Hypothesis: First-Degree Inbreeding Facilitates Chromosomal Speciation
AUTHOR: Allen MacNeill
SOURCE: Original essay
COMMENTARY: That's up to you...
To help you enjoy the holiday, let me offer you a hypothesis that I have been working on to explain the origin of species in animals. The inspiration for this hypothesis was a debate at Uncommon Descent in which I have been embroiled for the past few days. The debate began with a discussion of the possibility of "virgin birth" in humans. The poster, DaveScot (not his real name) started out with a description of meiosis that contained an egregious error: that the first division of meiosis results in two diploid daughter cells. As every introductory biology student knows, this is incorrect: the first division of meiosis produces two haploid daughter cells in which the chromosomes are still double-stranded. The second division of meiosis is essentially a mitotic division, separating the sister chromatids in the double-stranded chromosomes of the first-division daughter cells.
The debate moved on, eventually centering on the subject of the chromosomal basis for speciation. I mentioned that speciation is the result of genetic isolation, and that in many cases (but not all) it is associated with chromosomal fission, fusion, inversion, and translocation events. For example, one of the main differences between humans and other great apes is that humans have one less pair of chromosomes; 46 instead of 48. Recent genomic research has shown that this difference is the result of the fusion of two of the chromosomes of great apes to form the human chromosome #2. This led to the following question from one of the participants in the debate:
"Wouldn't this fusion event have to occur within at least two members- one male, one female- of the same population in order for it to have any chance of getting passed on?"
To which I answered:
No. All that would need to happen to make this possible would be for two first-degree relatives carrying the translocation to mate and have offspring. First degree relatives (i.e. parents and offspring or full siblings) can easily have the same chromosomal mutation (i.e. a fusion/fission/translocation/inversion), as they would inherit it from a single parent. If they were to mate with each other (a not uncommon event among non-humans...and even among some humans), they would be able to produce fertile offspring carrying the same chromosomal mutation.
Yes, it is true that first degree mating carries with it the possibility of reinforcement of recessive lethal alleles. However, as many geneticists and evolutionary biologists have repeatedly pointed out, this is actually beneficial to the population within which such reinforcement happens, as the alleles are removed from the population as a result.
In other words, mating between first degree genetic relatives within a small, isolated population would have the effect of both removing deleterious alleles from the population and allowing chromosomal mutations to spread throughout the population, especially if such mutations were at all beneficial (although they would diffuse almost as well if they were selectively neutral, as would probably be the case given that no change in overall genetic information would have occurred).
Furthermore, the hypothesis that I have presented above squares very well with the currently prevailing theory of speciation: that of peripatric speciation, as first proposed by Ernst Mayr. According to Mayr's theory, speciation occurs most often in small, isolated populations on the periphery of large, panmictic populations. There is abundant natual history evidence that this is the case, especially in animals.
However, no one has yet explained how peripatric speciation would come to be associated with the kinds of chromosomal changes that we have been discussing. My hypothesis – that first-degree inbreeding facilitates chromosomal speciation – is an attempt to reconcile those two observations.
In a large, panmictic population, selection would tend to eliminate individuals who mate with first-degree relatives as a result of decreased viability due to inbreeding depression and the increased frequency of expression of homozygous lethal alleles.
However, in very small, isolated populations individuals who occasionally mate with first degree relatives (i.e. "facultative first degree inbreeders") could easily have a selective advantage of individuals who avoid mating with first degree relatives (i.e. "obligate outbreeders").
Males in particular would tend to loose less as the result of mating with first degree relatives, as their parental investment in offspring is lower (i.e. they can waste gametes and even zygotes by mating with their first degree relatives, without significantly decreasing their reproductive success).
However, even females can cut their losses by mating with first degree relatives if the likely alternative is failure to mate at all due to unavailability of non-relatives. This would especially be the case in small, isolated populations, which are exactly the kind of populations in which speciation is most likely to occur.
The effects described above would be facilitated by increased genomic homogeneity, such as would result from genetic bottlenecks and founder effects. This is because close inbreeding intensifies genomic homogeneity and decreases genetic variation, especially in isolated populations with decreased gene flow from other populations.
This hypothesis – that first degree inbreeding facilitates chromosomal speciation – immediately suggests a series of predictions, all of which are empirically testable:
• The frequency of mating between first degree relatives should be inversely correlated with effective breeding population size. That is, the smaller the effective breeding population, the greater the frequency of mating between first degree relatives (i.e. “first degree inbreeding”).
• The increased frequency of “first degree inbreeding” in such populations should be more pronounced in males. That is, males should be more likely to attempt mating with first degree relatives, especially in small, isolated populations.
• The frequency of “chromolocal mutations” (that is, chromosomal fission/fusion/inversion/translocation mutations) should also be inversely correlated with effective breeding population size. That is, the smaller the effective breeding population, the greater the frequency of viable “chromolocal mutations.”
• Peripatric speciation events should be correlated with small population size, chromolocal mutations, and first degree inbreeding.
• Speciation resulting from chromolocal mutations should be much less common in large, panmictic populations.
• First degree inbreeding should also be much less common in large, panmictic populations.
• The success rate of artificial (i.e. facilitated/forced) first degree mating should be directly correlated with the degree of inbreeding. That is, the more inbred a population, the more successful artificial first degree inbreeding should be.
• Paleogenomic analysis should find close correlations between genetic bottlenecks, founder events, and peripatric speciation events and the frequency of chromolocal mutations and genetic homogeneity (resulting from first degree inbreeding).
• Relatively large changes in phenotype resulting from chromolocal effects should be more common in small, isolated populations.
• Speciation should be easier (and therefore more frequent) among asexually reproducing eukaryotes, such as plants and parthenogenic animals (among whom aneuploidy is largely irrelevant).
Let me stress two things about the foregoing:
• What I am suggesting is, at this stage, merely a hypothesis, but one that generates a series of immediately testable predictions.
• The hypothesis is, of course, based on the idea that incest (i.e. first degree inbreeding) is the most likely explanation for the diffusion of chromolocal mutations throughout small, isolated populations of animals. Let me stress as strongly as possible that I am NOT advocating incest, I am simply pointing out that first degree inbreeding would facilitate the kind of chromolocal mutations that are often correlated with species differences in animals. The same is also true for plants, of course, but in plants we don't call it "incest," we call it "self-pollination."
I would like to also add at the end of this presentation that my reading of John Davison's papers in which he details his "semi-meiotic hypothesis" for the origin of species were an indirect inspiration for my own efforts. While his hypothesis would work, its most significant drawback is that it requires an almost unlimited number of independent "reinventions" of the same mechanism (i.e. semi-meiosis) for speciation that results from chromolocal effects to be the basis for speciation throughout the animal kingdom. Not impossible, but extremely unlikely.
By contrast, my "first degree inbreeding hypothesis" does not require independent "reinventions" of semi-meiosis at all. The only thing it requires is that first-degree inbreeding occur in small, isolated populations of animals, an easily testable prediction that does not require elaborate genetic mechanisms to produce the predicted outcome: that is, genetic isolation and subsequent speciation.
I am a little perplexed at why no one has yet proposed this mechanism, given the fact that it is already used as the explanation for speciation in plants via polyploidy. The only explanation that seems reasonable to me is that most evolutionary biologists assume that animals will always avoid mating with first-degree relatives as a result of the increased frequency of inbreeding depression and expression of homozygous lethal alleles that result from it.
Anyway, that's my hypothesis in brief. Oh, and one more thing: why the turkey at the head of this post? To commemorate Thanksgiving, of course, but also because turkeys are known to exhibit significant numbers of parthenogenesis. That is, a significant proportion of male turkeys are the result of the development of an unfertilized egg. They are male, not female (as would be the case in parthenogenetic mammals) because males are the homogametic sex in birds; they are ZZ, whereas females are ZW (the Z and W chromosomes corresponding in function to the X and Y chromosomes in mammals). It has not escaped my notice that parthenogenesis would greatly facilitate the kind of chromosomal speciation I have outlined above. Hence, the turkey can stand as an emblem of the First-Degree Inbreeding Hypothesis for Chromosomal Speciation in Animals.
Have a great turkey day, folks!
Comments, criticisms, and suggestions are warmly welcomed!