Roles of mutation and selection in speciation: from Hugo de Vries to the modern genomic era

Abstract

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.

FIG. 1.—

Inferred polyploidization events during the evolution of angiosperms. Circles indicate suspected genome duplication events. Approximate time scale is shown below the tree. Modified from Adams and Wendel (2005).

FIG. 2.—

Gene order relationships in the region around Saccharomyces cerevisiae SSN6 and its homologs in the species before and after genome duplication. Each ortholog is shown by a different color. Gene names are given at the top in italics. Reciprocal gene loss shown by a red box supports the Oka model of speciation. Abbreviations are as follows: A. gos, Ashbya gossypii; K. lac, Kluyveromyces lactis; C. gla, Candida glabrata; S. cas, S. castellii; and S. cer, S. cerevisiae. Modified from Scannell et al. (2006).

FIG. 3.—

Loss of duplicate genes after genome duplication in four species of yeasts. The numbers in squares represent the numbers of loci, which were derived by genome duplication in the ancestral species and have been retained in the genome. Numbers (–) on branches indicate the numbers of loci, in which one of the duplicate genes was lost. In total, 2,723 duplicate loci were analyzed. Modified from Scannell et al. (2006).

FIG. 4.—

Oka model of speciation by duplicate gene mutations. A and B are duplicate genes. A₀ and B₀ are the original normal alleles, and A₁ and B₂ are lethal mutations.

FIG. 5.—

DM model of evolution of reproductive isolation. A₀, A₁, and A₂ represent alleles at the A locus, whereas B₀, B₁, and B₂ represent alleles at the B locus. (A) Diploid model. (B) Haploid (gamete) model.

FIG. 6.—

Distribution of d_N/d_S ratio between the Drosophila melanogaster and D. simulans genes. A total of 5,314 protein-coding genes having one-to-one orthologs among 12 Drosophila species were used. The d_N and d_S values were computed by the modified Nei-Gojobori method (Zhang et al. 1998) with a transition/transversion ratio of 2.

FIG. 7.—

Male sterility caused by different combinations of alleles at the SaF and SaM loci in rice. Modified from Long et al. (2008).

FIG. 8.—

A model of species specificity of gamete recognition between lysin and VERL in abalone. Modified from Nei and Zhang (1998).

FIG. 9.—

Stepwise mutation model for hybrid sterility (or inviability) genes. (A) In the stepwise mutation model, the forward and backward mutation may occur. (B) The fertilities for various haplotypes for loci A and B (two-locus model) and genotypes for locus A (one-locus model) are given by 0 (infertile) or 1 (fertile). Distantly related haplotypes or genotypes are infertile.

FIG. 10.—

Typical crossing experiments in Xiphophorus species. X⁺ and X⁻ represent the presence and absence of the Xmrk gene, respectively. R⁺ and R⁻ represent the presence and absence of the R gene. F₁ hybrids (X⁺X⁻, R⁺R⁻) express benign melanoma, but they are shown with that of the normal type in this figure. One quarter of backcross offspring will develop melanoma. Modified from Schartl (2008).