About this Journal Submit a Manuscript Table of Contents
International Journal of Evolutionary Biology
Volume 2012 (2012), Article ID 301894, 9 pages
http://dx.doi.org/10.1155/2012/301894
Review Article

Chromatin Evolution and Molecular Drive in Speciation

Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8572, Japan

Received 14 July 2011; Accepted 5 October 2011

Academic Editor: Chau-Ti Ting

Copyright © 2012 Kyoichi Sawamura. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Are there biological generalities that underlie hybrid sterility or inviability? Recently, around a dozen “speciation genes” have been identified mainly in Drosophila, and the biological functions of these genes are revealing molecular generalities. Major cases of hybrid sterility and inviability seem to result from chromatin evolution and molecular drive in speciation. Repetitive satellite DNAs within heterochromatin, especially at centromeres, evolve rapidly through molecular drive mechanisms (both meiotic and centromeric). Chromatin-binding proteins, therefore, must also evolve rapidly to maintain binding capability. As a result, chromatin binding proteins may not be able to interact with chromosomes from another species in a hybrid, causing hybrid sterility and inviability.

1. Introduction

Are there biological generalities that underlie hybrid sterility or inviability? In other words, do common mechanisms dictate that mules and leopons, for example, are sterile? The widely accepted Dobzhansky-Muller incompatibility (DMI) model of reproductive isolation [1, 2] does not provide an answer to this question. Instead, the DMI model only predicts that combinations of incompatible genes from different species lead to sterile or inviable hybrids. According to Mayr [3], reproductive isolation is an accidental byproduct of speciation. Recently, around a dozen “speciation genes” have been identified, and the biological functions of these genes are revealing molecular generalities that control hybrid sterility and inviability [48] (but see [9]). They are chromatin evolution and molecular drive in speciation.

Dover [10] argues, “In the case of many families of genes and noncoding sequences…, fixation of mutations within a population may proceed as a consequence of molecular mechanisms of turnover within the genome [i.e., molecular drive]. …There are circumstances in which the unusual concerted pattern of fixation permits the establishment of biological novelty and species discontinuities [i.e., reproductive isolation]…” Genes encoding heterochromatin proteins may have evolved rapidly to counteract mutations within repetitive DNA sequences in heterochromatin, which accumulate by molecular drive. The molecular drive theory once dominated the field of speciation, supported by the discovery that selfish transposable elements cause hybrid dysgenesis [1114]. However, this hypothesis has been discounted, as there is no direct evidence that transposons are involved in reproductive isolation [15, 16] (but see [17, 18]). Even the most contemporary textbook concerning speciation [19] does not cite the Dover’s [10].

2. Lhr and Hmr of Drosophila

When Drosophila melanogaster females mate with Drosophila simulans males, only weak, sterile, female hybrids eclose, as male hybrids die during larval stages [20]. Watanabe [21] discovered a D. simulans mutation, Lethal hybrid rescue (Lhr), that prevents hybrid larval lethality and restores female hybrid vigor [22]. It was thought that the wild-type allele of D. simulans Lhr was incompatible with X-linked genes from D. melanogaster. It has since been demonstrated that Lhr encodes a heterochromatin protein, HP3, which contains a boundary element-associated factor 32/Su(var)3-7/Stonewall (BESS) domain [2325]. The X-linked Hybrid male rescue (Hmr) of D. melanogaster [26] has an effect similar to Lhr when mutated, and it also restores female hybrid fertility in this context [27]. Hmr encodes a DNA-binding protein with two myb/SANT-like in Adf-1 (MADF) domains [28].

LHR and HMR may physically interact through their BESS and MADF domains and may colocalize to specific chromatin regions. LHR also interacts with the heterochromatin proteins HP1 and HP6, as demonstrated by yeast two-hybrid (Y2H) experiments, RNA interference (RNAi) knockdown, and Bayesian network analysis [23, 25, 2931]. The ratio of the number of nonsynonymous substitutions per nonsynonymous site to the number of synonymous substitutions per synonymous site (Ka/Ks) [32] and McDonald-Kreitman (MK) test [33] indicate that Hmr and a subset of genes encoding heterochromatin proteins (including Lhr and HP6) have evolved under positive selection [23, 28, 31, 34]. The involvement of Lhr and Hmr in reproductive isolation is reminiscent of speciation mediated by molecular drive. A comprehensive analysis of LHR, but not HMR, binding sites in the genome has been performed [35].

3. zhr of Drosophila

Involvement of heterochromatic repetitive sequences in hybrid inviability is evident when crosses between D. simulans females and D. melanogaster males (reciprocal to the cross discussed above) are analyzed. Progeny from this cross are sterile, male hybrids, as most female hybrids die during embryogenesis [20, 36]. We discovered zygotic hybrid rescue (zhr), a D. melanogaster gene that prevents female embryonic lethality in this context [37]. Genetic analyses using chromosome deficiencies and duplications [3840] indicate that female hybrids are rescued if the number of 359-bp repetitive sequences (1.688 satellite) on the D. melanogaster X chromosome is decreased. In addition, hybrids of both sexes are inviable when repetitive sequences are added. In embryos from D. simulans mothers, chromatin regions rich in the 1.688 satellite are not properly condensed [41], resulting in mitotic defects such as chromosome bridges and irregularly spaced nuclei [41, 42].

The 1.688 satellite was one of the earliest sequences cloned in Drosophila [43, 44] and represents more than 4% of the D. melanogaster genome [4547]. Related sequences are present in D. simulans, but the homology is low [4851]. Heterochromatin regions rich in the 1.688 satellite may represent binding sites for the putative HMR/LHR complex. However, because zhr only affects hybrid viability when D. simulans females are crossed to D. melanogaster males (not the reciprocal cross), the larval and embryonic hybrid-inviability phenotypes associated with these crosses were thought to be independent (see [37, 52] for additional evidence). However, the possibility remains that female hybrids from D. melanogaster mothers are viable because proteins necessary to cope with D. melanogaster heterochromatin on the X chromosome are supplied maternally. This explanation is consistent with the model proposed by [53, 54]. Identification of proteins that bind to the 1.688 heterochromatin satellite will be informative [5558]. maternal hybrid rescue (mhr) of D. simulans [52] and Simulans hybrid females rescue (Shfr) [59] represent loci encoding strong 1.688-binding candidates.

Although the 1.688 satellite does not seem to encode any proteins, it is transcribed in ovaries and silenced by the RNAi machinery. This silencing is mediated by repeat-associated small interfering RNA, also called Piwi-associated RNA [60]. In hybrids, failure to silence the 1.688 satellite may lead to heterochromatin decondensation and lethality [54]. Finally, the hybrid lethal on the X (hlx) locus of D. mauritiana affects viability of D. simulans hybrids and has been mapped to heterochromatin [61]. It will be interesting to determine whether this locus also consists of repetitive sequences, similar to zhr.

4. OdsH of Drosophila

In reciprocal crosses between D. mauritiana and D. simulans, female hybrids are fertile but male hybrids are sterile [62]. Many genes have been identified that affect this male hybrid sterility (for a review see [63]). These loci are scattered throughout the two genomes, but an X-linked gene, Odysseus (Ods), plays a particularly important role. When the D. mauritiana allele of Ods is cointrogressed with a closely linked gene onto the D. simulans genetic background, males become sterile [64, 65]. This hybrid male sterility gene has been isolated as Ods-site homeobox (OdsH) [66]. OdsH is paralogous to uncoordinated-4 (unc-4), which is expressed in postmitotic neurons and epidermal cells [67]. In Drosophila, OdsH is thought to have arisen through gene duplication and neofunctionalization, thereby assuming a novel role in spermatogenesis [66, 68, 69]. Ample evidence suggests that OdsH, especially its DNA-binding homeodomain, has evolved under positive selection [66, 69]. Four genes downregulated in sterile male hybrids are thought to lie downstream of OdsH [70]. And misexpressed genes are disproportionately more common on autosomes than on the X in the males with OdsH introgression [71]. Regulatory regions of these genes may contain binding sites for the OdsH transcription factor.

Alternatively, but not mutually exclusively, Bayes and Malik [72] suggested that the ODSH protein localizes to evolutionarily dynamic loci in heterochromatin and that ODSH abundance and localization during premeiotic phases of spermatogenesis are different between D. simulans and D. mauritiana. ODSH from D. mauritiana associates with the heterochromatic Y chromosome of D. simulans, leading to decondensation and male hybrid sterility [72]. These data reveal that rapid heterochromatin evolution affects the onset of male hybrid sterility [72], in addition to hybrid inviability [37, 41]. However, it remains unclear which DNA sequences ODSH binds with the highest affinity.

5. Nup160 and Nup96 of Drosophila

The discovery of strains that restore the fertility of D. simulans/D. melanogaster female hybrids [73] provided the tools to introgress D. simulans chromosomal segments onto the D. melanogaster genetic background [74]. Both male and female introgression homozygotes successfully made were sterile, and the genes responsible for the male and female sterility have been mapped [7577]. Among them, Nucleoporin 160 (Nup160) of D. simulans was identified as the gene underlying female sterility on the D. melanogaster genetic background [78]. Both D. simulans Nup160 and Nucleoporin 96 (Nup96), which also encodes a component protein of the nuclear pore complex (NPC), cause inviability in D. melanogaster/D. simulans male hybrids [7880]. This is independent of the F1 hybrid inviability that can be rescued by Lhr mutation and is only revealed in introgression bearers or hemizygotes made from D. melanogaster deficiencies [81, 82].

Population genetics studies have indicated that positive selection is operating in seven nucleoporin genes, including Nup160 and Nup96 [79, 80, 83] and have revealed significant correlated evolution between them [84]. Several hypotheses have been proposed for why nucleoporins are evolving so rapidly in Drosophila [7880, 83], but here I will focus on the hypothesis most highly related to the molecular drive theory. The NPC forms channels that allow transport of macromolecules between the nucleus and cytoplasm (for a recent review see [85]). In addition, NPC components also function in kinetochore/spindle formation and transcriptional regulation (i.e., dosage compensation) [8691]. The evolution of scaffold nucleoporins (the NUP107-160 complex) may have accelerated to recognize repetitive sequences in centromeric heterochromatin. In this way, incompatible NPCs may result in hybrid sterility and inviability through improper kinetochore formation. Alternatively, small RNAs derived from repetitive DNA sequences may not be properly trafficked in cells with incompatible NPCs. This leads to chromatin decondensation and, ultimately, sterility or inviability. Such a model has been proposed in the meiotic drive system of D. melanogaster (see below). In this case, mislocalized and truncated Ran GTPase Activating Protein (RanGAP), which is encoded by Segregation distortion (Sd) [92], disrupts proper nuclear transport of small RNAs derived from Responder (Rsp) and ribonucleoprotein complexes that are required to suppress the Rsp satellites [54, 93].

6. Prdm9 of Mice

Evidence for chromatin mechanisms in speciation is not restricted to Drosophila. In the cross between Mus musculus musculus and M. m. domesticus, female hybrids are fertile, but male hybrids are sterile (for a review see [94]; see also [95, 96]). Backcross analyses have indicated that three or more independently segregating loci are involved in this male hybrid sterility. One gene, Hybrid sterility 1 (Hst1) of M. m. domesticus, is polymorphic: the Hst1s allele causes sterility, but Hst1f does not [97]. This situation is similar to the hybrid rescue mutations in Drosophila. The Hst1 locus was mapped to the PR domain zinc finger protein 9 (Prdm9) gene, where PR stands for PRDIBF1 and RIZ homology. Prdm9 encodes a histone H3 lysine 4 (H3K4) trimethyltransferase [98], which is also known as the Meisetz, meiosis-induced factor containing a PR/SET domain and a zinc-finger motif [99]. Hybrid males sterilized by the Prdm9 introgression exhibit frequent dissociation of the X and Y chromosomes during meiosis [98], similar to the sterile male hybrid from a cross between M. m. musculus and M. spretus [100102]. A gene involved in M. musculus/M. spretus male hybrid sterility and a gene responsible for X-Y dissociation in M. m. musculus/M. m. molossinus hybrid males (the latter termed Sex-chromosome association (Sxa)) have been mapped to the pseudoautosomal region of the X chromosome [103, 104]. The heterochromatin content of this region is quantitatively different among species or subspecies [105, 106].

The DNA-binding domain of PRDM9 consists of multiple, tandem C2H2 zinc finger domains and is evolving rapidly under positive selection in diverse metazoans, including rodents and primates. Rapid evolution of this binding domain likely results from recurrent selection for binding specificity to satellite DNAs [107109]. The interaction between PRDM9 and repetitive sequences also affects meiotic recombination [110112]. Histone H3 modifications are typical epigenetic events that determine chromatin status (for reviews see [113, 114]). Genomic regions characterized by heterochromatin-mediated gene silencing are rich in histone H3K9 methylation and have few histone acetylations. In contrast, histones in transcriptionally active euchromatic regions are highly acetylated and methylated at H3K4. Interestingly, chromatin structures regulated by H3K9 methylation, Su(var)3-9, HP1, or the RNAi pathway are required to maintain the structural integrity of tandemly repeated, heterochromatic sequences, like the 1.688 satellite, in D. melanogaster [115].

7. Three Drives in Speciation

The meiotic drive model of male hybrid sterility assumes an arms race between meiotic drive genes and suppressor genes in which male hybrids exhibit segregation distortion or sterility if they inherit drive genes, but not their corresponding suppressors [116, 117]. At first, this model was not accepted because cryptic segregation distortion was not detected in interspecies crosses of Drosophila [118, 119]. In the cross between D. mauritiana and D. simulans, one gene involved in male hybrid sterility is not separable from the meiotic drive gene, too much yin (tmy), by recombination [120]. In addition, the gene Overdrive (Ovd) causes both male hybrid sterility and meiotic drive in aged males when D. pseudoobscura pseudoobscura is crossed with D. p. bogotana [121, 122]. Interestingly, Ovd encodes a protein that contains a MADF DNA-binding domain [122], similar to HMR of D. melanogaster [28].

In the context of speciation, meiotic drive can be the manifestation of molecular drive. The most common example of this phenomenon is centromere drive. The centromere drive model assumes that both DNA and protein components of centromeric chromatin are evolving rapidly and that incompatibilities between rapidly evolving centromeric components may be responsible for hybrid sterility [123]. In particular, the expansion of centromeric repetitive sequences provides more microtubule attachment sites, thereby creating a stronger centromere that tends to be included in the oocyte nucleus [123]. This represents an alternative force from molecular drive that is distinct from a variety of mutational processes that include replication slippage, unequal exchange, transposition, and excision [10, 124126]. To suppress potential nondisjunction of chromosomes that carry expanded satellite DNAs, the gene centromere identifier (cid) has evolved rapidly in diverse organisms including Drosophila [127, 128]. cid encodes centromeric histone H3-like, a homologue of human Centromere protein A (CENP-A). Examples of centromeric repeats affecting meiotic drive include the Rsp locus of D. melanogaster, which is the target of Sd [129], and the Cent728 repeat, which is responsible for female meiotic drive in the Monkeyflower hybrid between Mimulus guttatus and Mimulus nasutus [130].

8. Applicability and Related Issues

Above I proposed a theory that hybrid sterility and inviability are generally the manifestation of chromatin evolution and molecular drive in the context of speciation, but I do not claim that this model explains every case. Among hybrid incompatibility genes discussed in recent review papers, only 10 of 18 (Table  1 of [5]), 8 of 14 (Table  1 of [6]), and 7 of 14 (Table  S1 of [9]) are consistent with this theory. In addition, as most hybrid incompatibility data are from Drosophila, a different trend may appear if reproductive isolation genes are identified from diverse taxa. A famous exception to this theory involves the JYalpha gene in Drosophila. JYalpha encodes a protein with sodium/potassium-exchanging ATPase activity and is located on chromosome 4 in D. melanogaster but on chromosome 3 in D. simulans. Therefore, males carrying homozygous introgression of D. simulans chromosome 4 on the D. melanogaster genetic background are sterile, as they do not inherit JYalpha from either species [131133]. This is an example of male hybrid sterility caused by gene transposition between species, which is consistent with the gene duplication and nonfunctionalization model of speciation [134].

Haldane’s rule is generally observed when hybrid sterility and inviability are encountered. This 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 (XY or ZW)] sex” [135]. This rule is empirical and seems to be a composite phenomenon [136138], although the dominance theory is applicable in most cases [139]. Here I propose an additional explanation for Haldane’s rule, based on chromatin evolution and molecular drive in speciation. In hybrid animals, chromatin-binding proteins supplied from one species may not be able to recognize the other species’ Y or W chromosome, as these chromosomes are generally heterochromatic and have high levels of repetitive satellite DNAs. This results in meiotic or mitotic chromosome decondensation or nondisjunction and leads to hybrid sterility or inviability in the heterogametic sex.

There are several chromatin state systems that have not been discussed yet, which may be related to the present issue. First, inactivation of the X chromosome in primary spermatocytes is necessary for the normal progression of spermatogenesis in heterogametic (XY) males [140] (but see [141, 142]), a process termed meiotic sex chromosome inactivation (MSCI). In some cases, male hybrid sterility may result from ineffective MSCI, as DNA-binding proteins may not be able to recognize and inactivate X chromosomes from different species (e.g., [63, 102]). Second, genomic imprinting affects a subset of genes, resulting in monoallelic and parent-of-origin-specific expression. This process usually depends on DNA methylation or histone modification (e.g., [143146]). Species-specific variations in epigenetic marks may disrupt imprinting and lead to hybrid inviability. This can explain classic observations of unilateral incompatibility in rodent and flowering plant species (e.g., [147150]).

9. Conclusion

As has been discussed in this paper, major cases of hybrid sterility and inviability seem to result from chromatin evolution and molecular drive in speciation (Table 1). Repetitive satellite DNAs within heterochromatin, especially at centromeres, evolve rapidly through molecular drive mechanisms (both meiotic and centromeric). Chromatin-binding proteins, therefore, must also evolve rapidly to maintain binding capability. As a result, chromatin-binding proteins may not be able to interact with chromosomes from another species in a hybrid, causing hybrid sterility and inviability (Figure 1).

tab1
Table 1: Hybrid incompatibility genes mentioned in the current paper. Whether data concerning these genes are consistent or inconsistent with the current hypothesis is indicated.
301894.fig.001
Figure 1: A hybrid sterility and inviability model based on chromatin evolution and molecular drive in speciation. Repetitive satellite DNAs evolve rapidly, thereby accelerating the evolution of chromatin-binding proteins (from the common ancestor to species 1 and species 2). Hybrids are sterile or inviable because the chromatin-binding proteins from species 2 cannot recognize the repetitive sequences of species 1.

Acknowledgment

The author’s current study is supported by a Grant-in-Aid for Scientific Research (21570001) from the Japan Society for the Promotion of Science.

References

  1. T. Dobzhansky, Genetics and the Origin of Species, Columbia University Press, New York, NY, USA, 1937.
  2. H. J. Muller, “Bearing of the Drosophila work on systematics,” in The New Systematics, J. S. Huxley, Ed., pp. 185–268, Claredon Press, Oxford, UK, 1940.
  3. E. Mayr, Systematics and the Origin of Species, Columbia University Press, New York, NY, USA, 1942.
  4. P. Michalak, “Epigenetic, transposon and small RNA determinants of hybrid dysfunctions,” Heredity, vol. 102, no. 1, pp. 45–50, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. N. A. Johnson, “Hybrid incompatibility genes: remnants of a genomic battlefield?” Trends in Genetics, vol. 26, no. 7, pp. 317–325, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. D. C. Presgraves, “The molecular evolutionary basis of species formation,” Nature Reviews Genetics, vol. 11, no. 3, pp. 175–180, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. S. R. McDermott and M. A. F. Noor, “The role of meiotic drive in hybrid male sterility,” Philosophical Transactions of the Royal Society B, vol. 365, no. 1544, pp. 1265–1272, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. C. D. Meiklejohn and Y. Tao, “Genetic conflict and sex chromosome evolution,” Trends in Ecology and Evolution, vol. 25, no. 4, pp. 215–223, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. P. Nosil and D. Schluter, “The genes underlying the process of speciation,” Trends in Ecology and Evolution, vol. 26, no. 4, pp. 160–167, 2011.
  10. G. Dover, “Molecular drive: a cohesive mode of species evolution,” Nature, vol. 299, no. 5879, pp. 111–117, 1982. View at Publisher · View at Google Scholar · View at Scopus
  11. W. R. Engels and C. R. Preston, “Hybrid dysgenesis in Drosophila melanogaster: the biology of female and male sterility,” Genetics, vol. 92, no. 1, pp. 161–174, 1979. View at Scopus
  12. W. F. Doolittle and C. Sapienza, “Selfish genes, the phenotype paradigm and genome evolution,” Nature, vol. 284, no. 5757, pp. 601–603, 1980. View at Scopus
  13. M. G. Kidwell, “Intraspecific hybrid sterility,” in The Genetics and Biology of Drosophila, M. Ashburner, H. L. Carson, and J. N. Thompson Jr., Eds., vol. 3c, pp. 125–154, Academic Press, London, UK, 1983.
  14. M. R. Rose and W. F. Doolittle, “Molecular biological mechanisms of speciation,” Science, vol. 220, no. 4593, pp. 157–162, 1983. View at Scopus
  15. J. A. Coyne, “Mutation rates in hybrids between sibling species of Drosophila,” Heredity, vol. 63, p. 2, 1989. View at Scopus
  16. J. Hey, “Speciation via hybrid dysgenesis: negative evidence from the Drosophila affinis subgroup,” Genetica, vol. 78, no. 2, pp. 97–103, 1989. View at Publisher · View at Google Scholar · View at Scopus
  17. R. J. Waugh O'Neill, M. J. O'Neill, and J. A. Marshall Graves, “Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid,” Nature, vol. 393, no. 6680, pp. 68–72, 1998. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. M. Labrador, M. Farré, F. Utzet, and A. Fontdevila, “Interspecific hybridization increases transposition rates of Osvaldo,” Molecular Biology and Evolution, vol. 16, no. 7, pp. 931–937, 1999. View at Scopus
  19. J. A. Coyne and H. A. Orr, Speciation, Sinauer Associates, Sunderland, Mass, USA, 2004.
  20. A. H. Sturtevant, “Genetic studies on Drosophila simulans. I. Introduction. Hybrids with Drosophila melanogaster,” Genetics, vol. 5, no. 5, pp. 488–500, 1920.
  21. T. K. Watanabe, “A gene that rescues the lethal hybrids between Drosophila melanogaster and D. simulans,” Japanese Journal of Genetics, vol. 54, no. 5, pp. 325–331, 1979. View at Scopus
  22. D. A. Barbash, J. Roote, and M. Ashburner, “The Drosophila melanogaster Hybrid male rescue gene causes inviability in male and female species hybrids,” Genetics, vol. 154, no. 4, pp. 1747–1771, 2000. View at Scopus
  23. N. J. Brideau, H. A. Flores, J. Wang, S. Maheshwari, X. Wang, and D. A. Barbash, “Two Dobzhansky-Muller Genes interact to cause hybrid lethality in Drosophila,” Science, vol. 314, no. 5803, pp. 1292–1295, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. S. R. Prigent, H. Matsubayashi, and M. T. Yamamoto, “Transgenic Drosophila simulans strains prove the identity of the speciation gene Lethal hybrid rescue,” Genes and Genetic Systems, vol. 84, no. 5, pp. 353–360, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. F. Greil, E. De Wit, H. J. Bussemaker, and B. Van Steensel, “HP1 controls genomic targeting of four novel heterochromatin proteins in Drosophila,” EMBO Journal, vol. 26, no. 3, pp. 741–751, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. P. Hutter and M. Ashburner, “Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species,” Nature, vol. 327, no. 6120, pp. 331–333, 1987. View at Scopus
  27. D. A. Barbash and M. Ashburner, “A novel system of fertility rescue in Drosophila hybrids reveals a link between hybrid lethality and female sterility,” Genetics, vol. 163, no. 1, pp. 217–226, 2003. View at Scopus
  28. D. A. Barbash, D. F. Siino, A. M. Tarone, and J. Roote, “A rapidly evolving MYB-related protein causes species isolation in Drosophila,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 9, pp. 5302–5307, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. L. Giot, J. S. Bader, C. Brouwer et al., “A Protein interaction map of Drosophila melanogaster,” Science, vol. 302, no. 5651, pp. 1727–1736, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. B. Van Steensel, U. Braunschweig, G. J. Filion, M. Chen, J. G. Van Bemmel, and T. Ideker, “Bayesian network analysis of targeting interactions in chromatin,” Genome Research, vol. 20, no. 2, pp. 190–200, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. N. J. Brideau and D. A. Barbash, “Functional conservation of the Drosophila hybrid incompatibility gene Lhr,” BMC Evolutionary Biology, vol. 11, no. 1, article 57, 2011. View at Publisher · View at Google Scholar · View at PubMed
  32. M. Nei, Molecular Evolutionary Genetics, Columbia University Press, New York, NY, USA, 1987.
  33. J. H. McDonald and M. Kreitman, “Adaptive protein evolution at the Adh locus in Drosophila,” Nature, vol. 351, no. 6328, pp. 652–654, 1991. View at Scopus
  34. D. A. Barbash, P. Awadalla, and A. M. Tarone, “Functional divergence caused by ancient positive selection of a Drosophila hybrid incompatibility locus,” PLoS Biology, vol. 2, no. 6, Article ID e142, 2004. View at Publisher · View at Google Scholar · View at PubMed
  35. G. J. Filion, J. G. van Bemmel, U. Braunschweig et al., “Systematic protein location mapping reveals five principal chromatin types in Drosophila cells,” Cell, vol. 143, no. 2, pp. 212–224, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. E. Hadorn, “Zur autonomie und phasenspezifität der latalität von bastarden zwischen Drosophila melanogaster und Drosophila simulans,” Revue Suisse de Zoologie, vol. 68, no. 2, pp. 197–207, 1961.
  37. K. Sawamura, M. T. Yamamoto, and T. K. Watanabe, “Hybrid lethal systems in the Drosophila melanogaster species complex. II. The Zygotic hybrid rescue (Zhr) gene of D. melanogaster,” Genetics, vol. 133, no. 2, pp. 307–313, 1993. View at Scopus
  38. K. Sawamura and M. T. Yamamoto, “Cytogenetical localization of Zygotic hybrid rescue (Zhr), a Drosophila melanogaster gene that rescues interspecific hybrids from embryonic lethality,” Molecular and General Genetics, vol. 239, no. 3, pp. 441–449, 1993. View at Scopus
  39. K. Sawamura, A. Fujita, R. Yokoyama et al., “Molecular and genetic dissection of a reproductive isolation gene, zygotic hybrid rescue, of Drosophila melanogaster,” Japanese Journal of Genetics, vol. 70, no. 2, pp. 223–232, 1995. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Sawamura and M. T. Yamamoto, “Characterization of a reproductive isolation gene, zygotic hybrid rescue, of Drosophila melanogaster by using minichromosomes,” Heredity, vol. 79, no. 1, pp. 97–103, 1997. View at Publisher · View at Google Scholar · View at Scopus
  41. P. M. Ferree and D. A. Barbash, “Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila,” PLoS Biology, vol. 7, no. 10, Article ID e1000234, 2009. View at Publisher · View at Google Scholar · View at PubMed
  42. K. Sawamura, C. I. Wu, and T. L. Karr, “Early development and lethality in D. simulans/D. melanogaster hybrids,” in Proceedings of the Annual Drosophila Research Conference, vol. 38, p. 175, 1997.
  43. M. Carlson and D. Brutlag, “Cloning and characterization of a complex satellite DNA from Drosophila melanogaster,” Cell, vol. 11, no. 2, pp. 371–381, 1977. View at Scopus
  44. T. Hsieh and D. Brutlag, “Sequence and sequence variation within the 1.688 g/cm3 satellite DNA of Drosophila melanogaster,” Journal of Molecular Biology, vol. 135, no. 2, pp. 465–481, 1979. View at Scopus
  45. D. L. Brutlag, “Molecular arrangement and evolution of heterochromatic DNA,” Annual Review of Genetics, vol. 14, pp. 121–144, 1980. View at Scopus
  46. A. J. Hilliker and R. Appels, “Pleiotropic effects associated with the deletion of heterochromatin surrounding rDNA on the X chromosome of Drosophila,” Chromosoma, vol. 86, no. 4, pp. 469–490, 1982. View at Scopus
  47. A. R. Lohe, A. J. Hilliker, and P. A. Roberts, “Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster,” Genetics, vol. 134, no. 4, pp. 1149–1174, 1993. View at Scopus
  48. S. R. Barnes, D. A. Webb, and G. Dover, “The distribution of satellite and main-band DNA components in the melanogaster species subgroup of Drosophila. I. Fractionation of DNA in actinomycin D and distamycin A density gradients,” Chromosoma, vol. 67, no. 4, pp. 341–363, 1978. View at Scopus
  49. T. Strachan, E. Coen, D. Webb, and G. Dover, “Modes and rates of change of complex DNA families of Drosophila,” Journal of Molecular Biology, vol. 158, no. 1, pp. 37–54, 1982. View at Scopus
  50. T. Strachan, D. Webb, and G. A. Dover, “Transition stages of molecular drive in multiple-copy DNA families in Drosophila,” EMBO Journal, vol. 4, no. 7, pp. 1701–1708, 1985.
  51. A. R. Lohe and D. L. Brutlag, “Identical satellite DNA sequences in sibling species of Drosophila,” Journal of Molecular Biology, vol. 194, no. 2, pp. 161–170, 1987. View at Scopus
  52. K. Sawamura, T. Taira, and T. K. Watanabe, “Hybrid lethal systems in the Drosophila melanogaster species complex. I. The maternal hybrid rescue (mhr) gene of Drosophila simulans,” Genetics, vol. 133, no. 2, pp. 299–305, 1993. View at Scopus
  53. P. Hutter, J. Roote, and M. Ashburner, “A genetic basis for the inviability of hybrids between sibling species of Drosophila,” Genetics, vol. 124, no. 4, pp. 909–920, 1990. View at Scopus
  54. P. M. Ferree and D. A. Barbash, “Distorted sex ratios: a window into RNAi-mediated silencing,” PLoS Biology, vol. 5, no. 11, Article ID e303, pp. 2453–2457, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. T. S. Hsieh and D. L. Brutlag, “A protein that preferentially binds Drosophila satellite DNA,” Proceedings of the National Academy of Sciences of the United States of America, vol. 76, no. 2, pp. 726–730, 1979. View at Scopus
  56. E. Käs and U. K. Laemmli, “In vivo topoisomerase II cleavage of the Drosophila histone and satellite III repeats: DNA sequence and structural characteristics,” EMBO Journal, vol. 11, no. 2, pp. 705–716, 1992. View at Scopus
  57. W. F. Marshall, A. Straight, J. F. Marko et al., “Interphase chromosomes undergo constrained diffusional motion in living cells,” Current Biology, vol. 7, no. 12, pp. 930–939, 1997. View at Scopus
  58. R. Blattes, C. Monod, G. Susbielle et al., “Displacement of D1, HP1 and topoisomerase II from satellite heterochromatin by a specific polyamide,” EMBO Journal, vol. 25, no. 11, pp. 2397–2408, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. M. C. Carracedo, A. Asenjo, and P. Casares, “Location of Shfr a new gene that rescues hybrid female viability in crosses between Drosophila simulans females and D. melanogaster males,” Heredity, vol. 84, no. 6, pp. 630–638, 2000. View at Publisher · View at Google Scholar · View at Scopus
  60. L. Usakin, J. Abad, V. V. Vagin, B. De Pablos, A. Villasante, and V. A. Gvozdev, “Transcription of the 1.688 satellite DNA family is under the control of RNA interference machinery in Drosophila melanogaster ovaries,” Genetics, vol. 176, no. 2, pp. 1343–1349, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. M. V. Cattani and D. C. Presgraves, “Genetics and lineage-specific evolution of a lethal hybrid incompatibility between Drosophila mauritiana and its sibling species,” Genetics, vol. 181, no. 4, pp. 1545–1555, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. J. David, F. Lemeunier, L. Tsacas, and C. Bocquet, “Hybridization of a new species, Drosophila mauritiana with D. Melanogaster and D. simulans,” Annales de Genetique, vol. 17, no. 4, pp. 235–241, 1974. View at Scopus
  63. C. I. Wu and M. F. Palopoli, “Genetics of postmating reproductive isolation in animals,” Annual Review of Genetics, vol. 28, pp. 283–308, 1994. View at Scopus
  64. D. E. Perez, C. I. Wu, N. A. Johnson, and M. L. Wu, “Genetics of reproductive isolation in the Drosophila simulans clade: DNA marker-assisted mapping and characterization of a hybrid-male sterility gene, Odysseus (Ods),” Genetics, vol. 134, no. 1, pp. 261–275, 1993. View at Scopus
  65. D. E. Perez and C. I. Wu, “Further characterization of the Odysseus locus of hybrid sterility in Drosophila: one gene is not enough,” Genetics, vol. 140, no. 1, pp. 201–206, 1995. View at Scopus
  66. C. T. Ting, S. C. Tsaur, M. L. Wu, and C. I. Wu, “A rapidly evolving homeobox at the site of a hybrid sterility gene,” Science, vol. 282, no. 5393, pp. 1501–1504, 1998. View at Scopus
  67. K. Tabuchi, S. Yoshikawa, Y. Yuasa, K. Sawamoto, and H. Okano, “A novel Drosophila paired-like homeobox gene related to Caenorhabditis elegans unc-4 is expressed in subsets of postmitotic neurons and epidermal cells,” Neuroscience Letters, vol. 257, no. 1, pp. 49–52, 1998. View at Publisher · View at Google Scholar · View at Scopus
  68. C. T. Ting, S. C. Tsaur, S. Sun, W. E. Browne, N. H. Patel, and C. I. Wu, “Gene duplication and speciation in Drosophila: evidence from the Odysseus locus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 33, pp. 12232–12235, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  69. S. Sun, C. T. Ting, and C. I. Wu, “The normal function of a speciation gene, Odysseus, and its hybrid sterility effect,” Science, vol. 305, no. 5680, pp. 81–83, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  70. P. Michalak and M. A. F. Noor, “Association of misexpression with sterility in hybrids of Drosophila simulans and D. mauritiana,” Journal of Molecular Evolution, vol. 59, no. 2, pp. 277–282, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  71. X. Lu, J. A. Shapiro, C. T. Ting et al., “Genome-wide misexpression of X-linked versus autosomal genes associated with hybrid male sterility,” Genome Research, vol. 20, no. 8, pp. 1097–1102, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  72. J. J. Bayes and H. S. Malik, “Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species,” Science, vol. 326, no. 5959, pp. 1538–1541, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  73. A. W. Davis, J. Roote, T. Morley, K. Sawamura, S. Herrmann, and M. Ashburner, “Rescue of hybrid sterility in crosses between D. melanogaster and D. simulans,” Nature, vol. 380, no. 6570, pp. 157–159, 1996. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  74. K. Sawamura, A. W. Davis, and C. I. Wu, “Genetic analysis of speciation by means of introgression into Drosophila melanogaster,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 6, pp. 2652–2655, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  75. K. Sawamura and M. T. Yamamoto, “The minimal interspecific introgression resulting in male sterility in Drosophila,” Genetical Research, vol. 84, no. 2, pp. 81–86, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. K. Sawamura, T. L. Karr, and M. T. Yamamoto, “Genetics of hybrid inviability and sterility in Drosophila: dissection of introgression of D. simulans genes in D. melanogaster genome,” Genetica, vol. 120, no. 1–3, pp. 253–260, 2004. View at Publisher · View at Google Scholar · View at Scopus
  77. K. Sawamura, J. Roote, C. I. Wu, and M. T. Yamamoto, “Genetic complexity underlying hybrid male sterility in Drosophila,” Genetics, vol. 166, no. 2, pp. 789–796, 2004. View at Publisher · View at Google Scholar · View at Scopus
  78. K. Sawamura, K. Maehara, S. Mashino et al., “Introgression of Drosophila simulans nuclear pore protein 160 in Drosophila melanogaster alone does not cause inviability but does cause female sterility,” Genetics, vol. 186, no. 2, pp. 669–676, 2010. View at Publisher · View at Google Scholar · View at PubMed
  79. D. C. Presgraves, L. Balagopalan, S. M. Abmayr, and H. A. Orr, “Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila,” Nature, vol. 423, no. 6941, pp. 715–719, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  80. S. Tang and D. C. Presgraves, “Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities,” Science, vol. 323, no. 5915, pp. 779–782, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  81. K. Sawamura, “Genetics of hybrid inviability and sterility in Drosophila: the Drosophila melanogaster-Drosophila simulans case,” Plant Species Biology, vol. 15, no. 3, pp. 237–247, 2000. View at Publisher · View at Google Scholar · View at Scopus
  82. D. C. Presgraves, “A fine-scale genetic analysis of hybrid incompatibilities in Drosophila,” Genetics, vol. 163, no. 3, pp. 955–972, 2003. View at Scopus
  83. D. C. Presgraves and W. Stephan, “Pervasive adaptive evolution among interactors of the Drosophila hybrid inviability gene, Nup96,” Molecular Biology and Evolution, vol. 24, no. 1, pp. 306–314, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  84. N. L. Clark and C. F. Aquadro, “A novel method to detect proteins evolving at correlated rates: identifying new functional relationships between coevolving proteins,” Molecular Biology and Evolution, vol. 27, no. 5, pp. 1152–1161, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  85. A. Köhler and E. Hurt, “Gene regulation by nucleoporins and links to cancer,” Molecular Cell, vol. 38, no. 1, pp. 6–15, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  86. S. Mendjan, M. Taipale, J. Kind et al., “Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila,” Molecular Cell, vol. 21, no. 6, pp. 811–823, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  87. A. V. Orjalo, A. Arnaoutov, Z. Shen et al., “The Nup107-160 nucleoporin complex is required for correct bipolar spindle assembly,” Molecular Biology of the Cell, vol. 17, no. 9, pp. 3806–3818, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  88. M. Zuccolo, A. Alves, V. Galy et al., “The human Nup107-160 nuclear pore subcomplex contributes to proper kinetochore functions,” EMBO Journal, vol. 26, no. 7, pp. 1853–1864, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  89. M. Capelson, Y. Liang, R. Schulte, W. Mair, U. Wagner, and M. W. Hetzer, “Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes,” Cell, vol. 140, no. 3, pp. 372–383, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  90. R. K. Mishra, P. Chakraborty, A. Arnaoutov, B. M. A. Fontoura, and M. Dasso, “The Nup107-160 complex and γ-TuRC regulate microtubule polymerization at kinetochores,” Nature Cell Biology, vol. 12, no. 2, pp. 164–169, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  91. J. M. Vaquerizas, R. Suyama, J. Kind, K. Miura, N. M. Luscombe, and A. Akhtar, “Nuclear pore proteins Nup153 and megator define transcriptionally active regions in the Drosophila genome,” PLoS Genetics, vol. 6, no. 2, Article ID e1000846, 2010. View at Publisher · View at Google Scholar · View at PubMed
  92. C. Merrill, L. Bayraktaroglu, A. Kusano, and B. Ganetzky, “Truncated RanGAP encoded by the Segregation Distorter Locus of Drosophila,” Science, vol. 283, no. 5408, pp. 1742–1745, 1999. View at Publisher · View at Google Scholar · View at Scopus
  93. Y. Tao, J. P. Masly, L. Araripe, Y. Ke, and D. L. Hartl, “A sex-ratio meiotic drive system in Drosophila simulans. I: an autosomal suppressor,” PLoS Biology, vol. 5, no. 11, Article ID e292, pp. 2560–2575, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  94. J. Forejt, “Hybrid sterility in the mouse,” Trends in Genetics, vol. 12, no. 10, pp. 412–417, 1996. View at Publisher · View at Google Scholar · View at Scopus
  95. A. Oka, A. Mita, N. Sakurai-Yamatani et al., “Hybrid breakdown caused by substitution of the X chromosome between two mouse subspecies,” Genetics, vol. 166, no. 2, pp. 913–924, 2004. View at Publisher · View at Google Scholar · View at Scopus
  96. A. Oka, T. Aoto, Y. Totsuka et al., “Disruption of genetic interaction between two autosomal regions and the X chromosome causes reproductive isolation between mouse strains derived from different subspecies,” Genetics, vol. 175, no. 1, pp. 185–197, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  97. J. Forejt and P. Ivanyi, “Genetic studies on male sterility of hybrids between laboratory and wild mice (Mus musculus L.),” Genetical Research, vol. 24, no. 2, pp. 189–206, 1974. View at Scopus
  98. O. Mihola, Z. Trachtulec, C. Vlcek, J. C. Schimenti, and J. Forejt, “A mouse speciation gene encodes a meiotic histone H3 methyltransferase,” Science, vol. 323, no. 5912, pp. 373–375, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  99. K. Hayashi, K. Yoshida, and Y. Matsui, “A histone H3 methyltransferase controls epigenetic events required for meiotic prophase,” Nature, vol. 438, no. 7066, pp. 374–378, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  100. Y. Matsuda, T. Hirobe, and V. M. Chapman, “Genetic basis of X-Y chromosome dissociation and male sterility in interspecific hybrids,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 11, pp. 4850–4854, 1991. View at Scopus
  101. Y. Matsuda, P. B. Moens, and V. M. Chapman, “Deficiency of X and Y chromosomal pairing at meiotic prophase in spermatocytes of sterile interspecific hybrids between laboratory mice (Mus domesticus) and Mus spretus,” Chromosoma, vol. 101, no. 8, pp. 483–492, 1992. View at Publisher · View at Google Scholar · View at Scopus
  102. D. W. Hale, L. L. Washburn, and E. M. Eicher, “Meiotic abnormalities in hybrid mice of the C57BL/6J x Mus spretus cross suggest a cytogenetic basis for Haldane's rule of hybrid sterility,” Cytogenetics and Cell Genetics, vol. 63, no. 4, pp. 221–234, 1993. View at Scopus
  103. J. L. Guenet, C. Nagamine, D. Simon-Chazottes, X. Montagutelli, and F. Bonhomme, “Hst-3: an X-linked hybrid sterility gene,” Genetical Research, vol. 56, no. 2-3, pp. 163–165, 1990. View at Scopus
  104. H. T. Imai, M. Y. Wada, and K. Moriwaki, “The sex chromosome association (Sxa) gene is located on the X-chromosome in mice,” Japanese Journal of Genetics, vol. 65, no. 2, pp. 65–69, 1990. View at Publisher · View at Google Scholar · View at Scopus
  105. H. Winking, K. Nielsen, and A. Gropp, “Variable positions of NORs in Mus musculus,” Cytogenetics and Cell Genetics, vol. 26, no. 2–4, pp. 158–164, 1980. View at Scopus
  106. Y. Matsuda and V. M. Chapman, “In situ analysis of centromeric satellite DNA segregating in Mus species crosses,” Mammalian Genome, vol. 1, no. 2, pp. 71–77, 1990. View at Publisher · View at Google Scholar · View at Scopus
  107. P. L. Oliver, L. Goodstadt, J. J. Bayes et al., “Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa,” PLoS Genetics, vol. 5, no. 12, Article ID e1000753, 2009. View at Publisher · View at Google Scholar · View at PubMed
  108. J. H. Thomas, R. O. Emerson, and J. Shendure, “Extraordinary molecular evolution in the PRDM9 fertility gene,” PloS One, vol. 4, no. 12, article e8505, 2009.
  109. C. P. Ponting, “What are the genomic drivers of the rapid evolution of PRDM9?” Trends in Genetics, vol. 27, no. 5, pp. 165–171, 2011. View at Publisher · View at Google Scholar · View at PubMed
  110. F. Baudat, J. Buard, C. Grey et al., “PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice,” Science, vol. 327, no. 5967, pp. 836–840, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  111. S. Myers, R. Bowden, A. Tumian et al., “Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination,” Science, vol. 327, no. 5967, pp. 876–879, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  112. E. D. Parvanov, P. M. Petkov, and K. Paigen, “Prdm9 controls activation of mammalian recombination hotspots,” Science, vol. 327, no. 5967, p. 835, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  113. T. Jenuwein and C. D. Allis, “Translating the histone code,” Science, vol. 293, no. 5532, pp. 1074–1080, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  114. J. C. Peng and G. H. Karpen, “Epigenetic regulation of heterochromatic DNA stability,” Current Opinion in Genetics and Development, vol. 18, no. 2, pp. 204–211, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  115. J. C. Peng and G. H. Karpen, “H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability,” Nature Cell Biology, vol. 9, no. 1, pp. 25–35, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  116. S. H. Frank, “Divergence of meiotic drive-suppressors as an explanation for sex-biased hybrid sterility and inviability,” Evolution, vol. 45, no. 2, pp. 262–267, 1991.
  117. L. D. Hurst and A. Pomiankowski, “Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane's rule and related phenomena,” Genetics, vol. 128, no. 4, pp. 841–858, 1991. View at Scopus
  118. N. A. Johnson and C. I. Wu, “An empirical test of the meiotic drive models of hybrid sterility: sex- ratio data from hybrids between Drosophila simulans and Drosophila sechellia,” Genetics, vol. 130, no. 3, pp. 507–511, 1992. View at Scopus
  119. J. A. Coyne and H. A. Orr, “Further evidence against the involvement of meiotic drive in hybrid sterility,” Evolution, vol. 47, no. 2, pp. 685–687, 1993.
  120. Y. Tao, D. L. Hartl, and C. C. Laurie, “Sex-ratio segregation distortion associated with reproductive isolation in Drosophila,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 23, pp. 13183–13188, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  121. H. A. Orr and S. Irving, “Segregation distortion in hybrids between the Bogota and USA subspecies of Drosophila pseudoobscura,” Genetics, vol. 169, no. 2, pp. 671–682, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  122. N. Phadnis and H. A. Orr, “A single gene causes both male sterility and segregation distortion in Drosophila hybrids,” Science, vol. 323, no. 5912, pp. 376–379, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  123. S. Henikoff, K. Ahmad, and H. S. Malik, “The centromere paradox: stable inheritance with rapidly evolving DNA,” Science, vol. 293, no. 5532, pp. 1098–1102, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  124. G. P. Smith, “Evolution of repeated DNA sequences by unequal crossover,” Science, vol. 191, no. 4227, pp. 528–535, 1976. View at Scopus
  125. B. Charlesworth, P. Sniegowski, and W. Stephan, “The evolutionary dynamics of repetitive DNA in eukaryotes,” Nature, vol. 371, no. 6494, pp. 215–220, 1994. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  126. A. K. Csink and S. Henikoff, “Something from nothing: the evolution and utility of satellite repeats,” Trends in Genetics, vol. 14, no. 5, pp. 200–204, 1998. View at Publisher · View at Google Scholar · View at Scopus
  127. S. Henikoff, K. Ahmad, J. S. Platero, and B. Van Steensel, “Heterochromatic deposition of centromeric histone H3-like proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 2, pp. 716–721, 2000. View at Publisher · View at Google Scholar · View at Scopus
  128. H. S. Malik and S. Henikoff, “Adaptive evolution of Cid, a centromere-specific histone in Drosophila,” Genetics, vol. 157, no. 3, pp. 1293–1298, 2001. View at Scopus
  129. C. I. Wu, T. W. Lyttle, M. L. Wu, and G. F. Lin, “Association between a satellite DNA sequence and the responder of segregation distorter in D. melanogaster,” Cell, vol. 54, no. 2, pp. 179–189, 1988. View at Scopus
  130. L. Fishman and A. Saunders, “Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers,” Science, vol. 322, no. 5907, pp. 1559–1562, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  131. H. J. Muller and G. Pontecorvo, “Recombinants between Drosophila species the F1 hybrids of which are sterile,” Nature, vol. 146, no. 3693, pp. 199–200, 1940. View at Scopus
  132. H. A. Orr, “Mapping and characterization of a “speciation gene” in Drosophila,” Genetical Research, vol. 59, no. 2, pp. 73–80, 1992. View at Scopus
  133. J. P. Masly, C. D. Jones, M. A. F. Noor, J. Locke, and H. A. Orr, “Gene transposition as a cause of hybrid sterility in Drosophila,” Science, vol. 313, no. 5792, pp. 1448–1450, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  134. M. Lynch and A. G. Force, “The origin of interspecific genomic incompatibility via gene duplication,” American Naturalist, vol. 156, no. 6, pp. 590–605, 2000. View at Publisher · View at Google Scholar · View at Scopus
  135. J. B. S. Haldane, “Sex ratio and unisexual sterility in hybrid animals,” Journal of Genetics, vol. 12, no. 2, pp. 101–109, 1922. View at Publisher · View at Google Scholar · View at Scopus
  136. C. I. Wu, N. A. Johnson, and M. F. Palopoli, “Haldane's rule and its legacy: why are there so many sterile males?” Trends in Ecology and Evolution, vol. 11, no. 7, pp. 281–284, 1996. View at Publisher · View at Google Scholar · View at Scopus
  137. C. C. Laurie, “The weaker sex is heterogametic: 75 years of Haldane's rule,” Genetics, vol. 147, no. 3, pp. 937–951, 1997. View at Scopus
  138. R. J. Kulathinal and R. S. Singh, “The molecular basis of speciation: from patterns to processes, rules to mechanisms,” Journal of Genetics, vol. 87, no. 4, pp. 327–338, 2008. View at Publisher · View at Google Scholar · View at Scopus
  139. M. Turelli and H. A. Orr, “The dominance theory of Haldane’s rule,” Genetics, vol. 140, no. 1, pp. 389–402, 1995. View at Scopus
  140. E. Lifschytz and D. L. Lindsley, “The role of X-chromosome inactivation during spermatogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 69, no. 1, pp. 182–186, 1972. View at Scopus
  141. X. Lu and C.-I. Wu, “Sex, sex chromosomes and gene expression,” BMC Biology, vol. 9, article 30, 2011. View at Publisher · View at Google Scholar · View at PubMed
  142. L. M. Mikhaylova and D. I. Nurminsky, “Lack of global meiotic sex chromosome inactivation, and paucity of tissue-specific gene expression on the Drosophila X chromosome,” BMC Biology, vol. 9, article 29, 2011. View at Publisher · View at Google Scholar · View at PubMed
  143. D. Haig and C. Graham, “Genomic imprinting and the strange case of the insulin-like growth factor II receptor,” Cell, vol. 64, no. 6, pp. 1045–1046, 1991. View at Scopus
  144. T. Moore and D. Haig, “Genomic imprinting in mammalian development: a parental tug-of-war,” Trends in Genetics, vol. 7, no. 2, pp. 45–49, 1991. View at Scopus
  145. R. J. Scott and M. Spielman, “Deeper into the maize: new insights into genomic imprinting in plants,” BioEssays, vol. 28, no. 12, pp. 1167–1171, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  146. T. Kinoshita, Y. Ikeda, and R. Ishikawa, “Genomic imprinting: a balance between antagonistic roles of parental chromosomes,” Seminars in Cell and Developmental Biology, vol. 19, no. 6, pp. 574–579, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  147. U. Zechner, W. Shi, M. Hemberger et al., “Divergent genetic and epigenetic post-zygotic isolation mechanisms in Mus and Peromyscus,” Journal of Evolutionary Biology, vol. 17, no. 2, pp. 453–460, 2004. View at Publisher · View at Google Scholar · View at Scopus
  148. C. Josefsson, B. Dilkes, and L. Comai, “Parent-dependent loss of gene silencing during interspecies hybridization,” Current Biology, vol. 16, no. 13, pp. 1322–1328, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  149. T. Kinoshita, “Reproductive barrier and genomic imprinting in the endosperm of flowering plants,” Genes and Genetic Systems, vol. 82, no. 3, pp. 177–186, 2007. View at Publisher · View at Google Scholar · View at Scopus
  150. C. D. Wiley, H. H. Matundan, A. R. Duselis, A. T. Isaacs, and P. B. Vrana, “Patterns of hybrid loss of imprinting reveal tissue- and cluster-specific regulation,” PLoS One, vol. 3, no. 10, Article ID e3572, 2008. View at Publisher · View at Google Scholar · View at PubMed