Category Archives: evolution

When ecological opportunity knocks, does adaptive radiation answer?

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ResearchBlogging.orgOne of the most basic questions in evolutionary ecology is, “why are there more kinds of this kind of critter than that kind of critter?” As in, why are there more than twenty thousand species of orchids, but only one species of ginkgo? Why are there hundreds of thousands of species of beetles, but only four species of horseshoe crab? In a literature review just released online—and my first publication as lead author!—my coauthors and I assess the support for one hypothesis: that species multiply because of ecological opportunity.

Biologists interested in the origins of species diversity frequently focus on the phenomenon of adaptive radiation, the process by which a single species rapidly gives rise to many new species, each with different traits adapted to different lifestyles. Darwin’s finches, with their beaks shaped to suit to different foods [$a], are a classic case; the Anolis lizards of the Caribbean, which have repeatedly evolved into a handful of “ecomorphs” with different body sizes and shapes adapted to different perching locations [PDF], are another.

Why are there so many [insert taxon here]? Photos by Bill & Mark Bell (1 & 2), fturmog (3 & 4).

The two most influential theories of adaptive radiation—by G.G. Simpson and Dolph Schluter—have suggested that it results when a species encounters ecological opportunity. Ecological opportunity might be a newly-evolved trait, or a new habitat, or the extinction of a species’ competitors or predators. For instance, a butterfly might evolve a way to overcome the chemical defenses of an abundant plant species, or a plant introduced by humans to a new habitat might find that local pathogens aren’t as deadly to it as the ones in its native range. Ecological opportunities have the effect of granting access to new resources. We have pretty good evidence that this can allow individual populations to increase in number, and even evolve greater diversity—but is that enough to spur the rapid speciation that forms adaptive radiation?

Ecological opportunity ? adaptive radiation

We’re pretty sure about steps 1 and 3. We’re still trying to figure out step 2.

Readers in certain demographic groups may think this sounds like an underpants gnome problem. But it isn’t, exactly. The gnomes’ business model can’t get to from step 1 (collect underpants) to step 3 (profit) because they don’t have a step 2. Evolutionary ecologists, on the other hand, already have their step 3 in the phenomenon of adaptive radiation. Ecological opportunity looks like a good prospect for step 1 precisely because it suggests some plausible options for step 2.

When a population encounters ecological opportunity, the new habitat, new trait, or extinction of antagonists provides access to new resources, and relaxes natural selection on the population. This leads to three phenomena usually grouped together under the term ecological release

  • The population experiences density compensation—more individuals can live in a particular area, creating stronger competition within the population.
  • Because of this stronger competition within the population, or because there isn’t much competition from other species, members of the population venture into new habitats, or use new food resources.
  • The population becomes more diverse, either because of the relaxed selection, or because of competition-driven selection for using new habitat and new resources.

One or more of these three aspects of ecological release turn up whenever populations find new food resources, or escape predators and/or competitors. Density compensation has been widely observed in populations colonizing new habitats, especially islands; and experiments with sticklebacks and fruit flies [$a] suggest that the stronger competition resulting from density compensation can spur the population to become more diverse in its use of resources. Bacterial populations can even evolve different specialized forms—adaptive radiations in microcosm—when introduced to new food resources.

Anoles show signs of density compensation on Caribbean islands—is that the reason behind their diversification? (Pictured: Anolis oculatus.) Photo via WikiMedia Commons

But where’s the speciation?

However, the evolution of bigger, more diverse populations is not the same thing as the evolution of new species—and that’s what adaptive radiation is really all about. These changes resulting from ecological opportunity might directly promote speciation if stronger competition leads to disruptive natural selection. Similarly, the competition-driven incentive to colonize new habitats or exploit new food sources could expose some parts of the population to different forms of natural selection, eventually causing them to evolve into specialists on the new resources. Finally, even if speciation only happens when natural barriers cut off migration, maybe larger, more variable populations provide more diversity for vicariance events to divvy up.

This is all pretty speculative, though. We still don’t know how often—or how rarely—divergent natural selection contributes to making new species. One way to deal with this is to approach the question from the other direction: look backward at the history of existing species, rather than following what happens to populations immediately after ecological release.

A backward-looking approach might use statistical analyses of the evolutionary relationships between living things to identify points in time when species formed unusually fast, and try to identify the cause. Some of my coauthors from the review paper recently published an analysis of the evolutionary tree connecting all vertebrates, and found that speciation rates increased around the origins of the largest group of birds, a large portion of the lizards and snakes, and non-marsupial mammals, among others.

This is very much a starting point, but maybe by complementing similar studies with research on populations currently evolving in response to ecological opportunity, biologists can work our way closer to understanding the origins of the endless and beautiful forms of life on Earth.

References

Alfaro, M., Santini, F., Brock, C., Alamillo, H., Dornburg, A., Rabosky, D., Carnevale, G., & Harmon, L. (2009). Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc. Nat. Acad. Sci. USA, 106 (32), 13410-4 DOI: 10.1073/pnas.0811087106

Bolnick, D. (2001). Intraspecific competition favours niche width expansion in Drosophila melanogaster. Nature, 410 (6827), 463-6 DOI: 10.1038/35068555

Blumenthal, D., Mitchell, C., Pysek, P., & Jarosik, V. (2009). Synergy between pathogen release and resource availability in plant invasion. Proc. Nat. Acad. Sci. USA, 106 (19), 7899-904 DOI: 10.1073/pnas.0812607106

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

Kassen, R. (2009). Toward a general theory of adaptive radiation: Insights from microbial experimental evolution. Annals New York Acad. Sci., 1168 (1), 3-22 DOI: 10.1111/j.1749-6632.2009.04574.x

Losos, J. (1990). Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: An evolutionary analysis. Ecological Monographs, 60 (3), 369-88 DOI: 10.2307/1943062

Schluter, D. 2000. The Ecology of Adaptive Radiation. Oxford University Press. Google Books.

Simpson, G.G. 1949. Tempo and Mode in Evolution. Columbia University Press. Google Books

Svanbäck, R., & Bolnick, D. (2007). Intraspecific competition drives increased resource use diversity within a natural population. Proc. Royal Soc. B, 274 (1611), 839-44 DOI: 10.1098/rspb.2006.0198

Wheat, C., Vogel, H., Wittstock, U., Braby, M., Underwood, D., & Mitchell-Olds, T. (2007). The genetic basis of a plant insect coevolutionary key innovation. Proc. Nat. Acad. Sci. USA, 104 (51), 20427-31 DOI: 10.1073/pnas.0706229104

Yoder, J.B., Des Roches, S., Eastman, J.M., Gentry, L., Godsoe, W.K.W., Hagey, T., Jochimsen, D., Oswald, B.P., Robertson, J., Sarver, B.A.J., Schenk, J.J., Spear, S.F., & Harmon, L.J. (2010). Ecological opportunity and the origin of adaptive radiations. Journal of Evolutionary Biology DOI: 10.1111/j.1420-9101.2010.02029.x

#evol2010 day 2: In which sexes diverge and reptiles are disparate

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ResearchBlogging.orgIn day two, Evolution 2010 is already feeling a mite overwhelming. I started the morning in the SSE symposium on speciation and the origin of dimorphism, then spent the rest of the day bouncing from talk to talk and preparing for my own presentation, which is tomorrow at 9:30. I’m going to bed early tonight, I think.

There’s a new daily wrap-up podcast over at Evolution, Development, and Genomics, and, if you haven’t been following the conference on Twitter, check hashtag #evol2010 or this list of twittering attendees I’ve compiled.

What’s going on with snakes, anyway? Photo by Tambako the Jaguar.

Primary literature referenced

Bolnick, D. I. & Doebeli, M. (2003). Sexual dimorphism and adaptive speciation: Two sides of the same ecological coin. Evolution 57(11):2433-49 DOI: 10.1111/j.0014-3820.2003.tb01489.x.

Butler, M., & King, A. (2004). Phylogenetic comparative analysis: a modeling approach for adaptive evolution. The American Naturalist, 164 (6), 683-95 DOI: 10.1086/426002

#evol2010 day 1: In which chromosomes invert and sources sink

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ResearchBlogging.orgThe first day at Evolution 2010 has been a great one. The location in Portland is proving to be great in stereotypical ways: great beer from Rogue Ales, conference t-shirts by American Apparel. There’s pretty good chatter on Twitter this year under the hashtag #evol2010, and in a first for Evolution meeting coverage, there will be daily wrap-up audiocasts (in which I’ll be participating) at the blog Evolution, Development, and Genomics.

Amusingly, we’re sharing the Oregon Convention Center with a “Christian” homeschooling conference, but so far this has led to neither disruptions nor learning experiences.

Some highlights of the talks I’ve attended so far:

  • Jeffrey Feder proposed a new means by which chromosomal inversions might evolve, via a period of allopatric population isolation that allows a locally adaptive inversion to spread, followed by secondary contact during which gene flow creates selective pressure to reduce recombination that could break up the inversion.
  • Simone Des Roches presented new evidence that three lizard species, which have colonized a region of white sand in the New Mexican desert and subsequently evolved “blanched” coloration [PDF], are experiencing ecological release and density compensation. (Simone and her labmate Kayla Hardwick recently discussed their work in blog format.)
  • Chelsea Berns demonstrated that, alone among North American temperate hummingbirds, Ruby-throated hummingbird males have differently-shaped bills from Ruby-throated females.
  • Joel Sachs described the natural frequency and origins of rhizobial bacteria that “cheat” on their host plants.
  • Sheina Sim described host shifts in the apple maggot fly, Rhagoletis pomonella: the fly originally shifted from its native host, hawthorn, to domestic apples [PDF] when they were introduced to North America—now the fly has been introduced to the Pacific Northwest via transport of apples, and some populations have shifted back to hawthorns.
  • The American Society of Naturalists Vice Presidential symposium presented a large volume of work towards discovering the reasons for species’ range boundaries, including great syntheses of population genetic and experimental data for the wildflowers Mimulus cardinalis and Clarkia xantiana—one emerging theme is the importance of the balance of gene flow from healthy populations in the center of ranges to poorly-adapted populations at the edges.

Update, 1950h: The first Evolution 2010 audiocast is now live for download here.

Primary literature referenced

Feder, J., Chilcote, C., & Bush, G. (1988). Genetic differentiation between sympatric host races of the apple maggot fly Rhagoletis pomonella. Nature, 336 (6194), 61-64 DOI: 10.1038/336061a0

Rosenblum, E. (2006). Convergent evolution and divergent selection: lizards at the White Sands ecotone. The American Naturalist, 167 (1), 1-15 DOI: 10.1086/498397

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

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

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

Why make your own food when it doesn’t pay?

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ResearchBlogging.orgWe humans like to think we’re pretty complex – what with having invented the wheel, wars, New York, and so on – so we tend to forget that evolution doesn’t care about complexity. All that matters to natural selection is who makes the most babies, and sometimes complex adaptations can get in the way of that criterion. A study recently published on the always open-access PLoS ONE provides a good example of this principle in action – given the right selective pressures, photosynthetic organisms will give up on the whole photosynthesis thing.



Tiny Indianpipe (Monotropa) and giant Rafflesia, two plants that gave up photosynthesis. Photos by Bemep and Tamara van Molken.

Photosynthesis is clearly a complex adaptation, requiring specialized cellular structures and biochemical processes that can use light to power the synthesis of sugars. Complex enough for a whole additional organism, in fact, since the chloroplast, the cellular structure in which most eukaryotes conduct photosynthesis, probably originated as a symbiont that never left its host cell [$a]. (In some organisms, this process of becoming photosynthetic is still underway.) There are clear advantages to the ability to make your own food conferred by photosynthesis. Yet there are numerous examples of non-photosynthetic organisms with photosynthetic ancestors. For instance, plants as varied as the big, exotic Rafflesia or Monotropa, whose small white flowers are easy to spot in North American woods, have inactive chloroplasts and parasitize other plants. These cases are good reason to think that there may be selective conditions in which the cost of maintaining the mechanisms of photosynthesis outweighs the benefit of independent food production.

The new paper describes just such a set of selective conditions. The authors build a mathematical model of competition between microorganisms, such as flagellates, that can either be mixotrophs, able to conduct photosynthesis or capture prey to feed themselves, or heterotrophs, only able to sustain themselves by eating other critters. The model’s result hinges on two key facts of life for single-celled predators: (1) it turns out that the size of a flagellate cell determines what size of prey it is best able to capture [$a]; and (2) chloroplasts take up space in a cell, limiting the evolution of cell size.

The relative advantage of retaining photosynthesis, then, is directly related to the size range of available prey. Mixotrophs, whose cells are big enough to accommodate chloroplasts, are most efficient predators of larger prey; with no chloroplasts, heterotrophs can be small enough to take advantage of smaller prey. The question of which form wins out, then, relies on the distribution of available prey sizes and the light environment. If there’s lots of light for photosynthesis, mixotrophs can out-compete heterotrophs even if they don’t hunt very efficiently; but if there’s not much light and mostly small prey, the more efficient heterotrophs win.

The fact is, it’s rare for any given adaptation to be useful under all possible conditions. Biological structures or metabolic processes that become disused are no longer under selection for efficient performance of their original function – they are free to accumulate mutations that may make them degenerate into uselessness, or to be co-opted for entirely new functions. But if an adaptation is actually costly to maintain, then natural selection may eradicate it altogether.

References

de Castro, F., Gaedke, U., & Boenigk, J. (2009). Reverse evolution: Driving forces behind the loss of acquired photosynthetic traits. PLoS ONE, 4 (12) DOI: 10.1371/journal.pone.0008465

Hansen, B., P. K. Bjornsen, & P. J. Hansen (1994). The size ratio between planktonic predators and their prey.
Limnology and Oceanography, 39, 395-403

McFadden, G. (2001). Chloroplast origin and integration Plant Physiology, 125 (1), 50-3 DOI: 10.1104/pp.125.1.50

Why aren’t there more sickle-cell anemics in the Mediterranean?

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This post was chosen as an Editor's Selection for ResearchBlogging.orgThe story of sickle-cell anemia and its malaria-protective effects is a textbook case how environmental context determines the fitness of a given genetic profile. However, the evolution of human blood disorders in response to selection from malaria parasites might be more complicated than that textbook story.



Malaria-causing parasites (dark-stained) among human red blood cells (top), and “sickled” red blood cells (bottom). Photos via WikiMedia Commons.

Malaria is caused by mosquito-spread parasites that attack their hosts’ oxygen-bearing red blood cells. A particular mutation in the gene that codes for part of the hemoglobin molecule – the molecule that actually stores oxygen inside red blood cells – leads to deformed, sickle-shaped, blood cells. People who carry two copies of the sickle cell gene develop sickle-cell disease, in which the sickle-shaped cells reduce oxygen transport efficiency and interfere with blood circulation. People with only one copy of the sickle-cell gene are healthy, and better able to resist malaria infection than those with no copies. The textbook story is that, in regions where malaria is common, such as sub-Saharan Africa, the advantage of malaria resistance is enough to offset the fitness risk of carrying the sickle-cell gene – that one-fourth of children born to parents who each have one copy of the gene will themselves have two copies and develop sickle-cell disease.

However, there are regions like the Mediterranean where malaria has historically been prevalent, but in which the human population hasn’t evolved the higher frequency of sickle-cell genes that you’d expect from the scenario outlined above. A new paper in PNAS demonstrates that this may be because of interactions between the sickle-cell gene and another genetic blood disorder, thalassemia [$a].

Thalassemia is a class of genetic disorders affecting the protein subunits that comprise hemoglobin. Each hemoglobin molecule is formed by binding together two “alpha”-type subunits, and two “beta”-type subunits. If there is a shortage of correctly-formed subunits of either type, then hemoglobin formation is impaired, resulting in anemia or (if the mutation stops subunit production altogether) death. However, like sickle-cell genes, thalassemic mutations can confer resistance to malaria; and if alpha-thalassemia is paired with beta-thalassemia, the reduced production of both subunits can balance out.

As it happens, in combination with alpha-thalassemia, the sickle-cell gene’s malaria protection is neutralized. Using population genetic models, the new study’s authors show that this effect may have actively prevented the sickle-cell gene from establishing in the Mediterranean, where alpha- and beta-thalassemias are more common than in Africa. In the Mediterranean, the presence of beta-thalassemia genes reduces the fitness cost of (mild) alpha-thalassemia genes; and in the presence of alpha-thalassemia genes, the sickle-cell gene confers no protection to people with one copy but still induces sickle-cell disease in people with two copies.

These interactions between genes are called epistasis, and they can have dramatic impacts on evolution. Although I haven’t seen many cases as well-characterized as this one, epistasis is probably widespread in the complex systems of genomes, where thousands of regulatory and protein-coding genes interact to build living things.

References

Penman, B., Pybus, O., Weatherall, D., & Gupta, S. (2009). Epistatic interactions between genetic disorders of hemoglobin can explain why the sickle-cell gene is uncommon in the Mediterranean Proc. Nat. Acad. Sci. USA, 106 (50), 21242-6 DOI: 10.1073/pnas.0910840106