Dobzhansky, Bateson, and the genetics of speciation.
Explore the source record for details and available documents.
Animals↗
Biomedical subjects
H A Orr
Publications and source records attributed to H A Orr.
Somatic mutation favors the evolution of diploidy.
Explanation of diploidy have focused on advantages gained from masking deleterious mutations that are inherited. Recent theory has shown that these explanations are flawed. Indeed, we still lack any satisfactory explanation of diploidy in species that are asexual or that recombine only rarely. Here I consider a possibility first suggested by Efroimson in 1932, by Muller in 1964 and by Crow and Kimura in 1965: diploidy may provide protection against somatic, not inherited, mutations. I both compare the mean fitness of haploid and diploid populations that are asexual and investigate the invasion of "diploidy" alleles in sexual populations. When deleterious mutations are partially recessive and somatic mutation is sufficiently common, somatic mutation provides a clear advantage to diploidy in both asexual and sexual species.
Biological Evolution↗
The population genetics of speciation: the evolution of hybrid incompatibilities.
Speciation often results from the accumulation of "complementary genes," i.e., from genes that, while having no deleterious effect within species, cause inviability or sterility when brought together with genes from another species. Here I model speciation as the accumulation of genic incompatibilities between diverging populations. Several results are obtained. First, and most important, the number of genic incompatibilities between taxa increases much faster than linearly with time. In particular, the probability of speciation increases at least as fast as the square of the time since separation between two taxa. Second, as Muller realized, all hybrid incompatibilities must initially be asymmetric. Third, at loci that have diverged between taxa, evolutionarily derived alleles cause hybrid problems far more often than ancestral alleles. Last, it is "easier" to evolve complex hybrid incompatibilities requiring the simultaneous action of three or more loci than to evolve simple incompatibilities between pairs of genes. These results have several important implications for genetic analyses of speciation.
Alleles↗
The dominance theory of Haldane's rule.
"HALDANE's rule" states that, if species hybrids of one sex only are inviable or sterile, the afflicted sex is much more likely to be heterogametic (XY) than homogametic (XX). We show that most or all of the phenomena associated with HALDANE's rule can be explained by the simple hypothesis that alleles decreasing hybrid fitness are partially recessive. Under this hypothesis, the XY sex suffers more than the XX because X-linked alleles causing postzygotic isolation tend to have greater cumulative effects when hemizygous than when heterozygous, even though the XX sex carries twice as many such alleles. The dominance hypothesis can also account for the "large X effect," the disproportionate effect of the X chromosome on hybrid inviability/sterility. In addition, the dominance theory is consistent with: the long temporal lag between the evolution of heterogametic and homogametic postzygotic isolation, the frequency of exceptions to HALDANE's rule, puzzling Drosophila experiments in which "unbalanced" hybrid females, who carry two X chromosomes from the same species, remain fertile whereas F1 hybrid males are sterile, and the absence of cases of HALDANE's rule for hybrid inviability in mammals. We discuss several novel predictions that could lead to rejection of the dominance theory.
Alleles↗
Does diploidy increase the rate of adaptation?
Explanations of the evolution of diploidy have focused on the advantages gained from masking deleterious alleles. Recent theory has shown, however, that masking does not always provide an advantage to diploidy and would never favor diploidy in predominantly asexual organisms. We explore a neglected alternative theory which posits that, by doubling the genome size, diploids double the rate at which favorable mutations arise. Consequently, the rate of adaptation in diploids is presumed to be faster than in haploids. The rate of adaptation, however, depends not only on the rate of appearance of new favorable mutations but also on the rate at which these mutations are incorporated (which depends on the population size and on the dominance of favorable mutations). We show that, in both asexuals and sexuals, doubling the mutation rate via diploidy often does not accelerate the rate of adaptation. Indeed, under many conditions, diploidy slows adaptation.
Adaptation, Physiological↗
Haldane's rule has multiple genetic causes.
Haldane's rule states that "When in the F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous [heterogametic or XY] sex". This rule represents one of the few patterns characterizing animal speciation. Traditional explanations of Haldane's rule claim that heterogametic hybrids are unfit because they lack an X chromosome that is 'compatible' with the autosomes of one species. Recent work shows that this explanation is incorrect for hybrid sterility: contrary to prediction, homogametic hybrids carrying both X chromosomes from the same species remain fertile. Until now, similar tests have not been performed for hybrid inviability. Here I show that homogametic hybrids who carry both X chromosomes from the same species are inviable. These results show tht the genetic causes of Haldane's rule differ for hybrid sterility versus inviability. Haldane's rule does not, therefore, have a single genetic basis.
Animals↗
Meiotic drive and unisexual hybrid sterility: a comment.
Explore the source record for details and available documents.
Alleles↗
Mapping and characterization of a 'speciation gene' in Drosophila.
Almost nothing is known about the identity of the genes causing reproductive isolation between species. As a first step towards molecular isolation of a 'speciation gene', I mapped and partly characterized a gene causing hybrid male sterility in Drosophila. This analysis shows that sterility of D. melanogaster males who carry the 'dot' fourth chromosome from D. simulans is due entirely to a very small region of the D. simulans chromosome (including only about 5 salivary gland bands or approximately 250 kb of DNA). Thus the hybrid sterility effect of the D. simulans fourth chromosome is almost surely due to a single gene of very large effect (here named hms, hybrid male sterile). Hms is zygotically acting, and the D. simulans allele of hms is completely recessive. Furthermore, complementation tests suggest that hms is not an allele of any known locus in D. melanogaster.
Alleles↗
Loss of a paternal chromosome causes developmental anomalies among Drosophila hybrids.
Hybrids between Drosophila virilis and D. lummei suffer from developmental anomalies. Previous reports also suggest that these hybrids lose the D. lummei sixth chromosome early in development. Genetic and cytological data presented here confirm the loss of the microchromosome from both the soma and the germ-line of these hybrids and provide strong evidence that this loss causes the hybrid developmental anomalies.
Animals↗
A test of Fisher's theory of dominance.
One of the first patterns noticed by geneticists was that mutations are almost always recessive to their wild-type alleles. Several explanations of this striking pattern have been offered. The two most influential are Fisher's theory--which argues that dominance results from natural selection against recurring deleterious mutations--and Wright's theory--which argues that dominance results from the physiology of gene action. The debate over which of these theories is correct represents one of the most protracted controversies in the history of evolutionary biology. Here I test Fisher's theory by assessing the dominance of mutations in an organism that is typically haploid, the alga Chlamydomonas reinhardtii. The results show that mutations are recessive just as often among haploid as among diploid species. This result falsifies Fisher's theory of dominance and provides strong support for the alternative physiological theory.
Alleles↗
Developmental anomalies in Drosophila hybrids are apparently caused by loss of microchromosome.
Hybrids produced by crossing Drosophila virilis females to D. lummei males suffer from many developmental anomalies; the reciprocal hybridization yields normal offspring. Genetic analysis reveals that these anomalies involve a maternal effect: whether or not an individual will show an anomaly depends upon his mother's nuclear genotype. Several lines of evidence suggest that the proximal cause of the anomalies is the elimination of the D. lummei microchromosome (chromosome 6) from hybrids. Loss of the D. lummei microchromosome in this hybridization is known to involve a maternal effect (Evgen'ev, 1973), as mitosis in early development is under the control of maternally-acting genes.
Animals↗
Localization of genes causing postzygotic isolation in two hybridizations involving Drosophila pseudoobscura.
The genes causing postzygotic isolation in two Drosophila hybridizations were localized to regions of the X chromosome. The X has a large effect on D. pseudoobscura pseudoobscura ("U.S.A.")-D. pseudoobscura bogotana ("Bogota") hybrid male sterility. Recombination analysis shows that this effect is due entirely to a small chromosome region representing less than 20 per cent of the X. This result suggests that a single X-linked gene may be involved. A maximum likelihood mapping procedure places this hybrid sterility gene at position 50.3 (95 per cent limits = 46.9-54.4). Analysis also shows that this putative gene has a very large effect on hybrid fitness: substitution of a Bogota for a U.S.A. allele almost halves hybrid male fertility. The X-chromosome also has a large effect on male and female sterility in the D. pseudoobscura-D. persimilis hybridization. Male sterility in this cross appears to involve more X-linked genes than in the younger U.S.A.-Bogota hybridization: genes on both arms of the X are involved. Sterility of females, however, is caused by gene(s) restricted to the left arm of the X. Thus male and female sterility in this hybridization must involve some different loci. This result militates against the traditional explanation of Haldane's rule.
Animals↗
The genetics of postzygotic isolation in the Drosophila virilis group.
In a genetic study of postzygotic reproductive isolation among species of the Drosophila virilis group, we find that the X chromosome has the largest effect on male and female hybrid sterility and inviability. The X alone has a discernible effect on postzygotic isolation between closely related species. Hybridizations involving more distantly related species also show large X-effects, although the autosomes may also play a role. In the only hybridization yet subjected to such analysis, we show that hybrid male and female sterility result from the action of different X-linked loci. Our results accord with genetic studies of other taxa, and support the view that both Haldane's rule (heterogametic F1 sterility or inviability) and the large effect of the X chromosome on reproductive isolation result from the accumulation by natural selection of partially recessive or underdominant mutations. We also describe a method that allows genetic analysis of reproductive isolation between species that produce completely sterile or inviable hybrids. Such species pairs, which represent the final stage of speciation, cannot be analyzed by traditional methods. The X chromosome also plays an important role in postzygotic isolation between these species.
Animals↗
Does postzygotic isolation result from improper dosage compensation?
The X chromosome invariably has the largest effect on postzygotic isolation between animal species. One explanation of this pattern is that inviability and sterility result from a breakdown in the dosage compensation of X-linked genes in hybrids. In Drosophila, such breakdown could result from divergence of the genes used to assess the X/autosomal (X/A) ratio, and thus the sex, of an individual. I test this hypothesis by introducing mutant alleles of the Sex-lethal locus into Drosophila melanogaster-Drosophila simulans hybrids. These mutants "ignore" any perceived anomalous X/A ratio and thus can be used to ensure proper dosage compensation in hybrids. These mutants do not rescue hybrid viability or fertility, implying that postzygotic isolation in this hybridization does not result from a disruption of dosage compensation caused by divergence of the X/A counting system.
Alleles↗
Genetics of male and female sterility in hybrids of Drosophila pseudoobscura and D. persimilis.
The genetic basis of male and female sterility in hybrids of Drosophila pseudoobscura-Drosophila persimilis was studied using backcross analysis. Previous studies indirectly assessed male fertility by measuring testis size; these studies concluded that male sterility results from an X chromosome-autosome imbalance. By directly scoring for the production of motile sperm, male sterility is shown to be largely due to an incompatibility between genes on the X and Y chromosomes of these two species. These species have diverged at a minimum of nine loci affecting hybrid male fertility. Semisterility of hybrid females appears to result from an X chromosome-cytoplasm interaction; the X chromosome thus has the largest effect on sterility in both male and female hybrids. This is apparently the first analysis of the genetic basis of female sterility, or of sterility/inviability affecting both sexes, in an animal hybridization.
Animals↗
The "sizes" of mutations fixed in phenotypic evolution: a response to Clarke and Arthur.
Explore the source record for details and available documents.
Alleles↗