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. |
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.
4. Nei M and Nozawa M. 2011. Roles of mutation and selection in speciation: from Hugo de Vries to the modern genomic era. Genome Biol Evol 3:812-829