Male Viability Research Articles

RUNAWAY SEXUAL SELECTION LEADS TO GOOD GENES

Mate choice and sexual displays are widespread in nature, but their evolutionary benefits remain controversial. Theory predicts these traits can be favored by runaway sexual selection, in which preference and display reinforce one another due to genetic correlation; or by good genes benefits, in which mate choice is advantageous because extreme displays indicate a well-adapted genotype. However, these hypotheses are not mutually exclusive, and the adaptive benefits underlying mate choice can themselves evolve. In particular, examining how and why sexual displays become indicators of good genes is challenging in natural systems. Here, we use experimental evolution in "digital organisms" to demonstrate the origins of condition-dependent indicator displays following their spread due to a runaway process. Surprisingly, handicap-like costs are not necessary for displays to become indicators of male viability. Instead, a pleiotropic genetic architecture underlies both displays and viability. Runaway sexual selection and good genes benefits should thus be viewed as interacting mechanisms that reinforce one another.

Identification of Chromatin-Associated Regulators of MSL Complex Targeting in Drosophila Dosage Compensation

Sex chromosome dosage compensation in Drosophila provides a model for understanding how chromatin organization can modulate coordinate gene regulation. Male Drosophila increase the transcript levels of genes on the single male X approximately two-fold to equal the gene expression in females, which have two X-chromosomes. Dosage compensation is mediated by the Male-Specific Lethal (MSL) histone acetyltransferase complex. Five core components of the MSL complex were identified by genetic screens for genes that are specifically required for male viability and are dispensable for females. However, because dosage compensation must interface with the general transcriptional machinery, it is likely that identifying additional regulators that are not strictly male-specific will be key to understanding the process at a mechanistic level. Such regulators would not have been recovered from previous male-specific lethal screening strategies. Therefore, we have performed a cell culture-based, genome-wide RNAi screen to search for factors required for MSL targeting or function. Here we focus on the discovery of proteins that function to promote MSL complex recruitment to “chromatin entry sites,” which are proposed to be the initial sites of MSL targeting. We find that components of the NSL (Non-specific lethal) complex, and a previously unstudied zinc-finger protein, facilitate MSL targeting and display a striking enrichment at MSL entry sites. Identification of these factors provides new insight into how MSL complex establishes the specialized hyperactive chromatin required for dosage compensation in Drosophila.

Susceptibility of the male fitness phenotype to spontaneous mutation

Adult reproductive success can account for a large fraction of male fitness, however, we know relatively little about the susceptibility of reproductive traits to mutation-accumulation (MA). Estimates of the mutational rate of decline for adult fitness and its components are controversial in Drosophila melanogaster, and post-copulatory performance has not been examined. We therefore separately measured the consequences of MA for total male reproductive success and its major pre-copulatory and post-copulatory components: mating success and sperm competitive success. We also measured juvenile viability, an important fitness component that has been well studied in MA experiments. MA had strongly deleterious effects on both male viability and adult fitness, but the latter declined at a much greater rate. Mutational pressure on total fitness is thus much greater than would be predicted by viability alone. We also noted a significant and positive correlation between all adult traits and viability in the MA lines, suggesting pleiotropy of mutational effect as required by 'good genes' models of sexual selection.

Sex allocation and functional bias of quaternary and quinary flowers on same inflorescence in the hermaphrodite Ruta graveolens

Intra-inflorescence variation in floral traits is important to understand the pollination function of an inflorescence and the real reproductive outputs of a plant. Ruta graveolens (Rutaceae) produce both quaternary (four petals and eight stamens) and quinary (five petals and ten stamens) flowers on the same cymes, while their pollination roles and the effects on the reproductive success remained unexplored. We experimentally examined the biomass of female versus male organs and pollen viability and stigma receptivity to explore the sex allocation patterns between the flowers. The breeding systems and reproductive outputs through either female function (seed set) or male function (pollen dispersal) were also studied for quinary and quaternary flowers to determine whether there was functional bias. The results showed that R. graveolens was protandrous, with a mixed mating system. Its stamens could slowly move one by one and only dehisce when positioning at the flower center, which could greatly enhance pollen dispersal. The first-opened quinary flower allocated significantly higher resources (dry biomass) in female organs while quaternary flowers allocated more resource in male organs. The quaternary flowers experienced higher pollen limitation in seed production but were more successful in pollen dispersal and the quinary flowers reproduced both through female and male functions. Our data suggested that quinary and quaternary flower on same inflorescence in R. graveolens functioned mainly as the sex role that most resources were allocated, which probably reflect an adaptation for floral phenology and pollination process in this plant.

Cooperative and Antagonistic Contributions of Two Heterochromatin Proteins to Transcriptional Regulation of the Drosophila Sex Determination Decision

Eukaryotic nuclei contain regions of differentially staining chromatin (heterochromatin), which remain condensed throughout the cell cycle and are largely transcriptionally silent. RNAi knockdown of the highly conserved heterochromatin protein HP1 in Drosophila was previously shown to preferentially reduce male viability. Here we report a similar phenotype for the telomeric partner of HP1, HOAP, and roles for both proteins in regulating the Drosophila sex determination pathway. Specifically, these proteins regulate the critical decision in this pathway, firing of the establishment promoter of the masterswitch gene, Sex-lethal (Sxl). Female-specific activation of this promoter, SxlPe, is essential to females, as it provides SXL protein to initiate the productive female-specific splicing of later Sxl transcripts, which are transcribed from the maintenance promoter (SxlPm) in both sexes. HOAP mutants show inappropriate SxlPe firing in males and the concomitant inappropriate splicing of SxlPm-derived transcripts, while females show premature firing of SxlPe. HP1 mutants, by contrast, display SxlPm splicing defects in both sexes. Chromatin immunoprecipitation assays show both proteins are associated with SxlPe sequences. In embryos from HP1 mutant mothers and Sxl mutant fathers, female viability and RNA polymerase II recruitment to SxlPe are severely compromised. Our genetic and biochemical assays indicate a repressing activity for HOAP and both activating and repressing roles for HP1 at SxlPe.

Persistent occurrence of meiotic abnormalities in a new hexaploid cytotype of Thalictrum foetidum from Indian cold deserts

Thalictrum foetidum L. (Ranunculaceae), a morphologically variable and widely distributed species of temperate and alpine Himalayas is worked out cytologically for the first time from India. Earlier studies from outside India were restricted to chromosome counts and karyotypic analysis. We studied the male meiosis, microsporogenesis and pollen viability in the wild accessions from the cold deserts of Lahaul-Spiti, Kinnaur and Pangi Valley of Himachal Pradesh. Present cytomorphological surveys in the species record the existence of two distinct morphotypes involving plant size; colour and size of leaf/leaflet; dentation of leaflet lobes; and degree of leaf pubescence. All the accessions in the two morphovariants share the same meiotic chromosome number (n = 21) and adds a new intraspecific hexaploid cytotype. The accessions show the phenomenon of cytomixis involving transfer of chromatin material among proximate pollen mother cells (PMCs) and associated meiotic abnormalities like, out of plate bivalents, interchromosomal connections, and laggards, bridges and micronuclei at anaphases/telophases. Microsporogenesis results into abnormal sporads (tetrads with micronuclei, dyads, triads and polyads). The products of such sporads resulted into some pollen sterility and pollen grains of heterogeneous sizes. The persistent occurrence of phenomenon of cytomixis and associated meiotic abnormalities and consequently pollen sterility and pollen grains of heterogeneous sizes in the hexaploid cytotype of T. foetidum seems to be under some genetic factors associated with the genome.

Do Male Pied Flycatchers (Ficedula hypoleuca) Adjust Their Feeding Effort According to Egg Colour?

The colour of blue-green bird eggs has been hypothesized to signal female quality to attending males, who may adjust their level of investment in the brood accordingly. The hypothesis has gained support in studies of Spanish pied flycatchers Ficedula hypoleuca. We performed a cross-fostering experiment in a Norwegian population of pied flycatchers to provide an independent test of the sexually selected egg colour hypothesis in this species. Egg colour was not significantly correlated with estimates of female quality (clutch size, average egg volume, first egg laying date and feeding rate). There was a significant decrease in chroma and increase in brightness and egg volume during the laying sequence, with some marked differences between six-egg and seven-egg clutches that might reflect differences in female quality. However, we found no significant influence of egg colour (foster or original clutch) on male feeding rate or offspring viability (hatching success, average mass and fledging success) and no significant difference in feeding rate for males with six-egg and seven-egg foster or original clutches. We conclude that Norwegian male pied flycatchers do not use egg colour as a cue to female quality, thus questioning the generality of previous support for the sexually selected egg colour hypothesis from this species.

Female choice in the red mason bee,Osmia rufa(L.) (Megachilidae)

Females are often thought to use several cues and more than one modality in selection of a mate, possibly because they offer complementary information on a mate's suitability. In the red mason bee, Osmia rufa, we investigated the criteria a female uses to choose a mating partner. We hypothesized that the female uses male thorax vibrations and size as signs of male viability and male odor for kin discrimination and assessment of genetic relatedness. We therefore compared males that had been accepted by a female for copulation with those rejected, in terms of their size, their immediate precopulatory vibrations (using laser vibrometry), the genetic relatedness of unmated and mated pairs (using microsatellite markers) and emitted volatiles (using chemical analyses). Females showed a preference for intermediate-sized males that were slightly larger than the modal male size. Furthermore, male precopulatory vibration burst duration was significantly longer in males accepted for copulation compared with rejected males. Vibrations may indicate vigor and assure that males selected by females are metabolically active and healthy. Females preferentially copulated with males that were genetically more closely related, possibly to avoid outbreeding depression. Volatiles of the cuticular surface differed significantly between accepted and rejected males in the relative amounts of certain hydrocarbons, although the relationship between male odor and female preference was complex. Females may therefore also use differences in odor bouquet to select among males. Our investigations show that O. rufa females appear to use multiple cues in selecting a male. Future investigations are needed to demonstrate whether odor plays a role in kin recognition and how the multiple cues are integrated in mate choice by females.

Genetic Testing of the Hypothesis That Hybrid Male Lethality Results From a Failure in Dosage Compensation

Several recent studies have suggested that F(1) hybrid male lethality in crosses between Drosophila melanogaster and D. simulans is due to a failure in dosage compensation, caused by incompatibilities between D. simulans dosage compensation proteins and the D. melanogaster X chromosome. Contrary to the predictions of this hypothesis, mutations in four essential D. melanogaster dosage compensation genes are shown here to moderately increase rather than decrease hybrid male viability.

Why do females find ornaments attractive? The coercion-avoidance hypothesis

Vertebrates show two major classes of sexually dimorphic traits: weaponry and ornaments. However, Darwin could not explain why their expression varies so much across lineages. We argue that coercion-avoidance can explain both the existence and taxonomic distribution of ornaments. Females maximize their fitness when they can freely choose their mates, but males are expected to use sexually dimorphic weaponry not only to displace other males, but also to overcome female preferences and thus acquire matings by force whenever they can. Females should therefore avoid coercive males and avoid using weaponry as a criterion for male quality wherever possible, and rely on male viability indicators that cannot be used to coerce females (i.e. ornaments). Ornaments predominate in birds and weaponry in mammals because female choice is less costly in birds, due to higher intrinsic female behavioural freedom and lower male monopolization potential. We also predict that specialized coercive organs occur where females have low behavioural freedom but males benefit little from weaponry in male–male contests. A review of the empirical evidence supports the basic predictions of this coercion-avoidance hypothesis. We also present a simple mathematical model that confirms the logic of this hypothesis.

REVERSING MOTHER'S CURSE: SELECTION ON MALE MITOCHONDRIAL FITNESS EFFECTS

Many essential organelles and endosymbionts exhibit a strict matrilineal pattern of inheritance. The absence of paternal transmission of such extranuclear components is thought to preclude a response to selection on their effects on male viability and fertility. We overturn this dogma by showing that two mechanisms, inbreeding and kin selection, allow mitochondria to respond to selection on both male viability and fertility. Even modest levels of inbreeding allow such a response to selection when there are direct fitness effects of mitochondria on male fertility because inbreeding associates male fertility traits with mitochondrial matrilines. Male viability effects of mitochondria are also selectable whenever there are indirect fitness effects of males on the fitness of their sisters. When either of these effects is sufficiently strong, we show that there are conditions that allow the spread of mitochondria with direct effects that are harmful to females, contrary to standard expectation. We discuss the implications of our findings for the evolution of organelles and endosymbionts and genomic conflict.

Biologia reprodutiva de Acacia mearnsii De Wild.: receptividade de estigmas

O objetivo deste trabalho foi analisar a receptividade de estigmas de Acacia mearnsii De Wild. em 20 árvores da Área de Produção de Sementes (APS) da Fazenda Locatelli, da empresa SETA S.A., no município de Butiá (RS) e comparar os períodos de receptividade de estigmas e de viabilidade polínica em diversas fases da abertura floral. Foi utilizado como método de colorimetria o reagente de Baker para indicar a receptividade e a viabilidade. As análises foram conduzidas em delineamento inteiramente casualizado e a estatística χ2 foi utilizada para verificar a significância dos eventos estudados. Foi observada receptividade no início da abertura floral (71%), alcançando a total receptividade (100%) em plena antese. A viabilidade polínica foi detectada no início da antese (77%) e em total abertura floral (88%). Na fase de senescência foram observados estigmas receptivos (50%) e políades viáveis (23%). Há sobreposição da fase de viabilidade masculina e de receptividade feminina, aumentando as chances de autopolinização. Na maioria das árvores analisadas (85%) foi observada a total receptividade (100%) nos estigmas amostrados. Em três árvores (15%) observou-se uma média inferior a 95% de estigmas receptivos. Não foi observada diferença significativa pelo teste do χ2 na receptividade dos estigmas no germoplasma analisado, sugerindo que o genótipo não interfere diretamente para a receptividade dos estigmas.

Consequences of inbreeding depression due to sex-linked loci for the maintenance of males and outcrossing in branchiopod crustaceans

Androdioecy, where males co-occur with hermaphrodites, is a rare sexual system in plants and animals. It has a scattered phylogenetic distribution, but it is common and has persisted for long periods of evolutionary time in branchiopod crustaceans. An earlier model of the maintenance of males with hermaphrodites in this group, by Otto et al. (1993), considered the importance of male-hermaphrodite encounter rates, sperm limitation, male versus hermaphrodite viability and inbreeding depression suffered by selfed progeny. Here I advance this model in two ways: (1) by exploring the conditions that would allow the invasion of hermaphrodites into a dioecious population and that of females into an androdioecious population; and (2) by incorporating a term that accounts for the potential effects of genetic load linked to a dominant hermaphrodite-determining allele in androdioecious populations. The new model makes plausible sense of observations made in populations of the species Eulimnadia texana, one of a number of related species whose common ancestor evolved hermaphroditism (and androdioecy) from dioecy. In particular, it offers an explanation for the long evolutionary persistence of androdioecy in branchiopods and suggests reasons for why dioecy has not re-evolved in the clade. Finally, it provides a rather unusual illustration of the implications of the degeneration of loci linked to a sex-determining locus.

Male barn swallows use different resource allocation rules to produce ornamental tail feathers

Sexual ornaments compete for resources with other functional traits. Such resource allocation trade-offs should ensure the honesty of sexual ornaments according to the Zahavi’s handicap principle. However, the existence of costly signals could not be enough to guarantee honesty if different individuals invest different proportions of their limited resources in ornaments. Then, a certain level of sexual signaling would correspond to several levels of individual condition. Here, we explore whether there are different resource allocation rules in tail feather ornaments between males within a barn swallow (Hirundo rustica) population and whether these different rules confer different viability to males. We assessed the proportion of resources invested in ornamental feathers compared with other functional feathers moulted and growing during the same period at expenses of the same resources. We found that 1) different males allocate a different proportion of resources to ornamental feathers in relation to functional feathers and this proportion is repeatable between years and 2) male survival likelihood decreased as the proportion of resources allocated to ornamental feathers increased. Survival costs associated with increased investments in ornaments can maintain the sexual signaling system honest at population level but do not preclude the existence of an array of different allocation rules between males. Thus, males with different viability can produce ornamental feathers of the same length. These results show that the relationship between male viability and ornament expression can be less straightforward than considered previously. Key words: barn swallow, honesty, resource allocation, sexual ornaments, tail feathers, tradeoff. [Behav Ecol]

X‐chromosome targeting and dosage compensation are mediated by distinct domains in MSL‐3

In Drosophila, dosage compensation of X-linked genes is achieved by transcriptional upregulation of the male X chromosome. Genetic and biochemical studies have demonstrated that male-specific lethal (MSL) proteins together with roX RNAs regulate this process. Here, we show that MSL-3 is essential for cell viability and that three domains in the protein have distinct roles in dosage compensation. The chromo-barrel domain (CBD) is not necessary for MSL targeting to the male X chromosome but is important for male viability and equalization of X-linked gene transcription. The polar region cooperates with the CBD in MSL-3 function, whereas the MRG domain is responsible for targeting the protein to the X chromosome. Our results demonstrate that MSL-3 localization to the male X chromosome and transcriptional upregulation of X-linked genes are two separable functions of the MSL-3 protein.

A Family Knockout of All Four Drosophila Metallothioneins Reveals a Central Role in Copper Homeostasis and Detoxification

Metallothioneins are ubiquitous, small, cysteine-rich proteins with the ability to bind heavy metals. In spite of their biochemical characterization, their in vivo function remains elusive. Here, we report the generation of a metallothionein gene family knockout in Drosophila melanogaster by targeted disruption of all four genes (MtnA to -D). These flies are viable if raised in standard laboratory food. During development, however, they are highly sensitive to copper, cadmium, and (to a lesser extent) zinc load. Metallothionein expression is particularly important for male viability; while copper load during development affects males and females equally, adult males lacking metallothioneins display a severely reduced life span, possibly due to copper-mediated oxidative stress. Using various reporter gene constructs, we find that different metallothioneins are expressed with virtually the same tissue specificity in larvae, notably in the intestinal tract at sites of metal accumulation, including the midgut's "copper cells." The same expression pattern is observed with a synthetic minipromoter consisting only of four tandem metal response elements. From these and other experiments, we conclude that tissue specificity of metallothionein expression is a consequence, rather than a cause, of metal distribution in the organism. The bright orange luminescence of copper accumulated in copper cells of the midgut is severely reduced in the metallothionein gene family knockout, as well as in mutants of metal-responsive transcription factor 1 (MTF-1), the main regulator of metallothionein expression. This indicates that an in vivo metallothionein-copper complex forms the basis of this luminescence. Strikingly, metallothionein mutants show an increased, MTF-1-dependent induction of metallothionein promoters in response to copper, cadmium, silver, zinc, and mercury. We conclude that free metal, but not metallothionein-bound metal, triggers the activation of MTF-1 and that metallothioneins regulate their own expression by a negative feedback loop.

The severity of roX1 mutations is predicted by MSL localization on the X chromosome

Dosage compensation equalizes the expression of sex-linked genes between males and females. Most genes on the X chromosome of male Drosophila are transcribed at an increased level, contributing to compensation. The roX1 and roX2 genes produce non-coding transcripts that localize along the X-chromosome of male flies. Although lacking sequence similarity, they are necessary but redundant components of a system that up-regulates gene expression. Simultaneous mutation of both roX genes disrupts the X-limited distribution of proteins that modify chromatin to enhance gene expression. We have generated and characterized loss of function roX1 alleles that display a continuum of activity. Those that support intermediate male survival have strikingly reduced RNA accumulation, while alleles with minor contributions to male viability typically lack detectable transcript accumulation. Severely mutated roX1 alleles retain some ability to direct modifying proteins to the X chromosome. This ability predicts the level of male survival that each allele supports. This points to a peripheral or transient role for roX in the RNA and protein complex that binds to and regulates the X chromosome.

The Effect of Male Mating Competitiveness, Developmental Rate, and Viability of Larvae and Pupae in Drosophila melanogaster Heterozygous for the Temperature-Sensitive Lethal Mutation l(2)M167 DTS on the Dynamics of the Mutation Elimination from the Population

The dependence of selection on an introduced mutation 1(2)M167DTS on male mating competitiveness, viability, and developmental rate of larvae and pupae of Drosophila melanogaster, heterozygous for this mutation, was examined in population experiments with preset conditions. The limitations of fitness parameters of individuals l(2)M167DTS/+ relative to individuals +/+ were estimated according to the conditions of the experiment and phenotypic characteristics of the mutation studied. Under conditions of limited food supply and dependence on emergence time in each generation, the sequence of female mating was shown to be of less importance than the order of medium utilization by the progeny of a certain genotype related to the male success in the first mating. The limiting factors acting on the l(2)M167DTS mutation were viability and developmental rate.

Sequence-specific targeting of MSL complex regulates transcription of the roX RNA genes.

In Drosophila, dosage compensation is controlled by the male-specific lethal (MSL) complex consisting of at least five proteins and two noncoding RNAs, roX1 and roX2. The roX RNAs function in targeting MSL complex to the X chromosome, and roX transgenes can nucleate spreading of the MSL complex into flanking chromatin when inserted on an autosome. An MSL-binding site (DHS, DNaseI hypersensitive site) has been identified in each roX gene. Here, we investigate the functions of the DHS using transgenic deletion analyses and reporter assays. We find that MSL interaction with the DHS counteracts constitutive repression at roX1, resulting in male-specific expression of roX1 RNA. Surprisingly, the DHS is not required for initiation of cis spreading of MSL complex, instead local transcription of roX RNAs correlates with extensive spreading.

Mate Choice, Male Condition-Dependent Ornamentation and MHC in the Pheasant

The Hamilton and Zuk model predicts that genes for resistance to various pathogens may be continuously heritable due to selection disequilibria caused by coadaptional cycles of hosts and pathogens. The model further suggests that the expression of male secondary ornaments is condition-dependent and that only individuals with superior genetic disease resistance and vigour can fully express exaggerated secondary ornaments. Female choice is therefore expected to discriminate among males on the basis of secondary sexual characters in order to pass on genes for disease resistance that improve fitness in the offspring. In wild ring-necked pheasants, Phasianus colchicus, of the Revinge area in southern Sweden, females prefer to mate with long-spurred males and data on reproductive success indicate that they may improve their chicks' survival rate by doing so. Male spur length is positively correlated with age, body size and viability. MHC genotyping for both class I and class II B of pheasant males trapped in the study area identified eight MHC haplotypes and a total of 17 different MHC genotypes. Multivariate analyses revealed that MHC genotype is significantly associated with variation in both male spur length and male viability. These data indicate that polymorphic genes with a central role in immune recognition can be associated with viability and the expression of a condition-dependent intersexually selected male trait, thus supporting essential parts of the Hamilton and Zuk model. (Less)