A test for Y‐linked additive and epistatic effects on surviving bacterial infections in Drosophila melanogaster

Y‐ and W‐chromosomes offer a theoretically powerful way for sexual dimorphism to evolve. Consistent with this possibility, Drosophila melanogaster Y‐chromosomes can influence gene regulation throughout the genome; particularly immune‐related genes. In order for Y‐linked regulatory variation (YRV) to contribute to adaptive evolution it must be comprised of additive genetic variance, such that variable Ys induce consistent phenotypic effects within the local gene pool. We assessed the potential for Y‐chromosomes to adaptively shape gram‐negative and gram‐positive bacterial defence by introgressing Ys across multiple genetic haplotypes from the same population. We found no Y‐linked additive effects on immune phenotypes, suggesting a restricted role for the Y to facilitate dimorphic evolution. We did find, however, a large magnitude Y by background interaction that induced rank order reversals of Y‐effects across the backgrounds (i.e. sign epistasis). Thus, Y‐chromosome effects appeared consistent within backgrounds, but highly variable among backgrounds. This large sign epistatic effect could constrain monomorphic selection in both sexes, considering that autosomal alleles under selection must spend half of their time in a male background where relative fitness values are altered. If the pattern described here is consistent for other traits or within other XY (or ZW) systems, then YRV may represent a universal constraint to autosomal trait evolution.     

Context‐dependent effects of Y chromosome and mitochondrial haplotype on male locomotive activity in Drosophila melanogaster

Some regions of the genome exhibit sexual asymmetries in inheritance and are thus subjected to sex‐biased evolutionary forces. Maternal inheritance of mitochondrial DNA (mtDNA) enables mtDNA mutations harmful to males, but not females, to accumulate. In the face of male‐harmful mtDNA mutation accumulation, selection will favour the evolution of compensatory modifiers in the nuclear genome that offset fitness losses to males. The Y chromosome is a candidate to host these modifiers, because it is paternally inherited, known to harbour an abundance of genetic variation for male fertility, and therefore likely to be under strong selection to uphold male viability. Here, we test for intergenomic interactions involving mtDNA and Y chromosomes in male Drosophila melanogaster. Specifically, we examine effects of each of these genomic regions, and their interaction, on locomotive activity, across different environmental contexts – both dietary and social. We found that both the mtDNA haplotype and Y chromosome haplotype affected activity in males assayed in an environment perceived as social. These effects, however, were not evident in males assayed in perceived solitary environments, and neither social nor solitary treatments revealed evidence for intergenomic interactions. Finally, the magnitude and direction of these genetic effects was further contingent on the diet treatment of the males. Thus, genes within the mtDNA and Y chromosome are involved in genotype‐by‐environment interactions. These interactions might contribute to the maintenance of genetic variation within these asymmetrically inherited gene regions and complicate the dynamics of genetic interactions between the mtDNA and the Y chromosome.     

Phenotypic effects of the Y chromosome are variable and structured in hybrids among house mouse recombinant lines

Hybrid zones between divergent populations sieve genomes into blocks that introgress across the zone, and blocks that do not, depending on selection between interacting genes. Consistent with Haldane's rule, the Y chromosome has been considered counterselected and hence not to introgress across the European house mouse hybrid zone. However, recent studies detected massive invasion of M. m. musculus Y chromosomes into M. m. domesticus territory. To understand mechanisms facilitating Y spread, we created 31 recombinant lines from eight wild‐derived strains representing four localities within the two mouse subspecies. These lines were reciprocally crossed and resulting F1 hybrid males scored for five phenotypic traits associated with male fitness. Molecular analyses of 51 Y‐linked SNPs attributed ~50% of genetic variation to differences between the subspecies and 8% to differentiation within both taxa. A striking proportion, 21% (frequencies of sperm head abnormalities) and 42% (frequencies of sperm tail dissociations), of phenotypic variation was explained by geographic Y chromosome variants. Our crossing design allowed this explanatory power to be examined across a hierarchical scale from subspecific to local intrastrain effects. We found that divergence and variation were expressed diversely in different phenotypic traits and varied across the whole hierarchical scale. This finding adds another dimension of complexity to studies of Y introgression not only across the house mouse hybrid zone but potentially also in other contact zones.     

Autosomal suppression and fitness costs of an old driving X chromosome in Drosophila testacea

Driving X chromosomes (X^Ds) bias their own transmission through males by killing Y‐bearing gametes. These chromosomes can in theory spread rapidly in populations and cause extinction, but many are found as balanced polymorphisms or as “cryptic” X^Ds shut down by drive suppressors. The relative likelihood of these outcomes and the evolutionary pathways through which they come about are not well understood. An X^D was recently discovered in the mycophagous fly, Drosophila testacea, presenting the opportunity to compare this X^D with the well‐studied X^D of its sister species, Drosophila neotestacea. Comparing features of independently evolved X^Ds in young sister species is a promising avenue towards understanding how X^Ds and their counteracting forces change over time. In contrast to the X^D of D. neotestacea, we find that the X^D of D. testacea is old, with its origin predating the radiation of three species: D. testacea, D. neotestacea and their shared sister species, Drosophila orientacea. Motivated by the suggestion that older X^Ds should be more deleterious to carriers, we assessed the effect of the X^D on both male and female fertility. Unlike what is known from D. neotestacea, we found a strong fitness cost in females homozygous for the X^D in D. testacea: a large proportion of homozygous females failed to produce offspring after being housed with males for several days. Our male fertility experiments show that although X^D male fertility is lower under sperm‐depleting conditions, X^D males have comparable fertility to males carrying a standard X chromosome under a free‐mating regime, which may better approximate conditions in wild populations of D. testacea. Lastly, we demonstrate the presence of autosomal suppression of X chromosome drive. Our results provide support for a model of X^D evolution where the dynamics of young X^Ds are governed by fitness consequences in males, whereas in older X^D systems, both suppression and fitness consequences in females likely supersede male fitness costs.     

Two Tests of Y Chromosomal Variation in Male Fertility of Drosophila Melanogaster

Deficiency mapping with Y autosome translocations has shown that the Y chromosome of Drosophila melanogaster carries genes that are essential to male fertility. While the qualitative behavior of these lesions provides important insight into the physiological importance of the Y chromosome, quantitative variation in effects on male fertility among extant Y chromosomes in natural populations may have a significant effect on the evolution of the Y chromosome. Here a series of 36 Y chromosome replacement lines were tested in two ways designed to detect subtle variation in effects on male fertility and total male fitness. The first test involved crossing males from the 36 lines to an excess of females in an attempt to measure differences in male mating success (virility) and male fecundity. The second test challenged males bearing each of the 36 Y chromosomes to competition in populations with males bearing a standard, phenotypically marked (BsY) chromosome. These tests indicated that the Y chromosome lines did not differ significantly in either male fertility or total fitness, but that interactions with autosomes approached significance. A deterministic population genetic model was developed allowing Y autosome interaction in fertility, and it is shown that, consistent with the experimental observations, this model cannot protect Y-linked polymorphism.     

Intergenomic interactions between mitochondrial and Y‐linked genes shape male mating patterns and fertility in Drosophila melanogaster

Under maternal inheritance, mitochondrial genomes are prone to accumulate mutations that exhibit male‐biased effects. Such mutations should, however, place selection on the nuclear genome for modifier adaptations that mitigate mitochondrial‐incurred male harm. One gene region that might harbor such modifiers is the Y‐chromosome, given the abundance of Y‐linked variation for male fertility, and because Y‐linked modifiers would not exert antagonistic effects in females because they would be found only in males. Recent studies in Drosophila revealed a set of nuclear genes whose expression is sensitive to allelic variation among mtDNA‐ and Y‐haplotypes, suggesting these genes might be entwined in evolutionary conflict between mtDNA and Y. Here, we test whether genetic variation across mtDNA and Y haplotypes, sourced from three disjunct populations, interacts to affect male mating patterns and fertility across 10 days of early life in D. melanogaster. We also investigate whether coevolved mito‐Y combinations outperform their evolutionarily novel counterparts, as predicted if the interacting Y‐linked variance is comprised of modifier adaptations. Although we found no evidence that coevolved mito‐Y combinations outperformed their novel counterparts, interactions between mtDNA and Y‐chromosomes affected male mating patterns. These interactions were dependent on male age; thus male reproductive success was shaped by G × G × E interactions.     

Polymorphisms in a desaturase 2 ortholog associate with cuticular hydrocarbon and male mating success variation in a natural population of Drosophila serrata

Elucidating the nature of genetic variation underlying both sexually selected traits and the fitness components of sexual selection is essential to understanding the broader consequences of sexual selection as an evolutionary process. To date, there have been relatively few attempts to connect the genetic variance in sexually selected traits with segregating DNA sequence polymorphisms. We set out to address this in a well‐characterized sexual selection system – the cuticular hydrocarbons (CHCs) of Drosophila serrata – using an indirect association study design that allowed simultaneous estimation of the genetic variance in CHCs, sexual fitness and single nucleotide polymorphism (SNP) effects in an outbred population. We cloned and sequenced an ortholog of the D. melanogaster desaturase 2 gene, previously shown to affect CHC biosynthesis in D. melanogaster, and associated 36 SNPs with minor allele frequencies > 0.02 with variance in CHCs and sexual fitness. Three SNPs had significant multivariate associations with CHC phenotype (q‐value < 0.05). At these loci, minor alleles had multivariate effects on CHCs that were weakly associated with the multivariate direction of sexual selection operating on these traits. Two of these SNPs had pleiotropic associations with male mating success, suggesting these variants may underlie responses to sexual selection due to this locus. There were 15 significant male mating success associations (q‐value < 0.1), and interestingly, we detected a nonrandom pattern in the relationship between allele frequency and direction of effect on male mating success. The minor‐frequency allele usually reduced male mating success, suggesting a positive association between male mating success and total fitness at this locus.     

Occasional recombination of a selfish X‐chromosome may permit its persistence at high frequencies in the wild

The sex‐ratio X‐chromosome (SR) is a selfish chromosome that promotes its own transmission to the next generation by destroying Y‐bearing sperm in the testes of carrier males. In some natural populations of the fly Drosophila neotestacea, up to 30% of the X‐chromosomes are SR chromosomes. To investigate the molecular evolutionary history and consequences of SR, we sequenced SR and standard (ST) males at 11 X‐linked loci that span the ST X‐chromosome and at seven arbitrarily chosen autosomal loci from a sample of D. neotestacea males from throughout the species range. We found that the evolutionary relationship between ST and SR varies among individual markers, but genetic differentiation between SR and ST is chromosome‐wide and likely due to large chromosomal inversions that suppress recombination. However, SR does not consist of a single multilocus haplotype: we find evidence for gene flow between ST and SR at every locus assayed. Furthermore, we do not find long‐distance linkage disequilibrium within SR chromosomes, suggesting that recombination occurs in females homozygous for SR. Finally, polymorphism on SR is reduced compared to that on ST, and loci displaying signatures of selection on ST do not show similar patterns on SR. Thus, even if selection is less effective on SR, our results suggest that gene flow with ST and recombination between SR chromosomes may prevent the accumulation of deleterious mutations and allow its long‐term persistence at relatively high frequencies.     

Analysis of transposable elements and organellar DNA in male and female genomes of a species with a huge Y chromosome reveals distinct Y centromeres

Few angiosperms have distinct Y chromosomes. Among those that do are Silene latifolia (Caryophyllaceae), Rumex acetosa (Polygonaceae) and Coccinia grandis (Cucurbitaceae), the latter having a male/female difference of 10% of the total genome (female individuals have a 0.85 pg genome, male individuals 0.94 pg), due to a Y chromosome that arose about 3 million years ago. We compared the sequence composition of male and female C. grandis plants and determined the chromosomal distribution of repetitive and organellar DNA with probes developed from 21 types of repetitive DNA, including 16 mobile elements. The size of the Y chromosome is largely due to the accumulation of certain repeats, such as members of the Ty1/copia and Ty3/gypsy superfamilies, an unclassified element and a satellite, but also plastome‐ and chondriome‐derived sequences. An abundant tandem repeat with a unit size of 144 bp stains the centromeres of the X chromosome and the autosomes, but is absent from the Y centromere. Immunostaining with pericentromere‐specific markers for anti‐histone H3Ser10ph and H2AThr120ph revealed a Y‐specific extension of these histone marks. That the Y centromere has a different make‐up from all the remaining centromeres raises questions about its spindle attachment, and suggests that centromeric or pericentromeric chromatin might be involved in the suppression of recombination.     

Hybrid dysgenesis-induced Y chromosomal sterility in Drosophila melanogaster

Summary Dysgenic hybrids of Drosophila melanogaster were screened for the induction of mutations in the Y chromosomal fertility genes. Out of 2,417 Y chromosomes analysed 13 male steriles (ms (Y)) were isolated. This high rate of mutation is most probably due to the unusually large physical size of the fertility genes.     

Common Mechanisms of Y Chromosome Evolution

Y chromosome evolution is characterized by the expansion of genetic inertness along the Y chromosome and changes in the chromosome structure, especially the tendency of becoming heterochromatic. It is generally assumed that the sex chromosome pair has developed from a pair of homologues. In an evolutionary process the proto-Y-chromosome, with a very short differential segment, develops in its final stage into a completely heterochromatic and to a great extends genetically eroded Y chromosome. The constraints evolving the Y chromosome have been the objects of speculation since the discovery of sex chromosomes. Several models have been suggested. We use the exceptional situation of the in Drosophila mirandato analyze the molecular process in progress involved in Y chromosome evolution. We suggest that the first steps in the switch from a euchromatic proto-Y-chromosome into a completely heterochromatic Y chromosome are driven by the accumulation of transposable elements, especially retrotransposons inserted along the evolving nonrecombining part of the Y chromosome. In this evolutionary process trapping and accumulation of retrotransposons on the proto-Y-chromosome should lead to conformational changes that are responsible for successive silencing of euchromatic genes, both intact or already mutated ones and eventually transform functionally euchromatic domains into genetically inert heterochromatin. Accumulation of further mutations, deletions, and duplications followed by the evolution and expansion of tandem repetitive sequence motifs of high copy number (satellite sequences) together with a few vital genes for male fertility will then represent the final state of the degenerated Y chromosome. This revised version was published online in July 2006 with corrections to the Cover Date.     

Clustering of loci controlling species differences in male chemical bouquets of sympatric Heliconius butterflies

The degree to which loci promoting reproductive isolation cluster in the genome—that is, the genetic architecture of reproductive isolation—can influence the tempo and mode of speciation. Tight linkage between these loci can facilitate speciation in the face of gene flow. Pheromones play a role in reproductive isolation in many Lepidoptera species, and the role of endogenously produced compounds as secondary metabolites decreases the likelihood of pleiotropy associated with many barrier loci. Heliconius butterflies use male sex pheromones to both court females (aphrodisiac wing pheromones) and ward off male courtship (male‐transferred antiaphrodisiac genital pheromones), and it is likely that these compounds play a role in reproductive isolation between Heliconius species. Using a set of backcross hybrids between H. melpomene and H. cydno, we investigated the genetic architecture of putative male pheromone compound production. We found a set of 40 significant quantitative trait loci (QTL) representing 33 potential pheromone compounds. QTL clustered significantly on two chromosomes, chromosome 8 for genital compounds and chromosome 20 for wing compounds, and chromosome 20 was enriched for potential pheromone biosynthesis genes. There was minimal overlap between pheromone QTL and known QTL for mate choice and color pattern. Nonetheless, we did detect linkage between a QTL for wing androconial area and optix, a color pattern locus known to play a role in reproductive isolation in these species. This tight clustering of putative pheromone loci might contribute to coincident reproductive isolating barriers, facilitating speciation despite ongoing gene flow.     

The Y chromosome as a target for acquired and amplified genetic material in evolution

The special properties of the Y chromosome stem form the fact that it is a non-recombining degenerate derivative of the X chromosome. The absence of homologous recombination between the X and the Y chromosome leads to gradual degeneration of various Y chromosome genes on an evolutionary timescale. The absence of recombination, however, also favors the accumulation of transposable elements on the Y chromosome during its evolution, as seen with both Drosophila and mammalian Y chromosomes. Alongside these processes, the acquisition and amplification of autosomal male benefit genes occur. This review will focus on recent studies that reveal the autosome-acquired genes on the Y chromosome of both Drosophila and humans. The evolution of the acquired and amplified genes on the Y chromosome is also discussed. Molecular and comparative analyses of Y-linked repeats in the Drosophila melanogaster genome demonstrate that there was a period of their degeneration followed by a period of their integration into RNAi silencing, which was beneficial for male fertility. Finally, the function of non-coding RNA produced by amplified Y chromosome genetic elements will be discussed.     

Correlation between recombination frequency and fitness in Drosophila melanogaster

The origin and maintenance of genetic recombination are unsettled evolutionary issues. Genetic variation affecting recombination frequency appears to be pervasive in nature, suggesting that natural selection must increase recombination frequency under some circumstances. However, theoretical arguments and experimental evidence indicate that the frequency of recombination should be reduced by natural selection.A hypothesis not previously explored is that recombination modifiers may directly affect the fitness of their carriers; rather than only indirectly (through the production of recombinant progeny) as generally assumed. We have tested this hypothesis by examining three fitness components (viability, male fertility, and female fecundity) in Drosophila melanogaster homozygous for second chromosomes isolated from a natural population. Then, we have measured the frequency of recombination in flies heterozygous for each wild second chromosome and a chromosome carrying five recessive alleles.The results indicate that genes modulating the frequency of recombination have direct effects on fitness as proposed by the hypothesis. However, the correlation between frequency of recombination and fitness is negative. Thus, the riddle of recombination remains unexplained and, in fact, more puzzling that ever.     

Y‐chromosome and mtDNA variation confirms independent domestications and directional hybridization in South American camelids

Investigations of genetic diversity and domestication in South American camelids (SAC) have relied on autosomal microsatellite and maternally‐inherited mitochondrial data. We present the first integrated analysis of domestic and wild SAC combining male and female sex‐specific markers (male specific Y‐chromosome and female‐specific mtDNA sequence variation) to assess: (i) hypotheses about the origin of domestic camelids, (ii) directionality of introgression among domestic and/or wild taxa as evidence of hybridization and (iii) currently recognized subspecies patterns. Three male‐specific Y‐chromosome markers and control region sequences of mitochondrial DNA are studied here. Although no sequence variation was found in SRY and ZFY, there were seven variable sites in DBY generating five haplotypes on the Y‐chromosome. The haplotype network showed clear separation between haplogroups of guanaco–llama and vicuña–alpaca, indicating two genetically distinct patrilineages with near absence of shared haplotypes between guanacos and vicuñas. Although we document some examples of directional hybridization, the patterns strongly support the hypothesis that llama (Lama glama) is derived from guanaco (Lama guanicoe) and the alpaca (Vicugna pacos) from vicuña (Vicugna vicugna). Within male guanacos we identified a haplogroup formed by three haplotypes with different geographical distributions, the northernmost of which (Peru and northern Chile) was also observed in llamas, supporting the commonly held hypothesis that llamas were domesticated from the northernmost populations of guanacos (L. g. cacilensis). Southern guanacos shared the other two haplotypes. A second haplogroup, consisting of two haplotypes, was mostly present in vicuñas and alpacas. However, Y‐chromosome variation did not distinguish the two subspecies of vicuñas.     

Inbreeding alters intersexual fitness correlations in Drosophila simulans.

Intralocus sexual conflict results from sexually antagonistic selection on traits shared by the sexes. This can displace males and females from their respective fitness optima, and negative intersexual correlations (r_mf) for fitness are the unequivocal indicator of this evolutionary conflict. It has recently been suggested that intersexual fitness correlations can vary depending on the segregating genetic variation present in a population, and one way to alter genetic variation and test this idea is via inbreeding. Here, we test whether intersexual correlations for fitness vary with inbreeding in Drosophila simulans isolines reared under homogenous conditions. We measured male and female fitness at different times following the establishment of isofemale lines and found that the sign of the association between the two measures varied with time after initial inbreeding. Our results are consistent with suggestions that the type of genetic variation segregating within a population can determine the extent of intralocus sexual conflict and also support the idea that sexually antagonistic alleles segregate for longer in populations than alleles with sexually concordant effects.     

Population‐dependent reproducible deviation from natural bread wheat genome in synthetic hexaploid wheat

Sequence elimination is one of the main mechanisms that increases the divergence among homoeologous chromosomes after allopolyploidization to enhance the stability of recently established lineages, but it can cause a loss of some economically important genes. Synthetic hexaploid wheat (SHW) is an important source of genetic variation to the natural hexaploid wheat (NHW) genepool that has low genetic diversity. Here, we investigated the change between SHW and NHW genomes by utilizing a large germplasm set of primary synthetics and synthetic derivatives. Reproducible segment elimination (RSE) was declared if a large chromosomal chunk (>5 cM) produced no aligned reads in more than five SHWs. RSE in five genomic regions was the major source of variation between SHW and NHW. One RSE eliminated almost the complete short arm of chromosome 1B, which contains major genes for flour quality, disease resistance and different enzymes. The occurrence of RSE was highly dependent on the choice of diploid and tetraploid parental lines, their ancestral subpopulation and admixture, e.g. SHWs derived from Triticum dicoccon or from one of two Aegilops tauschii subpopulations were almost free of RSE, while highly admixed parents had higher RSE rates. The rate of RSE in synthetic derivatives was almost double that in primary synthetics. Genome‐wide association analysis detected four loci with minor effects on the occurrence of RSE, indicating that both parental lines and genetic factors were affecting the occurrence of RSE. Therefore, pre‐pre‐breeding strategies should be applied before introducing SHW into pre‐breeding programs to ensure genomic stability and avoid undesirable gene loss.     

Sperm competitive advantage of a rare mitochondrial haplogroup linked to differential expression of mitochondrial oxidative phosphorylation genes

Maternal inheritance of mitochondria creates a sex‐specific selective sieve through which mitochondrial mutations harmful to males but not females accumulate and contribute to sexual differences in longevity and disease susceptibility. Because eggs and sperm are under disruptive selection, sperm are predicted to be particularly vulnerable to the genetic load generated by maternal inheritance, yet evidence for mitochondrial involvement in male fertility is limited and controversial. Here, we exploit the coexistence of two divergent mitochondrial haplogroups (A and B2) in a Neotropical arachnid to investigate the role of mitochondria in sperm competition. DNA profiling demonstrated that B2‐carrying males sired more than three times as many offspring in sperm competition experiments than A males, and this B2 competitive advantage cannot be explained by female mitochondrial haplogroup or male nuclear genetic background. RNA‐Seq of testicular tissues implicates differential expression of mitochondrial oxidative phosphorylation (OXPHOS) genes in the B2 competitive advantage, including a 22‐fold upregulation of atp8 in B2 males. Previous comparative genomic analyses have revealed functionally significant amino acid substitutions in differentially expressed genes, indicating that the mitochondrial haplogroups differ not only in expression but also in DNA sequence and protein functioning. However, mitochondrial haplogroup had no effect on sperm number or sperm viability, and, when females were mated to a single male, neither male haplogroup, female haplogroup nor the interaction between male/female haplogroup significantly affected female reproductive success. Our findings therefore suggest that mitochondrial effects on male reproduction may often go undetected in noncompetitive contexts and may prove more important in nature than is currently appreciated.