Evolution Of Hybrid Sterility Research Articles

Recurrent gene co-amplification on Drosophila X and Y chromosomes.

Y chromosomes often contain amplified genes which can increase dosage of male fertility genes and counteract degeneration via gene conversion. Here we identify genes with increased copy number on both X and Y chromosomes in various species of Drosophila, a pattern that has previously been associated with sex chromosome drive involving the Slx and Sly gene families in mice. We show that recurrent X/Y co-amplification appears to be an important evolutionary force that has shaped gene content evolution of sex chromosomes in Drosophila. We demonstrate that convergent acquisition and amplification of testis expressed gene families are common on Drosophila sex chromosomes, and especially on recently formed ones, and we carefully characterize one putative novel X/Y co-amplification system. We find that co-amplification of the S-Lap1/GAPsec gene pair on both the X and the Y chromosome occurred independently several times in members of the D. obscura group, where this normally autosomal gene pair is sex-linked due to a sex chromosome—autosome fusion. We explore several evolutionary scenarios that would explain this pattern of co-amplification. Investigation of gene expression and short RNA profiles at the S-Lap1/GAPsec system suggest that, like Slx/Sly in mice, these genes may be remnants of a cryptic sex chromosome drive system, however additional transgenic experiments will be necessary to validate this model. Regardless of whether sex chromosome drive is responsible for this co-amplification, our findings suggest that recurrent gene duplications between X and Y sex chromosomes could have a widespread effect on genomic and evolutionary patterns, including the epigenetic regulation of sex chromosomes, the distribution of sex-biased genes, and the evolution of hybrid sterility.

Hybrid sterility increases with genetic distance in snubnose darters (Percidae: Etheostoma)

The process of speciation is often synonymous with the evolution of reproductive isolation, and the tempo at which reproductive barriers evolve can provide insight into the underlying mechanisms of divergence. Darters are a diverse group of North American freshwater fish in which behavioral isolation appears to evolve rapidly; however, little is known about hybrid sterility among darter species. Here, six allopatric pairs of darter species were hybridized via in vitro fertilization and offspring were reared to reproductive age. Hybrid sterility appears more pronounced in male hybrids. Additionally, levels of hybrid sterility increase with genetic distance across species pairs. Understanding sex determination and sex-specific gene expression in darters will provide further insight into the evolution of hybrid sterility.

Genome diversity and divergence in Drosophila mauritiana: multiple signatures of faster X evolution.

Drosophila mauritiana is an Indian Ocean island endemic species that diverged from its two sister species, Drosophila simulans and Drosophila sechellia, approximately 240,000 years ago. Multiple forms of incomplete reproductive isolation have evolved among these species, including sexual, gametic, ecological, and intrinsic postzygotic barriers, with crosses among all three species conforming to Haldane’s rule: F1 hybrid males are sterile and F1 hybrid females are fertile. Extensive genetic resources and the fertility of hybrid females have made D. mauritiana, in particular, an important model for speciation genetics. Analyses between D. mauritiana and both of its siblings have shown that the X chromosome makes a disproportionate contribution to hybrid male sterility. But why the X plays a special role in the evolution of hybrid sterility in these, and other, species remains an unsolved problem. To complement functional genetic analyses, we have investigated the population genomics of D. mauritiana, giving special attention to differences between the X and the autosomes. We present a de novo genome assembly of D. mauritiana annotated with RNAseq data and a whole-genome analysis of polymorphism and divergence from ten individuals. Our analyses show that, relative to the autosomes, the X chromosome has reduced nucleotide diversity but elevated nucleotide divergence; an excess of recurrent adaptive evolution at its protein-coding genes; an excess of recent, strong selective sweeps; and a large excess of satellite DNA. Interestingly, one of two centimorgan-scale selective sweeps on the D. mauritiana X chromosome spans a region containing two sex-ratio meiotic drive elements and a high concentration of satellite DNA. Furthermore, genes with roles in reproduction and chromosome biology are enriched among genes that have histories of recurrent adaptive protein evolution. Together, these genome-wide analyses suggest that genetic conflict and frequent positive natural selection on the X chromosome have shaped the molecular evolutionary history of D. mauritiana, refining our understanding of the possible causes of the large X-effect in speciation.

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

Genetic conflict and sex chromosome evolution

Chromosomal sex determination systems create the opportunity for the evolution of selfish genetic elements that increase the transmission of one sex chromosome at the expense of its homolog. Because such selfish elements on sex chromosomes can reduce fertility and distort the sex ratio of progeny, unlinked suppressors are expected to evolve, bringing different regions of the genome into conflict over the meiotic transmission of the sex chromosomes. Here we argue that recurrent genetic conflict over sex chromosome transmission is an important evolutionary force that has shaped a wide range of seemingly disparate phenomena including the epigenetic regulation of genes expressed in the germline, the distribution of genes in the genome, and the evolution of hybrid sterility between species.

Speciation through evolution of sex-linked genes

Identification of genes involved in reproductive isolation opens novel ways to investigate links between stages of the speciation process. Are the genes coding for ecological adaptations and sexual isolation the same that eventually lead to hybrid sterility and inviability? We review the role of sex-linked genes at different stages of speciation based on four main differences between sex chromosomes and autosomes; (1) relative speed of evolution, (2) non-random accumulation of genes, (3) exposure of incompatible recessive genes in hybrids and (4) recombination rate. At early stages of population divergence ecological differences appear mainly determined by autosomal genes, but fast-evolving sex-linked genes are likely to play an important role for the evolution of sexual isolation by coding for traits with sex-specific fitness effects (for example, primary and secondary sexual traits). Empirical evidence supports this expectation but mainly in female-heterogametic taxa. By contrast, there is clear evidence for both strong X- and Z-linkage of hybrid sterility and inviability at later stages of speciation. Hence genes coding for sexual isolation traits are more likely to eventually cause hybrid sterility when they are sex-linked. We conclude that the link between sexual isolation and evolution of hybrid sterility is more intuitive in male-heterogametic taxa because recessive sexually antagonistic genes are expected to quickly accumulate on the X-chromosome. However, the broader range of sexual traits that are expected to accumulate on the Z-chromosome may facilitate adaptive speciation in female-heterogametic species by allowing male signals and female preferences to remain in linkage disequilibrium despite periods of gene flow.

The genetics of reproductive isolation in the Drosophila simulans clade: X vs. autosomal effects and male vs. female effects.

A strong effect of homozygous autosomal regions on reproductive isolation was found for crosses between the species in the Drosophila simulans clade. Second chromosome regions were introgressed from D. mauritiana and D. sechellia into D. simulans and tested for their homozygous effects on hybrid male and hybrid female sterility and inviability. Most introgressions are fertile as heterozygotes, yet produce sterile male offspring when made homozygous. The density of homozygous autosomal factors contributing to hybrid male sterility is comparable to the density of X chromosome factors for this level of resolution. Female sterility was also revealed, yet the disparity between male and female levels of sterility was great, with male sterility being up to 23 times greater than female sterility. Complete hybrid inviability was also associated with some regions of the second chromosome, yet there were no strong sex differences. In conclusion, we find no evidence to support a strong X chromosome bias in the evolution of hybrid sterility or inviability but do find a very strong sex bias in the evolution of hybrid sterility. In light of these findings, we reevaluate the current models proposed to explain the genetic pattern of reproductive isolation.