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The “Big Four,” part IV: Migration

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This post is the last in a special series about four fundamental forces in evolution: natural selection, mutation, genetic drift, and migration.

Edited 8 April 2011: Following some interesting comments from population geneticist Lou Jost, I’ve edited my characterization of the rule of thumb that one migrant per generation is generally enough to prevent populations from differentiating.

It’s the little differences. I mean, they got the same shit over there that we got here, but it’s just—it’s just there it’s a little different.
— Vincent, Pulp Fiction

ResearchBlogging.orgDifferent places are different from each other. This is a truism bordering on tautology, but it also has real implications for the ways in which life evolves and diversifies. The specific differences between one environment and another shape how well living things can move between those environments, and what happens when they do—the evolutionary consequences of migration.

Canada geese on the wing. Photo by Brian Guest (giant rebus).

Individuals moving between populations can alter the evolution of those populations in a number of ways [$a]. Migration introduces traits from one population into another, making it a source of variation not unlike mutation. Migration can swamp out the effects of local natural selection, if enough migrants come from a population experiencing a different selective regime. Migration from a larger population to a smaller one can offset the loss of variation to genetic drift; but a small group of individuals migrating to an empty habitat can be strongly affected by drift. Depending on what species concept you prefer, migration between two populations is either what prevents them from becoming separate species, or what conclusively proves that they are the same species.

Migration mixes things up

Strictly speaking, I’m not talking simply about the movement of living things from place to place, but about gene flow, which also requires interbreeding between migrants and the populations to which they migrate. Individuals might be able to travel to another environment, and even do so frequently, but fail to survive when they get there [PDF], or fail to find a mate in the local population, or have offspring that are themselves less fit than the offspring of the locals. Because tracking each of these steps directly is daunting at best, most population biology studies estimate the rate of successful migration by proxy, using some measure of the genetic similarity of populations—the more migrants successfully move between populations, the more similar the traits and gene frequencies of those populations will be.

The rate of gene flow between two populations is essentially a measure of how much those populations evolve as a single unit—if there’s no gene flow, selection or drift can eventually make the two populations into completely different things. An effective migration rate of one migrant per generation is has been generally understood to be enough to prevent drift from causing populations to diverge [$a]. (But there are significant objections to the one-migrant-per-generation rule of thumb, including the question of how we determine that populations have differentiated! See the discussion of this in the comments.) Populations linked by migration along several intervening populations may be isolated by distance [PDF] if the line of connecting populations is long enough.

If natural selection is operating in different directions in the two populations, more migration is necessary to prevent them evolving different traits. If individual genes experience different selection in each population, then those genes may still evolve differently even as migration continues to mix in neutral genes [PDF]. This movement of genes across recognized population and species boundaries is called introgression.

Gene flow versus selection

The bird-pollinated Iris fulva (left) can sometimes hybridize with bee-pollinated I. brevicaulis, but pollinators favor hybrids that look more like the parent species. Photos by Matt N Charlotte and Jim Petranka.

One well-documented case of gene flow between apparently “good” species is that of the Louisiana irises Iris fulva and I. brevicaulis. These two species fill fairly distinct ecological niches: red-orange I. fulva is mainly pollinated by hummingbirds, and grows in very wet conditions; blue I. brevicaulis is pollinated by bees, and grows best in drier habitats.

Yet when the two species co-occur, they sometimes do cross-pollinate. What prevents the two species from merging into a single iris? (Perhaps it would have purple flowers.) Natural selection, in this case, overwhelms migration. Experimentally created fulva–brevicaulis hybrids grown in wet conditions are more likely to survive if they carry specific genes from wet-tolerant fulva; and pollinators tend to favor hybrids that look more like their preferred parent species. I. fulva and I. brevicaulis share some genes that don’t affect wet tolerance or pollinator attraction, but generally remain separate evolutionary entities.

This kind of partial reproductive isolation is most widely documented in plants, but it has been found in all sorts of organisms—even the chipmunks Tamias ruficaudus and T. amoenus [PDF]. In an evolving world, this shouldn’t be surprising—it makes sense to find many cases of partial reproductive isolation as populations evolve toward the point of being separate species. Sometimes, of course, divergent selection weakens, or previous barriers to migration are removed, and populations re-merge into single evolutionary entities. But sometimes, the balance of the selection, mutation, drift, and migration is just right for just long enough to create a new, independently evolving form of life. And thus, as Darwin wrote, “endless forms most beautiful have been, and are being, evolved.”

References

Arnold, M., Hamrick, J., & Bennett, B. (1990). Allozyme variation in Louisiana irises: a test for introgression and hybrid speciation. Heredity, 65 (3), 297-306 DOI: 10.1038/hdy.1990.99

Good J.M., Hird S., Reid N., Demboski J.R., Steppan S.J., Martin-Nims T.R., & Sullivan J. (2008). Ancient hybridization and mitochondrial capture between two species of chipmunks. Molecular ecology, 17 (5), 1313-27 PMID: 18302691

Hedrick, P.W. (2005). Genetics of Populations. Boston: Jones and Bartlett Publishers. Google Books.

Martin, N.H., Bouck, A.C., & Arnold, M.L. (2005). Detecting adaptive trait introgression between Iris fulva and I. brevicaulis in highly selective field conditions. Genetics, 172 (4), 2481-9 DOI: 10.1534/genetics.105.053538

Martin, N., Sapir, Y., & Arnold, M. (2008). The genetic architecture of reproductive isolation in Louisiana irises: Pollination syndromes and pollinator preferences. Evolution, 62 (4), 740-52 DOI: 10.1111/j.1558-5646.2008.00342.x

Nosil, P., Egan, S., & Funk, D. (2008). Heterogeneous genomic differentiation between walking-stick ecotypes: “Isolation by adaptation” and multiple roles for divergent selection. Evolution, 62 (2), 316-36 DOI: 10.1111/j.1558-5646.2007.00299.x

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

Slatkin, M. (1987). Gene flow and the geographic structure of natural populations. Science, 236 (4803), 787-92 DOI: 10.1126/science.3576198

Wang, J. (2004). Application of the one-migrant-per-generation rule to conservation and management. Conservation Biology, 18 (2), 332-43 DOI: 10.1111/j.1523-1739.2004.00440.x

Wright, S.J. (1943). Isolation by distance. Genetics, 28, 139-56 PMCID: PMC1209196

Freeloading cuckoos force their hosts to diversify

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ResearchBlogging.orgAshy-throated parrotbills have a problem every time breeding season rolls around: how do they know whether the eggs in their nests are their own, or those of the common cuckoo? A study recently released in PLoS ONE suggests that one population of parrotbills fights this brood parasitism by laying eggs of different colors.

Common cuckoos lay eggs that mimic those of the host birds they trick into raising cuckoo chicks. Photo by Sergey Yeliseev.

Brood parasitism, in which one bird species lays its eggs in another bird’s nest, has long been considered a likely cause of coevolution [$a] between brood parasites and their hosts, because the interaction exerts strong natural selection on both species. Hosts suffer major fitness consequences if they take on the raising of another bird’s chick—and brood parasite chicks are often bigger, and more aggressive, than their adoptive “siblings,” sometimes pushing them right out of the nest. On the other hand, brood parasites run the risk of losing their offspring to hosts who can recognize a strange egg and eject it from the nest.

One way to avoid raising a cuckoo chick is to lay eggs that look different from cuckoo eggs. Cuckoos counteract this defense by evolving eggs that match their most common hosts—a selective regime proposed to explain rapid rates of species formation in parasitic cuckoo lineages. In the new study, Yang et al. show that this pattern plays out within a single population of ashy-throated parrotbills and the cuckoos that parasitize them. At a forested nature reserve in southwestern China, the team found that parrotbills lay eggs of three different colors: white, blue, or (rarely) pale blue. Common cuckoos in the same area also laid eggs of those three colors, in about the same proportions as the parrotbills—and cuckoo eggs were usually found in host nests with eggs of the same color. Experimental introduction of eggs into parrotbill nests confirmed that parrotbills were more likely to reject eggs colored differently from their own.

That result captures many of the necessary conditions for coevolution between ashy-throated parrotbills and the local cuckoo population; the frequency with which parrotbills reject eggs unlike their own should exert strong selection on the cuckoos, and (conversely) the frequency with which parrotbills fail to reject cuckoo eggs that look like their own should exert selection on the hosts. This isn’t the first case in which brood parasites have apparently forced their hosts to diversify, however—notably, African village weaverbirds evolved less varied egg patterning after being introduced into parasite-free habitats on Mauritius and Hispaniola.

References

Krüger, O., Sorenson, M., & Davies, N. (2009). Does coevolution promote species richness in parasitic cuckoos? Proc. Royal Soc. B, 276 (1674), 3871-9 DOI: 10.1098/rspb.2009.1142

Lahti, D. (2005). Evolution of bird eggs in the absence of cuckoo parasitism. Proc. Nat. Acad. Sci. USA, 102 (50), 18057-62 DOI: 10.1073/pnas.0508930102

Rothstein, S. (1990). A model system for coevolution: Avian brood parasitism. Ann. Rev. Ecology and Systematics, 21 (1), 481-508 DOI: 10.1146/annurev.es.21.110190.002405

Yang, C., Liang, W., Cai, Y., Shi, S., Takasu, F., Møller, A., Antonov, A., Fossøy, F., Moksnes, A., Røskaft, E., & Stokke, B. (2010). Coevolution in action: Disruptive selection on egg colour in an avian brood parasite and its host. PLoS ONE, 5 (5) DOI: 10.1371/journal.pone.0010816

The “Big Four,” part III: Genetic drift

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This post is the third in a special series about four fundamental forces in evolution: natural selection, mutation, genetic drift, and migration.

ResearchBlogging.orgHave a coin handy? Flip it.

If your coin is fair, I can guess that it’s come up heads and have a fifty percent chance, or probability equal to 0.5, that I’ve guessed correctly. Now, flip the coin ten times in a row. How many times did heads come up? Again, the best guess is that it came up five times—but it’s not all that unlikely that it came up six times, or four, or even as many as eight.

God may not play dice, but evolution does. Photo by jcotherals.

Now, if you flipped the coin an infinite number of times, then exactly fifty percent of the total flips would be heads. But who has time for that? Similarly, populations of living organisms are not infinite—often far from it—and this means that the frequency of genes in those finite populations can change as a result of the same phenomenon at work on your coin. Biologists call this genetic drift.

Evolution at random

The basic principle behind genetic drift is that each generation is a process of sampling from the parental population to create a population of offspring. As most folks know from discussions of opinion polls, smaller samples tend to be less representative of the pool from which they are drawn. Say a population of annual plants begins with equal numbers of plants bearing blue flowers or white flowers. If only ten seeds survive from that population to form the next generation, you would expect them to be five blue-flowered and five white-flowered seeds. However, it’s just like flipping a coin ten times: the probability of drawing six blue seeds is actually a little less than 21%, or one in five. The probability of drawing nine blue seeds is almost one in one hundred—small, but hardly impossible.

Consider, too, that once you draw six blue seeds, it becomes slightly more likely that you’ll draw seven in the next generation, which makes it slightly more likely you’ll draw eight in the next. Repeated selection of small samples means that traits can drift to fixation (or loss, depending on your perspective), so that everyone in the population has the same trait. Rare traits are more likely to be lost to drift, and large populations are less prone to its effects. This is nicely illustrated in this online simulation from the University of Connecticut—over time, a focal gene fixes or disappears from the population as a function of the population size and the initial frequency of the gene.

In general, drift interferes with the efficient operation of natural selection. Even in relatively large populations, the probability that a new beneficial mutation will become fixed is approximately twice the selective benefit of that mutation—typically very small. (This is from a 1927 paper by J.B.S. Haldane that doesn’t seem to be online in any form, but which is discussed by Otto and Whitlock in a 1997 paper extending the classic result.) In a small enough population, a trait can become fixed even if it reduces its carriers’ fitness [PDF].

Evolving differences without selection

As I’ve discussed above, the effect of drift in a single population is to reduce variation as rare traits are lost to chance. This means that, when more than one independently-evolving population is considered, drift actually increases variation among them [$a], as different traits fix or are lost in each. That is, drift can make isolated populations evolve into different species even if they experience identical regimes of natural selection.

Woodland salamanders (genus Plethodon: left, P. vehiculum; right, P. yonahlossee) have diversified not by adapting to different environments, but by being homebodies. Photos by squamatologist.

A flagship example of this sort of non-adaptive diversification are the woodland salamanders of eastern North America, genus Plethodon. Woodland salamanders are quite diverse, having accumulated more than 40 species in the last 27 million years, but all of these species live in more or less the same habitat, under the leaf litter in moist Appalachian forests, and many are “cryptic” species distinguishable only by DNA analysis. How, then, did Plethodon become so diverse?

The answer is simply that woodland salamanders don’t travel very well. Salamanders need moist environments–they breathe through their skin, which doesn’t work well if it dries out—and so have difficulty moving from one stream drainage to another. This means that it doesn’t take much distance to isolate one Plethodon population from another, allowing drift to take them in different directions. Salamanders form new species, in other words, by staying at home.

This effect of drift means that biologists must adjust their “null” expectation when they observe differences in natural populations—the mere fact that some Joshua trees look different from other Joshua trees does not necessarily mean that natural selection has created those differences. Furthermore, the degree to which drift or selection can generate differences among populations depends strongly on the fourth force in the Big Four, which I’ll discuss next week: migration.

References

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

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. Royal Soc. B, 273 (1586), 539-46 DOI: 10.1098/rspb.2005.3326

Lande, R. (1992). Neutral theory of quantitative genetic variance in an island model with local extinction and colonization. Evolution, 46 (2), 381-9 DOI: 10.2307/2409859

Otto S.P., & Whitlock M.C. (1997). The probability of fixation in populations of changing size. Genetics, 146 (2), 723-33 PMID: 9178020

Wright S (1931). Evolution in Mendelian populations. Genetics, 16 (2), 97-159 PMID: 17246615

The “Big Four,” part II: Mutation

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This post is the second in a special series about four fundamental forces in evolution: natural selection, mutation, genetic drift, and migration.

This post was chosen as an Editor's Selection for ResearchBlogging.orgIn order for populations to change over time, to descend with modification, as Darwin originally put it, something has to create the modifications. That something is mutation.

A mutation of large effect? Photo by Cayusa.

A mutation is any change to an individual’s genetic code, whether caused by an external factor like radiation, or an error in the DNA copying that takes place every time an individual cell divides. However, not all mutations are created equal.

First and foremost, for a mutation to have any future existence beyond the individual in which it occurs, it must be in a cell that will go towards forming the next generation, a germline cell. In sexually reproducing species, this means sperm or egg cells, or the progenitor cells in the testes or ovaries that form them. Second, for a mutation to be “visible” to natural selection, it must have some effect on fitness, the number of offspring an individual carrying the mutation is likely to have. The genetic code determines how and when individual cells make proteins, and proteins determine phenotypes, the visible characteristics of living things. However, many changes to the genetic code don’t affect their carriers’ fitness. Mutations might be more or less neutral because

  • They occur in regions of the genome that don’t code for proteins or control protein production—so-called “junk” DNA.
  • They are synonymous substitutions, which occur in a protein-coding region of DNA, but don’t alter the protein produced.
  • They alter a protein, but not in a way that changes its function [PDF].
  • They alter a protein’s function and an individual’s phenotype, but in a way that doesn’t affect how many offspring that individual has.

Neutral mutations are actually quite important for biological studies—DNA fingerprinting and population genetics studies rely on them. Their frequencies evolve at random, reflecting the history of the populations that carry them rather than the effects of natural selection.

Favorable new mutations sweep the population


TOP: DNA sequences from a population are variable (blue) before a new mutation (red dot) arises; after it “sweeps,” every individual carries the allele as well as identical sequence nearby (red). BOTTOM: a figure from Linnen et al. (2009), demonstrates this pattern in deer mice. Images from Pritchard et al. (2010), fig. 3 and Linnen et al. (2009), fig. 4.

The variation introduced by neutral mutations—or, rather its absence—can help identify regions of the genome where selection is active. When a new gene arises by mutation, and it is strongly favored by selection, it can quickly spread through a population. In species that remix their genomes through sexual selection, the region of the genome containing a useful new gene can recombine into many different genetic backgrounds—but the closer a region of DNA is to the favored mutation, the less likely it is to recombine and separate from it. Thus, a region of the genome rather larger than the gene favored by selection is carried along until everyone in the population has the same DNA sequence.

When a new mutation takes over a population in this manner, it’s called a selective sweep, and the pattern it produces has been used to identify genes recently favored by selection in many different species, including humans. For instance, Linnen et al. documented reduced genetic variation in the neighborhood of gene variant responsible for light-colored fur in deer mice to demonstrate that it spread rapidly through the population after the mice colonized a region with light-colored sand.

Fuel for the engine of natural selection

Selective sweeps highlight how natural selection acts in opposition to mutation: mutation introduces new variation into populations, and natural selection causes the most fit variants to spread—potentially until the whole population carries the same trait. At the same time, selection requires variation in order to operate. If everyone is identical, then everyone has the same expected number of offspring, and the next generation will look just like the current one.

Because of this, natural selection can only operate as rapidly as mutation can introduce new variation from which to select. We know of specific cases in which selection seems to have “stalled” for lack of heritable variation. For instance, the fly Drosophila birchii lives in rainforest habitats along the northeast coast of Australia. Fly populations from the driest locations in this range have greater tolerance for dry conditions, but they also have virtually no heritable variation for drought tolerance [PDF]—and the authors suggest that this could limit the flies’ ability to evolve in response to climate change.

In other cases, though, biologists have found that mutation seems to provide new variation at least as fast as selection can remove it, leading to sustained, long-term evolution of experimental populations [PDF]. One important factor that may determine the outcome of this mutation-selection balancing act is actually the size of the population—more individuals means more opportunities for mutations to occur.

So the rate at which new mutations accumulate in a population depends on many factors, not the least of which are how you choose to measure that rate, and the fitness effects of the counted mutations. (Does a mutation “count” as soon as it occurs in a cell’s nucleus, or only when it has passed on to the next generation, or only when it has spread to everyone in a population?) Ultimately, populations evolve through a constant tension between the effects of mutation, natural selection, and the subject of next week’s Big Four force: genetic drift.

References

Barton, N., & Keightley, P. (2002). Understanding quantitative genetic variation. Nature Reviews Genetics, 3 (1), 11-21 DOI: 10.1038/nrg700

Drake J.W., Charlesworth B., Charlesworth D., & Crow J.F. (1998). Rates of spontaneous mutation. Genetics, 148 (4), 1667-86 PMID: 9560386

García-Dorado, A., Ávila, V., Sánchez-Molano, E., Manrique, A., & López-Fanjul, C. (2007). The build up of mutation-selection-drift balance in laboratory Drosophila populations. Evolution, 61 (3), 653-65 DOI: 10.1111/j.1558-5646.2007.00052.x

Hoffmann, A., Hallas R.J., Dean J.A., & Schiffer M. (2003). Low potential for climatic stress adaptation in a rainforest Drosophila species. Science, 301 (5629), 100-2 DOI: 10.1126/science.1084296

Keightly, PD. (2003). Mutational variation and long-term selection response. Pages 227-48 in Plant Breeding Reviews, Volume 24, part I. J. Janick, ed. John Wiley & Sons. Google Books.

Linnen, C., Kingsley, E., Jensen, J., & Hoekstra, H. (2009). On the origin and spread of an adaptive allele in deer mice. Science, 325 (5944), 1095-8 DOI: 10.1126/science.1175826

Pritchard, J., Pickrell, J., & Coop, G. (2010). The genetics of human adaptation: Hard sweeps, soft sweeps, and polygenic adaptation. Current Biology, 20 (4) DOI: 10.1016/j.cub.2009.11.055

Tokuriki, N., & Tawfik, D. (2009). Protein dynamism and evolvability. Science, 324 (5924), 203-7 DOI: 10.1126/science.1169375

The “Big Four,” part I: Natural selection

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This post is the first in a special series about four fundamental forces in evolution: natural selection, mutation, genetic drift, and migration.

This post was chosen as an Editor's Selection for ResearchBlogging.orgAmong non-biologists, the best-known of the Big Four forces of evolution is almost certainly natural selection. We’ve all heard the catchphrase “survival of the fittest,” and that’s a pretty good, if reductive, summing up of the principle. In more precise terms, here’s how natural selection works:

  • Natural populations of living things vary. Deer vary in how fast they can run, plants vary in how much drought they can tolerate, birds vary in their ability to catch prey or collect seeds—no two critters of the same species are exactly alike.
  • Some of those variable traits determine how many offspring living things have. How well you avoid predators, fight off disease, and collect food all determine how many babies you can make.
  • Many of those variable traits are heritable, passed on from parents to offspring. Faster deer usually have faster fauns; drought-tolerant plants make drought-tolerant seeds.

With these three conditions in place, natural selection occurs: heritable traits that help make more babies become more common. That is, if you have a trait that lets you support more offspring than your neighbor, you’ll have more children than your neighbor, and they’ll have more children than your neighbor’s children, and so on.

Fitness-versus-phenotype regressions for directional, stabilizing, and disruptive selection. Graphic by jby.

Measuring selection

Put this way, natural selection is simply a relationship between fitness, the number of offspring an organism can produce (often reported in comparison to the rest of the local population), and phenotype, the value of one or more traits of that organism (wing length, running speed, number of flowers produced, &c). Biologists can measure selection in natural populations by estimating this relationship between fitness (or a proxy for fitness, like growth rate), and phenotypes. Such an analysis should produce something like the regression graphs to the right, in which the relationship might be directional, with greater- (or smaller-) than-average phenotypes having greater fitness; stabilizing, with the average phenotype value having greater fitness; or disruptive, with extreme phenotype values having greater fitness. The slope of the line, or the shape of the curve, is a measure of the strength of natural selection [PDF] on an organism’s phenotype. This approach to measuring selection has been widely applied, and in 2001 a group of biologists led by Joel Kingsolver collected more than 2,500 estimates of the strength of natural selection [PDF].

How strong is selection?

Kingsolver et al. found that selection was usually surprisingly weak. Studies with the largest sample sizes, and the most statistical power to detect selection, mostly found directional selection strength (that is, the slope of the fitness-phenotype regression) less than 0.1, and the strength of stabilizing or disruptive selection was similarly low. Does this mean selection doesn’t matter in the short-term evolution of natural populations?

Probably not. The average selection strength estimates from the Kingsolver et al. dataset are actually stronger than selection strength assumed in most mathematical models of evolution. Furthermore, the collected estimates of selection had “long tailed” distributions—a small number of studies found quite strong selection, up to ten times as strong as the average. So maybe rare but strong bouts of selection have disproportionate impact over the long term.

Peter and Rosemary Grant have documented decades of shifting natural selection on Darwin’s finches (Geospiza spp.). Photo by Igooch.

Taking the finch by the beak

Part of the problem with assessing selection in nature is that most datasets measure selection over just one or a few years. One exception is the case of Darwin’s finches in the Galapagos Islands. The Galapagos offers a wide variety of habitat types, and experiences substantial year-to-year environmental variation—a landscape that should exert all sorts of natural selection on its occupants. Peter and Rosemary Grant have studied Galapagos finches for decades now, and found that selection is continuously at work on these unassuming birds. (The Grants’ book How and Why Species Multiply sums up their research program for a lay audience.)

Much of the Grants’ work has focused on the finches’ beaks, which largely determine what food the birds can eat. The distribution of seed sizes available on different Galapagos islands strongly predicts [PDF] the size of finches’ beaks on those islands. In 1989, the Grants published estimates of selection on beak size in the finch species Geospiza conirostris following a drastic wet-to-dry climactic shift that radically changed what foods were available to the finches. They found strong selection [$a], with fitness-phenotype regression slopes as high as 0.37. What’s more, the direction of selection changed dramatically from a very wet year to the dry year immediately afterward, as the finches were forced to move from feeding on small seeds and arthropods—which gave the advantage to shorter beaks—to hard-to-crack seeds, which required deep beaks.

The Grants’ longer-term study of selection on Galapagos finches confirms this image of selection swinging back and forth unpredictably [PDF]. From 1972 to 2001, they tracked populations of the finch species G. scandens and G. fortis, and saw both more gradual long-term changes in the finches’ body size and beak measurements as well as sudden sharp shifts. These changes continually altered the ability of the two species to hybridize, so that some years they were more reproductively isolated than others—and conditions in any one year were poor indicators of what would be going on five, ten, or twenty years later.

So when does selection matter?

The Grants’ study makes natural selection look as shifting and impermanent as the wind. How can it shape patterns of evolution over millions of years, then? One possibility is that trends may emerge over longer periods of time, as wobbly selection moves species in new directions in a drunkard’s walk, with two steps forward, then one step back, then four steps forward. Another is that lasting trends only occur when speciation intervenes to lock in fleeting changes due to variable natural selection [$a]. Much also depends on how selection interacts with mutation, genetic drift, and migration, as I’ll discuss in the rest of this series.

And here’s a shameless plug for a t-shirt. Photo by jby.

References

Futuyma, D. (1987). On the role of species in anagenesis. The American Naturalist, 130 (3), 465-73 DOI: 10.1086/284724

Grant, B.R., & Grant, P.R. (1989). Natural selection in a population of Darwin’s finches. The American Naturalist, 133 (3), 377-93 DOI: 10.1086/284924

Grant, P.R., & Grant, B.R. (2002). Unpredictable evolution in a 30-Year study of Darwin’s finches. Science, 296 (5568), 707-11 DOI: 10.1126/science.1070315

Grant, P.R. and B.R. Grant. (2008) How and Why Species Mutliply: The Radiation of Darwin’s Finches. Princeton University Press. Google Books.

Kingsolver, J., Hoekstra, H., Hoekstra, J., Berrigan, D., Vignieri, S., Hill, C., Hoang, A., Gibert, P., & Beerli, P. (2001). The Strength of phenotypic selection in natural populations. The American Naturalist, 157 (3), 245-261 DOI: 10.1086/319193

Lande, R. (1976). Natural selection and random genetic drift in phenotypic evolution. Evolution, 30 (2), 314-34 DOI: 10.2307/2407703

Johnson, T., & Barton, N. (2005). Theoretical models of selection and mutation on quantitative traits. Phil. Trans. R. Soc. B, 360 (1459), 1411-25 DOI: 10.1098/rstb.2005.1667

Schluter, D., & Grant, P. (1984). Determinants of morphological patterns in communities of Darwin’s finches. The American Naturalist, 123 (2), 175-96 DOI: 10.1086/284196

Back to basics: The “Big Four”

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ResearchBlogging.orgThe nice thing about a field season away from all regular internet access is that it gives you a real sabbatical of a sort—a chance to reassess plans and set new goals. One of the new goals I set myself this last field season was to introduce a new kind of topic here at Denim and Tweed.

Most of my writing about science at D&T focuses on recently published discoveries in evolution and ecology. It’s fun writing, and it coincides neatly with my regular journal reading, and I intend to keep doing it. But I’ve discovered that when I want to put new work in context, I often need to discuss fundamental concepts of evolutionary biology that aren’t necessarily common knowledge, such as genetic drift or sexual selection. However, I rarely have room to explain these concepts in depth within a blog post devoted to something else.

So maybe the solution is to devote some posts to explaining these “basics.” I’m going to start with a series of posts on the “Big Four” processes of population genetics. These are the four processes that account, in one way or another, for every change in the frequency of genes within natural populations. In other words, the Big Four account for much of evolution itself. They are:

  • Natural selection, changes in gene frequencies due to fitness advantages, or disadvantages, associated with different genes.
  • Mutation, the source of new forms of genes;
  • Genetic drift, or changes in gene frequencies that arise from the way probability works in finite populations; and
  • Migration, or changes in gene frequencies due to the movement of organisms from site to site.

Lay readers may be surprised both by what we know, and what we don’t, about how these four processes operate in nature. Natural selection is relatively easy to measure, and apparently ubiquitous [PDF] in natural populations—but we don’t know how often the resulting short-term changes impact evolution over millions of years. Mutation, the source of variation on which natural selection acts, seems to vary widely among living things. Genetic drift means that a trait can come to dominate a population even if it has no fitness effect—or sometimes a deleterious one. Finally, migration across variable landscapes can interact with selection, drift, and mutation [$a] to completely alter their effects.

I’ll devote one post each to selection, mutation, drift, and migration, discussing classic findings as well as more recent scientific discoveries about each. They’ll arrive as my usual mid-week science posts for the next four weeks, and I’ll update this post with links to the others as they go online—so if this looks worth following, you can either bookmark this post, or subscribe to D&T’s RSS Feed.

Natural selection, mutation, genetic drift, and migration act together to shape the evolution of natural populations. Photo by jby.

References

Drake JW, Charlesworth B, Charlesworth D, & Crow JF (1998). Rates of spontaneous mutation. Genetics, 148 (4), 1667-86 PMID: 9560386

Kingsolver, J., Hoekstra, H., Hoekstra, J., Berrigan, D., Vignieri, S., Hill, C., Hoang, A., Gibert, P., & Beerli, P. (2001). The strength of phenotypic selection in natural populations. The American Naturalist, 157 (3), 245-61 DOI: 10.1086/319193

Slatkin, M. (1987). Gene flow and the geographic structure of natural populations. Science, 236 (4803), 787-92 DOI: 10.1126/science.3576198

Wright S (1931). Evolution in Mendelian populations. Genetics, 16 (2), 97-159 PMID: 17246615

Invasive species runs out of evolutionary “steam” as it invades

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ResearchBlogging.orgFor invasive plants, flowering time is a trait that may often be under selection during colonization—when a plant flowers determines its climatic tolerances, its vulnerability to herbivores, and its compatibility with the local pollinator community. In a study just released online at Proceedings of the Royal Society B, Colautti and coauthors examined the evolution of this trait in a plant that has swept across eastern North America since its introduction from Europe: purple loosestrife, and found that it may be reaching the evolutionary limits of its invasive-ness.


Purple loosestrife, Lythrum salicaria, may be running out of evolutionary steam as it invades more northerly climes. Photo by Steve_C.

Loosestrife, like many organisms, faces a trade-off in establishing a time to reproduce, between early flowering and accumulating resources for seed production. Early flowering means producing fewer seeds, or provisioning them less thoroughly—but as loosestrife colonizes more and more northerly climes, it will be under selection to flower earlier in compensation for shorter and shorter growing seasons.

But natural selection can only do so much. In order for natural selection to operate on a population, individuals in the population must vary in some trait that affects how many offspring they produce—if all individuals have the same trait value, or the same number of offspring, they’ll all have equal chances to contribute to the next generation, which will probably look pretty much like the parental generation. Furthermore, species colonizing new territory may actually lose variation, either because new popualtions may be founded by just a few individuals, or because of the action of natural selection itself. Finally, there may be a point at which plants simply cannot flower any earlier, because they must reach a certain developmental point before reproducing.

Add these up for an invasive species moving north, and you might expect that the most recently-arrived (and most northerly) populations would flower earlier, and have less variation in flowering time, than more southerly populations. Using theoretical and experimental approaches, Colautti et al. show that exactly this process is occurring in purple loosestrife. They first built a mathematical model of natural selection acting on flowering time, which behaved as I’ve outlined above. They followed this by raising loosestrife seeds from northern and southern populations together in experimental sites located at different latitudes, and found that, even raised in southern conditions, seeds from northern sites grew into smaller, less productive plants. Raised in greenhouse conditions, seeds from southern populations produced plants with a much wider range of flowering times than seeds from northern populations. Together, these suggest that loosestrife has evolved earlier flowering times at northern sites—and may be running out of variation, the raw material for natural selection, as it moves north.

Invasive species often evolve in response to their new habitats, and force native species to evolve in response to their arrival. As they colonize Australia, for instance, cane toads (soon to be a major motion picture) have evolved longer legs [PDF] so as to win the race for unoccupied breeding ponds; and exerted selection on native black snakes to tolerate the toads’ defensive toxins and to attack the toads less frequently. Better models of how newly introduced species respond to and exert natural selection may help conservation biologists anticipate the results of biological invasions.

References

Colautti, R., Eckert, C., & Barrett, S. (2010). Evolutionary constraints on adaptive evolution during range expansion in an invasive plant. Proc. R. Soc. B DOI: 10.1098/rspb.2009.2231

Phillips, B., Brown, G., Webb, J., & Shine, R. (2006). Invasion and the evolution of speed in toads. Nature, 439 (7078) DOI: 10.1038/439803a

Phillips, B., & Shine, R. (2006). An invasive species induces rapid adaptive change in a native predator: cane toads and black snakes in Australia Proc. R. Soc. B, 273 (1593), 1545-50 DOI: 10.1098/rspb.2006.3479

Vellend, M., Harmon, L., Lockwood, J., Mayfield, M., Hughes, A., Wares, J., & Sax, D. (2007). Effects of exotic species on evolutionary diversification Trends in Ecology & Evolution, 22 (9), 481-8 DOI: 10.1016/j.tree.2007.02.017

Caught between birds and squirrels, limber pines go both ways

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ResearchBlogging.orgResponding to natural selection often means compromising between different selective forces. A brief paper published online early at Evolution documents one such case – limber pine trees’ compromise between protecting their seeds from squirrels, and making them accessible to the birds that disperse them. Pulled between these conflicting selective sources, some limber pine populations grow cones in a wider variety of shapes [$a].



Cones of the limber pine must balance protection against squirrels with accessibility for seed-dispersing Clark’s nutcrackers. Photos by Fool-On-The-Hill and almiyi.

Seeds of the limber pine are cache-dispersed by Clark’s nutcrackers. That is, the birds collect pine seeds to cache as a winter food source, but they collect many more than they need, and forget lots of them, and forgotten seeds are often able to sprout. However, squirrels also like pine seeds, and they harvest them before the birds start caching seeds. These two seed-harvesters generate conflicting selection on limber pine cones [$a]. Nutcrackers go for cones with lots of seeds protected by thinner scales; but so do squirrels.

However, pine-nut-eating squirrels are not present everywhere limber pines grow. The new study’s authors, Siepielski and Benkman, take advantage of this quirk of distributions to perform a natural experiment, comparing pines that only need to satisfy their seed dispersers with pines that also need to defend against seed predators. Surveying cone shapes in populations of each class, they found that limber pine populations facing conflicting selection were bimodal, with trees mainly growing either squirrel-defended short, thick-scaled cones, or nutcracker-friendly longer, thin-scaled cones. Populations growing in regions without squirrels produced only nutcracker-friendly cones.

This apparently simple pattern conceals more complicated dynamics – in fact, as the authors disclose in the Discussion section, many other limber pine populations are solely composed of trees producing squirrel-defended cones. This is because, when pines establish in areas with large squirrel populations, nutcrackers may never colonize the area, or may visit less frequently and disperse fewer seeds. Without nutcracker dispersal, seeds are mainly dispersed after the cones fall, by rodent species that (unlike squirrels) forage on the ground. This makes squirrel defense the only selective priority. Populations displaying both cone types probably only arise in unique conditions, the authors say, where squirrels are present but not at high density.

References

Siepielski, A., & Benkman, C. (2007). Convergent patterns in the selection mosaic for two North American bird-dispersed pines. Ecological Monographs, 77 (2), 203-20 DOI: 10.1890/06-0929

Siepielski, A., & Benkman, C. (2009). Conflicting selection from an antagonist and a mutualist enhances phenotypic variation in a plant. Evolution DOI: 10.1111/j.1558-5646.2009.00867.x

Bats can hold their liquor

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ResearchBlogging.orgA new paper in PLoS ONE tests the alcohol tolerances of nectar-eating bats. Believe it or not, there is a scientific purpose.

Alcohol isn’t a vice exclusive to humans. Animals that eat fruit or nectar may accidentally imbibe if they eat past-ripe fruit or nectar that has had time to ferment. Some species, like the pentail treeshrew, have evolved tolerances that surpass our own capacities – and some, like cedar waxwings, get distinctly tipsy after a few bad berries. Alcohol tolerance effectively expands the potential food supply, by allowing consumption of fruit or nectar that’s a little past the metaphorical sell-by date.


Artibeus lituratus, one of the bat species tested for alcohol tolerance by Orbach et al. Photo by Setsuo Tahara.

In the new study, Dara Orbach and colleagues captured several individuals each from a variety of nectar-feeding bat species found near their field station in Belize. They fed the bats a sugar-water solution approximating nectar, spiking a randomly-chosen subset with ethanol. The bats were then released to fly through an obstacle course, where microphones were placed to record their echolocation calls. The authors figured that intoxication would manifest in difficulty navigating the obstacles, possibly in connection with distortions of echolocation.

However, bats fed alcohol performed as well as bats fed plain sugar water. Different species varied in how they handled the alcohol, though. The authors dosed the bats with alcohol in proportion to their body weight, but saliva tests just before the experiment revealed quite a bit of variation in actual blood alcohol concentration for individuals from different species. Evidently some species metabolized the alcohol, and others were able to fly straight even with a BAC that would put a human in jail for DUI.

Reference

Orbach, D., Veselka, N., Dzal, Y., Lazure, L., & Fenton, M. (2010). Drinking and flying: Does alcohol consumption affect the flight and echolocation performance of Phyllostomid bats? PLoS ONE, 5 (2) DOI: 10.1371/journal.pone.0008993

Dethroning the Red Queen?

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ResearchBlogging.orgRegular readers of Denim and Tweed know that I’m fascinated by the evolution of species interactions: interactions between plants and nitrogen-fixing bacteria, Joshua trees and yucca moths, parasitoid wasps and butterflies, and between ants and the trees they guard. I tend to think that coevolutionary interactions not only determine the health of natural populations, but shape their evolutionary history. But would I feel that way if I were a paleontologist?

Running just to stay in place

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.

References

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