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The Segregation Distorter (SD) system of Drosophila melanogaster is one the best-characterized meiotic drive complexes known. SD gains an unfair transmission advantage through heterozygous SD/SD+ males by incapacitating SD+-bearing spermatids so that virtually all progeny inherit SD. Segregation distorter (Sd), the primary distorting locus in the SD complex, is a truncated duplication of the RanGAP gene, a major regulator of the small GTPase Ran, which has several functions including the maintenance of the nucleocytoplasmic RanGTP concentration gradient that mediates nuclear transport. The truncated Sd-RanGAP protein is enzymatically active but mislocalizes to the nucleus where it somehow causes distortion. Here I present data consistent with the idea that wild-type RanGAP, and possibly other loci able to influence the RanGTP gradient, has been caught up in an ancient genetic conflict that predates the SD complex. The legacy of this conflict could include the unexpectedly rapid evolution of nuclear transport-related proteins, the accumulation of chromosomal inversions, the recruitment of gene duplications, and the turnover of repetitive sequences in the centric heterochromatin. BioEssays 29:386–391, 2007. © 2007 Wiley Periodicals, Inc.

Postzygotic reproductive isolation is characterized by two striking empirical patterns. The first is Haldane's rule—the preferential inviability or sterility of species hybrids of the heterogametic (XY) sex. The second is the so-called large X effect—substitution of one species's X chromosome for another's has a disproportionately large effect on hybrid fitness compared to similar substitution of an autosome. Although the first rule has been well-established, the second rule remains controversial. Here, we dissect the genetic causes of these two rules using a genome-wide introgression analysis of Drosophila mauritiana chromosome segments in an otherwise D. sechellia genetic background. We find that recessive hybrid incompatibilities outnumber dominant ones and that hybrid male steriles outnumber all other types of incompatibility, consistent with the dominance and faster-male theories of Haldane's rule, respectively. We also find that, although X-linked and autosomal introgressions are of similar size, most X-linked introgressions cause hybrid male sterility (60%) whereas few autosomal introgressions do (18%). Our results thus confirm the large X effect and identify its proximate cause: incompatibilities causing hybrid male sterility have a higher density on the X chromosome than on the autosomes. We evaluate several hypotheses for the evolutionary cause of this excess of X-linked hybrid male sterility., Author Summary The evolution of reproductive isolation is a fundamental step in the origin of species. One kind of reproductive isolation, the sterility and inviability of species hybrids, is characterized by two of the strongest rules in evolutionary biology. The first is Haldane's rule: for species crosses in which just one hybrid sex is sterile or inviable, it tends to be the sex defined by having a pair of dissimilar sex chromosomes (e.g., the “XY” of males in humans). The second rule is the large X effect: the X chromosome has a disproportionately large effect on hybrid fitness. We dissected the genetic causes of these two rules of speciation by replacing many small chromosomal segments of the fruit fly Drosophila sechellia with those of a closely related species, D. mauritiana. Together, these segments cover 70% of the genome. We found that virtually all segments causing hybrid sterility or inviability act recessively and that hybrid male sterility is by far the most common type of hybrid incompatibility, confirming two leading theories about the causes of Haldane's rule. We also found that X-linked segments are more likely to cause hybrid male sterility than similarly sized autosomal segments. These results show that the large X effect is caused by a higher density of hybrid incompatibilities on the X chromosome., A genome-wide introgression analysis of Drosophila mauritiana chromosome segments in an otherwise D. sechellia genetic background confirms the large X effect, a cornerstone of speciation theory, and reveals its cause.

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: F(1) hybrid males are sterile and F(1) 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.

In multicellular organisms, telomerase is required to maintain telomere length in the germline but is dispensable in the soma. Mice, for example, express telomerase in somatic and germline tissues, while humans express telomerase almost exclusively in the germline. As a result, when telomeres of human somatic cells reach a critical length the cells enter irreversible growth arrest called replicative senescence. Replicative senescence is believed to be an anticancer mechanism that limits cell proliferation. The difference between mice and humans led to the hypothesis that repression of telomerase in somatic cells has evolved as a tumor-suppressor adaptation in large, long-lived organisms. We tested whether regulation of telomerase activity coevolves with lifespan and body mass using comparative analysis of 15 rodent species with highly diverse lifespans and body masses. Here we show that telomerase activity does not coevolve with lifespan but instead coevolves with body mass: larger rodents repress telomerase activity in somatic cells. These results suggest that large body mass presents a greater risk of cancer than long lifespan, and large animals evolve repression of telomerase activity to mitigate that risk.

Nup96 is involved in a lethal hybrid incompatibility between 2 fruit fly species, Drosophila melanogaster and Drosophila simulans. Recurrent adaptive evolution drove the rapid functional divergence of Nup96 in both the D. melanogaster and the D. simulans lineages. Functional divergence of Nup96 between these 2 species is unexpected as Nup96 encodes part of the Nup 107 subcomplex, an architectural component of nuclear pore complexes, the macromolecular channels in nuclear envelopes that mediate nucleocytoplasmic traffic in all eukaryotes. Here we study the evolutionary histories of 5 of Nup96's protein interactors-3 stable Nupl07 subcomplex proteins (Nup75, Nupl07, and Nupl33) and 2 mobile nucleoporins (Nup98 and Nup 153)-and show that all 5 have experienced recurrent adaptive evolution. These results are consistent with selection-driven coevolution among molecular interactors within species causing the incidental evolution of incompatible interactions seen in hybrids between species. We suggest that genetic conflict-driven processes may have contributed to the rapid molecular evolution of Nup107 subcomplex genes.

Whole genome sequence analyses have confirmed that gene duplication and divergence play major roles in genome evolution. But the details of how young, functionally redundant gene duplicates escape mutational degradation have remained elusive. Several recent studies show that new genes survive because they evolve new, and sometimes essential, functions.

Population genetic theory shows that the efficacy of natural selection is limited by linkage—selection at one site interferes with selection at linked sites. Such interference slows adaptation in asexual genomes and may explain the evolutionary advantage of sex. Here, we test for two signatures of constraint caused by linkage in a sexual genome, by using sequence data from 255 Drosophila melanogaster and Drosophila simulans loci. We find that ( i ) the rate of protein adaptation is reduced in regions of low recombination, and ( ii ) evolution at strongly selected amino acid sites interferes with optimal codon usage at weakly selected, tightly linked synonymous sites. Together these findings suggest that linkage limits the rate and degree of adaptation even in recombining genomes.

Sperm and female reproductive tract morphology are among the most rapidly evolving characters known in insects. To investigate whether interspecific variation in these traits results from divergent coevolution we examined testis size, sperm length and female reproductive tract morphology for evidence of correlated evolution using 13 species of diopsid stalk-eyed flies. We found that sperm dimorphism (the simultaneous production of two size classes of sperm by individual males) is ancestral and occurs in four genera while sperm monomorphism evolved once and persists in one genus. The length of 'long-sperm' types, though unrelated to male body or testis size, exhibits correlated evolution with two regions of the female reproductive tract, the spermathecae and ventral receptacle, where sperm are typically stored and used for fertilization, respectively. Two lines of evidence indicate that 'short sperm', which are probably incapable of fertilization, coevolve with spermathecae. First, loss of sperm dimorphism coincides phylogenetically with reduction or loss of spermathecae. Second, evolutionary change in short-sperm length correlates with change in spermathecal size but not spermathecal duct length or ventral receptacle length. Morphological coevolution between sperm and female reproductive tracts is consistent with a history of female-mediated selection on sperm length.

Haldane's rule states that species hybrids of the XY sex are preferentially sterile or inviable. In all taxa known to obey this rule, the Y is inert and X-linked genes show full expression in XY individuals. Until recently, all theories of Haldane's rule depended on this hemizygosity. A test of Haldane's rule in animals lacking a hemizygous sex—mosquitoes having two functional sex chromosomes in both sexes—reveals that these species show Haldane's rule for sterility but not inviability. A related group having a “normal” hemizygous X obeys Haldane's rule for both sterility and inviability. These results support the faster male and dominance theories of Haldane's rule.

I present patterns characterizing the evolution of intrinsic postzygotic isolation in Lepidoptera by analyzing data from the literature on genetic distance, strength of hybrid sterility and inviability, biogeography, and natural hybridization. Using genetic distance as a proxy for time, I investigate the time-course of the evolution of postzygotic isolation and the waiting times to particular hybrid fitness problems. The results show that postzygotic isolation increases gradually as species diverge, but that hybrid sterility evolves faster than hybrid inviability. The overwhelming preponderance of female-specific hybrid problems in Lepidoptera shows that Haldane's rule (the preferential sterility or inviability of the heterogametic sex) is well obeyed. Together the rates and patterns characterizing the accumulation of postzygotic isolation allow several tests of the composite theory of Haldane's rule. Interestingly, comparing these data with those from Drosophila reveals that Haldane's rule for sterility evolves as fast (if not faster) in Lepidoptera. Finally, I show that a substantial fraction of sympatric species hybridizes in nature and that the majority of these suffer some level of hybrid sterility or inviability.

Evolutionary biologists have long recognized that the sterility and inviability of species hybrids must involve incompatible epistatic interactions between two (or more) genes. The first pair of such hybrid incompatibility genes has now been identified.

SummaryOne of the strongest rules of biological diversity — the observation that more species live on large islands than on small ones — is usually attributed to the balance between colonization and extinction. But speciation on islands cannot be ignored.

Meiotically driven sex chromosomes can quickly spread to fixation and cause population extinction unless balanced by selection or suppressed by genetic modifiers. We report results of genetic analyses that demonstrate that extreme female-biased sex ratios in two sister species of stalk-eyed flies, Cyrtodiopsis dalmanni and C. whitei, are due to a meiotic drive element on the X chromosome (Xd). Relatively high frequencies of Xd in C. dalmanni and C. whitei (13–17% and 29%, respectively) cause female-biased sex ratios in natural populations of both species. Sex ratio distortion is associated with spermatid degeneration in male carriers of Xd. Variation in sex ratios is caused by Y-linked and autosomal factors that decrease the intensity of meiotic drive. Y-linked polymorphism for resistance to drive exists in C. dalmanni in which a resistant Y chromosome reduces the intensity and reverses the direction of meiotic drive. When paired with Xd, modifying Y chromosomes (Ym) cause the transmission of predominantly Y-bearing sperm, and on average, production of 63% male progeny. The absence of sex ratio distortion in closely related monomorphic outgroup species suggests that this meiotic drive system may predate the origin of C. whitei and C. dalmanni. We discuss factors likely to be involved in the persistence of these sex-linked polymorphisms and consider the impact of Xd on the operational sex ratio and the intensity of sexual selection in these extremely sexually dimorphic flies.

SummaryTheory predicts that, as species diverge from one another, the number of genetic incompatibilities causing sterility or inviability in interspecies hybrids grows faster than linearly, or snowballs. Two new genetic analyses now provide the first empirical support for this snowball effect.