natural selection

The keywords to the article include, "carnivorous marsupial" and "precocious breeding." What better teaser could you possibly hope for?

Tasmanian devils are dying because of a transmissible cell line infection, or "cancer," decimating their population. In fact, in some places it's killing 9 out of 10, which is way beyond decimation.

The new paper by Menna Jones and colleagues claims that the population is evolving toward a radical life history solution to the problem: Tasmanian devils are starting to mate and have large litters after a single year, before they have a chance to succumb to the disease:

This change in life history is associated with almost complete mortality of individuals from this infectious cancer past their first year of adult life. Devils have shown their capacity to respond to this disease-induced increased adult mortality with a 16-fold increase in the proportion of individuals exhibiting precocious sexual maturity. These patterns are documented in five populations where there are data from before and after disease arrival and subsequent population impacts. To our knowledge, this is the first known case of infectious disease leading to increased early reproduction in a mammal.

It's a simple response: young breeders used to have lower fitness, because of competition from older adults. Now, the high mortality after the first year has made it a losing strategy to wait to reproduce. When the early breeders are the only ones having many offspring, the population will evolve quickly to early breeding.

References:

Jones ME, Cockburn A, Hamede R, Hawkins C, Hesterman H, Lachish S, Mann D, McCallum H, Pemberton D. 2008. Life-history change in disease-ravaged Tasmanian devil populations. Proc Nat Acad Sci USA (in press) doi:10.1073/pnas.0711236105

This is the first in a series of essays titled, "Practical Evolution." Here are links to the whole series and the series introduction. I've decided to break the articles up into two parts, so that a full essay will appear in two successive weeks. So if you enjoy the current installment, by all means come back on Friday, when I will follow the threads of dispersal by way of an obnoxious animal pest right back to hominids.

Probably the most well-known weed species in America is the one growing so prolifically in my yard: the dandelion. Any kid can tell you why dandelions spread so quickly: Their seeds are carried by the wind.

But for all their blowing of the puff-heads, as Goodwin calls them, my kids haven't noticed what seems so obvious to me. Dandelions are almost indestructible. Pull them up and their leaves will dry, but the flowers on the dead-looking plants continue to develop seeds and puff out. Leave just a little of the taproot in the ground, and new leaves will sprout hydra-like from all directions. Gretchen drenched a goodly portion of our sidewalk dandelions last year with boiling water, wilting the leaves like spinach. Some of them really died. The rest sprouted right back.

Even when we're talking about dainty little parasol-like seeds, much depends on the size of the whole package. The part that looks like a "seed," a botanist calls an achene, which is technically a kind of fruit. The sunflower seeds that teenagers spit at softball games are fruits, too, but don't try telling that to their mothers. The dandelion's parachute, or pappus, is connected to the achene by one long shaft. A large, massive achene will tend to fall faster and won't blow very far except in a very strong wind. Sunflowers and coneflowers go for the big achene strategy, which the winter-resident birds really appreciate come January. Dandelions go the opposite way: small achene, big pappus. That's why weedy coneflowers are only a problem within five feet of my perennial beds, while weedy dandelions are in every disturbed field in the country.

Barkley Sound, Broken Islands group

A remarkable botanical field study has been carried out over the last twenty-seven years by Martin Cody, in Barkley Sound, British Columbia. In 1981, Cody began keeping track of the plants on a few of the small islands that dot the Sound. After a few years, the study had changed into something grander than a simple plant census: Cody's 2006 book on the subject begins, "This is a book about a field study that just grew and grew." For more than twenty years, Cody and his students have counted plants on hundreds of tiny islands, most under a few hundred square meters in size. Many of these islands are so small that a species may disappear from them entirely, only to be re-established later by new colonists. With his careful censuses, Cody could determine when populations were newly founded, and when they became locally extinct.

By 1996, Cody had amassed information about weedy plants that had colonized dozens of the tiny islands of Barkley Sound. These plants all originally had come from Europe, including dandelions, their close relative cat's-ear (Hypochaeris radicata), wall lettuce (Mycelis (Lactuca) muralis), and woodland groundsel (Senecio sylvaticus). That means that all the plants are recent colonists, and they have all been carried to the islands by the wind, each using similar seed packages that include an achene and pappus.

What makes a successful colonist? The first seeds to reach one of these tiny islands have done an exceptional thing: Wind has carried them across a large body of water to reach a tiny speck of virgin soil. Only the tiniest achenes tend to make this unlikely journey, and only if their parachutes are big enough to carry them.

Cody and his student, Jacob Overton, took some of these seeds from both island and mainland populations and embarked on a series of experiments. First, they set a stopwatch and dropped the seeds to see how fast they fell. The results of this seed drop were pretty much the same as when kids tie little parachutes onto green army men. Generally, the bigger the parachute, the slower the descent. But if the achene is small enough, even a very small pappus may be enough to keep it aloft. The key is the ratio: the volume of the pappus compared to that of the achene.

Seed head of wall lettuce (Mycelis muralis) with five achenes remaining

There's nothing very surprising about this: The wind carries small seeds farther, particularly if they have big parachutes. Plants that bear this kind of seed have only a tiny chance of colonizing an island. But plants with big achenes and little parachutes may have no chance of colonizing new islands at all. So by sorting seeds, the wind and sea also sort the genes of the colonizing plants.

Indeed, Cody and Overton found that new populations of these plants on islands produce the kind of seeds that occasionally skip across to new islands. For example, the youngest island populations of wall lettuce — less than four years old — have the tiniest achenes. Their parachutes are small, too, but they generate a lot of loft. If the seeds of mainland wall lettuce are like a green army man tied to a kleenex, the first island colonists are like a BB stuck to a postage stamp.

Wall lettuce populations that manage to stick around on an island make a change. After ten years, they are producing achenes just as big as the mainland populations. But instead of big, fluffy parachutes, they grow smaller, stunted ones. Like green army men tied to smaller and smaller postage stamps, these seeds aren't made for dispersal. They drop fast, right next door to their parents.

More dispersal is not always better, even if you're a weed. A windy day might carry your seeds far away, but what if you live on a tiny island? Your seeds will be carried right off into the ocean. Worse, even if you live on a large island in Barkley Sound, there may be only a small strip of good habitat. Too far toward the water and you're drowned by storm surges; too far inland and you have to compete with larger, more established plants. For these island weeds, the plants that disperse the least have more new seedlings.

Cat's-ear

Adaptable as they are, dandelions have done a poor job colonizing these tiny islands. The best of these weed species have managed to invade one island in five. Dandelions are found on less than a fourth that many. Despite their fame for being windblown, dandelion seeds actually drop faster than the wispy seeds of the other species on these islands. The rare colonists that do reach an island tend to last less than two years.

Their relative, cat's-ear, has done better. Since it carries its flowers higher, on branched stems, cat's-ear makes more headway into grassy areas away from the beach, giving it a bit more area to work with. As a result, its populations become extinct only a third as much turnover as dandelions. LIke the wall lettuce, the island cat's-ear populations are different from the mainland, sporting big achenes and small parachutes. Dropping their seeds nearby seems to make a big difference as to whether their populations will persist.

Natural selection seems to have changed the island populations of both these weeds, favoring lower dispersal. But how do we know it is really selection on dispersal, and not just something about the islands affecting seed size?

Woodland groundsel, another of the weedy asters on the islands, provides one natural experiment. Cody and Overton dropped dozens of groundsel seeds from twenty populations, and found that the sizes of achenes and pappus made no difference at all to the speed that the seeds drop to the ground. Small groundsel achenes drop just as fast as large ones, no less than if Galileo had dropped them from the Leaning Tower. Even if selection had favored faster drop times, woodland groundsel achenes and pappus volumes should not have changed. And in fact, Cody and Overton found that they didn't change: island populations of woodland groundsel have proportions almost exactly the same as the mainland.

Another experiment has been carried out in the most unlikely location. Hawksbeards (genus Crepis), also relatives of the dandelion, are common weeds spread across the Old World and into North America. Like dandelions, the hawksbeard Crepis sancta can colonize urban habitat, including the tiny patches of bare ground that cities leave in sidewalks for trees to grow. These are the urban equivalent of the tiny islands in Barkley Sound: sometimes far apart, they are separated by stretches of inhospitable concrete. In Montpelier, France, during the last few years Pierre-Olivier Cheptou and his colleagues have performed the urban version of Martin Cody's work: counting plants and collecting seeds from the small hawksbeard colonies around the city. What it lacks in rugged charm, Montpelier makes up in record-keeping — knowing when the sidewalks were built, the researchers could work out the ages of different hawksbeard populations.

Unlike dandelions, C. sancta produces two different kinds of seeds: one with the achene and pappus carried on the wind, and another with no pappus at all. These seeds without parachutes do not go far; they scatter near the mother plant. That makes them bad for colonizing new patches of ground, but really good for establishing a sustained presence in one patch.

Compared to the rural C. sancta population, urban plants have more of the no-parachute seeds. These plants cast fewer seeds to the wind, and drop more on the ground to sprout nearby. Like the islands of Barkley Sound, these urban islands select for low dispersal.

Cheptou and his coworkers were able to go farther than Cody and Overton: They planted the seeds from urban patches in a greenhouse alongside seeds from the rural areas outside of town. The urban/rural differences were still present in the greenhouse plants, showing that growing in a small patch is not enough to change the seeds. Instead, the differences are caused by differences in genes, the result of selection on the urban plants.

What is more, they grew their own small patches of C. sancta, replicating the conditions of the urban plants. The seed heads of the real urban populations were the equal of those after 12 to 13 generations of selection on their fake urban patches. This rapid pace of selection on the urban plants matches that on the islands of Barkley Sound, where wall lettuce and cat's-ear repeatedly showed strongest changes after only a few generations.

The cycle of founding new island populations and their subsequent extinction.

Colonization is a filter: Only certain individuals may have the right combination of traits to cross a significant barrier and inhabit a new place. But the traits that enable individuals to make such crossings are not always very good for staying in the new place.

For certain species, selection yields a complicated pattern. A plant that is a local failure may be a global success, as it casts its seeds to far-off places, a few of which may grow into significant new populations. Such high-dispersing plants may do very poorly as a new population grows, but may be the only ones with a chance to escape when local extinction looms. High-dispersing individuals are also the ones most likely to carry their genes from one population to another, providing the potential for adaptations across the species as a whole.

Without dispersal, a species may become moribund, unable to change in the face of new challenges. At the extreme, this has been called "evolutionary suicide." Traits that are selected locally, because they enhance the reproduction of individuals in the species, may nevertheless doom the species as a whole by reducing adaptability to changing conditions. The cost of maintaining the ability to change is a constant unstable balance between dispersal and staying power.

For the weeds of Barkley Sound, this unstable balance ultimately favors the colonizers. New island populations do not last long. The local selection in favor of lower dispersal helps them to persist for a time, but on the scale of centuries all of them will fail, only to be replaced by new colonists from elsewhere.

Friday: We turn from plant parachutes to animal dispersal mechanisms. And by "mechanisms" I mean, "legs."

Notes:

I am indebted to George Cox, whose excellent Alien Species and Evolution: The Evolutionary Ecology of Exotic Plants, Animals, Microbes, and Interacting Native Species (2004) gives a good account of Cody and Overton's study of island weeds. I can't say enough good things about this book.

Martin Cody's book, Plants on Islands: Diversity And Dynamics on a Continental Archipelago, gives an account of the history of his field project, as well as reviews of the many areas of ecology that it has helped to illuminate.

Many readers may notice that there is another factor besides low dispersal potential by which selection might favor large achenes in these plant species. Larger seeds may be advantageous because, with more stored energy, they may tend to germinate more readily or grow more quickly, thus making them more competitive. In this circumstance, selection would pertain to energy allocation or reproductive effort, rather than dispersal. I'll be discussing that form of selection in a later essay. In the present cases, dispersal is indicated as the target of selection, but seed size and energy allocation may also be involved.

If seed morphology makes so little difference to drop time in Senecio sylvaticus, you may wonder what maintains achene size and pappus volume in this species. At least, that's what I wondered. Without more information it is hard to say, but I would hypothesize that achene and pappus volume may be genetically correlated in a way that is hard to select for one and not the other. In the other species, the selection on achene size and pappus volume is apparently antagonistic -- larger achenes are favored at the same time as smaller pappus. If these two traits are strongly genetically correlated, it becomes harder to select for lower dispersal. It would also be worth investigating whether other traits besides these volumes may have evolved in the island populations.

The rapid evolution of urban hawksbeard (Crepis sancta) was examined by Cheptou et al. (2008). Pierre-Olivier Cheptou has a webpage at CEFE, including a description of Crepis sancta as a model system.

Photo credits:

Dandelion seeds: Photo by Piccolo Namek, on Wikimedia. GPL license.

Barkley Sound: Photo by Sam Wilson (BaylorBear78) on Flickr. Creative commons noncommercial share-alike license.

Cat's-ear: Photo by Ian Boyd, on Flickr. Creative Commons noncommercial attribution license.

Wall lettuce: Photo by Mollivan John, on Flickr. Creative Commons noncommercial attribution license.

Colonization figure: Figure 1 from Cody and Overton, 1996.

References:

Cheptou, P-O, Carrue O, Souifed S, Cantarel A. 2008. Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proc Nat Acad Sci USA 105:3796-3799. doi:10.1073/pnas.0708446105

Cody ML. 2006. Plants on Islands: Diversity and Dynamics on a Continental Archipelago. University of California Press, Berkeley, CA.

Cody ML, Overton JM, 1996. Short-term evolution of reduced dispersal in island plant populations. J Ecol 84:53-61.

Cox G. 2004. Alien Species and Evolution. Island Press, Washington.

That's the thrust of a technical comment by Graham Coop and colleagues, now online in Molecular Biology and Evolution. The letter refers to the extraction of FOXP2 from two Neandertal specimens from El Sidrón, by Johannes Krause and colleagues, reported last year (I wrote about the paper here).

First, the bad news. The current letter raises the prospect of contamination. Notably, the controls applied by Krause et al. (2007) may be relatively weak evidence against contamination, because of polymorphism within large human comparative samples. The tests rely on the assumption that there is little DNA from living humans in the samples. But if we cannot distinguish Neandertal from human DNA with great accuracy, then we will be mistaken some proportion of the time. Krause et al.'s test, based on derived human alleles absent from the Neandertal genome draft, can still go wrong if the human contaminants happen to have all the ancestral (non-derived) human alleles.

Well, that seems to be the story these days with Neandertal DNA extraction. No test of contamination is good enough. (And remember, that every "test" of contamination is really a procedure for excluding the hypothesis that ancient sequences are identical to recent ones.)

Now, the more interesting news. Coop and colleagues verify that the selective sweep affecting human FOXP2 was indeed recent -- they estimate 42,000 years ago:

To demonstrate this, we estimated the time of the most recent common ancestor (tMRCA) of the selected haplotype (see Figure 1), using an approach sometimes called phylogenetic dating (Thomson et al. 2000; Hudson 2007). This method does not make assumptions about demography and selection, but only requires that the mutations in the intron be neutral or nearly neutral. Taking this approach, we obtained a mean tMRCA of 42 Kya (see SOM for details). While there is considerable uncertainty associated with this estimate, it is surprisingly recent if selection took place over 300 Kya (see SOM). In other words, the selective scenario proposed by the authors cannot account readily for patterns of variation in modern humans. Given that we have no power to detect a beneficial substitution that occurred over 250 Kya, (cf. Sabeti et al. 2006) yet we see a footprint of positive selection at FOXP2, the conclusion of a recent selective sweep at FOXP2 is not surprising (Coop et al. 2008:3-4).

FOXP2 is in one of the ENCODE regions, so its variation is pretty well known. This is not a problematic case: it has a very limited amount of variation around it, and has a strong excess of rare alleles, both signs of a recent sweep.

Coop and colleagues suggest that the beneficial human allele spread into Neandertals (or vice versa) by low levels of gene flow coupled with its selective advantage -- in other words, introgression.

They do allow for an alternative -- perhaps the two amino-acid-coding mutations were not the target of selection, but instead some linked locus. This would not erase the necessity of gene flow from Neandertals, but would question whether this gene flow had involved the FOXP2-language scenario, since it might be some linked gene unrelated to language.

(CORRECTION (2008/04/18): If selection were on a linked site, then Neandertals might share the human-derived amino acids as a result of ancient shared ancestry with humans, while the linked selected sweep might be absent in Neandertals, not necessitating any gene flow.)

I doubt this hypothesis of a linked sweep, since the two sites with human-derived substitutions are otherwise very strongly conserved among mammals. This looks like a credible target for recent selection. But the hypothesis of selection on a linked site cannot presently be tested.

So that's the story. It seems very likely that Neandertals got the language gene from us, or us from them, long after many other genes in the two populations diverged. I write "many" rather than "most" because we haven't really been able to assess the proportion of derived alleles shared by humans and Neandertals. The completion of the draft sequence may help, but I'm afraid that the specter of contamination is going to keep on being raised whenever a part of the Neandertal draft genome looks humanlike.

(via Dienekes)

References:

Coop G, Bullaughey K, Luca F, Przeworski M. 2008. The timing of selection at the human FOXP2 gene. Mol Biol Evol (in press) doi:10.1093/molbev/msn091

The PNAS Early Edition this week includes a paper by bee genome researchers Amro Zayed and Charles Whitfield. After a short review of honeybee phylogeny, they demonstrate two things:

1. An ancient dispersal of honeybees from Africa into Europe was accompanied by a pulse of positive selection on coding genes, amounting to selection on approximately 10 percent of bee genes.

2. As Africanized bees have spread across South and into North America, adaptive genes from the existing populations of European bees have introgressed into the Africanized population, increasing under positive selection.

These are remarkable parallels to the worldwide evolution of humans. In bees, the geographic pattern is not the same, and the timescale is different, but the overall genetic impact is quite similar.

Here's the bee history:

In its native range, A. mellifera is classified into approximately two dozen subspecies, which are further organized into four major geographically and genetically distinct groups: African, Western and Central Asian (hereafter referred to as Asian), Eastern European, and Western and Northern European (hereafter referred to as West European) (9-11). European honey bees were introduced by humans to the New World by European settlers as early as the 1600s. In Brazil in 1956, an intentional introduction of African honey bees (A. mellifera scutellata), which hybridized with previously introduced European bees, led to the establishment and spread of the highly invasive and economically devastating Africanized honey bees in North America and South America (12). Subsequent studies have shown that Africanized bees are predominantly African in ancestry with minor but consistent contribution from European genotypes (11, 12). Using recently developed SNP panels, Whitfield et al . (11) demonstrated that the honey bee originated in Africa and subsequently expanded into Eurasia in two or more independent ancient expansions. One expansion gave rise to Western European honey bees, and at least one other independent expansion gave rise to Asian and Eastern European honey bees. Honey bee subspecies vary in a host of phenotypic traits, such as morphology, behavior, physiology, and gene expression (9-11, 13, 14) (Zayed and Whitfield 2008:3421).

I was not aware of the initial dispersals of bees into Europe and Asia. The genetic data show that the Western European strains are the ones with the most adaptive evolution since their dispersal from Africa. The separate ancient bee dispersals were documented by Whitfield et al. (2006), but they were not able to provide date estimates for the ancient dispersals, and none are attempted in this study.

This is the kind of test that ought to fail in most wild populations. Without a shift in the adaptive landscape, the fraction of new mutations with potential adaptive value is bound to be small -- because species are optimized to the environments that they have occupied for a long time. But European bees have a number of recent environmental changes, ranging from the simple effect of moving from a tropical to a temperate environment, the need to use new and different flora, and the effects of domestication. In a very numerous, rapidly dispersing species, these effects led to a rapid adaptive response in a large proportion of genes. These are the basic principles underlying the recent acceleration of positive selection in our lineage also.

The introgression of European genes into the dispersing Africanized bees in the Americas is interesting, because it seems counter-intuitive. The main differences between Africanized bees and European bees involve adaptations to climate. European bees put up lots of honey for the winter, and swarm less frequently, in addition to being more sedate. African bees don't bother with as much honey, which together with their more frequent swarming would seem to be a good fit for the tropical pattern of seasonality. These African traits explain why the African bees have spread at the expense of the European bees across the tropical New World. But Africanized bees have picked up a lot of genes from the European bees in the New World.

The authors propose some possible explanations:

The adaptive value of functional (coding) portions of Western European genomes could be related to positive selection on novel variation in West European bees, to positive selection on novel hybrid gene combinations, and/or to selection for heterozygous genotypes. Our study thus provides direct evidence that invasive populations can exploit hybridization in an adaptive fashion -- a finding of immense relevance to understanding the dynamics of biological invasions (Zayed and Whitfield 2008:3424).

In other words, behavioral correlates of climate may be a target of selection and introgression -- I would speculate because of the intrinsic rarity of adaptive mutations in these functions.

This is a relatively course-grained analysis of positive selection, since the study basically averages within SNP categories, determining F_ST between pairs of populations. For non-coding SNPs, the Africanized bees are very similar to African bees (F_ST = 0.05), while for coding SNPs they are twice as divergent (F_ST = 0.10). That's a lot of difference in allele frequencies over a short time; it must have been caused by strong positive selection across a broad sample of loci. They do not attempt the same kind of "10% of genes" estimate for the introgression, but their figures show that it is quite significant across their data.

I don't know but it may be a while before this initial study can be followed up with recombination based selection tests, because of this little known fact: bees have a recombination rate of 19 cM/Mb -- roughly 15 times higher than humans. Still, Whitfield et al. (2006) found an excess of linkage disequilibrium in the West European subspecies of bees. It now seems likely that some of this LD is explained by the widespread selection documented in the current study.

In other words, the genetic structure of global bee populations provides another strong example of the importance of rapid evolution in abundant species, coupled with ecological changes. Bees also now provide a strong example of adaptive introgression -- in this case, within a very tightly timed dispersal with known climatic conditions.

References:

Zayed A, Whitfield CW. 2008. A genome-wide signature of positive selection in ancient and recent invasive expansions of the honey bee Apis mellifera. Proc Nat Acad Sci USA 105:3421-3426. doi:10.1073/pnas.0800107105

Whitfield CW and 9 others. 2006. Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera. Science 314:642-645. doi:10.1126/science.1132772