Sexual conflict and the alternation of haploid and diploid generations

Land plants possess a multicellular diploid stage (sporophyte) that begins development while attached to a multicellular haploid progenitor (gametophyte). Although the closest algal relatives of land plants lack a multicellular sporophyte, they do produce a zygote that grows while attached to the maternal gametophyte. The diploid offspring shares one haploid set of genes with the haploid mother that supplies it with resources and a paternal haploid complement that is not shared with the mother. Sexual conflict can arise within the diploid offspring because the offspring's maternal genome will be transmitted in its entirety to all other sexual and asexual offspring that the mother may produce, but the offspring's paternally derived genes may be absent from these other offspring. Thus, the selective forces favouring the evolution of genomic imprinting may have been present from the origin of modern land plants. In bryophytes, where gametophytes are long-lived and capable of multiple bouts of asexual and sexual reproduction, we predict strong sexual conflict over allocation to sporophytes. Female gametophytes of pteridophytes produce a single sporophyte and often lack means of asexual reproduction. Therefore, sexual conflict is predicted to be attenuated. Finally, we explore similarities among models of mate choice, offspring choice and segregation distortion.     

The paternal sex ratio chromosome in the parasitic wasp Trichogramma kaykai condenses the paternal chromosomes into a dense chromatin mass.

A recently discovered B chromosome in the parasitoid wasp Trichogramma kaykai was found to be transmitted through males only. Shortly after fertilization, this chromosome eliminates the paternal chromosome set leaving the maternal chromosomes and itself intact. Consequently, the sex ratio in these wasps is changed in favour of males by modifying fertilized diploid eggs into male haploid offspring. In this study, we show that in fertilized eggs at the first mitosis the paternal sex ratio (PSR) chromosome condenses the paternal chromosomes into a so-called paternal chromatin mass (PCM). During this process, the PSR chromosome is morphologically unaffected and is incorporated into the nucleus containing the maternal chromosomes. In the first five mitotic divisions, 67% of the PCMs are associated with one of the nuclei in the embryo. Furthermore, in embryos with an unassociated PCM, all nuclei are at the same mitotic stage, whereas 68% of the PCM-associated nuclei are at a different mitotic phase than the other nuclei in the embryo. Our observations reveal an obvious similarity of the mode of action of the PSR chromosome in T. kaykai with that of the PSR-induced paternal genome loss in the unrelated wasp Nasonia vitripennis.     

No evidence for absence of paternal mtDNA in male progeny from pair matings of the mussel Mytilus galloprovincialis

The claim that a Mytilus galloprovincialis male failed to transmit mtDNA to its sons in controlled crosses is shown to be false. At present there is no evidence for mussel males lacking a paternal mtDNA. This makes unlikely the hypothesis that maternal genomes may become paternally transmitted by invading the germ line of males that lack a paternal genome.     

The relationship between DNA methylation and chromosome imprinting in the coccid Planococcus citri

The phenomenon of chromosome, or genomic, imprinting indicates the relevance of parental origin in determining functional differences between alleles, homologous chromosomes, or haploid sets. In mealybug males (Homoptera, Coccoidea), the haploid set of paternal origin undergoes heterochromatization at midcleavage and remains so in most of the tissues. This different behavior of the two haploid sets, which depends on their parental origin, represents one of the most striking examples of chromosome imprinting. In mammals, DNA methylation has been postulated as a possible molecular mechanism to differentially imprint DNA sequences during spermatogenesis or oogenesis. In the present article we addressed the role of DNA methylation in the imprinting of whole haploid sets as it occurs in Coccids. We investigated the DNA methylation patterns at both the molecular and chromosomal level in the mealybug Planococcus citri. We found that in both males and females the paternally derived haploid set is hypomethylated with respect to the maternally derived one. Therefore, in males, it is the paternally derived hypomethylated haploid set that is heterochromatized. Our data suggest that the two haploid sets are imprinted by parent-of-origin-specific DNA methylation with no correlation with the known gene-silencing properties of this base modification.     

Biochemical evidence of haplodiploidy in the whiteflyBemisia tabaci

Polymorphic esterase and acetylcholinesterase alleles in the whiteflyBemisia tabaci were studied using electrophoretic and colorimetric assays. The segregation of these alleles between parental and F₁ generations provided unequivocal evidence of haplodiploidy in this pest species. Unmated females, heterozygous at a polymorphic locus, produced a 1:1 ratio of haploid males expressing either of the maternal alleles. Although male offspring were produced by both virgin and mated females, the segregation of alleles showed they were always haploid (hemizygous) for the marker enzymes. Females only arose from fertilized eggs and invariably expressed paternal and maternal alleles.     

Experimental analysis of a paternally inherited extrachromosomal factor

Virtually all known cases of extrachromosomal inheritance involve cytoplasmic inheritance through the maternal line. Recently, a paternally transmitted factor that causes the production of all-male families has been discovered in a parasitic wasp. The wasp has haplodiploid sex determination: male offspring are haploid and usually develop from unfertilized eggs, whereas females are diploid and usually develop from fertilized eggs. It has been postulated that this paternal sex-ratio factor (psr) is either (1) an infectious agent (a venereal disease) that is transmitted to the female reproductive tract during copulation with an infected male and, subsequently, causes all-male families or (2) a male cytoplasmic factor that is transmitted by sperm to eggs upon egg fertilization and, somehow, causes loss of the paternal set of chromosomes.—Experimental evidence is presented which shows that the factor requires egg fertilization for transmission to the next generation; therefore, it is likely to be a cytoplasmic factor. Significant potential intragenomic conflict results from the presence of this factor and two other sex-ratio distorters in this wasp species.     

Marker-assisted selection to increase effective population size by reducing Mendelian segregation variance

Using both the genetic drift and inbreeding approaches, we derive more general equations for effective size (N(e)) of a diploid species under random mating. These equations show explicitly that inbreeding or genetic drift comes from two sources, the variation in the number of offspring from each parent and the variation in contribution between these parents' own paternally and maternally derived genes to their offspring. The first source can be easily and effectively controlled by choosing an equal number of offspring from each family, while the second can be manipulated by using information on genetic markers to reduce the variance due to Mendelian segregation. Marker-assisted selection (MAS) methods to increase N(e) for the whole genome with single or multiple marker loci per chromosome, different numbers of males, and females are developed and implemented in stochastic simulations. The analytical and simulation results show that, although in principle N(e) can be increased indefinitely, the efficiency of MAS is restricted in practice by the amount of marker information, the genome size, and the number of marker-genotyped offspring per family. The assumptions made in developing the theory and methods and the applications of MAS in conservation are discussed.     

Haplodiploidy as an outcome of coevolution between male-killing cytoplasmic elements and their hosts

Haplodiploidy (encompassing both arrhenotoky and paternal genome elimination) could have originated from coevolution between male-killing endosymbiotic bacteria and their hosts. In insects, haplodiploidy tends to arise in lineages that rely on maternally transmitted bacteria for nutrition and that have gregarious broods in which competition between siblings may occur. When siblings compete, there is strong selection on maternally transmitted elements to kill males. I consider a hypothetical bacterial phenotype that renders male zygotes effectively haploid by preventing chromosome decondensation in male-determining sperm nuclei. By causing high male mortality, such a phenotype can be advantageous to the bacterial lineage. By eliminating paternal genes, it can also be advantageous to the host female. A simple model shows that the host female will benefit under a wide range of values for the efficiency of resource re-allocation, the efficiency of transmission, and the viability of haploid males. This hypothesis helps to explain the ecological correlates of the origins of haplodiploidy, as well as such otherwise puzzling phenomena as obligate cannibalism by male Micromalthus beetles, reversion to diploidy by aposymbiotic male stictococcid scale insects, and the bizarre genomic constitution of scale insect bacteriomes.     

Heteroplasmy suggests paternal co-transmission of multiple genomes and pervasive reversion of maternally into paternally transmitted genomes of mussel (Mytilus) mitochondrial DNA

Marine mussels of the genus Mytilus have two types of mitochondrial DNA with separate paternal and maternal inheritance. Females are homoplasmic for an F genome that is transmitted to all offspring, whereas males are heteroplasmic for this F genome and for a highly diverged (> 20%) M genome that is transmitted only to sons. Here we provide phylogenetic evidence based on lrRNA sequence data that most of the paternal genomes in European M. trossulus have an introgressive female M. edulis origin and are nearly indistinguishable in sequence from F types of M. trossulus. This observation is best explained by the hypothesis that introgressed F type molecules have recently invaded the paternal route and have assumed the role of M molecules, then resetting to zero the time of sequence divergence between M and F lineages. European M. trossulus shows a high prevalence of males heteroplasmic for three different mitochondrial DNA types all having the same two paternal types and the same maternal type, consistent with paternal co-transmission of multiple genomes. Co-transmission of the same genomes must apparently operate uninterruptedly for several generations in spite of the very different evolutionary origin of the specific molecules that are transmitted paternally and maternally in European M. trossulus.     

Mapping of paternal-sex-ratio deletion chromosomes localizes multiple regions involved in expression and transmission

The paternal-sex-ratio (PSR) chromosome in the parasitic wasp Nasonia vitripennis is a submetacentric supernumerary (B chromosome). Males transmit PSR, but after fertilization it causes the loss of the paternal autosomes. Paternal genome loss caused by PSR results in the conversion of a female (diploid) zygote into a male (haploid) under haplodiploid sex determination. In this study, site-specific markers were developed to assay deletion derivatives of PSR. Both polymerase chain reaction and Southern hybridization were used to detect the presence/absence of 16 single-site markers on a set of 20 functional and nine nonfunctional deletion chromosomes. Based on the pattern of marker loss on the deletion chromosomes, the basic organization of PSR was revealed. Two sets of markers were deleted independently, apparently representing the two arms of the submetacentric chromosome. The presence or absence of specific regions was examined in relation to phenotypic characteristics of the deletion chromosomes; ability to cause paternal genome loss, and stability in mitotic cell divisions. Rather than identifying a single region on PSR as being responsible for PSR function, the results suggest that the retention of one of two chromosomal regions is sufficient for causing paternal genome loss. Furthermore, a region was identified that is tightly correlated with mitotic stability, as measured from chromosomal transmission rates. Functional chromosomes with short-arm deletions had high (approximately 100%) transmission rates, whereas functional chromosomes with long-arm deletions had low (approximately 85%) transmission rates.     

The evolution and suppression of male suicide under paternal genome elimination

Different genetic systems can be both the cause and the consequence of genetic conflict over the transmission of genes, obscuring their evolutionary origin. For instance, with paternal genome elimination (PGE), found in some insects and mites, both sexes develop from fertilized eggs, but in males the paternally derived chromosomes are either lost (embryonic PGE) or deactivated (germline PGE) during embryogenesis and not transmitted to the next generation. Evolution of germline PGE requires two transitions: (1) elimination of the paternal genome during spermatogenesis; (2) deactivation of the paternal genome early in development. Hypotheses for the evolution of PGE have mainly focused on the first transition. However, maternal genes seem to be responsible for the deactivation and here we investigate if maternal suppression could have evolved in response to paternally expressed male suicide genes. We show that sibling competition can cause such genes to spread quickly and that inbreeding is necessary to prevent fixation of male suicide, and subsequent population extinction. Once male-suicide has evolved, maternally expressed suppressor genes can invade in the population. Our results highlight the rich opportunity for genetic conflict in asymmetric genetic systems and the counterintuitive phenotypes that can evolve as a result.     

Hyperthermia of male Drosophila melanogaster meiocytes induces abnormalities in both paternal and maternal sex chromosome sets of the offspring

Nondisjunction and loss of sex chromosomes caused by exposure of male Drosophila melanogaster to heat shock (HS) (37 degrees C for 1 h) has been studied to determine the role of mutation l(1)ts403 (sbr10) in the control of chromosome segregation during cell division. Hyperthermia of males at the pupal stage has been demonstrated to increase the number of offspring with abnormalities of not only paternal, but also maternal sex chromosome sets. According to the criterion used, there is a temperature-sensitive period of spermatogenesis, which presumably coincides with meiosis. Phenotypes of some individuals correspond to the presence of two sex chromosomes of obtained from the same parent. The frequency of abnormal chromosome sets in the offspring of male carriers of the sbr10 mutation is about two times higher than in the offspring of males without this mutation.     

Induction of paternal genome loss by the paternal-sex-ratio chromosome and cytoplasmic incompatibility bacteria (Wolbachia): A comparative study of early embryonic events

Paternal genome loss (PGL) during early embryogenesis is caused by two different genetic elements in the parasitoid wasp, Nasonia vitripennis. Paternal sex ratio (PSR) is a paternally inherited supernumerary chromosome that disrupts condensation of the paternal chromosomes by the first mitotic division of fertilized eggs. Bacteria belonging to the genus Wolbachia are present in Nasonia eggs and also disrupt paternal chromosome condensation in crosses between cytoplasmically incompatible strains. Cytoplasmic incompatibility Wolbachia are widespread in insects, whereas PSR is specific to this wasp. PGL results in production of male progeny in Nasonia due to haplodiploid sex determination. The cytological events associated with PGL induced by the PSR chromosome and by Wolbachia were compared by fluorescent light microscopy using the fluorochrome Hoescht 33258. Cytological examination of eggs fertilized with PSR-bearing sperm revealed that a dense paternal chromatin mass forms prior to the first metaphase. Quantification of chromatin by epifluorescence indicates that this mass does undergo replication along with the maternal chromatin prior to the first mitotic division but does not replicate during later mitotic cycles. Contrary to previous reports using other staining methods, the paternal chromatin mass remains condensed during interphase and persists over subsequent mitotic cycles, at least until formation of the syncytial blastoderm and cellularization, at which time it remains near the center of the egg with the yolk nuclei. Wolbachia-induced PGL shows several marked differences. Most notable is that the paternal chromatin mass is more diffuse and tends to be fragmented during the first mitotic division, with portions becoming associated with the daughter nuclei. Nuclei containing portions of the paternal chromatin mass appear to be delayed in subsequent mitotic divisions relative to nuclei free of paternal chromatin. Crosses combining incompatibility with PSR were cytologically similar to Wolbachia-induced PGL, although shearing of the paternal chromatin mass was reduced. Wolbachia may, therefore, block an earlier stage of paternal chromatin processing in the fertilized eggs than does PSR. © 1995 Wiley-Liss, Inc.     

Chromosome rearrangements and survival of androgenetic rainbow trout (Oncorhynchus mykiss)

The purpose of this work was to quantify the impact of spontaneous and X-radiation-induced chromosome rearrangements on survival rate of androgenetic rainbow trout (Oncorhynchus mykiss). Various doses of X irradiation (50, 150, 250, 350 Gy) were used for inactivation of nuclear DNA in oocytes. After the irradiation, eggs were inseminated with normal sperm from 4 males derived from a strain characterized by Robertsonian rearrangements and length polymorphism of the Y chromosome. The haploid zygotes were exposed to a high hydrostatic pressure (7000 psi) to duplicate the paternal DNA. Neither Robertsonian chromosome polymorphism nor the Y chromosome morphology impaired the viability of the androgenetic embryos and alevins. Moreover, survival of eyed embryos of the androgenetic rainbow trout increased significantly with increasing doses of oocyte X irradiation. After 6 months of rearing, only specimens from the 250 and 350 Gy variants survived. The number of fingerlings with remnants of the maternal genome in the forms of chromosome fragments was higher in the 250 Gy group. Intraindividual variation of chromosome fragment number was observed, and some individuals exhibited haploid/diploid mosaicism and body malformations. Individuals irradiated with less than 250 Gy died, presumably because of the conflict between intact paternally derived chromosomes and the residues of maternal genome in the form of chromosome fragments.     

Influence of postzygotic reproductive isolation on the interspecific transmission of the paternal sex ratio chromosome in Trichogramma

The paternal sex ratio (PSR) chromosome is a supernumerary chromosome that causes the destruction of the paternal chromosome set in the first mitosis in a fertilized egg. It is known from parasitoid wasps in the genera Nasonia and Trichogramma (Hymenoptera). In these haplodiploids, the egg fertilized by sperm carrying PSR matures as a haploid male that again carries, and is capable of transmitting, the PSR chromosome. Because of its unique transmission behavior, the PSR chromosome may be easily transmitted between species. This study tests whether the interspecific transmission of PSR between Trichogramma kaykai Pinto and Stouthamer and Trichogramma deion Pinto and Oatman (Hymenoptera: Trichogrammatidae) is affected by two types of postzygotic reproductive isolation, i.e., hybrid inviability and hybrid sterility. The results show that PSR can rescue fertilized eggs that would normally be inviable in the interspecific cross and the rescued eggs develop into male offspring that carry PSR. The results suggest that the two types of postzygotic reproductive isolation have no effect on the transmission of PSR between the two Trichogramma species.     

Nonrandom chromosome arrangements in germ line nuclei of Sciara coprophila males: the basis for nonrandom chromosome segregation on the meiosis I spindle

Meiosis I in males of the Dipteran Sciara coprophila results in the nonrandom distribution of maternally and paternally derived chromosome sets to the two division products. Based on an earlier study (Kubai, D.F. 1982. J. Cell Biol. 93:655-669), I suggested that the meiosis I spindle does not play a direct role in the nonrandom sorting of chromosomes but that, instead, haploid sets are already separated in prophase nuclei well before the onset of spindle formation. Here I report more direct evidence that this hypothesis is true; this evidence was gained from ultrastructural reconstruction analyses of the arrangement of chromosomes in germ line nuclei (prophase nuclei in spermatogonia and spermatocytes) of males heterozygous for an X- autosome chromosome translocation. Because of this translocation, the maternal and paternal chromosome sets are distinguishable, so it is possible to demonstrate that (a) the two haploid chromosome sets occupy distinct maternal and paternal nuclear compartments and that (b) nuclei are oriented so that the two haploid chromosome sets have consistent relationships to a well-defined cellular axis. The consequences of such nonrandom aspects of nuclear structure for chromosome behavior on premeiotic and meiotic spindles are discussed.     

Female‐dependent transmission of paternal mtDNA is a shared feature of bivalve species with doubly uniparental inheritance (DUI) of mitochondrial DNA

Several species from a number of bivalve molluscan families are known to have a paternally transmitted mitochondrial genome, along with the standard maternally transmitted one. The main characteristic of the phenomenon, known as doubly uniparental inheritance (DUI), is the coupling of sex and mtDNA inheritance: males receive both genomes but transmit only the paternal to their progeny; females either do not have the paternal genome or, if they do, they do not transmit it to their progeny. In the families Mytilidae and Veneridae, both of which have DUI, a female individual is either female‐biased (it produces only, or nearly so, female progeny), male‐biased (it produces mainly male progeny) or non‐biased (it produces both genders in intermediate frequencies). Here we present evidence for a same pattern in the freshwater mussel, Unio delphinus (Unionidae). These results suggest that the maternal control of whether a fertilized egg will develop into a male or a female individual (and the associated feature of whether it will inherited or not inherit the paternal mtDNA) is a general characteristic of species with DUI.     

Cytoplasmic Incompatibility and Bacterial Density in Nasonia Vitripennis

Cytoplasmically (maternally) inherited bacteria that cause reproductive incompatibility between strains are widespread among insects. In the parasitoid wasp Nasonia, incompatibility results in improper condensation and fragmentation of the paternal chromosomes in fertilized eggs. Some form of genome imprinting may be involved. Because of haplodiploidy, incompatibility results in conversion of (diploid) female eggs into (haploid) males. Experiments show that bacterial density is correlated with compatibility differences between male and female Nasonia. Males from strains with high bacterial numbers are incompatible with females from strains with lower numbers. Temporal changes in compatibility of females after tetracycline treatment are generally correlated with decreases in bacterial levels in eggs. However, complete loss of bacteria in mature eggs precedes conversion of eggs to the ``asymbiont' compatibility type by 3-4 days. This result is consistent with a critical ``imprinting' period during egg maturation, when cytoplasmic bacteria determine compatibility. Consequent inheritance of reduced bacterial numbers in F(1) progeny has different effects on compatibility type of subsequent male vs. female progeny. In some cases, partial incompatibility occurs which results in reduced offspring numbers, apparently due to incomplete paternal chromosome elimination resulting in aneuploidy.     

A high-density genetic linkage map of a black spruce (Picea mariana) × red spruce (Picea rubens) interspecific hybrid

Genetic maps provide an important genomic resource of basic and applied significance. Spruce (Picea) has a very large genome size (between 0.85 × 1010 and 2.4 × 1010 bp; 8.5-24.0 pg/1C, a mean of 17.7 pg/1C ). We have constructed a near-saturated genetic linkage map for an interspecific backcross (BC1) hybrid of black spruce (BS; Picea mariana (Mill.) B.S.P.) and red spruce (RS; Picea rubens Sarg.), using selectively amplified microsatellite polymorphic loci (SAMPL) markers. A total of 2284 SAMPL markers were resolved using 31 SAMPL-MseI selective nucleotide primer combinations. Of these, 1216 SAMPL markers showing Mendelian segregation were mapped, whereas 1068 (46.8%) SAMPL fragments showed segregation distortion at α = 0.05. Maternal, paternal, and consensus maps consistently coalesced into 12 linkage groups, corresponding to the haploid chromosome number (1n = 1x = 12) of 12 in the genus Picea. The maternal BS map consisted of 814 markers distributed over 12 linkage groups, covering 1670 cM, with a mean map distance of 2.1 cM between adjacent markers. The paternal BS × RS map consisted of 773 markers distributed over 12 linkage groups, covering 1563 cM, with a mean map distance of 2.0 cM between adjacent markers. The consensus interspecific hybrid BC1 map consisted of 1216 markers distributed over 12 linkage groups, covering 1865 cM (98% genome coverage), with a mean map distance of 1.5 cM between adjacent markers. The genetic map reported here provides an important genomic resource in Picea, Pinaceae, and conifers.