Scanning electron micrograph of Shewanella putrefaciens. Photo by EMSL.
This week at Nothing in Biology Makes Sense!, Sarah Hird explains a new theoretical study proposing that species concepts are hard to define for microorganisms not because just because they reproduce asexually and trade genetic code like playing cards … but simply because they’re small and numerous.
Specifically, the product of mutation rate and carrying capacity (uK) needs to be below a certain threshold for species to form. This is because there needs to be a small amount of variation relative to the amount of niche space available or no clear “best” type will emerge that can outcompete all the other types quickly enough to become established. If mutation rate is high, there are too many available types. If carrying capacity is high, there is no way to limit who’s there at all. Many other things are happening with this paper, but their big conclusion, put plainly, is that if there is too much variation, differentiation cannot occur.
Models of speciation that involve ongoing gene flow remain controversial because gene flow is expected to homogenize differences between populations. However, genome-level effects may facilitate speciation with gene flow. For example, selection against immigrants may have the effect of reducing realized gene flow, even at loci that are not under divergent selection (Rundle & Nosil 2005). This global reduction in gene flow and increased divergence across the genome due to divergent selection is termed ‘Genome Hitchhiking’ (Feder et al. 2012). Genome hitchhiking may be enhanced by fitness epistasis – multiple loci interacting synergistically to cause reductions in fitness that are greater than selection acting on any one locus.
It turns out that speciation is more probable in models that don’t treat genes like independently evolving beans in a beanbag, bearing out a classic criticism of simple speciation models made most prominently by Ernst Mayr. However, true linkage among the selected genes isn’t necessary, either. All in all, this is an exciting new development for those of us who think natural selection might be important in forming new species, so you should definitely go read the whole thing.◼
Equipped with the core genome sequence, the team collected still more sequence data from ten male flycatchers of each species, and aligned these additional sequences to the genome sequence, identifying millions of sites that vary within the two species, and millions of sites where they share variants. They scanned through all these sites to identify points in the genome where differences between the two small samples of flycatchers were completely fixed — that is, sites where all the collared flycatcher sequences carried one variant, and all the pied flycatcher sequences carried a different variant. The frequency of these fixed differences varied considerably across the genome, but there are dozens of spots where they’re especially concentrated, forming peaks of differentiation.
To learn what all those “islands of divergence” could tell us about how the two flycatchers came to be different species, go read the whole thing.◼
In 1989, Diane Dodd reared fruit flies (Drosophila pseudoobscura) from a common stock on two different food sources: starch and maltose. She found that after multiple generations of isolation on their separate substrates, starch-flies preferred to mate with starch-flies and maltose-flies preferred to mate with maltose-flies. The result was robust and repeatable, but the reason why and its mechanism were unknown.
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.
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.
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.
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
New species form when separate populations of related organisms are no longer able to interbreed. Reproductive isolation can arise if two populations evolve different mating behaviors, or lifestyles so different that individuals from different populations don’t even encounter each other—but it need not mean that matings between the two populations never occur. In fact, speciation can arise in the face of quite a lot of interbreeding, so long as the hybrids produced by interbreeding are less fit than “purebred” individuals.
This is what seems to be occurring in populations of Edith’s checkerspot, a small butterfly native to Western North America. Checkerspot populations in California use a wide variety of different host plants, and a recent study has shown that the offspring of parents from different host plants are maladapted in the wild.
Examination of checkerspot populations that have access to only one of the two host plants suggests that each plant is best used in rather different ways. For instance, Pedicularis-using checkerspot females lay lots of eggs on a few plants, while Collinsia-using females lay a few eggs on each of a large number of plants. Once they hatch, larvae from Pedicularis populations feed on leaves closer to the ground than larvae from Collinsia populations, which makes sense since Pedicularis grows lower in general.
If these differences have a genetic basis, then hybrid checkerspots might exhibit intermediate behaviors, which might not work so well on either host plant. To test for this “hybrid inviability,” the new study’s authors crossed checkerspots from populations encountering only one host plant or the other, and then tested the hybrids’ performance in the field—and what they found confirms those predictions.
The Goldilocks principle—intermediate is better–doesn’t apply to hybrid checkerspots. Hybrid caterpillars foraged on leaves at an intermediate height on both host plants, and grew more slowly than purebred caterpillars. Hybrid females laid an intermediate number of eggs on both host plants, and laid them at an intermediate height. This left their offspring in a poor position for foraging after they hatched—and indeed, they grew more slowly than larvae hatched from eggs that were laid at the “traditional” heights on the host plants.
So it looks as though natural selection for better performance on Collinsia has led to the evolution of checkerspots that are at a disadvantage using Pedicularis (and vice versa). This even to the point that hybrids, which feed and oviposit in ways that are only somewhat different from the optimum, pay performance costs.
What’s interesting, though, is that this hasn’t led to greater genetic differentiation of checkerspot populations using different host plants; as assessed using randomly-selected genetic markers, there is an isolation-by-distance effect, but no effect of host plant use. (The authors cite a previous study using about 400 AFLP loci [PDF].) That suggests that only a few genes are responsible for the observed adaptive differences, and that natural hybridization between checkerspot populations using different hosts may be mixing together the rest of the genome.
McBride, C., & Singer, M. (2010). Field studies reveal strong postmating isolation between ecologically divergent butterfly populations. PLoS Biology, 8 (10) DOI: 10.1371/journal.pbio.1000529
Singer, M.C., & Wee, B. (2005). Spatial pattern in checkerspot butterfly-host plant association at local, metapopulation and regional scales. Annales Zoologici Fennici, 42, 347-61
Most evolutionary biologists believe that the easiest means for two populations to become reproductively isolated—a first step to splitting into different species—is a physical barrier to movement. Mountain ranges, deep river valleys, or the sheer distance between an island and the mainland—the opportunities for allopatric speciation are all over the place. Unless, of course, you remember that the planet’s largest habitat is the ocean, and there aren’t such obvious physical barriers out at sea.
How do fish and other marine organisms form new species, then? Maybe they’re more likely to speciate as a result of natural selection that varies among otherwise connected marine habitats. For instance, a new study of rockfish finds evidence that this new species in this group usually form by adapting to conditions found at different oceanic depths [$a].
Two rockfish species, Sebastes atrovirens and Sebastes chrysomelas. Photos by brian.gratwicke.
The rockfish genus Sebastes contains several dozen species, but many of them occur in about the same regions of the Pacific ocean. Rather than being separated by physical distance, the group has diversified into different ecological niches, from the intertidal zone down to depths of 600 meters. The new study’s author, Travis Ingram, wanted to determine whether these habitat differences or geographic distance has more often been the cause of rockfish speciation, which he did using two major analyses.
In the first, Ingram asked whether pairs of rockfish species were more or less likely to occupy the same latitudes, and the same depth ranges, as they diverged over time. Allopatric speciation would lead to closely-related rockfish species occupying separate latitude ranges, but Ingram found the opposite. On the other hand, closely-related rockfish species are less likely to live at the same depth in the ocean—so depth, not geographic distance, seems to be important in rockfish speciation.
Ingram’s second analysis takes advantage of the general principle that traits associated with forming new species should change relatively rapidly at about the same time as speciation events, rather than at a uniform rate over time. Traits that undergo this speciational evolution can be distinguished from traits that don’t based on the relationship between trait values of related species. The idea is to compare the trait values for pairs of species drawn from the group of interest—if the differences in trait values are more strongly correlated with the number of speciation events that have occurred since the pair of species last shared a common ancestor than with the raw time since that common ancestry, the trait has probably evolved in speciational fashion.
This is the pattern Ingram found in the depths occupied by different species of rockfish. Changes in depth range occupied by rockfish were associated with speciation events, rather than evolving steadily over time. How these changes could have contributed to reproductive isolation is another question—different depth habitats present rockfish with different kinds of predators and prey, but also with different light environments for visual mating signals. One or more of these environmental differences could create the sort of divergent natural selection that can lead to reproductive isolation and speciation.
Ingram, T. (2010). Speciation along a depth gradient in a marine adaptive radiation. Proc. Royal Soc. B : 10.1098/rspb.2010.1127
The idea that interactions between species matter goes all the way back to the origins of evolutionary biology in the writing of Charles Darwin:
What a struggle between the several kinds of trees must here have gone on during long centuries, each annually scattering its seeds by the thousand; what war between insect and insect – between insects, snails, and other animals with birds and beasts of prey – all striving to increase, and all feeding on each other or on the trees or their seeds and seedlings, or on the other plants which first clothed the ground and thus checked the growth of the trees! (On the Origin of Species, 1859: 74-5)
This image of constant struggle among living things was more formally encapsulated in a 1973 paper by Leigh Van Valen (which paper is not, alas, available online), who proposed that constant coevolution with other species should mean that natural populations of living things are constantly adapting – in response to competitors, mutualists, predators, parasites – without gaining ground in the struggle, because the other species are also adapting. Van Valen lifted an image from Lewis Carroll’s Through the Looking-Glass, in which the Red Queen tells Alice that, in the strange world of Looking-Glass Land, “… it takes all the running you can do, to keep in the same place.”
They were running hand in hand, and the Queen went so fast that it was all she could do to keep up with her … The most curious part of the thing was, that the trees and the other things around them never seemed to changed their places at all.
“… it takes all the running you can do, to keep in the same place.” Image from Through the Looking-Glass, via VictorianWeb.
Thus, this idea that fuels much of my research, and a great deal of scientific study over the last three decades, is often identified with the Red Queen. What is interesting about this result is that Van Valen wasn’t interested in species interactions as such; he was trying to explain a pattern in the fossil record – that, for a wide variety of living things, the probability that a species would go extinct was independent of its age. That is, species that have been around for ten million years are no better adapted to their environments than species that have just formed; the probability of extinction is constant.
Van Valen’s explanation for this result was that something must constantly act to prevent living things from becoming better adapted, and better able to resist extinction, over time – specifically, the Red Queen’s race against other living things. Whenever a species “loses” the race, it goes extinct, regardless of how long the race has been up to that point. A similar pattern applies to the creation of new species – if coevolutionary interactions often help create reproductive isolation, then new species should also form at a roughly constant rate [$a]. Since this is what we observe, many biologists conclude that coevolution is responsible for the diversity of life on Earth.
What if the race doesn’t matter?
Fortunately for the advance of knowledge, however, not all evolutionary biologists have the same perspective. Paleontologists, for instance, tend to think that the year-to-year dynamics of the Red Queen race don’t make much difference in the longer run, over millions of years. They’d argue that most of the evolutionary change induced by coevolution between species is too variable and fleeting to have much effect on the rates at which species are formed and go extinct. Under this view, random geological events – continents splitting, mountain ranges rising, volcanoes erupting – are more likely to create new species and force them to extinction.
What matters more in the history of life, the biological environment, or the physical environment? Photos by Martin Heigan and Cedric Favero.
This competing model should also lead to a roughly constant rate of species formation and extinction, but it predicts a different pattern of variation around that constant rate than the coevolutionary Red Queen does. If most speciation and extinction events are caused by coevolution, then the time periods between speciation events should follow a normal distribution – forming a “bell curve” with most periods close to the average length, and symmetrical tails of longer and shorter periods of time. On the other hand, if many different, individually rare geological events are the most common cause of speciation and extinction, the periods between speciation events should follow an exponential distribution, with most periods being shorter than the average, but a long tail of longer periods as well.
This contrast is the crux of a study recently published in Nature. The paper’s authors, Venditti et al., examined 101 evolutionary trees estimated from genetic data, including groups like the dog family, roses, and bees. For each group’s evolutionary tree, they determined the distribution of the lengths of time periods between speciation events. A majority of the trees – 78% – supported the exponential model. That is, 78% of the groups of organisms examined had evolved and diversified in a fashion best explained by geology, not coevolution. None of the groups fit the normal distribution, and only 8% fit the related lognormal distribution.
The Red Queen is dead, long live the Red Queen!
This result suggests that within many groups of organisms, the physical environment is a more common cause of reproductive isolation or extinction than the biological environment. However, this isn’t to say that species interactions don’t matter. As Van Valen originally noted, extinction rates may be roughly constant within large groups of organisms, like those examined by Venditti et al., but those constant rates vary from group to group. These differences in rate may still depend on species interactions, because species interactions can shape how prone a population is to reproductive isolation.
For instance, a group of plants that has lousy seed dispersers may form new species in response to much smaller, and more common, geological barriers than a group of plants whose seeds can travel for hundreds of miles. Additionally, species interactions that promote diversity within the interacting species may mean that when geology creates isolation, the resultant daughter species are more different from each other than they would otherwise be, and less likely to re-merge if they come into contact again. Under that scenario, speciation caused by the physical environment would act to preserve variation [$a] created by the biological environment.
So, perhaps the Red Queen doesn’t operate the way we thought she did, with constant coevolutionary races spinning off new species and killing off others. But that hardly means that Red Queen processes don’t matter in the long run.
Benton, M. (2010). Evolutionary biology: New take on the Red Queen. Nature, 463 (7279), 306-7 DOI: 10.1038/463306a
Futuyma, D. (1987). On the role of species in anagenesis. The American Naturalist, 130 (3), 465-73 DOI: 10.1086/284724
Stenseth, N., & Maynard Smith, J. (1984). Coevolution in ecosystems: Red Queen evolution or stasis? Evolution, 38 (4), 870-80 DOI: 10.2307/2408397
Van Valen, L. (1973). A new evolutionary law. Evolutionary Theory, 1 (1), 1-30
Venditti, C., Meade, A., & Pagel, M. (2009). Phylogenies reveal new interpretation of speciation and the Red Queen. Nature, 463 (7279), 349-52 DOI: 10.1038/nature08630
Many different factors can conspire to create reproductive isolation between populations and, ultimately, separate species. Disentangling them is often tricky, but a study recently published in PNAS takes a crack, and demonstrates that two populations of leaf beetles are divided by food preferences, not genetics [$-a]
Some populations of the leaf beetle Neochlamisus bebbianae eat red maple, and others eat willow; each type grows better on their native host plant. Hybrids between the two species are possible, and they don’t grow as rapidly when raised on either host. This might mean that ecology — adaptation to the different host plants — is creating reproductive isolation between the two forms of Neochlamisus. But it might also mean that the two forms are genetically incompatible.
Many species are separated by intrinsic genetic incompatibility. In these cases, hybrids have reduced fitness, or die outright, because the two species have evolved separately in such a way that mixed genomes cannot produce important proteins correctly. One example was recently found in two lines of the wildflower Arabidopsis thaliana — both lines had duplicate copies of an important gene, and in each line a different copy mutated into non-functionality, so some hybrids between the two lacked any functional copies [$-a].
To differentiate between this kind of genetic incompatibility and ecological isolation, coauthors Egan and Funk conducted not one but two generations of hybridization between maple and willow Neochlamisus populations. In the first (F1) generation, they bred parents from each host-specialized type; but in the second they performed a “backcross,” breeding the F1 hybrids with mates from one or the other of the parental populations.
This produced a population of backcrossed hybrids with 3/4 of their genes from one parental type, and 1/4 from the other. If intrinsic incompatibility separated the types, then these backcrossed hybrids would grow poorly no matter what their host plant. However, if adaptation to separate host plants isolates the types, then backcrossed hybrids would perform better on the host plant of the type with which they shared more genes. This is what Egan and Funk found — backcrossed hybrid larvae grew faster on maple if they shared more genes with maple-type Neochlamisus, and similarly for willow.
Bikard, D., Patel, D., Le Mette, C., Giorgi, V., Camilleri, C., Bennett, M., & Loudet, O. (2009). Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana Science, 323 (5914), 623-6 DOI: 10.1126/science.1165917
Egan, S., & Funk, D. (2009). Ecologically dependent postmating isolation between sympatric host forms of Neochlamisus bebbianae leaf beetles Proc. Nat. Acad. Sci. USA, 106 (46), 19426-31 DOI: 10.1073/pnas.0909424106
Among the flowering plants, groups with flowers adapted to a narrower range of pollinators — the more specialized ones, like orchids or mints — tend to contain more species. Why? The classic hypothesis is that coevolution between plants and their pollinators leads to more pollinator-specialized plants, which are then more likely to become reproductively isolated, and eventually form separate species. However, I’ve just finished reading a review article that suggests an interesting alternative: that angiosperms may not be diverse because they’re specialized, but specialize because they’re diverse [$-a].
The review’s authors, Armbruster and Muchhala, first lay out a list of possible mechanisms connecting diversity and specialization. Three of them have specialization creating diversity, by (1) creating reproductive isolation, (2) enhancing isolation created by other forces, or (3) reducing extinction rates. Finally, there’s the possibility that diversity creates specialization, by (4) essentially forcing plants to divvy up the available pollinator community more and more finely.
Collinsia heterophylla, a member of a plant genus probably shaped by competition. Photo by Ken-Ichi.
The first two mechanisms are, as far as I’m concerned, contained within the classic specialization-creates-diversity hypothesis classically advanced by Verne Grant, that increased floral specialization makes it easier to form new species [$-a]. The third is a bit odd — generally, ecologists think that increased specialization means an increased, not a decreased, risk of extinction [$-a]. It’s intuitive that if you rely on fewer pollinator species, you can afford to lose fewer of them, and you have fewer opportunities to colonize new sites; so on the one hand, you’re at greater risk of local extinction, and on the other, you have difficulty establishing new populations. However, as Armbruster and Muchhala point out, this process should make more-specialized plant groups less diverse, which is the opposite of what we see.
The fourth hypothesis, that competition for pollinators causes greater to create greater specialization, leads to predictions that nicely differentiate it from the classic hypothesis: that hybridization between related flowering plants should be rare, and that plants should rarely occur in the same community as their closest evolutionary relatives. The first is important because it gives a reason to specialize on one or a few available pollinators — if a plant can’t reproduce with nearby relatives, all the pollen it exchanges with them represents wasted effort, and may actually interfere with pollen transfer from members of its own species. The second is a consequence of that process; plants are most likely to be able to hybridize with their evolutionary sisters, so successful speciation will usually require geographic or ecological isolation.
The authors then evaluate the evidence for these predictions in four plant genera with which they have prior experience: Dalechampia, Collinsia (pictured above), Burmeistera, and Stylidium. For these four groups, they find good support for the diversity-causes-specialization hypothesis — few natural, or even artificial hybrids, and few co-occurring sister species. To some degree, then, the new hypothesis is an effect of a researcher’s favorite study systems influencing their perspective on the broader picture of evolution. Armbruster and Muchhala give the same treatment to orchids, and find that for the most diverse angiosperm family, natural hybrids and co-occuring sister species are not rare. This ambiguity makes the review more interesting — it overturns the causation commonly inferred from the correlation between diversity and specialization, but it doesn’t make the mistake of sweepingly assuming the opposite instead.
Armbruster, W., & Muchhala, N. (2008). Associations between floral specialization and species diversity: Cause, effect, or correlation? Evolutionary Ecology, 23 (1), 159-79 DOI: 10.1007/s10682-008-9259-z
V. Grant (1949). Pollination systems as isolating mechanisms in angiosperms. Evolution, 3, 82-97
Johnson, S.D., & Steiner, K.E. (2000). Generalization versus specialization in plant pollination systems Trends in Ecology & Evolution, 15 (4), 140-3 DOI: 10.1016/S0169-5347(99)01811-X
Sargent, R. (2004). Floral symmetry affects speciation rates in angiosperms Proc. R. Soc. B, 271 (1539), 603-608 DOI: 10.1098/rspb.2003.2644