Seed dispersal by ants: A lousy way to travel, a good way to diversify

ResearchBlogging.orgNew in the always open-access PLoS One: turns out that a great way to make new species, if you’re a plant, is to have your seeds dispersed by ants. This is because ants aren’t very good at seed dispersal.

Seed dispersal by ants, or myrmecochory, works very much like dispersal by fruit-eating birds and mammals: ant-dispersed seeds typically have a fatty attachment, called an elaiosome, that looks tasty to ants. Ants collect elaiosome-bearing seeds, bring them back to their nest, pry off the tasty bit, and then discard the rest of the seed. This leaves the seed safely underground in an ant-midden, ready to germinate — a great way to dodge seed-eating critters and avoid competition from its parent plant and siblings [$-a].

Bloodroot seeds, with ant-attracting
Photo by cotinis.

I didn’t learn about myrmecochory until after I’d finished undergrad — which is surprising, because it was going on under right my nose every time I went out into the Appalachian woods near campus. Lots of wildflowers [$-a] have ant-dispersed seeds, including bloodroot, touch-me-not, and good old trillium. It’s an extremely popular dispersal mechanism, having evolved independently multiple times on every continent except Antarctica. Really, me not knowing about myrmecochory is kind of like not knowing about fruit!

Ant dispersal is also associated with increased species diversity. In the new article, Lengyel et al. use a classic analysis method called sister group comparison to test the hypothesis that ant-dispersed plant groups contain more species than the most closely-related plant group. And they do, by a long way: on average, myrmecochorous groups contain twice as many species as their non-myrmecochorous sister groups. Why is this? As the authors conclude, it’s probably a side consequence of ant dispersal — ants don’t move seeds very far from where they collect them.

Recent evidence from genetic studies shows that limited seed dispersal in myrmecochory can lead to strong genetic structure within populations even at spatial scales as small as a few meters. The failure of myrmecochores to maintain gene flow across barriers may lead to reproductive isolation of sub-populations, which may facilitate speciation. [In-text references omitted.]

So myrmecochorous plants, like Appalachian salamanders [$-a] and tropical white-eyes [$-a], make lots of new species not because their unique characteristics give them some adaptive advantage (although, to be sure, there are advantages to ant dispersal), but because ants do a lousy job moving seeds between populations, leaving them free to follow their own evolutionary trajectories.

Lengyel et al. argue that myrmecochory is a key innovation, a trait that helps a group of organisms spread and diversify in the process evolutionary biologists call adaptive radiation. Based on their results, I have to agree — ant dispersal is strongly associated with evolutionary diversification. But the speciation that myrmecochory promotes is an accident, a side effect. We often think of key innovations promoting speciation by adaptive means, by allowing one group of species to outcompete others. Clearly, however, a key innovation can also be a trait that makes the accident of speciation a little more likely.


Beattie, A.J., & Culver, D.C. (1981). The guild of myrmecochores in the herbaceous flora of West Virginia forests. Ecology, 62, 107-15 DOI:

Giladi, I. (2006). Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos, 112 (3), 481-92 DOI: 10.1111/j.0030-1299.2006.14258.x

Kozak, K., Weisrock, D., & Larson, A. (2006). Rapid lineage accumulation in a non-adaptive radiation: phylogenetic analysis of diversification rates in eastern North American woodland salamanders (Plethodontidae: Plethodon). Proc. R. Soc. B, 273 (1586), 539-46 DOI: 10.1098/rspb.2005.3326

Lengyel, S., Gove, A., Latimer, A., Majer, J., & Dunn, R. (2009). Ants sow the seeds of global diversification in flowering plants. PLoS ONE, 4 (5) DOI: 10.1371/journal.pone.0005480

Moyle, R., Filardi, C., Smith, C., & Diamond, J. (2009). Explosive Pleistocene diversification and hemispheric expansion of a “great speciator.” Proc. Nat. Acad. Sci. USA, 106 (6), 1863-8 DOI: 10.1073/pnas.0809861105


Speciation changes ecosystem

ResearchBlogging.orgWe know that ecosystem processes can act on organisms to help create reproductive isolation and speciation – now, a new paper released online in advance of publication in Nature shows that speciation can change the ecosystem [$-a].

The study’s authors are a group of University of British Columbia scientists, including Luke Harmon (who occasionally blogs at Dechronization) and Simone Des Roches, who have since come to my department at UI as a faculty member and doctoral student, respectively. They focus on the case of ecological speciation in sticklebacks (Gasterosteus aculeatus), which have repeatedly into evolved two reproductively isolated, ecologically different forms [$-a] after colonizing North American freshwater lakes from the ocean about 10,000 years ago. One of the two forms is “limnetic,” living in open water near the surface and feeding on plankton; the other is “benthic,” living on lake bottoms and feeding on invertebrates.

A stickleback
Photo by frequency.

Harmon et al. reasoned that the presence of these two different fish must have a substantial effect on lake food webs. To test this hypothesis, they set up mesocosms – big cattle tanks seeded with a standard mix of sediment, plankton, and invertebrates – and introduced either (1) sticklebacks of the “generalized” type ancestral to the benthic and limnetic types, (2) either the benthic or limnetic type alone, or (3) both the benthic and limnetic types together. They found that the fish species present in the mesocosm strongly affected the plankton species diversity – limnetic-type nearly eliminated one of their preferred prey species – and on measures of total ecosystem productivity and metabolic activity.

Perhaps the most important effect was on dissolved organic content (DOC) and light transmission in the water column. Mesocosms containing both fish types had about the same amount of (non-living) organic material as those containing the generalist ancestor, but the two-species treatment changed the DOC composition to make the water column more transparent to light. In a real lake, this effect could significantly change the productivity and composition of the aquatic plant community, which would in turn reshape the rest of the food web.

The buzzword for this phenomenon is “ecosystem engineering,” which the ESA blog puts front-and-center in its discussion of this paper. I think Harmon et al.‘s result is most interesting as the closing of a feedback loop between the ecosystem and a population undergoing speciation. It’s evidence that a speciation event can actually alter the conditions that created it in the first place – which might prevent future speciation events, or create opportunities for new ones.


Harmon, L., B. Matthews, S. Des Roches, J. Chase, J. Shurin, & D. Schluter (2009). Evolutionary diversification in stickleback affects ecosystem functioning Nature DOI: 10.1038/nature07974

Vines, T., & D. Schluter (2006). Strong assortative mating between allopatric sticklebacks as a by-product of adaptation to different environments Proc. R. Soc. B, 273 (1589), 911-6 DOI: 10.1098/rspb.2005.3387


That “mystery of mysteries”: What makes a species?

ResearchBlogging.orgIn a special issue of Philosophical Transactions of the Royal Society on speciation, James Mallet argues that the Biological Species Concept is at odds with Charles Darwin’s original ideas about what a species is – and that current research supports Darwin [$-a].

When The Origin of Species was first published, biologists mostly thought species were easy to recognize – they looked different from each other, and they couldn’t successfully interbreed with each other. This view was a problem for Darwin’s ideas about gradual evolution by natural selection, since gradual divergence shouldn’t give rise to nice, discrete species. In fact, as Darwin argued, different groups of organisms exhibit a whole spectrum of reproductive isolation, from complete interfertility to total isolation – and the degree of isolation is not easy to predict based on how similar organisms look. In Darwin’s description, species are just labels that humans put on clusters of similar-looking organisms.

By the mid-Twentieth Century, evolutionary biologists favored what is commonly called the Biological Species Concept (BSC), defining species as non-interbreeding populations of living things. Research on speciation has accordingly focused on the ways that evolution creates reproductive isolation between populations. Mallet argues that this amounts to an abandonment of Darwin’s insights, and that by focusing on isolating mechanisms, biologists have returned to viewing species as distinct, “real” entities, missing much of the evolutionary process as a result.

I’m not sure I believe the distinction that Mallet makes between Darwin’s description of species and the BSC; they seem to me more different in their emphasis than in their fundamentals. Darwin was interested in demonstrating that species arise gradually, as accidents of adaptation to different environments – and, as Mallet says, he was trying to overcome the then-predominant view that species were real, discrete entities instead of the names that humans assign to clusters of similar organisms. Research motivated by the BSC generally takes this view as well, but it’s interested in the processes that create such clusters, and can prevent them from merging into nearby clusters by interbreeding.

Two types of Joshua tree
Photo by jby.

Research on the evolution of isolating mechanisms necessarily focuses on cases where isolation is incomplete, somewhere between complete speciation and free interbreeding. A prime example is my lab’s research on the two pollinator-associated types of Joshua tree, Yucca brevifolia. It’s not clear that the two types are reproductively isolated – preliminary genetic data suggests they’re not [PDF] – even though they’re pollinated by different moth species, and classified as separate subspecies, the taller Y. brevifolia brevifolia and the short, bushy Y. brevifolia jaegeriana. They may be on the way to becoming different species, but they’re not there yet. Two other examples out of the endless forms available: marine snails that choose mates by their slime trails, and wildflowers that would interbreed if only they could survive each other’s habitat.

As Mallet concludes in the more empirical part of his review, this is what we see across the diversity of life: a continuum of reproductive isolation between populations, not a granular world of neatly divided, obviously different species. Rather than over-simplifying this reality, the Biological Species Concept gives us a framework through which to understand it.


Darwin, C. 1859. On the Origin of Species by Means of Natural Selection. First ed. London: John Murray. Full text on Google Books.

Mallet, J. (2008). Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation Phil. Trans. R. Soc. B, 363 (1506), 2971-86 DOI: 10.1098/rstb.2008.0081

Smith, C., W. Godsoe, S. Tank, J. Yoder, & O. Pellmyr (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


Want to speciate? Stay home.

ResearchBlogging.orgI’ve said it before, and I’ll say it again: the formation of new species is almost always an accident. There you are, adapting to changes in your obligate pollinator, or the local environment – and suddenly, you can’t mate with the folks on the other side of the mountain. That’s the lesson I take from an article in last week’s PNAS, which suggests that a diverse group of birds got that way by being homebodies [$-a]

Oriental white-eye
(Zosterops palpebrosus)

Photo by Lip Kee.

The authors (including Jared Diamond, who communicated the paper to PNAS), set out to determine why there are so many species of white-eyes, a group of songbirds distributed across Africa, Southeast Asia, and the southern Pacific. They built a phylogeny for the group, calibrated it to real time using the geological dates of origin for Pacific islands occupied by white-eyes, and then estimated the rate at which the group produced new species. They found, as reported by, that the largest group of white-eyes have one of the fastest species-accumulation rates recorded in vertebrates, about 1.6 new species every million years.

That’s a weird result, when you think about it – we’re talking about birds, and widely-distributed birds, here. All things being equal, speciation is facilitated by lack of movement – Appalachian salamanders, for instance, diversified largely because they’re too gimpy to move between stream drainages very often [$-a]. Furthermore, the authors say, white-eyes don’t display a lot of ecological differences that might contribute to isolation. So how did they speciate at a record-setting pace?

The solution? The authors propose that white-eyes are prone to rapid changes in their dispersal ability. As evidence, they cite numerous cases in which white-eyes must have crossed great distances to colonize one island, then failed to make it across much smaller distances to colonize others nearby. Nodding to Diamond’s groundbreaking work on human history and cultural evolution, they compare this to the colonization of Polynesia, in which people stopped traveling long distances as the chance of discovering an uninhabited island decreased.


K.H. Kozak, D.W. Weisrock, A. Larson (2006). Rapid lineage accumulation in a non-adaptive radiation: phylogenetic analysis of diversification rates in eastern North American woodland salamanders (Plethodontidae: Plethodon) Proceedings of the Royal Society B: Biological Sciences, 273 (1586), 539-46 DOI: 10.1098/rspb.2005.3326

R.G. Moyle, C.E. Filardi, C.E. Smith, J. Diamond (2009). Explosive Pleistocene diversification and hemispheric expansion of a “great speciator” Proceedings of the National Academy of Sciences, 106 (6), 1863-8 DOI: 10.1073/pnas.0809861105


Natural selection and speciation, 150 years later

ResearchBlogging.orgScience kicks off the week of Darwin’s 200th with a special section devoted to the latest on speciation [$-a], the literal origin of species. It includes a new review by Dolph Schluter, discussing the role of natural selection speciation [$-a], which suggests a new way to think about selection creating reproductive isolation.

Schluter contrasts ecological speciation, in which reproductive isolation arises in the course of adaptation to different environments, “mutation-order” speciation – isolation arising by the accumulation of different genetic and morphological changes in the course of adaptation to the same (or the same kind of) environment. That is, natural selection can cause a population to split into two species if different parts of population are “solving” different ecological problems, or if they arrive at different “answers” to the same problem.

The mutation-order scenario makes sense, though it’s new to me. As an example, Schluter cites a recent study in Mimulus in which a mutation of the mitochondrial DNA in one population creates sterile males in hybridization with other populations [$-a]. He proposes that much mutation-order speciation occurs because of conflict between different levels of natural selection, as when “selfish genes” create reproductive incompatibilities in the course of spreading through a host population. This is a departure from what biologists usually consider speciation by natural selection, but Schluter makes an interesting point.


A.L. Case, J.H. Willis (2008). Hybrid male sterility in Mimulus (Phrymaceae) is associated with a geographically restricted mitochondrial rearrangement Evolution, 62 (5), 1026-39 DOI: 10.1111/j.1558-5646.2008.00360.x

D. Schluter (2009). Evidence for ecological speciation and its alternative Science, 323 (5915), 737-41 DOI: 10.1126/science.1160006

A. Sugden, C. Ash, B. Hanson, L. Zahn (2009). Happy birthday, Mr. Darwin Science, 323 (5915) DOI: 10.1126/science.323.5915.727


Arrested development, and reproductive incompatibility, from duplicate genes

ResearchBlogging.orgSpeciation isn’t something that evolution sets out to do – it just sort of happens. One day, a species colonizes two sides of a river, say, migration across the river drops off, and then a few million years of genetic drift later, there are two species where once there was one. The question is, what’s the final genetic change that makes the accident of speciation irrevocable?

A paper in this week’s Science pinpoints exactly that change. Bikard and coauthors report that, in the little flowering plant Arabidopsis thaliana (the plant world’s answer to white lab mice and Drosophila fruit flies), it only takes one duplicated gene to finalize speciation [$-a]. It’s a clear-cut case of a classic speciation scenario, BatesonDobzhanskyMuller incompatibility.

Arabidopsis thaliana
Photo by tico bassie.

It all comes down to gene duplication, which I’ve discussed before in the context of the trouble it gives to genetic analysis. Making copies of an entire genome is an error-prone process, and sometimes a whole gene gets duplicated twice. If that extra copy is inherited, it means that the carrier has redundant coding for whatever the original gene does – so now one copy can mutate without affecting its carrier’s fitness. Often this just results in loss of function for the mutating copy – sometimes it leads to new gene functions. In Arabidopsis, it’s lead to reproductive incompatibility between two strains of the plant that took different evolutionary paths.

Bikard et al. noticed that, when they crossed two strains of Arabidopsis, the resulting seeds didn’t include every possible combination of the parental strains’ genes – and a few seeds grew short, not-quite-healthy looking roots when germinated. Some of the hybrid seeds just died in mid-development. With a lot more controlled crosses, the authors narrowed the candidate genes down to a pair that normally work together in synthesizing the essential amino acid histidine. Each of the two parental strains had working copies of the two genes – but when you crossed them, sometimes the seeds couldn’t produce histidine, and so they snuffed it.

This looked like the above-mentioned (and awkwardly named) Bateson-Dobzhansky-Muller incompatibility [$-a], which is an old idea about how populations evolve reproductive incompatibilities to become separate species. Under B-D-M incompatibility, a new gene evolves in one population that doesn’t work if it interacts with genes from the other. Imagine if Windows users didn’t have to share documents with Mac users: as the two operating systems went through multiple redesigns and their respective versions of Microsoft Office(TM) were revised to keep up, it might no longer be possible to read a Mac-written Word document on a Windows machine.

Here, as Bikard et al. showed, one of the histidine-producing genes in Arabidopsis was accidentally duplicated – and one copy mutated into non-functionality. The catch is that, in the two partially incompatible strains, different copies went nonfunctional. So now, when the two lines are crossed, a small fraction of the seeds produced get nonfunctional copies of the duplicated gene. They die. And where once there were two strains of Arabidopsis thaliana, there’s something a little more like two separate species, all because of what boils down to the flip of a coin.


D. Bikard, D. Patel, C. Le Mette, V. Giorgi, C. Camilleri, M.J. Bennett, O. Loudet (2009). Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana Science, 323 (5914), 623-6 DOI: 10.1126/science.1165917

K. Bomblies, D Weigel (2007). Arabidopsis — a model genus for speciation Current Op. Genet. & Dev., 17 (6), 500-4 DOI: 10.1016/j.gde.2007.09.006


Snail trails lead toward speciation

ResearchBlogging.orgFinding a mate is at the top of just about every to-do list in the animal kingdom. This might involve following the smell of pheromones or triangulating the source of a mating call; in the snail Littorina saxatilis, it turns out to require tracking your beloved by the trail of her slime [$-a].

That’s according to a paper in the latest issue of Evolution, in which Kerstin Johannesson and coauthors took video of male and female snails to catch slime trail-following in action. And it occurred to them that slime-following could be a component of speciation in L. saxatilis. This particular snail comes in two forms, or “ecotypes”: a small one that lives in the crevices of exposed rock faces and a larger one that lives in quieter, sheltered pools. When Johannesson et al. presented male snails with slime trails from each ecotype, the males preferred to follow trails made by females of their own ecotype.

This is what’s called assortative mating – preferentially mating with similar individuals – and it’s usually thought of as a first step towards speciation. Whether L. saxatilis ever eventually evolves into two species is another question, though. The world is full of experiments in speciation, where adaptation to local conditions or difficulty moving between populations can cause a species to begin diverging. But it’s just as likely that the forces pushing a species apart will change or disappear, and diverging groups re-merge into a single interbreeding population. Part of the fun of studying the natural world is finding things like snail’s slime trail discrimination, and trying to figure out what will happen next.


K. Johannesson, J.N. Havenhand, P.R. Jonsson, M. Lindegarth, A. Sundin, J. Hollander (2008). Male discrimintation of female mucous trails permits assortative mating in a marine snail species Evolution, 62 (12), 3178-84 DOI: 10.1111/j.1558-5646.2008.00510.x


Sympatric skepticism

ResearchBlogging.orgThe new issue of The Journal of Evolutionary Biology has a great article on a question that dates back to Darwin: sympatric speciation[$-a].

Sympatric speciation is simply speciation that occurs when a species splits into two reproductively isolated groups without any physical barrier arising between those groups. It’s often treated as the opposite of allopatric speciation, in which a species is split by some external barrier (a new mountain range, a river, &c) and the separated populations evolve on different trajectories until they’re unable to exchange genes even if the barrier is removed. There are a number of ways biologists think this can happen – for instance, a population of insects using two different, co-occurring host plants, might split into two species on the different hosts – but not many good cases where we’re pretty sure that it has happened.

In the new article, Kirkpatrick and his coauthors argue that the problem is one of definition. Sympatic speciation, as a concept, is set up to be impossible to test conclusively: Although it’s easy to show that two closely-related species occupy the same territory in the present, it’s rarely possible to show that they became different species while they were occupying the same territory at some point in the past, much less that they were “panmictic,” or freely interbreeding.

The problem for empiricists is that biogeographical sympatry is relatively straightforward to diagnose, but the initial condition of panmixia specified by population genetic models is virtually impossible to test.

As an alternative, the authors suggest ignoring the Platonic ideals of “allopatric” versus “sympatric” speciation, and instead concentrating on the interaction between divergent natural selection and gene flow in causing or preventing speciation. Not only is this sensible, it’s what most evolutionary ecologists are doing right now, anyway.


B.M. Fitzpatrick, J.A. Fordyce, S. Gavrilets (2008). What, if anything, is sympatric speciation? Journal of Evolutionary Biology, 1452-9 DOI: 10.1111/j.1420-9101.2008.01611.x


Joshua tree genetics suggest coevolutionary divergence

ResearchBlogging.orgThe latest results from the Pellmyr Lab’s ongoing study of Joshua tree and its pollinators are online as part of the new October issue of Evolution. It’s the cover article, no less. The study, whose lead author is Chris Smith (now on the faculty at Willamette University) compares patterns in the population genetics of Joshua trees and the moths that pollinate them, and shows that although the moths have become two separate species, the trees may not have followed suit [PDF].

Evolution cover
Photo by Chris Smith.

Female yucca moths carry pollen between Joshua tree flowers in special mouthparts. When she arrives at a new flower, the female moth lays her eggs inside it, then deliberately applies pollen to the flower’s receptive surface. When the fertilized flower develops into a fruit, the moth eggs hatch, and the larvae eat some of the seeds inside the fruit.

Among the yuccas, Joshua trees are unique because they’re pollinated by two species of moths, which are each other’s closest evolutionary relative. One species is found in the eastern part of Joshua tree’s range, the other in the west. Joshua trees from the east and west have differently-shaped flowers [PDF], which is consistent with the hypothesis that coevolution between moths and trees has driven both toward an evolutionary split.

“Western” Joshua trees at Joshua Tree National Park. Photo by me.

The new study goes deeper to look at genetic relationships between different populations of the moths and the trees, and what it finds isn’t as tidy as the earlier work might suggest: While Joshua trees’ morphology corresponds nicely to the split in the pollinators, the patterns visible in their chloroplast DNA does not. In some populations, trees look “eastern,” but have chloroplast DNA more closely related to “western” populations. This suggests that, although the moths have become separate species, they’re still moving between the two kinds of Joshua tree frequently enough that the trees haven’t quite split. Why do the two tree types look different, then? One possibility is coevolution with the two moth species, which might exert selection the trees in different ways.

There’s still a lot of work to do before we fully understand what’s going on here. Will Godsoe, the other doctoral student in our lab, is doing some intensive niche modeling to see how much environmental differences might be contributing to the patterns we see here. My own dissertation will look at whether the same incongruities turn up in nuclear DNA, which can have a different evolutionary history than that in the chloroplast.


W. Godsoe, J.B. Yoder, C.I. Smith, O. Pellmyr (2008). Coevolution and Divergence in the Joshua Tree/Yucca Moth Mutualism The American Naturalist, 171 (6), 816-23 DOI: 10.1086/587757

C.I. Smith, W.K.W. Godsoe, S. Tank, J.B. Yoder, O. Pellmyr (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


Ecological differences divide Mimulus guttatus

ResearchBlogging.orgReproductive isolation is the engine of evolutionary diversification. When two populations become unable to exchange genes, they’re effectively separate species, free to evolve on independent trajectories.

Biologists have documented many examples of reproductive isolation arising from all sorts of different interactions between organisms and their environments, including incompatibilities between gametes, adaptation to different pollinators (in plants), or the evolution of different sexual characteristics. The cover article for this month’s issue of Evolution describes another way reproductive isolation can arise – adaptation to different environments.

Mimulus guttatus
Photo by Dawn Endico.

The new paper, by Lowry et al., describes how different ecological conditions create reproductive isolation where there would otherwise be none [$-a]. The wildflower Mimulus guttatus grows all along the U.S. Pacific Coast. Some Mimulus populations grow inland, in coastal mountains, where the summers are hot and dry; others grow right on the coast, where fog provides moisture but plants have to tolerate salt spray from the sea. Plants from inland and coastal populations look quite different (inland = tall with big flowers; coastal = short with small flowers), and have previously been separated out into different subspecies. But are they actually isolated?

Lowry et al. found that inland and coastal plants perform poorly when transplanted to the others’ habitats, and that they flower at significantly different times. A population genetic analysis shows that the coastal and inland populations don’t exchange genes very often. But it’s possible to hybridize the two types in the greenhouse. In short, it looks like Mimulus is a case of what Nosil et al. called “immigrant inviability” [$-a]. Immigration between inland and coastal sites may be possible, and immigrants would (theoretically) be able to reproduce if they mated with plants from the local population – but before they get a chance, they’re nailed by summer drought (at inland sites) or salt spray (at coastal sites). So even before they’ve evolved fundamental incompatibilities, these two types of Mimulus are well on their way to being separate species.


D.B. Lowry, R.C. Rockwood, J.H. Willis (2008). Ecological reproductive isolation of coast and inland races of Mimulus guttatus. Evolution, 62 (9), 2196-214 DOI: 10.1111/j.1558-5646.2008.00457.x

P. Nosil, T.H. Vines, D.J. Funk (2005). Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution, 59 (4), 705-19 DOI: 10.1554/04-428