Cytoplasmic Sex Ratio Distorters Research Articles

Sex chromosomes control vertical transmission of feminizing Wolbachiasymbionts in an isopod.

Microbial endosymbiosis is widespread in animals, with major ecological and evolutionary implications. Successful symbiosis relies on efficient vertical transmission through host generations. However, when symbionts negatively affect host fitness, hosts are expected to evolve suppression of symbiont effects or transmission. Here, we show that sex chromosomes control vertical transmission of feminizing Wolbachia endosymbionts in the isopod Armadillidium nasatum. Theory predicts that the invasion of an XY/XX species by cytoplasmic sex ratio distorters is unlikely because it leads to fixation of the unusual (and often lethal or infertile) YY genotype. We demonstrate that A. nasatum X and Y sex chromosomes are genetically highly similar and that YY individuals are viable and fertile, thereby enabling Wolbachia spread in this XY-XX species. Nevertheless, we show that Wolbachia cannot drive fixation of YY individuals, because infected YY females do not transmit Wolbachia to their offspring, unlike XX and XY females. The genetic basis fits the model of a Y-linked recessive allele (associated with an X-linked dominant allele), in which the homozygous state suppresses Wolbachia transmission. Moreover, production of all-male progenies by infected YY females restores a balanced sex ratio at the host population level. This suggests that blocking of Wolbachia transmission by YY females may have evolved to suppress feminization, thereby offering a whole new perspective on the evolutionary interplay between microbial symbionts and host sex chromosomes.

Rapid comeback of males: evolution of male-killer suppression in a green lacewing population.

Evolutionary theory predicts that the spread of cytoplasmic sex ratio distorters leads to the evolution of host nuclear suppressors, although there are extremely few empirical observations of this phenomenon. Here, we demonstrate that a nuclear suppressor of a cytoplasmic male killer has spread rapidly in a population of the green lacewing Mallada desjardinsi An M. desjardinsi population, which was strongly female-biased in 2011 because of a high prevalence of the male-killing Spiroplasma endosymbiont, had a sex ratio near parity in 2016, despite a consistent Spiroplasma prevalence. Most of the offspring derived from individuals collected in 2016 had 1 : 1 sex ratios in subsequent generations. Contrastingly, all-female or female-biased broods appeared frequently from crossings of these female offspring with males derived from a laboratory line founded by individuals collected in 2011. These results suggest near-fixation of a nuclear suppressor against male killing in 2016 and reject the notion that a non-male-killing Spiroplasma variant has spread in the population. Consistently, no significant difference was detected in mitochondrial haplotype variation between 2011 and 2016. These findings, and earlier findings in the butterfly Hypolimnas bolina in Samoa, suggest that these quick events of male recovery occur more commonly than is generally appreciated.

Can Wolbachia (Rickettsiaceae) explain female-biased sex ratios in mountain pine beetles (Coleoptera: Curculionidae)?

AbstractWolbachia Hertig (Rickettsiales: Rickettsiaceae) is a genus of endosymbionts that are widespread in insects and can have important implications on population dynamics through cytoplasmic incompatibility or sex-ratio distortion. We considered Wolbachia as a possible explanation for female-biased sex ratios often observed in mountain pine beetle populations, Dendroctonus ponderosae Hopkins (Coleoptera: Curculionidae: Scolytinae), a major pest species in western Canada whose most recent outbreak and range expansion has killed many millions of mature lodgepole pine, Pinus contorta var. latifolia Engelmann (Pinaceae). We used wsp primers to screen for Wolbachia in 10 mountain pine beetle populations with varying degrees of female bias in southeast British Columbia and southwest Alberta, Canada. We found no evidence of Wolbachia in these populations and suggest that other factors may explain the sex-ratio bias.

The Effective Size of Populations Infected With Cytoplasmic Sex-Ratio Distorters

Many arthropod species are infected with maternally inherited endosymbionts that induce a shift in the sex ratio of their hosts by feminizing or killing males (cytoplasmic sex-ratio distorters, or SRDs). These endosymbionts can have profound impacts on evolutionary processes of their hosts. Here, I derive analytical expressions for the coalescent effective size N(e) of populations that are infected with SRDs. Irrespective of the type of SRD, N(e) for mitochondrial genes is given by the number of infected females. For nuclear genes, the effective population size generally decreases with increasing prevalence of the SRD and can be considerably lower than the actual size of the population. For example, with male-killing bacteria that have near perfect maternal transmission, N(e) is reduced by a factor that is given to a good approximation by the proportion of uninfected individuals in the population. The formulae derived here also yield the effective size of populations infected with mutualistic endosymbionts or maternally inherited bacteria that induce cytoplasmic incompatibility, although in these cases, the reduction in N(e) is expected to be less severe than for cytoplasmic SRDs.

Evolution of cytoplasmic sex ratio distorters: Effect of paternal transmission

Eukaryotic organisms carry various genetic factors the so-called cytoplasmic genetic elements (CGEs), in their cytoplasm. Numerous examples are known in which CGEs possess the ability to control sex determination of their host organisms and cause sex ratio distortion (SRD). In general, CGEs are inherited maternally from female hosts, via egg cytoplasm to offspring. Thus, the elements tend to evolve abilities to avoid entrance into “dead-end” males. Previous theoretical studies have revealed that, as long as maternal transmission is perfect, CGEs evolve the highest levels of ability to cause SRD. However, it is recently reported that some CGEs transmit from male to offspring through infection to female in mating. This raises the question of how such a paternal contribution alters selective forces and SRD evolution. In the present study, the evolutionary process of SRD ability of CGEs was analyzed theoretically. The main finding is that paternal transmission results in evolution towards intermediate levels of SRD. Further, coexistence was observed of different CGEs inducing different levels of SRD. These results point to the importance of paternal transmission in the evolution of CGEs.

A Gene’s‐Eye View of Symbiont Transmission

Symbiotic associations between species are ubiquitous, but we only poorly understand why some symbioses evolve to be mutualistic and others to be parasitic. One prominent hypothesis holds that vertical transmission of symbionts from host parents to their offspring selects for symbionts that are benign or beneficial, while horizontal transmission of symbionts among unrelated hosts selects for symbionts that are less beneficial or outright harmful. A long-standing challenge to this hypothesis, however, is the existence of selfish genetic elements (SGEs). SGEs are passed exclusively from parent to offspring and are able to spread and persist in populations despite reducing the fitness of their hosts. Here I show that SGEs are in fact consistent with the transmission mode hypothesis if one measures transmission from the perspective of host genes instead of host organisms. Both meiotic drive genes and cytoplasmic sex ratio distorters require horizontal transmission, in the form of outbred sex, to spread as parasites. Transmission from parent to offpsring does not constrain SGEs to evolve toward mutualism. The gene-centered perspective I present here is applicable to symbioses at all levels of selection and brings closer together our understandings of cooperation within and between species.

A Gene's-Eye View of Symbiont Transmission

Symbiotic associations between species are ubiquitous, but we only poorly understand why some symbioses evolve to be mutualistic and others to be parasitic. One prominent hypothesis holds that vertical transmission of symbionts from host parents to their offspring selects for symbionts that are benign or beneficial, while horizontal transmission of symbionts among unrelated hosts selects for symbionts that are less beneficial or outright harmful. A long‐standing challenge to this hypothesis, however, is the existence of selfish genetic elements (SGEs). SGEs are passed exclusively from parent to offspring and are able to spread and persist in populations despite reducing the fitness of their hosts. Here I show that SGEs are in fact consistent with the transmission mode hypothesis if one measures transmission from the perspective of host genes instead of host organisms. Both meiotic drive genes and cytoplasmic sex ratio distorters require horizontal transmission, in the form of outbred sex, to spread as parasites. Transmission from parent to offpsring does not constrain SGEs to evolve toward mutualism. The gene‐centered perspective I present here is applicable to symbioses at all levels of selection and brings closer together our understandings of cooperation within and between species.

Nasonia

What is Nasonia? A small (2–3mm) parasitoid wasp that oviposits in the pupae of flies (but not those of Drosophila!). This hymenopteran occurs naturally in bird nests and at carcasses. Three species are known: the cosmopolitan N. vitripennis and two endemic North American species, N. giraulti and N. longicornis. Nasonia is extremely easy to culture on commercially available host pupae, it has a short generation time (15 days at 25°C) and can be maintained in diapause for over one year. What is so special about Nasonia?Nasonia has haplodiploid reproduction; haploid males develop from unfertilized eggs and diploid females from fertilized eggs. Thus, all recessive traits are expressed directly in the male: this is the case for X chromosome genes in Drosophila, but with Nasonia it is true of the entire genome. An extensive forward genetic screen for developmental mutants has already been accomplished and the identification of candidate genes is under way. Unlike the honey bee and many other hymenopterans, Nasonia has no single locus complementary sex determination, which allows fully homozygous strains to be kept without inbreeding problems. Another major advantage of Nasonia is that the three species, which exhibit considerable morphological and behavioral differences, can produce viable and fertile hybrids in the laboratory. The genetic basis for these differences can thus be easily identified through QTL analysis. Nasonia is also very favorable for cell biology, with its very clear yolk and slow early development which allow easy imaging. A useful species for studying the evolution of development then? Yes. General patterns in development and evolution can only come from comparison of multiple organisms. Nasonia has a long germband mode of development, which facilitates comparison of expression patterns with Drosophila; in contrast the beetle Tribolium, also much used for studies of the evolution of development, exhibits short germband development. Transgenic and RNAi tools are also being developed for Nasonia. With respect to sex determination, it will be exciting to figure out how ploidy differences lead to determination of the two sexes. What aspects of evolutionary genetics might Nasonia illuminate?Nasonia is extensively used to study the evolution of sex ratios and speciation. Females vary the sex of their offspring by controlling whether eggs are fertilized. A number of non-Mendelian elements, including the ‘selfish’ paternal sex-ratio chromosome and cytoplasmic sex-ratio distorters illustrate genetic conflict over sex determination. Nasonia is one of the primary organisms used to investigate the evolution and mechanisms of action of Wolbachia, an intracellular bacterium which infects many arthropods. Finally, exciting work is being done, using the three cross-fertile species, on the genetic basis of hybrid incompatibilities and interspecies differences in morphology and behaviour (wingsize and courtship, for example). This takes advantage of exchange of genes or genomic regions between species and the construction of introgression lines in which a gene for a particular trait from one species is bred into another species' genetic background. Are there genomic tools available for Nasonia? Efforts are already underway to develop genetic and genomic tools for Nasonia. Visible genetic markers are known from all five chromosomes. Dense linkage maps containing RAPD, AFLP and microsatellite markers are available with a resolution of approximately 1cM, making possible whole genome screens for mutations and fine-scale mapping of genes. The total genome size is ∼335 Mb and 1cM corresponds to ∼100 Kb of genomic DNA. An embryonic cDNA library and a BAC library funded by NSF have been constructed, and the first attempts at positional cloning are underway, focusing on a major gene for wingsize. Where can I find out more?

Sorting out the effects of Wolbachia, genotype and inbreeding on life-history traits of a spider mite.

Wolbachia bacteria manipulate host reproduction by inducing cytoplasmic incompatibility (CI) and sex ratio distortion. Wolbachia are transmitted from mother to offspring through the cytoplasm of the egg. Therefore, reproduction of Wolbachia is tightly coupled to reproduction of its host. Mathematical analysis predicts that in the course of evolution, traits that reduce the physiological costs of the infection will be selectively favored. For a Wolbachia-host system to evolve, traits under selection must have some genetic component and variation must be present in the population. We have previously established that highly inbred isofemale lines of the two-spotted spider mite Tetranychus urticae may differ regarding the effects of infection by Wolbachia, and that at least some of the traits affected had a genetic component. However, the effects measured could have been affected by the fact that the lines were severely inbred prior to the experiments. In this paper we attempt to distinguish between the effects of Wolbachia, isofemale line, and inbreeding. We show that Wolbachia did not affect longevity but infected females produced smaller clutch sizes, more daughter-biased sex ratios and had decreased F1 mortality; between-line variation was found for clutch size, F1 mortality and sex ratio; finally, inbreeding resulted in an overall reduction of clutch sizes, and a change in survival curves and mean longevity.

The evolutionary dynamics of male-killers and their hosts.

Male-killing bacteria are cytoplasmic sex-ratio distorters that are transmitted vertically through females of their insect hosts. The killing of male hosts by their bacteria is thought to be an adaptive bacterial trait because it augments the fitness of female hosts carrying clonal relatives of those bacteria. Here we attempt to explain observations of multiple male-killers in natural host populations. First we show that such male-killer polymorphism cannot be explained by a classical model of male-killing. We then show that more complicated models incorporating the evolution of resistance in hosts can explain male-killer polymorphism. However, this is only likely if resistance genes are very costly. We also consider the long-term evolutionary dynamics of male-killers, and show that evolution towards progressively more 'efficient' male-killers can be thwarted by the appearance of host resistance. The presence of a resistance gene can allow a less efficient male-killer to outcompete its rival and hence reverse the trend towards more efficient transmission and reduced metabolic load on the host.

SEX DETERMINATION, SEX RATIOS, AND GENETIC CONFLICT

▪ Abstract Genetic mechanisms of sex determination are unexpectedly diverse and change rapidly during evolution. We review the role of genetic conflict as the driving force behind this diversity and turnover. Genetic conflict occurs when different components of a genetic system are subject to selection in opposite directions. Conflict may occur between genomes (including paternal-maternal and parental-zygotic conflicts) or within genomes (between cytoplasmic and nuclear genes or sex chromosomes and autosomes). The sex-determining system consists of parental sex-ratio genes, parental-effect sex determiners, and zygotic sex determiners, which are subject to different selection pressures because of differences in their modes of inheritance and expression. Genetic conflict theory is used to explain the evolution of several sex-determining mechanisms, including sex chromosome drive, cytoplasmic sex-ratio distortion, and cytoplasmic male sterility in plants. Although still limited, there is growing evidence that genetic conflict could be important in the evolution of sex-determining mechanisms.

Genetic conflicts.

Self-promoting elements (also called ultraselfish genes, selfish genes, or selfish genetic elements) are vertically transmitted genetic entities that manipulate their "host" so as to promote their own spread, usually at a cost to other genes within the genome. Examples of such elements include meiotic drive genes and cytoplasmic sex ratio distorters. The spread of a self-promoting element creates the context for the spread of a suppressor acting within the same genome. We may thus say that a genetic conflict exists between different components of the same genome. Here we investigate the properties of such conflicts. First we consider the potential diversity of genomic conflicts and show that every genetic system has potential conflicts. This is followed by analysis of the logic of conflicts. Just as Evolutionarily Stable Strategy (ESS) terminology provides a short cut for discussion of much in behavioral ecology, so the language of modifier analysis provides a useful terminology on which to base discussions of conflicts. After defining genetic conflict, we provide a general analysis of the conflicting parties, and note a distinction between competing and conflicting genes. We then provide a taxonomy of possible short- and long-term outcomes of conflicts, noting that potential conflict in an unconstrained system can never be removed, and that the course of evolution owing to conflict is often unpredictable. The latter is most particularly true for strong conflicts in which suppressors may take surprising forms. The possibility of extended conflicts in the form of "arms races" between element and suppressor is illustrated. The peculiar redundancy of these systems is one possible trace of conflict, and others are discussed. That homologous conflicts may find highly different expression is discussed by referring to the mechanistic differences that are thought to underlie the action of the two best-described meiotic drive genes, and by the multiplicity of forms of cytoplasmic sex ratio distorters. The theoretical analysis establishes a logical basis for thinking about conflicts, but fails to establish the importance of conflict in evolution. We illustrate this contentious issue through consideration of some phenomena for whose evolution conflict has been proposed as an important force: the evolution of sex, sex determination, species, recombination, and uniparental inheritance of cytoplasmic genes. In general, it is proposed that conflict may be a central force in the evolution of genetic systems. We conclude that an analysis of conflict and its general importance in evolution is greatly aided by application of the concept of genetic power. We consider the possible components of genetic power and ask whether and how power evolves.

Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane's rule and related phenomena.

Unisexual hybrid disruption can be accounted for by interactions between sex ratio distorters which have diverged in the species of the hybrid cross. One class of unisexual hybrid disruption is described by Haldane's rule, namely that the sex which is absent, inviable or sterile is the heterogametic sex. This effect is mainly due to incompatibility between X and Y chromosomes. We propose that this incompatibility is due to a mutual imbalance between meiotic drive genes, which are more likely to evolve on sex chromosomes than autosomes. The incidences of taxa with sex chromosome drive closely matches those where Haldane's rule applies: Aves, Mammalia, Lepidoptera and Diptera. We predict that Haldane's rule is not universal but is correct for taxa with sex chromosome meiotic drive. A second class of hybrid disruption affects the male of the species regardless of which sex is heterogametic. Typically the genes responsible for this form of disruption are cytoplasmic. These instances are accounted for by the release from suppression of cytoplasmic sex ratio distorters when in a novel nuclear cytotype. Due to the exclusively maternal transmission of cytoplasm, cytoplasmic sex ratio distorters cause only female-biased sex ratios. This asymmetry explains why hybrid disruption is limited to the male.

Evolutionary consequences of cytoplasmic sex ratio distorters

Computer simulations of diploid genetic models were used to examine the consequences of the spread of a cytoplasmic sex ratio distorter on the frequencies of nuclear sex-determination alleles and the spread of nuclear resistance alleles in female biased populations. The cytoplsmic elements considered here override the expression of the nuclear sex-determination genes, turning genetic males into females. When homozygous male genotypes are viable, a cytoplasmic sex ratio historter spreads in a population if the proportion of daughters produced by infected females exceeds the proportion of daughters produced by uninfected females. The equilibrium frequency of male phenotypes is the proportion of uninfected progeny produced by infected females. When homozygous male genotypes are lethal, the conditions for the spread of the cytoplasmic element are more stringent. The spread of a cytoplasmic sex ratio distorter causes an increase in the frequency of nuclear male sex-determination alleles as a result of the unusual combinations of genotypes which mate in infected populations. Eventually, a cytoplasmic element may replace the nuclear gene as the sex-determination mechanism. This occurs without selection. Nuclear genes conferring resistance to cytoplasmic sex ratio distorters generally increase in female biased populations and often restore a 1∶1 sex ratio despite continual selection on the cytoplasmic element to increase its transmission efficiency.

The coevolution of autosomal and cytoplasmic sex ratio factors

It is generally believed that the presence of cytoplasmic sex ratio distorters in a population causes selective pressure on autosomal genes for a compensatory shift in the sex ratio. Investigations reveal that when within lineage transmission of a cytoplasmic distorter of the primary sex ratio is 100%, no compensatory autosomal sex ratio shift is favored. When transmission is less than 100%, a synergistic interaction occurs between autosomal and cytoplasmic sex ratio factors which results in a polymorphic population with individuals producing either 100% sons (autosomal) or 100% daughters (cytoplasmic). The outcome will only occur if there is sufficient autosomal sex ratio variability in the population for 100% son production. Some cytoplasmic factors cause male larval death, rather than a shift in the primary sex ratio. Such factors have no effect upon autosomal sex ratio selection, and therefore no compensatory sex ratio shift is expected. Even low levels of inbreeding can selectively favor male-killing cytoplasmic factors. Basic models of cytoplasmic sex ratio distortion suggest that cytoplasmic distorters (with high transmission) should increase to or near fixation, thus potentially driving a population to extinction. Models indicate that haplodiploid species are less vulnerable to this population level selection than are diplodiploid species. Among diplodiploid species, cytoplasmic distorters with incomplete transmission will achieve lower frequencies in species without autosomal sex ratio variability.

Sex ratio distortion in populations and its possible role in insect suppression : Experimental studies with strains of Drosophila melanogaster carrying cytoplasmically-inherited male-killing spiroplasmas.

The possible role of cytoplasmic sex ratio (SR) distortion in insect population control has been assessed experimentally. In Drosophila melanogaster the agent responsible for SR distortion is a male-killing spiroplasma and SR strains are characterized by females producing daughters but few, if any, sons. Populations were constructed of wildtype and SR females (of various male-kill effectivenesses) plus males, in different proportions. The frequency of females in the populations was monitored regularly. Under some circumstances the frequency of females increased but not to fixation or population collapse. In most instances the frequency of females declined (to as low as 25% in some cases), then went through cycles of increase and decrease, with gradually reduced amplitude over time. This pattern of fluctuations was repeatable over cages.Independently, it was shown that SR females persisted in the cages for the length of the experiments. The unexpected extremely low frequencies of females found in cages established with an excess of females, raised the possibility of distorting a population by SR releases, and then when the female frequency is at its lowest point to add sterile male or similar load inducers to suppress the population. The possible role of density dependence is discussed.