No evidence for an intragenomic arms race under paternal genome elimination in Planococcus mealybugs

Genomic conflicts arising during reproduction might play an important role in shaping the striking diversity of reproductive strategies across life. Among these is paternal genome elimination (PGE), a form of haplodiploidy which has independently evolved several times in arthropods. PGE males are diploid but transmit maternally inherited chromosomes only, whereas paternal homologues are excluded from sperm. Mothers thereby effectively monopolize the parentage of sons, at the cost of the father's reproductive success. This creates striking conflict between the sexes that could result in a co‐evolutionary arms race between paternal and maternal genomes over gene transmission, yet empirical evidence that such an arms race indeed takes place under PGE is scarce. This study addresses this by testing whether PGE is complete when paternal genotypes are exposed to divergent maternal backgrounds in intraspecific and hybrid crosses of the citrus mealybug, Planococcus citri, and the closely related Planococcus ficus. We determined whether males can transmit genetic information through their sons by tracking inheritance of two traits in a three‐generation pedigree: microsatellite markers and sex‐specific pheromone preferences. Our results suggest leakages of single paternal chromosomes through males occurring at a low frequency, but we find no evidence for transmission of paternal pheromone preferences from fathers to sons. The absence of differences between hybrid and intraspecific crosses in leakage rate of paternal alleles suggests that a co‐evolutionary arms race cannot be demonstrated on this evolutionary timescale, but we conclude that there is scope for intragenomic conflict between parental genomes in mealybugs. Finally, we discuss how these paternal escapes can occur and what these findings may reveal about the evolutionary dynamics of this bizarre genetic system.     

Genetic conflict and changes in heterogametic mechanisms of sex determination

The consequences of cytoplasmic sex‐ratio distortion and host repression for the evolution of host sex‐determining mechanisms are examined. Analytical models and simulations are developed to investigate whether the interplay between sex‐ratio distorters and host masculinizers or resistance genes can cause heterogamety switching (changes between male and female heterogamety). Switches from female heterogamety to a system analogous to male heterogamety can occur when selection favours the spread of autosomal masculinizers. However, the evolutionary outcome depends on the type of repressor and costs associated with repression, and also on aspects of population structure. Under most conditions, systems evolved to a polymorphic sex‐determining state although many systems were characterized by numerical dominance of male heterogamety.     

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.     

Female resistance behaviour and progeny sex ratio in two Bradysia species (Diptera: Sciaridae) with paternal genome elimination

The relationship between female mating preferences and sex allocation has received considerable theoretical and empirical support. Typically, choosier females adjust their progeny sex ratio towards sons, who inherit the attractive traits of their father. However, in species with paternal genome elimination, where male sperm do not contain the paternal genome, predictions for the direction of progeny sex ratio biases and their relationship with female choosiness are atypical. Paternal genome elimination also creates a potential for male–female conflict over sex allocation, and any influence of female mate choice on sex ratio outcomes have interesting implications for sexually antagonistic coevolution. Within the Sciaridae (Diptera) are species that produce single‐sex progeny (monogenic species) and others in which progeny comprise both sexes (digenic species). Paternal genome elimination occurs in both species. We explore female mate resistance behaviour in a monogenic and digenic species of mushroom gnat from the genus Bradysia. Our experiments confirmed our theoretical predictions, revealing that in the monogenic and digenic species, females producing female‐biased progeny were more likely to have resisted at least one mating attempt.     

Invasion and fixation of sex-reversal genes

We simulated a meta-population with random dispersal among demes but local mating within demes to investigate conditions under which a dominant female-determining gene W, with no individual selection advantage, can invade and become fixed in females, changing the population from male to female heterogamety. Starting with one mutant W in a single deme, the interaction of sex ratio selection and random genetic drift causes W to be fixed among females more often than a comparable neutral mutation with no influence on sex determination, even when YY males have slightly reduced viability. Meta-population structure and interdeme selection can also favour the fixation of W. The reverse transition from female to male heterogamety can also occur with higher probability than for a comparable neutral mutation. These results help to explain the involvement of sex-determining genes in the evolution of sex chromosomes and in sexual selection and speciation.     

The red bayberry genome and genetic basis of sex determination

Morella rubra, red bayberry, is an economically important fruit tree in south China. Here, we assembled the first high‐quality genome for both a female and a male individual of red bayberry. The genome size was 313‐Mb, and 90% sequences were assembled into eight pseudo chromosome molecules, with 32 493 predicted genes. By whole‐genome comparison between the female and male and association analysis with sequences of bulked and individual DNA samples from female and male, a 59‐Kb region determining female was identified and located on distal end of pseudochromosome 8, which contains abundant transposable element and seven putative genes, four of them are related to sex floral development. This 59‐Kb female‐specific region was likely to be derived from duplication and rearrangement of paralogous genes and retained non‐recombinant in the female‐specific region. Sex‐specific molecular markers developed from candidate genes co‐segregated with sex in a genetically diverse female and male germplasm. We propose sex determination follow the ZW model of female heterogamety. The genome sequence of red bayberry provides a valuable resource for plant sex chromosome evolution and also provides important insights for molecular biology, genetics and modern breeding in Myricaceae family.     

Heritable variation of sex ratio in a polychaete worm

Ophryotrocha labronica is a gonochoristic polychaete worm whose sex determining mechanism and sex ratio control are supposed to be polygenic. From a lab population, whose sex ratio (i.e., proportion of males) was 0.5, the estimate of sex ratio heritability by offspring-father regression was 0.54 ± 0.15 and by offspring-mother regression was not significantly different from 0. Estimate of sex ratio repeatability between successive broods of a pair was 0.64 ± 0.33. Since female parents do not contribute in any way to the variability of sex ratio, sex ratio variation seems to be largely a paternal character. On the basis of these estimates we advance the hypothesis that in this species sex is determined by a multilocus genetic system, allowing the combined effects of a female major sex gene (which could give rise to a form of female heterogamety) and masculinizing modifiers. The hypothesis that the male sex has the least canalised sexual differentiation is supported by the observation that some old males developed oocytes.     

Paternal inheritance of the primary sex ratio in a copepod

Uniparentally inherited genetic elements are under strong selection to manipulate sex determination in their host and shift the host sex ratio towards the transmitting sex. For any sex-ratio trait, lineage analysis and quantitative genetics are important tools for characterizing the mode of inheritance (biparental vs. maternal vs. paternal) thereby narrowing the field of possible sex-determining mechanisms (e.g. polygenic, sex chromosomes with meiotic drive, cytoplasmic microorganisms). The primary sex ratio of the harpacticoid copepod, Tigriopus californicus is often male-biased and is highly variable among full sib families. We found that this extra-binomial variation for the primary sex ratio is paternally but not maternally transmitted in T. californicus. Paternal transmission of the primary sex ratio has been well documented in the haplo-diploid hymenoptera but is relatively rare in diplo-diploid organisms. If the sex-ratio trait is paternally transmitted in other closely related harpacticoid copepods it would explain why male biased primary sex ratios are so common in this group.     

Parental Care and Mate Choice in the Giant Water Bug Belostoma lutarium

Parental care and sexual selection are highly interrelated. Understanding the evolution of sex‐specific patterns of parental care and sexual selection is a major focus of current evolutionary ecology research and requires empirical studies that simultaneously quantify components of both parental care and sexual selection in a single species. In this study, we quantify the dynamics of paternal care and sexual selection in the giant water bug Belostoma lutarium. Specifically, we examined (1) which sex potentially experiences sexual selection, (2) which traits, if any, are associated with attaining a mate by males and/or females (i.e. which traits are potentially under selection), and (3) which male and female traits, if any, relate to paternal care and offspring survival. Our findings suggest that (1) males are likely the choosier sex and that heavier females are more likely to mate than smaller females, (2) that female body weight is under selection if female weight is a trait that is stable within a given individual and (3) body size is sexually dimorphic, with females being the larger sex in this species. There was no evidence of male or female traits being linked to offspring survival in this species, although this is potentially due to the lack of egg predators in our study. We discuss our findings in relation to the evolution of sex roles and future avenues of research in this species.     

Sex differences in life history drive evolutionary transitions among maternal,paternal, and bi‐parental care

Evolutionary transitions among maternal, paternal, and bi‐parental care have been common in many animal groups. We use a mathematical model to examine the effect of male and female life‐history characteristics (stage‐specific maturation and mortality) on evolutionary transitions among maternal, paternal, and bi‐parental care. When males and females are relatively similar – that is, when females initially invest relatively little into eggs and both sexes have similar mortality and maturation – transitions among different patterns of care are unlikely to be strongly favored. As males and females become more different, transitions are more likely. If females initially invest heavily into eggs and this reduces their expected future reproductive success, transitions to increased maternal care (paternal → maternal, paternal → bi‐parental, bi‐parental → maternal) are favored. This effect of anisogamy (i.e., the fact that females initially invest more into each individual zygote than males) might help explain the predominance of maternal care in nature and differs from previous work that found no effect of anisogamy on the origin of different sex‐specific patterns of care from an ancestral state of no care. When male mortality is high or male egg maturation rate is low, males have reduced future reproductive potential and transitions to increased paternal care (maternal → paternal, bi‐parental → paternal, maternal → bi‐parental) are favored. Offspring need (i.e., low offspring survival in the absence of care) also plays a role in transitions to paternal care. In general, basic life‐history differences between the sexes can drive evolutionary transitions among different sex‐specific patterns of care. The finding that simple life‐history differences can alone lead to transitions among maternal and paternal care suggests that the effect of inter‐sexual life‐history differences should be considered as a baseline scenario when attempting to understand how other factors (mate availability, sex differences in the costs of competing for mates) influence the evolution of parental care.     

Identification of sex‐specific molecular markers using restriction site‐associated DNA sequencing

A major barrier to evolutionary studies of sex determination and sex chromosomes has been a lack of information on the types of sex‐determining mechanisms that occur among different species. This is particularly problematic in groups where most species lack visually heteromorphic sex chromosomes, such as fish, amphibians and reptiles, because cytogenetic analyses will fail to identify the sex chromosomes in these species. We describe the use of restriction site‐associated DNA (RAD) sequencing, or RAD‐seq, to identify sex‐specific molecular markers and subsequently determine whether a species has male or female heterogamety. To test the accuracy of this technique, we examined the lizard Anolis carolinensis. We performed RAD‐seq on seven male and ten female A. carolinensis and found one male‐specific molecular marker. Anolis carolinensis has previously been shown to possess male heterogamety and the recently published A. carolinensis genome facilitated the characterization of the sex‐specific RAD‐seq marker. We validated the male specificity of the new marker using PCR on additional individuals and also found that it is conserved in some other Anolis species. We discuss the utility of using RAD‐seq to identify sex‐determining mechanisms in other species with cryptic or homomorphic sex chromosomes and the implications for the evolution of male heterogamety in Anolis.     

Novel evolutionary pathways of sex‐determining mechanisms

Evolutionary transitions between sex‐determining mechanisms (SDMs) are an enigma. Among vertebrates, individual sex (male or female) is primarily determined by either genes (genotypic sex determination, GSD) or embryonic incubation temperature (temperature‐dependent sex determination, TSD), and these mechanisms have undergone repeated evolutionary transitions. Despite this evolutionary lability, transitions from GSD (i.e. from male heterogamety, XX/XY, or female heterogamety, ZZ/ZW) to TSD are an evolutionary conundrum, as they appear to require crossing a fitness valley arising from the production of genotypes with reduced viability owing to being homogametic for degenerated sex chromosomes (YY or WW individuals). Moreover, it is unclear whether alternative (e.g. mixed) forms of sex determination can persist across evolutionary time. It has previously been suggested that transitions would be easy if temperature‐dependent sex reversal (e.g. XX male or XY female) was asymmetrical, occurring only in the homogametic sex. However, only recently has a mechanistic model of sex determination emerged that may allow such asymmetrical sex reversal. We demonstrate that selection for TSD in a realistic sex‐determining system can readily drive evolutionary transitions from GSD to TSD that do not require the production of YY or WW individuals. In XX/XY systems, sex reversal (female to male) occurs in a portion of the XX individuals only, leading to the loss of the Y allele (or chromosome) from the population as XX individuals mate with each other. The outcome is a population of XX individuals whose sex is determined by incubation temperature (TSD). Moreover, our model reveals a novel evolutionarily stable state representing a mixed‐mechanism system that has not been revealed by previous approaches. This study solves two long‐standing puzzles of the evolution of sex‐determining mechanisms by illuminating the evolutionary pathways and endpoints.     

Sperm competition generates evolution of increased paternal investment in a sex role‐reversed seed beetle

When males provide females with resources at mating, they can become the limiting sex in reproduction, in extreme cases leading to the reversal of typical courtship roles. The evolution of male provisioning is thought to be driven by male reproductive competition and selection for female fecundity enhancement. We used experimental evolution under male‐ or female‐biased sex ratios and limited or unlimited food regimes to investigate the relative roles of these routes to male provisioning in a sex role‐reversed beetle, Megabruchidius tonkineus, where males provide females with nutritious ejaculates. Males evolving under male‐biased sex ratios transferred larger ejaculates than did males from female‐biased populations, demonstrating a sizeable role for reproductive competition in the evolution of male provisioning. Although larger ejaculates elevated female lifetime offspring production, we found little evidence of selection for larger ejaculates via fecundity enhancement: males evolving under resource‐limited and unlimited conditions did not differ in mean ejaculate size. Resource limitation did, however, affect the evolution of conditional ejaculate allocation. Our results suggest that the resource provisioning that underpins sex role reversal in this system is the result of male–male reproductive competition rather than of direct selection for males to enhance female fecundity.     

Variation in parent–offspring kinship in socially monogamous systems with extra‐pair reproduction and inbreeding

Female extra‐pair reproduction in socially monogamous systems is predicted to cause cuckolded socially‐paired males to conditionally reduce paternal care, causing selection against extra‐pair reproduction and underlying polyandry. However, existing models and empirical studies have not explicitly considered that cuckolded males might be related to their socially‐paired female and/or to her extra‐pair mate, and therefore be related to extra‐pair offspring that they did not sire but could rear. Selection against paternal care, and hence against extra‐pair reproduction, might then be weakened. We derive metrics that quantify allele‐sharing between within‐pair and extra‐pair offspring and their mother and her socially‐paired male in terms of coefficients of kinship and inbreeding. We use song sparrow (Melospiza melodia) paternity and pedigree data to quantify these metrics, and thereby quantify the joint effects of extra‐pair reproduction and inbreeding on a brood's total allelic value to its socially‐paired parents. Cuckolded male song sparrows were almost always detectably related to extra‐pair offspring they reared. Consequently, although brood allelic value decreased substantially following female extra‐pair reproduction, this decrease was reduced by within‐pair and extra‐pair reproduction among relatives. Such complex variation in kinship within nuclear families should be incorporated into models considering coevolutionary dynamics of extra‐pair reproduction, parental care, and inbreeding.     

Widespread intersex differentiation across the stickleback genome – The signature of sexually antagonistic selection?

Females and males within a species commonly have distinct reproductive roles, and the associated traits may be under perpetual divergent natural selection between the sexes if their sex‐specific control has not yet evolved. Here, we explore whether such sexually antagonistic selection can be detected based on the magnitude of differentiation between the sexes across genome‐wide genetic polymorphisms by whole‐genome sequencing of large pools of female and male threespine stickleback fish. We find numerous autosomal genome regions exhibiting intersex allele frequency differences beyond the range plausible under pure sampling stochasticity. Alternative sequence alignment strategies rule out that these high‐differentiation regions represent sex chromosome segments misassembled into the autosomes. Instead, comparing allele frequencies and sequence read depth between the sexes reveals that regions of high intersex differentiation arise because autosomal chromosome segments got copied into the male‐specific sex chromosome (Y), where they acquired new mutations. Because the Y chromosome is missing in the stickleback reference genome, sequence reads derived from DNA copies on the Y chromosome still align to the original homologous regions on the autosomes. We argue that this phenomenon hampers the identification of sexually antagonistic selection within a genome, and can lead to spurious conclusions from population genomic analyses when the underlying samples differ in sex ratios. Because the hemizygous sex chromosome sequence (Y or W) is not represented in most reference genomes, these problems may apply broadly.     

What is behind the variation in mate quality dependent sex ratio adjustment? – A meta‐analysis

Theory predicts that parents adjust the sex ratio of their brood to the sexually selected traits of their mate because the reproductive success of sons may be more dependent on inherited paternal attractiveness than that of daughters. Empirical studies vary in terms of whether they support the theory, and this variation has often been regarded as evidence against sex ratio adjustment or has been ascribed to methodological differences. Applying phylogenetic meta‐analyses, we aimed to find biological explanations for the variation observed in songbirds. In particular, we tested the role extra‐pair paternity, because infidelity occurs in the majority of these species and may reduce the adaptive value of adjusting brood sex ratio to the phenotype of the social mate. However, we found that the variation in effect sizes was unrelated to the proportion of extra‐pair paternity. Thus future studies should consider that mate quality dependent sex ratio adjustment may be driven by direct (material) rather than indirect (genetic) benefits. We also tested if the effect sizes are influenced by whether the focal male trait is indeed under sexual selection as it is assumed by the sex allocation theory. We found that for male traits with proven role in sexual selection, effect sizes significantly differed from the null expectation of random production of sons and daughters. For male traits with only presumed sexual role in sexual selection, the deviation from the null expectation was less convincing, and the effect sizes were significantly smaller. This result indicates that studies that neglect the assumptions of the hypotheses concerned, may lead to the underestimation of the mean effect size and, eventually, false conclusions.     

Low rates of X‐Y recombination,not turnovers,account for homomorphic sex chromosomes in several diploid species of Palearctic green toads (Bufo viridis subgroup)

Contrasting with birds and mammals, most ectothermic vertebrates present homomorphic sex chromosomes, which might be due either to a high turnover rate or to occasional X‐Y recombination. We tested these two hypotheses in a group of Palearctic green toads that diverged some 3.3 million years ago. Using sibship analyses of sex‐linked markers, we show that all four species investigated share the same pair of sex chromosomes and a pattern of male heterogamety with drastically reduced X‐Y recombination in males. Phylogenetic analyses of sex‐linked sequences show that X and Y alleles cluster by species, not by gametolog. We conclude that X‐Y homomorphy and fine‐scale sequence similarity in these species do not stem from recent sex‐chromosome turnovers, but from occasional X‐Y recombination.     

The kin structure of sexual interactions

The origin of sexual reproduction involved the evolution of zygotes from separate genomes and, like other social processes, should therefore be amenable to analysis using kin selection theory. I consider how kin structure affects sexual interactions in three contexts—the evolution of sexual reproduction, sex allocation and sexual conflict. Kin structure helps explain the even-handed replication of paternal and maternal genes under outbreeding. Under inbreeding, it predicts altruistic failure to replicate by one half of the diploid genome. Kin structure predicts optimal sex ratios and potential conflicts over sex ratio within social groups and individuals. Sexual conflict predictably occurs as a function of (i) the probability that current sexual partners will reproduce together in future and (ii) between-partner relatedness. I conclude that systematically analysing the kin structure of sexual interactions helps illuminate their evolution.