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Thursday, January 08, 2009

Testing Natural Selection: Part 2

 
There are several interesting articles about evolution in the Januray 2009 issue of Scientific American. One of the most interesting is an article by H. Allen Orr of the University of Rochester (NY, USA). The magazine title is "Testing Natural Selection"1 and, as the title implies, the focus is on evolution by natural selection.

Orr's article gives us an opportunity to compare and contrast the views of an adaptationist (Orr) and a pluralistic approach to evolution.

In Testing Natural Selection: Part 1 we discussed two of Orr's opinions: (1) random genetic drift is not as common as most people think, and (2) most (if not all) visible phenotypic change is driven by natural selection.

Here, we discuss Orr's ideas about speciation.

When we say "speciation" we're talking about the biological species concept. Speciation occurs when two formerly compatible populations evolve to the point at which they can no longer interbreed. The key question is what causes this reproductive isolation and how does it evolve?
To contemporary biologists, then, the question of whether natural selection drives the origin of species reduces to the question of whether natural selection drives the origin of reproductive isolation.

For much of the 20th century, many evolutionists thought the answer was no. Instead they believed that genetic drift was the critical factor in speciation. One of the most intriguing findings from recent research on the origin of species is that the genetic drift hypothesis about the origin of species is probably wrong. Rather natural selection plays a major role in speciation.
Orr is correct to point out that random genetic drift is important in speciation. It's the mechanism described in many evolutionary biology textbooks, though it's not the mechanism that most people think about when they think about speciation.

Many biologists have always believed that natural selection plays a much more important role in speciation than random genetic drift. They aren't happy with the textbook description. Orr is one of these biologists. He now claims that the drift explanation is "probably wrong."

Let's think about what has to happen when two species become reproductively isolated. We'll use allopatric speciation as an example.2

We begin with a situation where two populations (races, subspecies) are geographically separated. There is very little gene flow between them so they evolve independently of each other. Over time, they may come to be different because each is adapting to different environments or they may just drift apart by accident. With respect to the actual speciation event, these differences don't matter.

From time to time, individuals from the two subspecies will interbreed to produce fertile offspring. This is responsible for limited gene flow between the subspecies and it proves that speciation has not occurred. If the barrier between the two populations breaks down they will merge back into a single population.

But if the two species have been separated for a long period of time, mutations that prevent interbreeding will accumulate and hybrids will become less and less viable until eventually no fertile hybrids are produced and speciation is complete. There are many ways that this can happen but a common hypothesis involves the build-up of post-zygotic genetic incompatibilities called Dobzhansky-Muller (D-M) incompatibilities.

How are D-M incompatibilites fixed in the population? If they interfere with the matings of individuals from the two populations then how come they don't contribute to infertility when individuals from the same population mate with each other? When the mutation first arises it seems to have a very strange property. It doesn't affect matings between an individual carrying the D-M allele and an individual not carrying that allele from the same population but it does affect matings between the individual carrying the new D-M allele and and an individual from the other population.

In order for this to happen there must already be some genetic differences between the two populations in terms of mating and reproduction. Those differences have accumulated in each of the populations but they must not have an effect on hybrid crosses. Presumably, the new D-M allele is not harmful in one genetic background but it is in the other.

Are these pre-existing potentiators neutral within a population, in which case they become fixed by random genetic drift? Or, are they beneficial in one of the populations, and not in the other, in which case they are fixed by natural selection? The general consensus has been that they are neutral within a population and they accumulate by accident. When enough of them become fixed the cumulative effect is to prevent hybridization. The last allele to arise, the D-M incompatibility allele, is the straw that breaks the camel's back.

Orr believes that the alleles are beneficial in one of the populations. Thus, according to him, reproductive isolation is driven by natural selection. He gives two examples.

The first one is the incomplete speciation in monkeyflower subspecies. I described this in an earlier posting [Speciation in Monkeyflowers], where I pointed out that the role of natural selection was not clear. The differences in flower color and pollinators could have arisen by selection if one postulates changes in the bee population but they could also be due to chance.

For an adaptationist like Allen Orr there's no doubt about what happened.
A good example is the evolutionary history of the two monkeyflower species mentioned earlier. Because their pollinators seldom visit the “wrong” species of monkeyflower, the two species are almost completely isolated reproductively. Even though both species sometimes occur in the same locations in North America, a bumblebee that visits M. lewisii almost never visits M. cardinalis, and a hummingbird that visits M. cardinalis almost never visits M. lewisii. Thus, pollen is rarely transferred between the two species. In fact, Schemske and his colleagues showed that pollinator differences alone account for 98 percent of the total blockage in gene flow between the two species. In this case, then, there can be no doubt that natural selection shaped the plants’ adaptations to distinct pollinators and gave rise to strong reproductive isolation.
This is not a good example of speciation by natural selection. We simply don't know if the flower color mutation spread in one of the populations because it conferred a selective advantage on individuals within that population.

Besides, these two "species" will still form viable hybrids so they're not really species in the first place.

The other example of presumed speciation by natural selection comes from studies on Drosophila There are several example of D-M incompatibility alleles that have been identified. In some of them, there is evidence at the sequence level for rapid fixation. If correct, this is a good indication that the alleles have become fixed by natural selection. The resulting reproductive isolation is an epiphenomenon.3

One example is OdsH in Drosophila mauritiana. It appears to result in an increase in sperm production so it may have been selected in the early population of this species, before it became a species. Presumably, the allele was beneficial in the genetic background that had evolved up to that point and presumably it was detrimental in the genetic background of whatever subspecies it was related to.

The genetic background is obviously part of the speciation event. I suppose that if even one of the D-M alleles is selected then it's fair to say that speciation by natural selection took place.

The question is whether this is common or not. Shucker et al. (2005) looked at post-zygotic reproduction isolation in two populations of grasshopper and provided evidence that all the D-M incompatibilities could be adequately explained by random genetic drift. We'll need to have many more examples in order to decide whether natural selection explains most speciation events.

Personally, I find it easier to understand how reproductive isolation could arise by accidental accumulation of many neutral alleles that eventually lead to reproductive isolation. It's harder to envisage alleles that confer a selective advantage within one population but are extremely detrimental in the other.

Orr doesn't agree.
The studies of the monkeyflower and of hybrid sterility in fruit flies only begin to scratch the surface of a large and growing literature that reveals the hand of natural selection in speciation. Indeed, most biologists now agree that natural selection is the key evolutionary force that drives not only evolutionary change within species but also the origin of new species. Although some laypeople continue to question the cogency or adequacy of natural selection, its status among evolutionary biologists in the past few decades has, perhaps ironically, only grown more secure.
I'm not an expert on speciation and I don't hang out with people who work in the field. However, my general impression from reading the scientific literature is that Orr's statements may be somewhat exaggerated. From what I can see, there are a great many evolutionary biologists who question the hegemony of natural selection. Their numbers seem to be growing, not shrinking.

I don't know where Orr is coming from when he implies that laypeople question the adequacy of natural selection. In my experience laypeople only think about natural selection. They have no idea that there are any other mechanisms of evolution.


1. The website title is "Testing Natural Selection with Genetics."

2. In allopatric speciation the two diverging populations are geographically separated. That's what makes them distinct populations. In sympatric speciation the two populations may exist in the same geographical and restricted gene flow between them is due to other factors. It's easier to visualize what's happening during allopatric speciation but the logic can apply to sympatric speciation as well.

3. I don't think Orr is actually proposing that there would be selection for reproductive isolation. How would that work?

Shuker, D.M., Underwood, K., King, T.M., and Butlin, R.K. (2005) Patterns of male sterility in a grasshopper hybrid zone imply accumulation of hybrid incompatibilities without selection. Proc. Roy. Soc. B 272:2491-2497. [DOI: 10.1098/rspb.2005.3242]

27 comments :

  1. sympatric - in the same place
    allopatric - divided by a geographic barrier

    Otherwise I agree with you 100% and that is how I teach about speciation (I explain how it works in both types of speciation so they get the lesson approximately twice).

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  2. Yeah I noticed the mixing up of 'allopatric' and 'sympatric'
    ;)

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  3. Some of the most compelling evidence for the importance of natural selection in speciation that Coyne and Orr present in their book come from laboratory studies. Briefly, when lab stocks of Drosophila are kept in the same environment, isolated lines do not become as reproductively isolated as those that kept in different environments (i.e., different selection pressures). This shows natural selection can accelerate the speciation process, even in allopatry.

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  4. Larry: "I don't think Orr is actually proposing that there would be selection for reproductive isolation. How would that work?"

    Ask a female donkey if she'd rather mate with a male donkey or a male horse.

    One way it works is that once two populations have been isolated for some time (but before the gene-flow door is slammed shut), enough differences have accumulated that hybrid matings are less advantagous (fewer and less fit offspring). At that point, any allele that would minimize or prevent hybrid crosses would be advantagous to both subspecies.

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  5. me: "... would be advantagous to both subspecies."

    er, make that "would be advantagous to those individuals (in either species) that had that allele".

    BTW, in Dawkins "Ancestors Tale" he describes an interesting phenomenon in the overlap of two subspecies of a North American frog (who were at one time isolated). IIRC, the mating-call pitch of individuals over most of the continent is almost exactly the same, except as you approach the overlap zone, where the pitch for one subspecies increases and the other decreases.

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  6. Wow... in this case, the answer to the Natural Selection/Random Genetic Drift question may be one of shades of gray - or being specific about what being selected. From the Drosophila work out of our lab and others, we know that there seems to be an association between gene misexpression in interspecific hybrids (i.e., improper expression relative to parental expression levels) and sterility in males (see Ortiz-Barrientos et al. 2007 for review). Furthermore, 'male-biased genes' (MBGs) (e.g., expressed more highly in males vs. females), are significantly over-represented among these misexpressed genes. Many MBGs are known to be expressed specifically in the testis or otherwise to be involved in reproductive function (see Haerty and Singh 2006). We know that these genes evolve rapidly, presumably due to sexual selection; furthermore, the more rapid the divergence of a gene between D. melanogaster and D. simulans the more misexpressed it tends to be in hybrids (Artieri et al. 2007).

    So, this may suggest that genes that are under frequent positive selection and are thus more likely to diverge between species (especially in the case of sexual selection) are more likely to be involved in DM incompatibilities. Johnson and Porter (2001) have looked at how directional selection in two incipient species can accelerate the process of post-zygotic reproductive isolation.

    I guess the point is that while these aren't examples of natural selection 'for' speciation genes, they may suggest that genes under various directional selection pressures would be more likely to be involved in DM incompatibilities and thus speciation.

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  7. Carlo already hinted that sexual selection can be important in speciation, and I believe this idea is gaining some popularity. There is an emerging awareness that sexual conflict can be extremely intense, sometimes brutal, and the genes involved tend to be among the fastest evolving in the genome. These processes may rapidly make two subpopulations genetically incompatible.

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  8. coturnix says,

    sympatric - in the same place
    allopatric - divided by a geographic barrier


    You are correct, of course.

    I fixed the posting. Sorry for any confusion. I got myself all in a twist because earlier drafts of this posting tried to explain sympatric speciation at the molecular level—that's very messy.

    I proofed this posting many times and there was something about it that bothered me. That's why it took so long. Finally I decided that it was just my imagination and I hit the "post" button.

    I need an editor. Want a job?

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  9. Divalent says,

    One way it works is that once two populations have been isolated for some time (but before the gene-flow door is slammed shut), enough differences have accumulated that hybrid matings are less advantagous (fewer and less fit offspring).

    OK, I'll accept that scenario.

    At that point, any allele that would minimize or prevent hybrid crosses would be advantagous to both subspecies.

    Why? Consider two subspecies of plants that are spreading their pollen in the wind. If the pollen grains land on a flower from the same population then the alleles will be passed on. If they land on a flower from the other population the alleles will still be passed on but with lower probability.

    Why would it be advantageous to eliminate the second possibility? Please explain the selective advantage in reducing the chances that your pollen grains will successfully fuse with an egg.

    If you don't like using a plant example then feel free to choose a protozoan like paramecium, of a fungus like yeast, or an animal like a mollusk.

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  10. Corneel says,

    Carlo already hinted that sexual selection can be important in speciation, and I believe this idea is gaining some popularity.

    I've noticed that adaptationists tend to be animal-centric as well mechanism-centric. This is a prime example.

    Please describe how sexual selection works in monkeyflowers, paramecium, bacteria, yeast, and mollusks.

    We're discussing general properties of speciation in biology so it's best to think about mechanisms that apply in all cases and not just in a small subset of living things.

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  11. Please describe how sexual selection works in monkeyflowers, paramecium, bacteria, yeast, and mollusks.

    When I posted my comment, I used sexual selection as an example of how directional selection could increase the rate at which DM incompatibilities accrue (this also applies to pre-zygotic isolation mechanisms such as differences in female-choice).

    While I think that the DM hypothesis requires only time and limited gene flow coupled to random drift, I simply wanted to point out the idea that selection can accelerate the process. Sexual selection is an obvious candidate in animals, but similar processes may play a role in non-animals (such as ecological specialization - anything that will accelerate divergence between species).

    Another thing to keep in mind is that while initial DM incompatibilities likely arise due to random genetic drift, they may then be selected upon because of reinforcement, or selection against the production of unfit hybrids. Thus evidence of selection at a 'speciation locus' may not actually underlie the initial speciation event, but rather subsequent reinforcement.

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  12. "Please describe how sexual selection works in monkeyflowers, paramecium, bacteria, yeast, and mollusks."

    Sexual conflict arises in sexually reproducing organisms, regardless of whether there is hermaphroditism. It will occur in plants, molluscs and (some) yeasts.

    Of course, for asexually reproducing animals, this mechanism falls flat. But then again, the biological species concept does not apply, and speciation becomes a more hairy concept altogether.

    Great post BTW, I liked reading it.

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  13. Oops. make that asexually reproducing organisms.

    I guess you're right that I am animal-centric, haha.

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  14. maybe drosophila-centric is teh case. For instance, many well-defined species of birds are separated mainly by pre-zygotic mechanisms, as mayr poitned out. Second, it is well documnented how flies that are raised ina given host (say, tomate vs cucumber) prefer to mayte with other flies also grown up in that fruit, and there is pretty good historical documentation of how this non-genetic learning can lead to moprhologically distinct, non-interbreeding populations. Which is always the first requisite: notice that no matter how much selection may be involved at any time, if you do not somehow reproductively separate the populations for at least a while to evolve on their own, there is nothing. The key point is reproductive isolation by whatever menas, incuding behavioral-epigenetic and geographical. Selection can have a role, but only after that first requisite has been fulfilled. selection, in itself, does not separate populations.

    As usual, its enough for selection to be found somewhere for someone to conclude the whole thing is driven by selection. Find your favorite part, blame it for the entire complex process.

    No comments about Orrs transparent foolishness about "all true scientssts think like me". Obviously he's feeling insecure, to have introduce such extra-scientific and shallow "pressure"

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  15. Me: "At that point, any allele that would minimize or prevent hybrid crosses would be advantagous to those individuals."

    Larry: "Why?"

    Opportunity and parental investment cost, particularly on the female side.

    Sperm and pollen can be a "dime-a-trillion", but eggs are always relatively more expensive and less plentiful. Females (animals and flowers) invest a lot in a more limited number of potential offspring than males, and so, all things being equal, would prefer to mate with males that will result in the greatest number of the most fit offspring.

    It really doesn't matter whether you consider a "one-offspring-a-year for 10 years" mammal or the hundreds of thousands of acorns a mature oak can produce in its lifetime. In a stable population each individual will *on average* parent two of the next generation.

    If your offpring are less fit hybrids, your odds of breaking even or doing better than average go down. If you develop a mutation that ensures your offspring are not hybrids (which others around you lack), your odds of doing better than average go up.

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  16. I'm wondering if, say disruptive selection may lead to the separation of populations, but since nobody talks about that I guess it's not very effective in comparison to mechanisms like good ole geographic isolation

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  17. I'm wondering if, say disruptive selection may lead to the separation of populations, but since nobody talks about that I guess it's not very effective in comparison to mechanisms like good ole geographic isolation

    Well......:

    Bolnick, D.I and Lau, O.L. (2008) Predictable patterns of disruptive selection in stickleback in postglacial lakes. American Naturalist, 172, 1-11.

    Disruptive selection is often assumed to be relatively rare, because it is dynamically unstable and hence should be transient. However, frequency-dependent interactions such as intraspecific competition may stabilize fitness minima and make disruptive selection more common. Such selection helps explain the maintenance of genetic variation and may even contribute to sympatric speciation. There is thus great interest in determining when and where disruptive selection is most likely. Here, we show that there is a general trend toward weak disruptive selection on trophic morphology in three-spine stickleback (Gasterosteus aculeatus) in 14 lakes on Vancouver Island. Selection is inferred from the observation that, within a lake, fish with intermediate gill raker morphology exhibited slower growth than phenotypically extreme individuals. Such selection has previously been shown to arise from intraspecific competition for alternate resources. However, not all environments are equally conducive to disruptive selection, which was strongest in intermediate-sized lakes where both littoral and pelagic prey are roughly balanced. Also, consistent with theory, we find that sexual dimorphism in trophic traits tends to mitigate disruptive selection. These results suggest that it may be possible to anticipate the kinds of environments and populations most likely to experience disruptive selection.

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  18. It seems (to me, not a scientist) like gene hitchhiking is a significant element that's being left out of discussion here.

    Rapid fixation of D-M alleles, if such alleles arise by mutation pretty frequently, doesn't necessarily mean those speciation-affecting genes are being selected for. If any sort of moderate selection is operating, neutral or slightly deleterious D-M incompatibilities could be spreading by chance. That's still natural selection causing speciation in the general sense, but does not require any complex assumptions about D-M genes being harmful in one population and not another. Even if all D-M genes did was reduce fertility between organisms with different alleles (making them always deleterious when they first appear), if they are hitchhiking to the point that they predominate in a population being selected for nearby genes, then they will become advantageous in that population (relative to the original allele).

    I guess the test for that would be pretty simple, and maybe has already been done: see if two lab populations subject to the same selective environment (different from the normal environment in which that line is kept) diverge as quickly as (or even quicker than) when one stock is in a standard environment and one in a different selective environment.

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  19. Disruptive selection is often assumed to be relatively rare, because it is dynamically unstable and hence should be transient.

    Is this necessarily the case? Thinking in terms of intraspecific competition, an individual that is exactly average for its species may be subject to fiercer competition precisely because it is average - it has no unique selling point that it can leverage.

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  20. Divalent tries to explain his claim that. "At that point, any allele that would minimize or prevent hybrid crosses would be advantagous to those individuals."

    Opportunity and parental investment cost, particularly on the female side.

    Sperm and pollen can be a "dime-a-trillion", but eggs are always relatively more expensive and less plentiful. Females (animals and flowers) invest a lot in a more limited number of potential offspring than males, and so, all things being equal, would prefer to mate with males that will result in the greatest number of the most fit offspring.


    I don't think this is relevant.

    It really doesn't matter whether you consider a "one-offspring-a-year for 10 years" mammal or the hundreds of thousands of acorns a mature oak can produce in its lifetime. In a stable population each individual will *on average* parent two of the next generation.

    If your offpring are less fit hybrids, your odds of breaking even or doing better than average go down. If you develop a mutation that ensures your offspring are not hybrids (which others around you lack), your odds of doing better than average go up.


    I think I see where you're coming from. Let's see if I understand.

    Imagine a female plant that receives pollen from two different sources. One source is a completely compatible member of the same subspecies and the other is from an individual of a different subspecies.

    In the absence of hybrid sterility, some of the hybrid seeds will be viable and will grow into fertile plants.

    Let's say a mutation arises that prevents fertilization by the pollen from the other subspecies. We'll assume that it arises in some individual in the hybrid zone because otherwise it would have no effect.

    Are you saying that there is a selective advantage to the species in blocking off this gene flow because some of the eggs that were previously fertilized by the "foreign" subspecies can now be fertilized by individuals from the same subspecies?

    I can see this being a possibility if most fertilization events in the hybrid zone involved a competition between pollen from the two subspecies. If you eliminate the less efficient pollen then there's an increase in the overall viability of the seeds.

    If you had to guess at the size of a selection coefficient for such a mutation, what would you suggest? Remember that in an adaptationist scenario it's not sufficient to identify a possible benefit—you also have to postulate that the benefit is substantial enough to become fixed in the population.

    Why would such a mutation, arising in the hybrid zone, spread to those plants that never see pollen from the other subspecies?

    Just out of curiosity, let's imagine that a mutation arises in the "foreign" subspecies that allows their pollen grains to overcome the blockage and produce hybrid plants again. Would that allele be selected in the "foreign" subspecies?

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  21. Leading up to the point of hybrid sterility (the closed door), there is gradual lowering of the fitness of hybrids. The general phenomenon is known as outbreeding depression. The two populations have evolved in isolated environments for some time, and so the complement of alleles that are nearly optimum for one subspecies may be different than for the other. (So a random mix of the two sets is liable to be suboptimum, even though both sets are optimized for the same environment). Additional problems can result from rarer translocations of genes from one chromosome to another in one population vs the other (i.e., changes that got fixed by drift!).

    It can show up (and penalize the mother's reproductive success) at several points: a decreased chance that a mating event results in fertilization, a decreased chance that fertilization results in a viable embryo/seed, and decreased fitness of otherwise viable offspring (their ability to survive and their reproductive success).

    For females, who usually have a practical limit to the maximum number of offspring they can produce in a lifetime, it can represent a substantial opportunity cost. It is very relevant, because to produce one less-fit offspring means that they didn’t produce one best-fit offspring. A female moose that aborts a non-viable fetus after 2 months of gestation has forever lost that one season’s chance to get an offspring into the next generation: a 100% loss. A pea pod that contains only has 3 viable seeds rather than 5 represents a 40% hit.

    Consider what might be going on right in the middle of the overlap zone: half the males that a female encounters (or half the pollen grains) are “high fitness”, the other half are “low fitness”. I could state a number to quantify low fitness (like 80%), but the point is not what I chose, but that it is less than 100%, and the fitness advantage of an allele that prevents it would be a function of the hybrid penalty. If the hybrid penalty is low, then perhaps the populations will rejoin and become remain a single species even if a blocking allele arises (because the advantage would be slight, and over time the gene flow would reduce it’s advantage). Or if the hybrid penalty is high, but a blocking allele doesn’t arise, perhaps the continued gene flow will eventually result in them rejoining.

    But if such allele does arise, there will be a fitness advantage, and so will be subject to selection. (which is the whole point of my comments here: as you wondered how such an allele could be selected for).

    You further ask how such an allele could spread to the rest of the population outside the overlap zone. One answer is to note that initially it won’t (see the frog example I referenced above: the difference in mating call frequency at the present time is only in the overlap zone). But ultimately I think the answer is that there will forever remain a selection pressure at the overlap zone (which, once established, will grow stronger as the now genetically separated populations evolve further apart and the hybrid penalty increases) and so selection at the overlap zone will remain a source of strong protection against elimination by “drift”. Consequently, “drift” will eventually replace it in the rest of the population not in contact with the overlap zone.

    [So if one were to study this in a population outside the overlap zone, it might look like neutral drift in a local area, but it would be selection pressure in another area that kept reseeding the allele. So the conclusion that neutral drift was responsible for controling the allele frequency would be in error. Run any model of “neutral drift” where one allele is prevented from being eliminated (such as by setting a floor of 1%), and they will ALL eventually be fixed (apparently) by “drift”.]

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  22. One more thing:

    Larry: “Just out of curiosity, let's imagine that a mutation arises in the "foreign" subspecies that allows their pollen grains to overcome the blockage and produce hybrid plants again. Would that allele be selected in the "foreign" subspecies?”

    You are raising an interesting related issue (touched on by Carlo and Corneel above): often what is good for the male is different than what is good for the female. A male is not as constrained in his reproductive opportunities as a female (and they typically make billions or trillions more gametes than females). He would prefer, if limited in choice, to mating 100% with the “right” females. But his best strategy is to mate with as many “right” females as he can, and then in addition, to also mate with as many “less right” females as possible. Four potential advantages of this strategy:

    1) by mating with as many “right” females as he can, he maximizes the chances his genes get into the best fit members of the next generation (well, duh!);

    2) by mating with as many “less right” females, he gets additional genes into the next generation, albeit into individuals that have lower odds of success (but not zero odds).

    3) by mating with as many “less right” females, he precludes those females from mating with their own “right” males, and so preventing other males from getting their “best fit” offspring in the next generation (meaning that his own “best fit” offspring are a bigger fraction of the “best fit” in the next generation, and so better able to compete against them).

    4) by mating with as many “less right” females, he increases the proportion of lesser-fit individuals in the next generation, and so increasing the relative fitness of his “best fit” offspring relative to the average of the rest of the population.

    So males have different incentives (although there are complications, which often depends upon other factors, such as the relative strength of the competition within the species to competition with other species, and whether, such in the case of plants, the "male" and "female" are the same individual). Males often would have such an incentive to overcome the block, but females would not.

    Females would have an incentive to detect this “cheating” to prevent mating with the wrong males, and so this "anti-block" strategy is liable to be the topic of sexual selection pressures. (The “battle of the sexes” is not just about who gets to control the TV remote or whether a new set of golf clubs is a wiser expenditure than purchasing a new vase for the front foyer).

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  23. Divalent, it seems like your proposals are heavily biased towards animals—especially large animals that have only a few offspring.

    I prefer to deal with models that apply to most species and not to just a specific small subset. I see that you can make a case for selection using moose and some other animals but those examples do not a generality make.

    For the vast majority of species it's simply not correct to say that one of the sexes makes a more serious investment than another. If your model of selection for hybrid infertility requires those rare exceptions then it's an exception, rather than a rule, that selection drives speciation.

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  24. Honestly, Larry, sometimes I think you troll your own blog. Nothing I said was limited to big mammals (and I mentioned pea and oaks as examples).

    Except for the details and the weight of the different factors, the general principle applies to ALL sexually reproducing species.

    Reproduction is expensive. Reproductive organs are consumers of resources. Gametes, particularly eggs, are often expensive to make. The strategies vary on a continuum ranging from heavy investment in a few (mammals), to a little investment in a lot (oaks), but in ALL cases any particular individual can produced a *finite* number of offspring that will have to compete to succeed in the next generation.

    It might be 10 little mooses (meese?), or 500,000 acorns, or 100 mayfly eggs. But all things being equal, parental success is a function of the fitness of those limited number of possible offspring.

    For the oak, what is better: 250,000 "best fit" acorns and 250,000 "lesser fit" acorns, OR 500,000 "best fit" acorns? For the moose: 5 "best fit" offspring and 5 lesser fit offspring, OR 10 "best fit" offspring? For the mayfly, 50 eggs with "best fit" genes and 50 with "lesser fit" genes, OR 100 with "best fit" genes?

    If you agree that in all cases it is better to have 100% of that finite number be "best fit", then it seems to me that it follows that it is an outcome that is subject to selection pressure.

    Virtually all species have stratgies that help them avoid mating with other species, for good reason. If hybrids are sterile, the loss is the effort expended to create (and, in mammals, to care for) that offspring and the lost opportunity to create an offspring that was not sterile. The difference is a matter of degree, not kind, when the consideration is a hybrid that is merely less fit. The average fitness of your offspring will be lower if ANY of that finite number is of a lower fitness. Both males and females have this same incentive. Although it is true that in some species males also have other competing incentives, those don't change the basic conclusion.

    I'm not sure why you can't grasp this.

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  25. Divalent asks,

    For the oak, what is better: 250,000 "best fit" acorns and 250,000 "lesser fit" acorns, OR 500,000 "best fit" acorns? For the moose: 5 "best fit" offspring and 5 lesser fit offspring, OR 10 "best fit" offspring? For the mayfly, 50 eggs with "best fit" genes and 50 with "lesser fit" genes, OR 100 with "best fit" genes?

    Your point depends on the difference between two different types of gamete. In order to make that clear let me re-phrase your question.

    "For the oak, what is better: 250,000 "best fit" pollen grains and 250,000 "lesser fit" pollen grains, OR 250,000 "best fit" pollen grains and 250,000 "no fit" ppollen grains? For the moose: 5 "best fit" inseminations and 5 lesser fit inseminations, OR 5 "best fit" inseminations and 5 "no fit" inseminations? For the mayfly, 50 "best fit" matings and 50 "lesser fit" matings, OR 50 "best fit" matings and 50 "no fit" matings?

    If you agree that in all cases it is better to have 100% of that finite number be "best fit", then it seems to me that it follows that it is an outcome that is subject to selection pressure.

    I don't agree with your scenarios because I think they are too simplistic. Imagine a female moose who mates with a male from the "foreign" population in the hybrid zone.

    What you're saying is that if she carries a new mutation causing her to produce no fertile offspring then she will be at a selective advantage over her sister who does not carry the new mutation and mates with the same male but has a 50% chance of producing offspring.

    Is that a fair summary of your position?

    I agree that you can make it work by invoking sexual selection (pre-zygotic infertility) but that wasn't what we were discussing.

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  26. It seems that the key here is whether mating opportunities for the female are limited relative to reproductive resources or opportunities. A flower that receives more pollen than it can use to make fruit (since the amount that a plant can invest in fruit is limited) would experience selective pressure to sort applicants (pollen). Many plants already sort pollen anyway to avoid selfing. I don't know how much of role prezygotic isolating mechanisms play in plants, if only because I don't know much about plants. I would, admittedly out of ignorance, suggest an alternate means for plants to choose 'paternity' of mature seeds. If you look at seed pods, say of peas or corn, very often it is noticeable that the pods are not full of seeds. This seems correlated to nutrient status, so thriving plants with plenty of water etc will produce larger more full seed pods. Other plants in a more difficult environment produce fewer seeds but this does not mean that they don't have equal access to pollen. So there could potentially be a mechanism to arrest development of some seeds, before a lot of resources are invested, and in some cases this might be related to 'paternity' of the seeds. While not having anything (as far as I know) to do with hybridizaton, apples commonly drop fruit early in its development in order to avoid over investment. So in cases of disease or a dry spring, trees will drop a substantial portion of their crop if resources will be spread too thinly. Since plants are already sorting the pollen and then the seeds later there is potential for them to maximize fitness of their offspring by discriminating against hybrid seeds or heterospecific pollen.

    As I said before, I don't know how much of a role prezygotic isolating mechanisms play in plant speciation. I suspect that various scenarios can cause speciation and the importance of each will differ between classes of organisms (does that make me a speciation pluralist?). For example, a hopeful monster type scenario seems much more likely among plants than among animals for two reasons. One is that plants are more robust to major genetic changes (like polyploidy) than animals are (probably because plants are more flexible in their morphology anyway). The other is that vegetative reproduction is extremely common among plants providing an easy mechanism for a single hopeful monster to found a population.

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  27. Larry: "I agree that you can make it work by invoking sexual selection (pre-zygotic infertility) but that wasn't what we were discussing."

    Doh! Boy, I got egg on my face! Of course I was considering pre-zygotic infertility.

    In the infamous words of Emily Natella: "never mind!"

    I'll go away and think about it, but off hand I'm now with you: I don't see how natural selection would operate here (using your converted version of my examples).

    For natural selection to work, it would (as you point out) have to be better for an individual to *just* have 1/2 as many "best fit" offspring, rather than 50% each of "best fit" and "lesser fit".

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