualism The American Naturalist, 171 (6), 816-823 DOI: 10.1086/587757
Marr, D., & Pellmyr, O. (2003). Effect of pollinator-inflicted ovule damage on floral abscission in the yucca-yucca moth mutualism: the role of mechanical and chemical factors Oecologia, 136 (2), 236-243 DOI: 10.1007/s00442-003-1279-3
Smith, C.I., Godsoe, W.K.W., Tank, S., Yoder, J.B., & Pellmyr, O. (2008). Distinguishing coevolution from covicariance in an obligate pollination mutualism: Asynchronous divergence in Joshua tree and its pollinators. Evolution, 62 (10), 2676-87 DOI: 10.1111/j.1558-5646.2008.00500.x
Smith, C.I., Drummond, C., Godsoe, W.K.W., Yoder, J.B., & Pellmyr, O. (2010). Host specificity and reproductive success of yucca moths (Tegeticula spp. Lepidoptera: Prodoxidae) mirror patterns of gene flow between host plant varieties of the Joshua tree (Yucca brevifolia: Agavaceae). Molecular Ecology DOI: 10.1111/j.1365-294X.2009.04428.x
Over at LiveScience, my collaborator Chris Smith describes the research we’ve done so far on the interaction between Joshua trees and their pollinators:
First, the match between the Joshua tree flowers and the moths’ ovipositors suggested that coevolution might have molded the relationship between the plant and the pollinator. Second, because the plants are completely dependent on the moths for reproduction, the differences in the flowers might have caused Joshua trees to split into two different species.
Yucca brevifolia in Tikaboo Valley, Nevada. Photo by jby.
With permission from my doctoral advisor, Olle Pellmyr, I’ve just uploaded a unique video to Vimeo: a yucca moth laying eggs in, then pollinating, a yucca flower. I don’t know why I didn’t think of this earlier — it’s great footage, and deserves to be seen more widely.
A female yucca moth mates, then collects pollen from a yucca flower in specialized mouthparts. She carries it to another flower where, as shown in the video, she drills into the floral pistil with her ovipositor and lays eggs inside, then climbs to the tip of the pistil and applies pollen to fertilize the flower. When the flower develops into a fruit, the eggs hatch and the caterpillars eat some of the seeds inside.
Yuccas and yucca moths are completely dependent on each other [PDF] — nothing else pollinates yuccas, and the moths have no other source of food (they don’t eat as adults). Recently, the Pellmyr lab has shown that this interaction may be leading to speciation in one yucca species, the Joshua tree — Joshua trees pollinated by two different species of yucca moths have differently-shaped flowers [PDF], but these two tree types may not be totally genetically isolated [PDF]. I’ve written about this work before — for more information about the interaction, check out Olle’s publication page.
Godsoe, W., Yoder, J., Smith, C., & Pellmyr, O. (2008). Coevolution and Divergence in the Joshua Tree/Yucca Moth Mutualism. The American Naturalist, 171 (6), 816-23 DOI: 10.1086/587757
Pellmyr, O. (2003). Yuccas, yucca moths, and coevolution: A review. Annals of the Missouri Botanical Garden, 90 (1) DOI: 10.2307/3298524
Smith, C., Godsoe, W., Tank, S., Yoder, J., & Pellmyr, O. (2008). Distinguishing coevolution from covicariance in an obligate pollination mutualism: Asynchronous divergence in Joshua tree and its pollinators. Evolution, 62 (10), 2676-87 DOI: 10.1111/j.1558-5646.2008.00500.x
A new Joshua tree study is just out in the current issue of New Phytologist, presenting an analysis of the environments occupied by the two different types of Joshua tree. The results demonstrate that the two tree types mostly grow in similar climatic conditions [PDF], which suggests that coevolution with its pollinators, not natural selection from differing environments, is responsible for the evolution of the two different tree types.
The Pellmyr Lab has been studying the two types of Joshua tree, which are pollinated by two separate, highly specialized moths, for several years now. Previous papers have shown that the two types of Joshua tree, first described in the 1970s based only on their vegetative features, are most strongly differentiated by the shape of their flowers [$-a]; and that, although the two moths are separate species, the two tree types are not fully genetically differentiated [PDF].
Hey, those Joshua trees look kinda
Photo by jby.
The latest paper is a chapter from the dissertation of Will Godsoe, who just received his doctorate last week. It presents an analysis that sidesteps a fundamental problem with studying long-lived, specialized organisms — they’re hard use in fully controlled experiments. To determine whether the two types of Joshua tree really evolved as a result of coevolution with their pollinators, we’d like to be able to eliminate the alternative hypothesis that the two types evolved in response to different environmental conditions. Except for a small contact zone in central Nevada, each tree type occurs in a different part of the Mojave desert, and the two regions do have some broad-scale differences in when they receive precipitation.
Ideally, to determine whether two plants have different environmental needs, you just perform an experimental transplant, growing each plant in the other’s environment to see whether it fares as well as it does at home. This isn’t really possible with Joshua trees, which are pretty tricky to sprout from seeds (I’ve tried), and which, in any event, take something like twenty years to mature. So Will proposed to use niche modeling methods instead. Niche models are statistical descriptions of environments where an organism is known to live, often used to predict where it could live. To build niche models for each type of Joshua tree, Will assembled location data we’d collected over several field seasons in the Mojave, then spent another field trip driving around the desert some more to fill in the gaps — he wanted locations where Joshua trees were definitely growing and where they definitely weren’t, to fully “inform” the models.
Using the location data, it was possible to determine what kinds of climates each Joshua tree type tended to occupy by cross-referencing with existing climate databases, then fitting statistical models to the results. The models produced for each tree type could then be compared — and, for the most part, they’re similar. That is, if you collected seeds from one tree type, planted them where the other type grows, and waited around for a few decades to check the result, you’d probably find that it grew as well as it did in its home range.
So, if differing climates don’t explain the origin of the two types of Joshua tree, does that leave no other possibility but the pollinating moths? Not exactly — there are lots of environmental variables that weren’t available for Will’s niche models, for instance, or there could be a third, completely unknown factor. But this does make coevolution with the moths a more plausible explanation. In light of some of our very latest results — which should be going to press fairly soon — coevolution is looking like a better and better possibility.
Godsoe, W., Strand, E., Smith, C.I., Yoder, J.B., Esque, T., & Pellmyr, O. (2009). Divergence in an obligate mutualism is not explained by divergent climatic factors New Phytologist, 183 (3), 589-99 DOI: 10.1111/j.1469-8137.2009.02942.x
Godsoe, W., Yoder, J.B., Smith, C.I., & Pellmyr, O. (2008). Coevolution and divergence in the Joshua tree/yucca moth mutualism The American Naturalist, 171 (6), 816-23 DOI: 10.1086/587757
Smith, C.I., Godsoe, W., Tank, S., Yoder, J.B., & Pellmyr, O. (2008). Distinguishing coevolution from covicariance in an obligate pollination mutualism: Asynchronous divergence in Joshua tree and its pollinators. Evolution, 62 (10), 2676-87 DOI: 10.1111/j.1558-5646.2008.00500.x
Some years, they don’t bloom. I’m just back from a week and a half of attempted fieldwork in Nevada, with a hiatus to Southern California for a lecture to a Desert Institute class. Very few Joshua trees were in flower, so the trip was kind of a bust. But it was still good to get out into the desert. The weather was only really cold a couple nights, and almost too warm in Palm Springs. When I drove back into Moscow this afternoon, it was snowing.