Evolution Of Hybrid Incompatibilities Research Articles

Hybrid Sterility, Genetic Conflict and Complex Speciation: Lessons From the Drosophila simulans Clade Species.

The three fruitfly species of the Drosophila simulans clade— D. simulans, D. mauritiana, and D. sechellia— have served as important models in speciation genetics for over 40 years. These species are reproductively isolated by geography, ecology, sexual signals, postmating-prezygotic interactions, and postzygotic genetic incompatibilities. All pairwise crosses between these species conform to Haldane’s rule, producing fertile F1 hybrid females and sterile F1 hybrid males. The close phylogenetic proximity of the D. simulans clade species to the model organism, D. melanogaster, has empowered genetic analyses of their species differences, including reproductive incompatibilities. But perhaps no phenotype has been subject to more continuous and intensive genetic scrutiny than hybrid male sterility. Here we review the history, progress, and current state of our understanding of hybrid male sterility among the D. simulans clade species. Our aim is to integrate the available information from experimental and population genetics analyses bearing on the causes and consequences of hybrid male sterility. We highlight numerous conclusions that have emerged as well as issues that remain unresolved. We focus on the special role of sex chromosomes, the fine-scale genetic architecture of hybrid male sterility, and the history of gene flow between species. The biggest surprises to emerge from this work are that (i) genetic conflicts may be an important general force in the evolution of hybrid incompatibility, (ii) hybrid male sterility is polygenic with contributions of complex epistasis, and (iii) speciation, even among these geographically allopatric taxa, has involved the interplay of gene flow, negative selection, and positive selection. These three conclusions are marked departures from the classical views of speciation that emerged from the modern evolutionary synthesis.

Gene duplicates cause hybrid lethality between sympatric species of Mimulus.

Hybrid incompatibilities play a critical role in the evolution and maintenance of species. We have discovered a simple genetic incompatibility that causes lethality in hybrids between two closely related species of yellow monkeyflower (Mimulus guttatus and M. nasutus). This hybrid incompatibility, which causes one sixteenth of F2 hybrid seedlings to lack chlorophyll and die shortly after germination, occurs between sympatric populations that are connected by ongoing interspecific gene flow. Using complimentary genetic mapping and gene expression analyses, we show that lethality occurs in hybrids that lack a functional copy of the critical photosynthetic gene pTAC14. In M. guttatus, this gene was duplicated, but the ancestral copy is no longer expressed. In M. nasutus, the duplication is missing altogether. As a result, hybrids die when they are homozygous for the nonfunctional M. guttatus copy and missing the duplicate from M. nasutus, apparently due to misregulated transcription of key photosynthetic genes. Our study indicates that neutral evolutionary processes may play an important role in the evolution of hybrid incompatibilities and opens the door to direct investigations of their contribution to reproductive isolation among naturally hybridizing species.

Evolution and Molecular Control of Hybrid Incompatibility in Plants.

Postzygotic reproductive isolation (RI) plays an important role in speciation. According to the stage at which it functions and the symptoms it displays, postzygotic RI can be called hybrid inviability, hybrid weakness or necrosis, hybrid sterility, or hybrid breakdown. In this review, we summarized new findings about hybrid incompatibilities in plants, most of which are from studies on Arabidopsis and rice. Recent progress suggests that hybrid incompatibility is a by-product of co-evolution either with “parasitic” selfish elements in the genome or with invasive microbes in the natural environment. We discuss the environmental influences on the expression of hybrid incompatibility and the possible effects of environment-dependent hybrid incompatibility on sympatric speciation. We also discuss the role of domestication on the evolution of hybrid incompatibilities.

The limited contribution of reciprocal gene loss to increased speciation rates following whole-genome duplication.

Hybrid incompatibilities contribute to reproductive isolation between species, allowing them to follow independent evolutionary trajectories. Since hybrid incompatibilities are by definition deleterious, they cannot be selected for directly and must arise as a by-product of evolutionary divergence. Divergent resolution of duplicate genes, a special case of Dobzhansky-Muller incompatibilities, is one mechanism by which hybrid incompatibility can evolve. Following whole-genome duplication, loss of gene copies could possibly increase the opportunity for divergent resolution and, hence, the evolution of hybrid incompatibilities. However, divergent resolution can take place only when populations are isolated in allopatry; genes lost within a species cannot contribute to future speciation. Furthermore, nearly complete allopatry is necessary for passive divergent resolution. Using mathematical models, we demonstrate that these two factors severely impede the ability of divergent resolution alone to increase speciation rates, except under very particular conditions. Instead, we find that the population dynamics of diverging lineages dominate this process, leading to a larger role for ecology relative to genetics in the origin of new species, even by passive mechanisms. Divergent resolution of duplicate genes might increase speciation rates in some clades at some times, but our results indicate that it alone is unlikely to account for the macroevolutionary success of polyploid clades.

Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus.

Author SummaryAdaptive evolution by natural selection is the primary force generating biological diversity. A critical question is whether the evolution of hybrid incompatibility, which is essential for the maintenance of species diversity, is caused by adaptive evolution. In this article, we investigate one of the most widely cited examples of ecological divergence driving the evolution of reproductive incompatibility, the strong association between hybrid lethality and copper tolerance in a copper mine population of the wildflower Mimulus guttatus. Hybrid lethality and tolerance of high levels of copper co-segregate as a single Mendelian locus. While copper tolerance and hybrid lethality are nearly universal in the mine population at Copperopolis, California, they are absent from adjacent off-mine populations, suggesting that reproductive isolation evolved rapidly as a pleiotropic by-product of recent adaptation to the mine environment. We find that copper tolerance and hybrid lethality are controlled by distinct loci, in tight genetic linkage. We also demonstrate that this genomic region has experienced strong recent selection and conclude that ecological selection for copper tolerance indirectly caused the neighboring hybrid lethality allele to hitchhike to high frequency. To our knowledge, this is the first case to demonstrate that reproductive isolation factors can evolve as an incidental by-product of adaptation to novel environments through genetic hitchhiking.

The genetics of sex chromosomes: evolution and implications for hybrid incompatibility.

Heteromorphic sex chromosomes, where one sex has two different types of sex chromosomes, face very different evolutionary consequences than do autosomes. Two important features of sex chromosomes arise from being present in only one copy in one of the sexes: dosage compensation and the meiotic silencing of sex chromosomes. Other differences arise because sex chromosomes spend unequal amounts of time in each sex. Thus, the impact of evolutionary processes (mutation, selection, genetic drift, and meiotic drive) differs substantially between each sex chromosome, and between the sex chromosomes and the autosomes. Sex chromosomes also play a disproportionate role in Haldane's rule and other important patterns related to hybrid incompatibility, and thus speciation. We review the consequences of sex chromosomes on hybrid incompatibility. A theme running through this review is that epigenetic processes, notably those related to chromatin, may be more important to the evolution of sex chromosomes and the evolution of hybrid incompatibility than previously recognized.

Darwinian Thinking: 150 Years after The Origin

hypothesis that adaptive divergence leads to speciation and to the evolution of traits and behaviors that influence the prospects for species coexistence. A key issue here is the role of character displacement in the origin and mainte- nance of diversity. Pfennig and Pfennig find substantial evidence that character displacement plays an important role in the evolution of species interactions and identify a number of additional areas that Darwin had not con- sidered, including sexual selection and phenotypic plas- ticity. Their paper clearly illustrates how Darwin's original observations continue to shape our thinking on the in- terface between ecology, behavior, and evolution. Of the many insightful observations presented in The Origin, perhaps none is more remarkable than Darwin's discussion of the evolution of hybrid sterility. He under- stood that sterility could not have evolved as an adaptation of individual species and that interactions in the hybrids stemming from the contributions of each parent caused incompatibilities, but without today's specific knowledge of genetics, he was unable to reach a satisfactory expla- nation. Presgraves (2010) reviews this topic in detail, in- cluding an historical perspective on the contributions by Darwin, Muller, and Dobzhansky to the problem. He also provides an overview of the recent advances in our un- derstanding of the genetic mechanisms that contribute to the evolution of hybrid incompatibilities. This includes evidence that genetic conflict, and not adaptive divergence, may be a primary cause of hybrid sterility and inviability. Darwin considered multiple sources of evidence to gain support for his theory of natural selection, including the evolution of both living and extinct organisms. Hunt (2010) describes Darwin's attempts to use the fossil record to test the hypothesis that evolution by natural selection is a gradual process. Darwin argued at the time that the record was too incomplete to provide an adequate test. Hunt reviews the current paleontological record and con- cludes that over short periods, rates of morphological evo- lution are sometimes considerably faster than Darwin had proposed. Sticklebacks provide a particularly illustrative case, where a nearly continuous record extending over the last 10 million years shows that most phenotypic evolution occurred over a brief period of approximately 1,000 gen- erations. Moreover, for a wide variety of organisms and

Functional divergence caused by ancient positive selection of a Drosophila hybrid incompatibility locus.

Interspecific hybrid lethality and sterility are a consequence of divergent evolution between species and serve to maintain the discrete identities of species. The evolution of hybrid incompatibilities has been described in widely accepted models by Dobzhansky and Muller where lineage-specific functional divergence is the essential characteristic of hybrid incompatibility genes. Experimentally tractable models are required to identify and test candidate hybrid incompatibility genes. Several Drosophila melanogaster genes involved in hybrid incompatibility have been identified but none has yet been shown to have functionally diverged in accordance with the Dobzhansky-Muller model. By introducing transgenic copies of the X-linked Hybrid male rescue (Hmr) gene into D. melanogaster from its sibling species D. simulans and D. mauritiana, we demonstrate that Hmr has functionally diverged to cause F1 hybrid incompatibility between these species. Consistent with the Dobzhansky-Muller model, we find that Hmr has diverged extensively in the D. melanogaster lineage, but we also find extensive divergence in the sibling-species lineage. Together, these findings implicate over 13% of the amino acids encoded by Hmr as candidates for causing hybrid incompatibility. The exceptional level of divergence at Hmr cannot be explained by neutral processes because we use phylogenetic methods and population genetic analyses to show that the elevated amino-acid divergence in both lineages is due to positive selection in the distant past—at least one million generations ago. Our findings suggest that multiple substitutions driven by natural selection may be a general phenomenon required to generate hybrid incompatibility alleles.

Multiplicity of infection and the evolution of hybrid incompatibility in segmented viruses.

Some viral genomes are divided into segments. When multiple viruses infect a single cell, progeny form by reassorted mixtures of genomic segments. Hybrid incompatibilities arise when a progeny virus has incompatible segments from different parental viruses. Hybrid incompatibility has been observed in influenza and in the multiparticle plant virus Dianthovirus. Hybrid incompatibility provides an opportunity to study rates of viral evolution, divergence and speciation, and the extent of epistatic interactions among components of the viral genome. This paper presents mathematical and computer simulation models to study hybrid incompatibility between diverging strains. The models identify multiplicity of infection as a key factor. When many viral particles infect each host cell, the effective ploidy of the genetic system is high. High ploidy dilutes the contribution of each locus to the phenotype, weakening the selective intensity on each locus. Weaker selection on variant alleles allows the population to maintain greater genetic diversity and to be more easily perturbed by stochastic fluctuations. Greater diversity and stochastic fluctuations explore more widely the space of epistatic interactions, causing more frequent shifts among favoured combinations of alleles. Variable ploidy of viral genetics differs from standard Mendelian genetics.

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.