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Tuesday, April 3, 2012

Polyploidy, Incompatibility Mutations, and Speciation

            The roles of mutation and natural selection in the formation of new species have been controversial for the last 150 years. It is often stated that Charles Darwin (1) did not solve the problem of origin of new species because he did not explain how a species splits into two or more species. Darwin was aware of the hybrid sterility and inviability between different species, but he had a difficulty to explain it by natural selection. At his time some authors suggested that hybrid sterility or inviability might be enhanced by natural selection because the mixing of two incipient species by hybridization is disadvantageous for the formation of new species. Darwin rejected this idea after examination of various cases of species hybridization and concluded that “hybrid sterility is not a specially acquired or endowed quality but is incidental on other acquired differences.

            de Vries (2) proposed a very different view called the mutation theory, in which new species or elementary species (meaning incipient species) are produced by single mutational events. According to this theory, new incipient species are suddenly produced and reproductively isolated from the parental species. Because this theory was based on experimental studies conducted with the evening primrose Oenthera lamarkiana, it was accepted by many biologists when it was proposed. About two decades later, however, the mutation theory was almost abandoned mainly because O. lamarkiana was found to be a heterozygote for chromosomal complexes and the mutant forms he found were mostly caused by chromosomal rearrangements derived from this unusual parental species. At the time of de Vries the genetic cause of mutations was not known, and he regarded any heritable changes of phenotypic characters as mutations. Later studies showed that at least one of the elementary species (O. gigas) he discovered was a tetraploid, and it established itself as a new species in self-fertilizing evening primrose. Therefore, he was right in his proposal of mutation theory. In fact, recent genomic data abundantly support his theory of origin of species by polyploidization or  chromosomal changes in plants (see illustration).

Circles indicate suspected genome duplication events.

In animals, however, the formation of new species by chromosomal mutations is rare, and new species are believed to be generated by genic mutations and natural selection. The models of genic speciation are complicated, and there are many different ways of generating hybrid weakness. In these cases most investigators have emphasized the importance of natural selection rather than mutation (3). Some authors implied that positive selection for incompatibility genes is important in speeding up speciation. In my view, the crucial event of speciation is the development of reproductive barriers between species, and this is accomplished mainly by incompatibility mutations.
Recently, Masafumi Nozawa and I (4) critically examined various papers concerned with speciation by re-analyzing molecular data available. We then reached the conclusion that the hybrid inviability or sterility is cause by incompatibility genes that are manifested when two different species are hybridized. The abstract of their paper is as follows:

One of the most important problems in evolutionary biology is to understand how new species are generated in nature. In the past, it was difficult to study this problem because our lifetime is too short to observe the entire process of speciation. In recent years, however, molecular and genomic techniques have been developed for identifying and studying the genes involved in speciation. Using these techniques, many investigators have already obtained new findings. At present, however, the results obtained are complex and quite confusing. We have therefore attempted to understand these findings coherently with a historical perspective and clarify the roles of mutation and natural selection in speciation. We have first indicated that the root of the currently burgeoning field of plant genomics goes back to Hugo de Vries, who proposed the mutation theory of evolution more than a century ago and that he unknowingly found the importance of polyploidy and chromosomal rearrangements in plant speciation. We have then shown that the currently popular Dobzhansky-Muller model of evolution of reproductive isolation is only one of many possible mechanisms. Some of them are Oka's model of duplicate gene mutations, multiallelic speciation, mutation-rescue model, segregation-distorter gene model, heterochromatin-associated speciation, single-locus model, etc. The occurrence of speciation also depends on the reproductive system, population size, bottleneck effects, and environmental factors, such as temperature and day length. Some authors emphasized the importance of natural selection to speed up speciation, but mutation is crucial in speciation because reproductive barriers cannot be generated without mutations.

Our conclusion is that hybrid inviability or sterility is a mere consequence of establishment of sets of genes that are compatible within species but incompatible between species. This is similar to Darwin’s conclusion. We therefore believe that both Darwin and de Vries were correct in visualizing the mechanism of formation of new species.
I would appreciate any of the comments on the Nei-Nozawa paper or any other matter.


1.  Darwin C. 1859. On the origin of species by means of natural selection or the preservation of favoured races in the struggle for life. Murray, London.
2. de Vries H. 1909. The mutation theory: Experiments and observations on the origin of species in the vegetable kingdom. Vol. I. The origin of species by mutation. English translation by Farmer, JB and Darbishire, AD. Open Court Publishing Company, Chicago.
3. Coyne JA and Orr HA. 2004. Speciation. Sinauer Associates, Sunderland, MA.


  1. I think we have been misled by Darwin, and that many if not most biologists, and the vast majority of anthropologists and human geneticists, simply haven't thought critically about it.

    I think things are less dichotomous than selection vs mutation. Selection, by definition, involves genetic change and as a cause of speciation it implies mating incompatibility for genetic reasons.

    Mutation (including inversions and copy number variants and so on) need not affect phenotypes and need not be related to selection in the usual Darwinian sense.

    Darwin simply assumed that adaptive differences were the mechanism of speciation. But that is obviously not the case by itself (humans are genetically variable, and from South America to South Africa have been separated for 100,000 or more years. We have numerous adaptive differences (e.g., skin color, body shape) and yet there is no sign of hybrid sterility etc.

    One question seems to have been whether 'selection' just changes allele frequencies while 'mutation' adds new alleles. Clearly both are involved (e.g., in human adaptations) and there are all sorts of new mutations within populations that have nothing to do with speciation in any serious way (as the rapidly accumulating whole genome sequences of humans show). Similarly, mating is compatible between most inbred mouse strains; they have been derived by artifical breeding with or without selection, and differ by millions of SNPs and so on. Yet they can mate.

    So the speciation question is really about how in any given case genomic mating incompatibility has arisen. Selection could be responsible, but non-adaptive mutation (no functional change, as in neutral mutations or inversions) can do this, too, I think that Allen Orr has shown small incompatibility changes in this sense among Drosophila species.

    In these senses adaptation and speciation are separate, quite unlike what Darwin thought. So isn't it the case that the questions don't add any controversy to basic ideas about adaptation or speciation, except that we need to recognize that each case is different?

  2. Charles Darwin clearly distinguished between mutation (generation of variations) and natural selection. His definition of natural selection is included in the title of the first edition of his 1859 book “On the Origin of Species by Means of Natural Selection or the Preservation of Favored Races in the Struggle for Life.” In terms of modern language, this means the saving or selection of advantageous mutations. In the 6th edition of the book, he also stated “Several writers have misapprehended or objected to the term Natural Selection. Some have even imagined that natural selection induces variability, whereas it implies only the preservation of such variations as arise and are beneficial to the being under the conditions of life” (1, p. 63).

    In the Chapter 5 of his book (Laws of Variation), he discussed how new variation appears in nature by “correlation of growth, use and disuse, and the direct action of the physical condition of life.” Because he did not know the genetic material, he had an erroneous concept of mutations including some elements of Lamarckism. However, his concept of natural selection is essentially the same as ours in population genetics. At present, of course, mutation means any change of genetic material, including genome duplication, gene duplication /deletion, nucleotide changes, recombination, transposon insertion/deletion, etc.

    At the time of neo-Darwinian era, however, phenotypic characters were used for studying genetic changes, and the nature of mutation was not clear. Some authors claimed that natural selection sometimes generates new genetic variations as Ken mentioned. However, this is clearly wrong, and I do not think we should continue using this idea anymore.

    In the Nei-Nozawa paper, we used the modern definition of mutation and natural selection, and I believe we have shown the importance of mutation in speciation. Of course, our paper is quite long, and one may have to spend some time to comprehend the meaning.

    In the case of speciation, we must consider only incompatibility genes that affect hybrid sterility or inviability. Mutation would certainly generate neutral or nearly neutral variations which become highly polymorphic in the population, but they are irrelevant for speciation. We have also shown that it would take hundreds of thousands of years to establish sterility barrier between different populations.


    1. Darwin C. 1872. On the origin of species by means of natural selection or the preservation of favored races in the struggle for life, 6th ed. Murray, London.