Friday, February 06, 2009

What Causes Speciation?

The latest issue or Science magazine contains a number of articles on speciation.

The one that most interests me is Schluter (2009), a paper that discusses mechanisms of speciation. Schulter begins with ...
It took evolutionary biologists nearly 150 years, but at last we can agree with Darwin that the origin of species, "that mystery of mysteries" (1), really does occur by means of natural selection (2–5). Not all species appear to evolve by selection, but the evidence suggests that most of them do. The effort leading up to this conclusion involved many experimental and conceptual advances, including a revision of the notion of speciation itself, 80 years after publication of On the Origin of the Species, to a definition based on reproductive isolation instead of morphological differences (6, 7).
I've heard this a lot recently but it doesn't make sense to me. How could the evolution of reproductive isolation be selected?
The main question today is how does selection lead to speciation? What are the mechanisms of natural selection, what genes are affected, and how do changes at these genes yield the habitat, behavioral, mechanical, chemical, physiological, and other incompatibilities that are the reproductive barriers between new species? As a start, the many ways by which new species might arise by selection can be grouped into two broad categories: ecological speciation and mutation-order speciation. Ecological speciation refers to the evolution of reproductive isolation between populations or subsets of a single population by adaptation to different environments or ecological niches (2, 8, 9). Natural selection is divergent, acting in contrasting directions between environments, which drives the fixation of different alleles, each advantageous in one environment but not in the other. Following G. S. Mani and B. C. Clarke (10), I define mutation-order speciation as the evolution of reproductive isolation by the chance occurrence and fixation of different alleles between populations adapting to similar selection pressures. Reproductive isolation evolves because populations fix distinct mutations that would nevertheless be advantageous in both of their environments. The relative importance of these two categories of mechanism for the origin of species in nature is unknown.
Is there an expert on speciation out there who can explain this? I understand how two incipient species can adapt to different environments and become morphologically distinct but I don't understand how this kind of adaptation leads to selection for reproductive isolation. This is a problem that we discussed earlier [Testing Natural Selection: Part 2].

The second mechanism is even more difficult for me. I understand how chance mutations can arise and become fixed but to my mind this isn't natural selection. It's speciation by random genetic drift. It's just an accident that the mutations being fixed in the separated populations happen to lead to reproductive isolation.

Schluter tells us that mutation-order speciation is "distinct from genetic drift." He seems to refer to it as "selection" of some sort without explaining why. ("The unidentified component of speciation, if built by selection and not genetic drift, could be the result of either ecological or mutation-order mechanisms.") He says that the mutations that give rise to reproductive isolation are "advantageous" in both populations but they just happened to occur in one of them and not the other. Again, the question is what sort of mutations favoring reproductive isolation would be "advantageous," and therefore selected?

If the mutation arises later on in the other species will it sweep to fixation and remove the reproductive isolation barrier?

It's not clear to me that we have identified the mechanisms of reproductive isolation in a large number of examples. Schluter seems to agree,
The most obvious shortcoming of our current understanding of speciation is that the threads connecting genes and selection are still few. We have many cases of ecological selection generating reproductive isolation with little knowledge of the genetic changes that allow it. We have strong signatures of positive selection at genes for reproductive isolation without enough knowledge of the mechanisms of selection behind them. But we hardly have time to complain. So many new model systems for speciation are being developed that the filling of major gaps is imminent. By the time we reach the bicentennial of the greatest book ever written, I expect that we will have that much more to celebrate.
Given our lack of knowledge how can biologists be so confident that Darwin was right? How do they know that most speciations are due to natural selection and not random genetic drift—especially since drift and accident seem to be intuitively more likely?

Is this an example of adaptationist bias or is there really lots of evidence to support speciation by natural selection?

Schluter, D. (2009) Evidence for Ecological Speciation and Its Alternative. Science 323: 737 - 741 [DOI: 10.1126/science.1160006]


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  2. I wouldn't consider myself an 'expert' on speciation, but let me try to approach the issue this way.

    Incipient speciation, need not be driven by positive selection. Different populations of a species may fix different alleles that create pre-zygotic (i.e., behavioral) and post-zygotic (i.e., genetic) barriers to gene flow. In such a case where two populations have randomly fixed variant alleles for female preference, for example, such that said preference is detectably different in each, then cross-populations hybrids may conceivably be at a disadvantage with respect to the pure population strains. Say females prefer red in one pop, and yellow in another. Hybrid males could be orange and thus less fit - or hybrid females could have their preferences messed up, leading to reduced discrimination and thus an excess in costly matings.

    Once the initial barrier is in place, selection could favor mechanisms that prevent the production of hybrids, which are very costly to females. Thus post-zygotic mechanisms can be favoured via reinforcement (see Ortiz-Barrientos et al. 2004).

    There's also several models that have shown that while incipient speciation need not involve selection, directional selection could act to speed up the accumulation of things like Dobzhansky-Muller incompatibilities (anything driving protein evolution could, by chance, conceivably lead to incompatibilities when these proteins are placed in an untested genetic background).

    So, while I believe that the consensus position on speciation is that it only requires drift and time, reinforcement has the potential to favour 'speciation genes' and play a major role in the process.

  3. I've read theorizing, but no empiricism. Are there published papers that survey genetic differences between closely related species to determine, of the genetic differences between them, which show selection effects and which do not? (Is there sufficient information in any of the published chimp/human comparisons to be able to get any sort of good handle on this?) This would at least give a start on data points regarding how much genetic divergence appears to be due to selection, and how much to drift.

  4. @Jud

    That question is far more difficult to answer than may be apparent! Drift is the null hypothesis against which evidence for selection is tested; thus not finding evidence of selection does not mean drift happened, only that the hypothesis of drift cannot be rejected. There are many papers that have done that for a variety of organisms (see Larracuente et al. 2008 for a recent example in fruit flies).

    However, I can try to weigh in on your question by pointing out that a further complication is found in the following: Once reproductive isolation sets in, all bets are off in terms of trying to figure out whether selection was 'the' cause of speciation. Most 'speciation genes' that have been studied appear to have been subject to selection, but this is likely due to reinforcement (see above) acting on any genes that prevent the production of unfit hybrids. Incompatibilities between species will accumulate with abandon after gene flow has ceased, and any evidence of selection in such genes need not have been caused specifically by selection 'for' speciation.

    However, one way that one may go about answering such a question is to see if there's more evidence for selection in very recently speciated pairs as compared to more ancient splits. This punctuational pattern would be consistent with speciation being often driven by rapid bouts of selection (either by directional selection for ecological adaptation, or reinforcement, etc.) followed by general stasis. I also happen to know a couple of people trying to get just such a study published as we speak.

  5. I think Divalent has already tried to explain it to you, but the short answer is: sexual reproduction (gamete production, secondary sexual characters, intrasex competition, mate attraction, mating, gestation, parental care etc) is not free - in terms of energetics, time, risk of injury and disease etc. If the products of variants or species have poor fitness or are nonviable than various barriers to reproduction will be positively selected.

    And before you blurt out 'Just-so stories,' why not crack the literature? There really is a research literature out there on this topic.

  6. Kieran wrote:

    "The only chance elements are the initial standing variation in each population (determined by the spatio-genetic layout the population, as well as the nature of the vicariance event), and the de novo genetic variation that arises thereafter through mutation."

    Indeed, but it precisely these events and no others that eventually result in any genetic incompatibility between the vicariant populations. Selection doesn't produce the variations, it simply preserves certain variations once they have arisen.

    Ergo, the "engine" of genetic incompatibility (which is the underlying "engine" of speciation, according to the "modern synthesis") is not selection, but rather the random processes that produce new genetic (and presumably phenotypic) variants.

    So, Larry, you are correct, and the author of the article in Science has it wrong.

    Interestingly, Darwin himself made essentially the same point in the Origin of Species. In Chapter 5 ("Hybridism") he very clearly argues that selection cannot possibly result in increasing degrees of hybrid sterility. In a nutshell, sterility cannot be selected for. Darwin suggests that variations unrelated to fitness eventually accumulate and produce the reproductive incompatibility that defines species.

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  8. Jud asks,

    I've read theorizing, but no empiricism. Are there published papers that survey genetic differences between closely related species to determine, of the genetic differences between them, which show selection effects and which do not?

    There are several papers on the actual mutations that give rise to reproductive incompatibility. In some cases the relevant allele appear to have been selected within one population because it is advantageous. In other cases the allele appears to have become common due to random genetic drift. [see Testing Natural Selection: Part 2 for an example of each type]

    Many scientists seem to think that selection is the dominant mechanism but as far as I can tell this is mostly bias without experimental support.

  9. anonymous says,

    And before you blurt out 'Just-so stories,' why not crack the literature? There really is a research literature out there on this topic.

    I've read quite a bit about speciation and I'm quite puzzled.

    A lot of the data is consistent with speciation by random genetic drift and that's why the textbooks mention it as an important possibility.

    When I read papers that claim to show speciation by natural selection they often seem unconvincing. The monkey flower example that we discussed a few weeks ago is a prime example.

    What puzzles me is that there are scientists who seem to be absolutely convinced that natural selection drives most speciation (reproductive isolation) when there doesn't seem to be very much solid evidence to support such a position.

  10. I don't think many people are convinced that natural selection drives incipient speciation. There is a consensus that speciation occurs predominantly in allopatry. That excludes the presence of natural selection "for" speciation. Upon secondary contact however, many populations are reproductively isolated to some extent. The question then is: are the genetic differences due to genetic drift or natural selection?
    I agree with Larry that there is a bias for adaptive explanations. Well, they are more interesting :-)

  11. How about the newly proposed hypothesis on the role of transposable elements (TEs) in speciation?

    In short, TEs are likely undergo fixation in small subpopulations by genetic drift. The more active they are in a particular subpopulation, the more likely they can diverge the subpopulation and prevent it being reabsorbed into the ancestral population. The main evidence are the outbursts of new families of TEs at phylogenetic nodes.

  12. Apparently, it cut the link: