Fitness consequences of the selfish supergene Segregation Distorter

Segregation distorters are selfish genetic elements that subvert Mendelian inheritance, often by destroying gametes that do not carry the distorter. Simple theoretical models predict that distorter alleles will either spread to fixation or stabilize at some high intermediate frequency. However, many distorters have substantially lower allele frequencies than predicted by simple models, suggesting that key sources of selection remain to be discovered. Here, we measured the fitness of Drosophila melanogaster adults and juveniles carrying zero, one or two copies of three different variants of the naturally occurring supergene Segregation Distorter (SD), in order to investigate why SD alleles remain relatively rare within populations despite being preferentially inherited. First, we show that the three SD variants differ in the severity and dominance of the fitness costs they impose on individuals carrying them. Second, SD‐carrying parents produced less fit offspring in some crosses, independent of offspring genotype, indicating that SD alleles can have nongenetic, transgenerational costs in addition to their direct costs. Third, we found that SD carriers sometimes produce a biased offspring sex ratio, perhaps due to off‐target effects of SD on the sex chromosomes. Finally, we used a theoretical model to investigate how sex ratio and transgenerational effects alter the population genetics of distorter alleles; accounting for these additional costs helps to explain why real‐world segregation distorter alleles are rarer than predicted.     

Contrasting patterns of X‐chromosome divergence underlie multiple sex‐ratio polymorphisms in stalk‐eyed flies

Sex‐linked segregation distorters cause offspring sex ratios to differ from equality. Theory predicts that such selfish alleles may either go to fixation and cause extinction, reach a stable polymorphism or initiate an evolutionary arms race with genetic modifiers. The extent to which a sex ratio distorter follows any of these trajectories in nature is poorly known. Here, we used X‐linked sequence and simple tandem repeat data for three sympatric species of stalk‐eyed flies (Teleopsis whitei and two cryptic species of T. dalmanni) to infer the evolution of distorting X chromosomes. By screening large numbers of field and recently laboratory‐bred flies, we found no evidence of males with strongly female‐biased sex ratio phenotypes (SR) in one species but high frequencies of SR males in the other two species. In the two species with SR males, we find contrasting patterns of X‐chromosome evolution. T. dalmanni‐1 shows chromosome‐wide differences between sex‐ratio (X^SR) and standard (X^ST) X chromosomes consistent with a relatively old sex‐ratio haplotype based on evidence including genetic divergence, an inversion polymorphism and reduced recombination among X^SR chromosomes relative to X^ST chromosomes. In contrast, we found no evidence of genetic divergence on the X between males with female‐biased and nonbiased sex ratios in T. whitei. Taken with previous studies that found evidence of genetic suppression of sex ratio distortion in this clade, our results illustrate that sex ratio modification in these flies is undergoing recurrent evolution with diverse genomic consequences.     

Competition at the Mouse t Complex: Rare Alleles Are Inherently Favored

We investigate the competition between alleles at a segregation distorter locus. The focus is on the invasion prospects of rare mutant distorter alleles in a population in which a wildtype and a resident distorter allele are present. The parameters are chosen to reflect the situation at the t complex of the house mouse, one of the best-studied examples of segregation distortion. By analyzing the invasion chances of rare alleles, we provide an analytical justification of earlier simulation results. We show that a new distorter allele can successfully invade even if it is inferior both at the gamete and at the individual level. In fact, newly arising distorter alleles have an inherent rareness advantage if their negative fitness consequences are restricted to homozygous condition. Likewise, rare mutant wildtype alleles may often invade even if their viability or fertility is reduced. As a consequence, the competition between alleles at a segregation distorter locus should lead to a high degree of polymorphism. We discuss the implications of this conclusion for the t complex of the house mouse and for the evolutionary stability of “honest” Mendelian segregation.     

Meiotic drive influences the outcome of sexually antagonistic selection at a linked locus

Most meiotic drivers, such as the t‐haplotype in Mus and the segregation distorter (SD) in Drosophila, act in a sex‐specific manner, gaining a transmission advantage through one sex although suffering only the fitness costs associated with the driver in the other. Their inheritance is thus more likely through one of the two sexes, a property they share with sexually antagonistic alleles. Previous theory has shown that pairs of linked loci segregating for sexually antagonistic alleles are more likely to remain polymorphic and that linkage disequilibrium accrues between them. I probe this similarity between drive and sexual antagonism and examine the evolution of chromosomes experiencing these selection pressures simultaneously. Reminiscent of previous theory, I find that: the opportunity for polymorphism increases for a sexually antagonistic locus that is physically linked to a driving locus; the opportunity for polymorphism at a driving locus also increases when linked to a sexually antagonistic locus; and stable linkage disequilibrium accompanies any polymorphic equilibrium. Additionally, I find that drive at a linked locus favours the fixation of sexually antagonistic alleles that benefit the sex in which drive occurs. Further, I show that under certain conditions reduced recombination between these two loci is selectively favoured. These theoretical results provide clear, testable predictions about the nature of sexually antagonistic variation on driving chromosomes and have implications for the evolution of genomic architecture.     

EVOLUTION AT THE MOUSE t COMPLEX: WHY IS THE t HAPLOTYPE PRESERVED AS AN INTEGRAL UNIT?

Abstract Segregation distorters are selfish genetic elements that bias Mendelian segregation in their favor. All well-known segregation distortion systems consist of one or more "distorter" loci that act upon a "responder" locus. At the t complex of the house mouse, segregation distortion is brought about by the harmful effect of t alleles at a number of distorter loci on the wild-type variant of the responder locus. The responder and distorter alleles are closely linked by a number of inversions, thus forming a coherent t haplotype. It has been conjectured that the close integration of the various components into a "complete" t haplotype has been crucial for the evolutionary success of these selfish genetic elements. By means of a population genetical metapopulation model, we show that this intuition may be unfounded. In fact, under most circumstances an "insensitive" t haplotype retaining only the responder did invade and reach a high frequency, despite the fact that this haplotype has a strong segregation disadvantage. For certain population structures, the complete t haplotype was even competitively excluded by partial t haplotypes with lower segregation ratios. Moreover, t haplotypes carrying one or more recessive lethals only prevailed over their nonlethal counterparts if the product of local population size and migration rate ( Nm ) was not much smaller or larger than one. These phenomena occurred for rather realistic fitness, segregation, and recombination values. It is therefore quite puzzling that partial t haplotypes are absent from natural house mousepopulations, and that t haplotypes carrying recessive lethals prevail over nonlethal t haplotypes.     

Horizontal gene transfer as a possible evolutionary predecessor of sexual reproduction

Computer modeling shows that high rates of lateral gene transfer (LGT), combined with homologous recombination, enhance selection efficiency, thus making it possible for organisms to acquire larger genomes without irreversible growth of mutation load. In prokaryotes, the optimal (high) rate of LGT cannot evolve because of the “suicidal effect” of modifiers, i.e., alleles that enhance LGT are systematically replaced by alleles that hinder LGT and never vice versa. Therefore, the latter alleles spread despite the fact that they reduce fitness of organisms and populations. This “conflict of interests” can be resolved via evolution of whole-genome reciprocal recombination, which effectively removes the basis for propagation of “selfish” modifiers. Eukaryotic sexual reproduction (amphimixis) probably appeared as the final result of evolution of mechanisms of LGT driven by selection for high interindividual recombination rate. Such selection could have been facilitated at the early stages of eukaryogenesis due to an increase in genome size and high mutation rate caused by higher O₂ concentration and invasion of group II introns.     

Molecular mechanisms of dominance evolution in Müllerian mimicry

Natural selection acting on dominance between adaptive alleles at polymorphic loci can be sufficiently strong for dominance to evolve. However, the molecular mechanisms underlying such evolution are generally unknown. Here, using Müllerian mimicry as a case‐study for adaptive morphological variation, we present a theoretical analysis of the invasion of dominance modifiers altering gene expression through different molecular mechanisms. Toxic species involved in Müllerian mimicry exhibit warning coloration, and converge morphologically with other toxic species of the local community, due to positive frequency‐dependent selection acting on these colorations. Polymorphism in warning coloration may be maintained by migration–selection balance with fine scale spatial heterogeneity. We modeled a dominance modifier locus altering the expression of the warning coloration locus, targeting one or several alleles, acting in cis or trans, and either enhancing or repressing expression. We confirmed that dominance could evolve when balanced polymorphism was maintained at the color locus. Dominance evolution could result from modifiers enhancing one allele specifically, irrespective of their linkage with the targeted locus. Nonspecific enhancers could also persist in populations, at frequencies tightly depending on their linkage with the targeted locus. Altogether, our results identify which mechanisms of expression alteration could lead to dominance evolution in polymorphic mimicry.     

Competition at the mouse t complex: rare alleles are inherently favored

We investigate the competition between alleles at a segregation distorter locus. The focus is on the invasion prospects of rare mutant distorter alleles in a population in which a wildtype and a resident distorter allele are present. The parameters are chosen to reflect the situation at the t complex of the house mouse, one of the best-studied examples of segregation distortion. By analyzing the invasion chances of rare alleles, we provide an analytical justification of earlier simulation results. We show that a new distorter allele can successfully invade even if it is inferior both at the gamete and at the individual level. In fact, newly arising distorter alleles have an inherent rareness advantage if their negative fitness consequences are restricted to homozygous condition. Likewise, rare mutant wildtype alleles may often invade even if their viability or fertility is reduced. As a consequence, the competition between alleles at a segregation distorter locus should lead to a high degree of polymorphism. We discuss the implications of this conclusion for the t complex of the house mouse and for the evolutionary stability of "honest" Mendelian segregation.     

High‐resolution insight into recombination events at the SD1 locus in rice

Recombination during meiosis plays an important role in genome evolution by reshuffling existing genetic variations into fresh combinations with the possibility of recovery of lost ancestral genotypes. While crossover (CO) events have been well studied, gene conversion events (GCs), which represent non‐reciprocal information transfer between chromosomes, are poorly documented and difficult to detect due to their relatively small converted tract size. Here, we document these GC events and their phenotypic effects at an important locus in rice containing the SD1 gene, where multiple defective alleles contributed to the semi‐dwarf phenotype of rice in the ‘Green Revolution’ of the 1960s. Here, physical separation of two defects allows recombination to generate the wild‐type SD1 gene, for which plant height can then be used as a reporter. By screening 18 000 F₂ progeny from a cross between two semi‐dwarf cultivars that carry these different defective alleles, we detected 24 GC events, indicating a conversion rate of ~3.3 × 10^?4 per marker per generation in a single meiotic cycle in rice. Furthermore, our data show that indels and single‐nucleotide polymorphisms (SNPs) do not differ significantly in GC rates, at least at the SD1 locus. Our results provide strong evidence that GC by itself can regain an ancestral phenotype that was lost through mutation. This GC detection approach is likely to be broadly applicable to natural or artificial alleles of other phenotype‐related functional genes, which are abundant in other plant genomes.     

Centromere‐associated meiotic drive and female fitness variation in Mimulus

Female meiotic drive, in which chromosomal variants preferentially segregate to the egg pole during asymmetric female meiosis, is a theoretically pervasive but still mysterious form of selfish evolution. Like other selfish genetic elements, driving chromosomes may be maintained as balanced polymorphisms by pleiotropic or linked fitness costs. A centromere‐associated driver (D) with a ～58:42 female‐specific transmission advantage occurs at intermediate frequency (32–40%) in the Iron Mountain population of the yellow monkeyflower, Mimulus guttatus. Previously determined male fertility costs are sufficient to prevent the fixation of D, but predict a higher equilibrium frequency. To better understand the dynamics and effects of D, we developed a new population genetic model and measured genotype‐specific lifetime female fitness in the wild. In three of four years, and across all years, D imposed significant recessive seedset costs, most likely due to hitchhiking by deleterious mutations. With both male and female costs as measured, and 58:42 drive, our model predicts an equilibrium frequency of D (38%) very close to the observed value. Thus, D represents a rare selfish genetic element whose local population genetic dynamics have been fully parameterized, and the observation of equilibrium sets the stage for investigations of coevolution with suppressors.     

Molecular evolution of the meiotic recombination pathway in mammals

Meiotic recombination shapes evolution and helps to ensure proper chromosome segregation in most species that reproduce sexually. Recombination itself evolves, with species showing considerable divergence in the rate of crossing‐over. However, the genetic basis of this divergence is poorly understood. Recombination events are produced via a complicated, but increasingly well‐described, cellular pathway. We apply a phylogenetic comparative approach to a carefully selected panel of genes involved in the processes leading to crossovers—spanning double‐strand break formation, strand invasion, the crossover/non‐crossover decision, and resolution—to reconstruct the evolution of the recombination pathway in eutherian mammals and identify components of the pathway likely to contribute to divergence between species. Eleven recombination genes, predominantly involved in the stabilization of homologous pairing and the crossover/non‐crossover decision, show evidence of rapid evolution and positive selection across mammals. We highlight TEX11 and associated genes involved in the synaptonemal complex and the early stages of the crossover/non‐crossover decision as candidates for the evolution of recombination rate. Evolutionary comparisons to MLH1 count, a surrogate for the number of crossovers, reveal a positive correlation between genome‐wide recombination rate and the rate of evolution at TEX11 across the mammalian phylogeny. Our results illustrate the power of viewing the evolution of recombination from a pathway perspective.     

The evolution of costly mate choice against segregation distorters

The evolution of female preference for male genetic quality remains a controversial topic in sexual selection research. One well‐known problem, known as the lek paradox, lies in understanding how variation in genetic quality is maintained in spite of natural selection and sexual selection against low‐quality alleles. Here, we theoretically investigate a scenario where females pay a direct fitness cost to avoid males carrying an autosomal segregation distorter. We show that preference evolution is greatly facilitated under such circumstances. Because the distorter is transmitted in a non‐Mendelian fashion, it can be maintained in the population despite directional sexual selection. The preference helps females avoid fitness costs associated with the distorter. Interestingly, we find that preference evolution is limited if the choice allele induces a very strong preference or if distortion is very strong. Moreover, the preference can only persist in the presence of a signal that reliably indicates a male's distorter genotype. Hence, even in a system where the lek paradox does not play a major role, costly preferences can only spread under specific circumstances. We discuss the importance of distorter systems for the evolution of costly female choice and potential implications for the use of artificial distorters in pest control.     

Population biology of a selfish sex ratio distorting element in a booklouse (Psocodea: Liposcelis)

Arthropods harbour a variety of selfish genetic elements that manipulate reproduction to be preferentially transmitted to future generations. A major ongoing question is to understand how these elements persist in nature. In this study, we examine the population dynamics of an unusual selfish sex ratio distorter in a recently discovered species of booklouse, Liposcelis sp. (Psocodea: Liposcelididae) to gain a better understanding of some of the factors that may affect the persistence of this element. Females that carry the selfish genetic element only ever produce daughters, although they are obligately sexual. These females also only transmit the maternal half of their genome. We performed a replicated population cage experiment, varying the initial frequency of females that harbour the selfish element, and following female frequencies for 20 months. The selfish genetic element persisted in all cages, often reaching very high (and thus severely female‐biased) frequencies. Surprisingly, we also found that females that carry the selfish genetic element had much lower fitness than their nondistorter counterparts, with lower lifetime fecundity, slower development and a shorter egg‐laying period. We suggest that differential fitness plays a role in the maintenance of the selfish genetic element in this species. We believe that the genetic system in this species, paternal genome elimination, which allows maternal control of offspring sex ratio, may also be important in the persistence of the selfish genetic element, highlighting the need to consider species with diverse ecologies and genetic systems when investigating the effects of sex ratio manipulators on host populations.     

The evolution of intratetrad mating rates

Intratetrad mating, the fusion of gametes formed in a single meiosis, has unusual consequences for genetic diversity, especially in genome regions linked to mating type loci. Here we investigate the fate of modifier alleles that alter the rate of intratetrad mating, under models of heterozygote advantage and of genetic load resulting from recurrent mutation. In both cases, intratetrad mating is favored if the recombination rate between the selected locus and mating type is less than the frequency of lethal recessive alleles at that locus in the population. Positive feedback often accelerates the invasion of modifiers to the intratetrad mating rate. Recombination rate and intratetrad mating rate exert indirect selection on one another, resulting in a cascading decline in outcrossing, even in the absence of any cost of sex. However, under recurrent mutation, alleles for obligate intratetrad mating invade only very slowly, perhaps explaining why outcrossing can persist at low frequencies in a largely intratetrad mating population.     

The paternal‐sex‐ratio (PSR) chromosome in natural populations of Nasonia (Hymenoptera: Chalcidoidea)

Selfish genetic elements may be important in promoting evolutionary change. Paternal sex ratio (PSR) is a selfish B chromosome that causes all‐male families in the haplodiploid parasitic wasp Nasonia vitripennis, by inducing paternal genome loss in fertilized eggs. The natural distribution and frequency of this chromosome in North American populations of N. vitripennis was investigated using a combination of phenotypic and molecular assays. Sampling throughout North America failed to recover PSR except from populations in the Great Basin area of western North America. Extensive sampling of Great Basin populations revealed PSR in frequencies ranging from 0 to 6% at different collection sites, and extended its distribution to Idaho and Wyoming. Intensive sampling in upstate New York did not detect the chromosome. Frequencies of the maternal‐sex ratio distorter (MSR), son killer (SK) and virgin females ranged from 0 to 12%. Paternal sex ratio may be restricted to the Great Basin because its spread is hampered by geographical barriers, or because populations in other areas are not conducive to PSR maintenance. However, it cannot be ruled out that PSR occurs in other regions at very low frequencies. The apparent limited distribution and low frequency of PSR suggest that it will have relatively little impact on genome evolution in Nasonia.     

A dominant, recombination-defective allele of Dmc1 causing male-specific sterility

DMC1 is a meiosis-specific homolog of bacterial RecA and eukaryotic RAD51 that can catalyze homologous DNA strand invasion and D-loop formation in vitro. DMC1-deficient mice and yeast are sterile due to defective meiotic recombination and chromosome synapsis. The authors identified a male dominant sterile allele of Dmc1, Dmc1^Mei11, encoding a missense mutation in the L2 DNA binding domain that abolishes strand invasion activity. Meiosis in male heterozygotes arrests in pachynema, characterized by incomplete chromosome synapsis and no crossing-over. Young heterozygous females have normal litter sizes despite having a decreased oocyte pool, a high incidence of meiosis I abnormalities, and susceptibility to premature ovarian failure. Dmc1^Mei11 exposes a sex difference in recombination in that a significant portion of female oocytes can compensate for DMC1 deficiency to undergo crossing-over and complete gametogenesis. Importantly, these data demonstrate that dominant alleles of meiosis genes can arise and propagate in populations, causing infertility and other reproductive consequences due to meiotic prophase I defects.     

A Dominant, Recombination-Defective Allele of Dmc1 Causing Male-Specific Sterility

DMC1 is a meiosis-specific homolog of bacterial RecA and eukaryotic RAD51 that can catalyze homologous DNA strand invasion and D-loop formation in vitro. DMC1-deficient mice and yeast are sterile due to defective meiotic recombination and chromosome synapsis. The authors identified a male dominant sterile allele of Dmc1, Dmc1^Mei11, encoding a missense mutation in the L2 DNA binding domain that abolishes strand invasion activity. Meiosis in male heterozygotes arrests in pachynema, characterized by incomplete chromosome synapsis and no crossing-over. Young heterozygous females have normal litter sizes despite having a decreased oocyte pool, a high incidence of meiosis I abnormalities, and susceptibility to premature ovarian failure. Dmc1^Mei11 exposes a sex difference in recombination in that a significant portion of female oocytes can compensate for DMC1 deficiency to undergo crossing-over and complete gametogenesis. Importantly, these data demonstrate that dominant alleles of meiosis genes can arise and propagate in populations, causing infertility and other reproductive consequences due to meiotic prophase I defects.     

Differences in the Rapid Knockdown and Lethal Effects of Aerosol Formulations against German Cockroach (Blattaria, Blattellidae) Strains

ABSTRACT The knockdown and lethal efficacies of five aerosol formulations including Combat Speed^® (AIs: 0.1 % imiprothrin and 0.3% cyphenothrin), Raid Power^® (AIs: 1.0% pyrethrin and 0.2% permethrin), Home Keeper^®, (AIs: 0.2% tetramethrin and 0.3% permethrin), Super Killer^® (AIs: 0.32% tetramethrin and 0.08% bioresmethrin), and Perma Kill‐K^® (AIs: 0.3% dichlorvos and 0.1% tetramethrin) against five strains of the German cockroach, Blattella germanica (L.) were assessed. The results show that the mean value of KT₅₀ (5.4 sec.) of Combat Speed^® was 4.5 and 3.1‐folds lower than those of Perma Kill‐K^® and Home Keeper^®, respectively. The mean value of KT₉₀ (9.0 sec; slope = 10.02) of Combat Speed^® was 3.8 to 5.8‐folds lower than Perma Kill‐K^®, Supper Killer^® and Home Keeper^®. As lethal effects, the mean value of LT₅₀ (17.3 sec.) of Combat Speed^® was over 26 folds lower than Supper Killer^® and Perma Kill‐K^®. The mean value of LT₉₀ (32.9 sec.) of Combat Speed^® was 37.4 and 15.1‐folds lower than those of Supper Killer^® and Perma Kill‐K^®, respectively. In general, Combat Speed^® and Raid Power^® were considered the insecticide aerosols with faster knockdown and higher lethal effects than Supper Killer^®, Perma Kill‐K^®, and Home Keeper^® against five strains of German cockroaches in Korea. Also, the knockdown and lethal effects of Supper Killer^®, Perma Kill‐K^®, and Home Keeper^® were highly variable depends on the strains.     

GENETIC EXCHANGES OF INTEINS BETWEEN PRASINOVIRUSES (PHYCODNAVIRIDAE)

Phylogenetic diversity in the Phycodnaviridae (double‐stranded DNA viruses infecting photosynthetic eukaryotes) is most often studied using their DNA polymerase gene (PolB). This gene and its translated protein product can harbor a selfish genetic element called an “intein” that disrupts the sequence of the host gene without affecting its activity. After translation, the intein peptide sequence self‐excises precisely, producing a functional ligated host protein. In addition, inteins can encode homing endonuclease (HEN) domains that permit the possibility of lateral transfers to intein‐free alleles. However, no clear evidence for their transfer between viruses has previously been shown. The objective of this paper was to determine whether recent transfers of inteins have occurred between prasinoviruses (Phycodnaviridae) that infect the Mamiellophyceae, an abundant and widespread class of unicellular green algae, by using DNA sequence analyses and cophylogenetic methods. Our results suggest that transfer among prasinoviruses is a dynamic ongoing process and, for the first time in the Phycodnaviridae family, we showed a recombination event within an intein.