Ontogenetic stage‐specific quantitative trait loci contribute to divergence in developmental trajectories of sexually dimorphic fins between medaka populations

Sexual dimorphism can evolve when males and females differ in phenotypic optima. Genetic constraints can, however, limit the evolution of sexual dimorphism. One possible constraint is derived from alleles expressed in both sexes. Because males and females share most of their genome, shared alleles with different fitness effects between sexes are faced with intralocus sexual conflict. Another potential constraint is derived from genetic correlations between developmental stages. Sexually dimorphic traits are often favoured at adult stages, but selected against as juvenile, so developmental decoupling of traits between ontogenetic stages may be necessary for the evolution of sexual dimorphism in adults. Resolving intralocus conflicts between sexes and ages is therefore a key to the evolution of age‐specific expression of sexual dimorphism. We investigated the genetic architecture of divergence in the ontogeny of sexual dimorphism between two populations of the Japanese medaka (Oryzias latipes) that differ in the magnitude of dimorphism in anal and dorsal fin length. Quantitative trait loci (QTL) mapping revealed that few QTL had consistent effects throughout ontogenetic stages and the majority of QTL change the sizes and directions of effects on fin growth rates during ontogeny. We also found that most QTL were sex‐specific, suggesting that intralocus sexual conflict is almost resolved. Our results indicate that sex‐ and age‐specific QTL enable the populations to achieve optimal developmental trajectories of sexually dimorphic traits in response to complex natural and sexual selection.     

Dioecy and the evolution of sex ratios in ants

Split sex ratios, when some colonies produce only male and others only female reproductives, is a common feature of social insects, especially ants. The most widely accepted explanation for split sex ratios was proposed by Boomsma and Grafen, and is driven by conflicts of interest among colonies that vary in relatedness. The predictions of the Boomsma–Grafen model have been confirmed in many cases, but contradicted in several others. We adapt a model for the evolution of dioecy in plants to make predictions about the evolution of split sex ratios in social insects. Reproductive specialization results from the instability of the evolutionarily stable strategy (ESS) sex ratio, and is independent of variation in relatedness. We test predictions of the model with data from a long-term study of harvester ants, and show that it correctly predicts the intermediate sex ratios we observe in our study species. The dioecy model provides a comprehensive framework for sex allocation that is based on the pay-offs to the colony via production of males and females, and is independent of the genetic variation among colonies. However, in populations where the conditions for the Boomsma–Grafen model hold, kin selection will still lead to an association between sex ratio and relatedness.     

TEMPERATURE‐DEPENDENT TURNOVERS IN SEX‐DETERMINATION MECHANISMS: A QUANTITATIVE MODEL

Sex determination is often seen as a dichotomous process: individual sex is assumed to be determined either by genetic (genotypic sex determination, GSD) or by environmental factors (environmental sex determination, ESD), most often temperature (temperature sex determination, TSD). We endorse an alternative view, which sees GSD and TSD as the ends of a continuum. Both effects interact a priori, because temperature can affect gene expression at any step along the sex‐determination cascade. We propose to define sex‐determination systems at the population‐ (rather than individual) level, via the proportion of variance in phenotypic sex stemming from genetic versus environmental factors, and we formalize this concept in a quantitative‐genetics framework. Sex is seen as a threshold trait underlain by a liability factor, and reaction norms allow modeling interactions between genotypic and temperature effects (seen as the necessary consequences of thermodynamic constraints on the underlying physiological processes). As this formalization shows, temperature changes (due to e.g., climatic changes or range expansions) are expected to provoke turnovers in sex‐ determination mechanisms, by inducing large‐scale sex reversal and thereby sex‐ratio selection for alternative sex‐determining genes. The frequency of turnovers and prevalence of homomorphic sex chromosomes in cold‐blooded vertebrates might thus directly relate to the temperature dependence in sex‐determination mechanisms.     

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.     

Conflict over condition‐dependent sex allocation can lead to mixed sex‐determination systems

Theory suggests that genetic conflicts drive turnovers between sex‐determining mechanisms, yet these studies only apply to cases where sex allocation is independent of environment or condition. Here, we model parent–offspring conflict in the presence of condition‐dependent sex allocation, where the environment has sex‐specific fitness consequences. Additionally, one sex is assumed to be more costly to produce than the other, which leads offspring to favor a sex ratio less biased toward the cheaper sex in comparison to the sex ratio favored by mothers. The scope for parent–offspring conflict depends on the relative frequency of both environments: when one environment is less common than the other, parent–offspring conflict can be reduced or even entirely absent, despite a biased population sex ratio. The model shows that conflict‐driven invasions of condition‐independent sex factors (e.g., sex chromosomes) result either in the loss of condition‐dependent sex allocation, or, interestingly, lead to stable mixtures of condition‐dependent and condition‐independent sex factors. The latter outcome corresponds to empirical observations in which sex chromosomes are present in organisms with environment‐dependent sex determination. Finally, conflict can also favor errors in environmental perception, potentially resulting in the loss of condition‐dependent sex allocation without genetic changes to sex‐determining loci.     

The evolution of sex ratios and sex-determining systems

Sex determination is a fundamental process governed by diverse mechanisms. Sex ratio selection is commonly implicated in the evolution of sex-determining systems, although formal models are rare. Here, we argue that, although sex ratio selection can induce shifts in sex determination, genomic conflicts between parents and offspring can explain why single-factor systems (e.g. XY/XX or ZW/ZZ) are common even in species that experience selection for biased sex ratios. Importantly, evolutionary shifts in sex determination do not always result in the biased production of sons and daughters sensu sex ratio theory. Thus, equal sex ratios might be an emergent character of sex-determining systems even when biased sex ratios are favored by selection.     

The evolution of unusual chromosomal systems in coccoids: extraordinary sex ratios revisited

Coccoids (scale insects) exhibit a wide variety of chromosomal systems. In many species, paternal chromosomes are eliminated from the male germline such that all of a male's sperm transmit an identical set of maternal chromosomes. In such species, an offspring's sex is determined by whether or not paternal chromosomes are inactivated in the egg's cytoplasm after fertilization. This paper presents a model of the evolution of paternal genome loss in coccoids from an ancestral system of XX-XO sex determination. The model is based on Hamilton's (1967) theory that different genetic elements within the genome have different unbeatable sex ratios. In this model (1) meiotic drive by the X chromosome in XO males causes female-biased sex ratios; (2) the maternal set of autosomes in males evolves effective sex linkage to exploit X-drive; and (3) genes expressed in mothers are selected to convert some of their XX daughters into sons. A similar model may explain the evolution of haplodiploidy.     

Dmrt1 polymorphism covaries with sex‐determination patterns in Rana temporaria

Patterns of sex‐chromosome differentiation and gonadal development have been shown to vary among populations of Rana temporaria along a latitudinal transect in Sweden. Frogs from the northern‐boreal population of Ammarnäs displayed well‐differentiated X and Y haplotypes, early gonadal differentiation, and a perfect match between phenotypic and genotypic sex. In contrast, no differentiated Y haplotypes could be detected in the southern population of Tvedöra, where juveniles furthermore showed delayed gonadal differentiation. Here, we show that Dmrt1, a gene that plays a key role in sex determination and sexual development across all metazoans, displays significant sex differentiation in Tvedöra, with a Y‐specific haplotype distinct from Ammarnäs. The differential segment is not only much shorter in Tvedöra than in Ammarnäs, it is also less differentiated and associates with both delayed gonadal differentiation and imperfect match between phenotypic and genotypic sex. Whereas Tvedöra juveniles with a local Y haplotype tend to ultimately develop as males, those without it may nevertheless become functional XX males, but with strongly female‐biased progeny. Our findings suggest that the variance in patterns of sex determination documented in common frogs might result from a genetic polymorphism within a small genomic region that contains Dmrt1. They also substantiate the view that recurrent convergences of sex determination toward a limited set of chromosome pairs may result from the co‐option of small genomic regions that harbor key genes from the sex‐determination pathway.     

XY FEMALES DO BETTER THAN THE XX IN THE AFRICAN PYGMY MOUSE,MUS MINUTOIDES

All therian mammals have a similar XY/XX sex‐determination system except for a dozen species. The African pygmy mouse, Mus minutoides, harbors an unconventional system in which all males are XY, and there are three types of females: the usual XX but also XX* and X*Y ones (the asterisk designates a sex‐reversal mutation on the X chromosome). The long‐term evolution of such a system is a paradox, because X*Y females are expected to face high reproductive costs (e.g., meiotic disruption and loss of unviable YY embryos), which should prevent invasion and maintenance of a sex‐reversal mutation. Hence, mechanisms for compensating for the costs could have evolved in M. minutoides. Data gathered from our laboratory colony revealed that X*Y females do compensate and even show enhanced reproductive performance in comparison to the XX and XX*; they produce significantly more offspring due to (i) a higher probability of breeding, (ii) an earlier first litter, and (iii) a larger litter size, linked to (iv) a greater ovulation rate. These findings confirm that rare conditions are needed for an atypical sex‐determination mechanism to evolve in mammals, and provide valuable insight into understanding modifications of systems with highly heteromorphic sex chromosomes.     

The origin of interlocus sexual conflict: is sex‐linkage important?

Sexual conflict has been proposed as a potential selective agent in the evolution of a variety of traits. Here, we present a simple model that investigates the initial conditions under which sex-linked and sex-limited harming alleles can invade a population. In this paper, we expand previous threshold models to study how sex-linkage and sex determination mechanisms affect the spreading conditions of a harming allele. Our models provide new insights into how sexual conflict could originate, showing that in diploid organisms the probability of a new harming allele spreading is independent of both the genetic sex determination system and the dominance relationships. However, the incidence of interlocus sexual conflicts in the initial steps of the invasion critically depends on the inheritance system.     

Partitioning of genetic variation across the genome using multimarker methods in a wild bird population

The underlying basis of genetic variation in quantitative traits, in terms of the number of causal variants and the size of their effects, is largely unknown in natural populations. The expectation is that complex quantitative trait variation is attributable to many, possibly interacting, causal variants, whose effects may depend upon the sex, age and the environment in which they are expressed. A recently developed methodology in animal breeding derives a value of relatedness among individuals from high‐density genomic marker data, to estimate additive genetic variance within livestock populations. Here, we adapt and test the effectiveness of these methods to partition genetic variation for complex traits across genomic regions within ecological study populations where individuals have varying degrees of relatedness. We then apply this approach for the first time to a natural population and demonstrate that genetic variation in wing length in the great tit (Parus major) reflects contributions from multiple genomic regions. We show that a polygenic additive mode of gene action best describes the patterns observed, and we find no evidence of dosage compensation for the sex chromosome. Our results suggest that most of the genomic regions that influence wing length have the same effects in both sexes. We found a limited amount of genetic variance in males that is attributed to regions that have no effects in females, which could facilitate the sexual dimorphism observed for this trait. Although this exploratory work focuses on one complex trait, the methodology is generally applicable to any trait for any laboratory or wild population, paving the way for investigating sex‐, age‐ and environment‐specific genetic effects and thus the underlying genetic architecture of phenotype in biological study systems.     

Male‐specific alleles in the Ryukyu drywood termite Neotermes sugioi

Sex‐determination systems often show remarkable diversity in upstream signals, although downstream genes are broadly conserved. Therefore, the downstream genes have been investigated in various taxa, but the most upstream signals determining sex in insects have been well‐described mainly in model organisms, including fruit flies and honey bees, and not in hemimetabolous insects such as termites. Identification of sex‐linked genetic markers in termites is important to the survey of primary sex‐determination signals. Here, we report male‐specific alleles at the microsatellite locus NK12‐1 in the Ryukyu drywood termite Neotermes sugioi (Kalotermitidae). This study provides the third example of a genetic marker linked with sexual phenotype in termites, which is a small but important step to elucidate the evolutionary process of the sex‐determination system in termites.     

Evolutionary transitions between mechanisms of sex determination in vertebrates

Sex in many organisms is a dichotomous phenotype--individuals are either male or female. The molecular pathways underlying sex determination are governed by the genetic contribution of parents to the zygote, the environment in which the zygote develops or interaction of the two, depending on the species. Systems in which multiple interacting influences or a continuously varying influence (such as temperature) determines a dichotomous outcome have at least one threshold. We show that when sex is viewed as a threshold trait, evolution in that threshold can permit novel transitions between genotypic and temperature-dependent sex determination (TSD) and remarkably, between male (XX/XY) and female (ZZ/ZW) heterogamety. Transitions are possible without substantive genotypic innovation of novel sex-determining mutations or transpositions, so that the master sex gene and sex chromosome pair can be retained in ZW-XY transitions. We also show that evolution in the threshold can explain all observed patterns in vertebrate TSD, when coupled with evolution in embryonic survivorship limits.     

High fidelity: extra‐pair fertilisations in eight Charadrius plover species are not associated with parental relatedness or social mating system

Extra‐pair paternity is a common reproductive strategy in many bird species. However, it remains unclear why extra‐pair paternity occurs and why it varies among species and populations. Plovers (Charadrius spp.) exhibit considerable variation in reproductive behaviour and ecology, making them excellent models to investigate the evolution of social and genetic mating systems. We investigated inter‐ and intra‐specific patterns of extra‐pair parentage and evaluated three major hypotheses explaining extra‐pair paternity using a comparative approach based on the microsatellite genotypes of 2049 individuals from 510 plover families sampled from twelve populations that constituted eight species. Extra‐pair paternity rates were very low (0 to 4.1% of chicks per population). No evidence was found in support of the sexual conflict or genetic compatibility hypotheses, and there was no seasonal pattern of extra‐pair paternity (EPP). The low prevalence of EPP is consistent with a number of alternative hypotheses, including the parental investment hypothesis, which suggests that high contribution to care by males restricts female plovers from engaging in extra‐pair copulations. Further studies are needed to critically test the importance of this hypothesis for mate choice in plovers.     

How to identify sex chromosomes and their turnover

Although sex is a fundamental component of eukaryotic reproduction, the genetic systems that control sex determination are highly variable. In many organisms the presence of sex chromosomes is associated with female or male development. Although certain groups possess stable and conserved sex chromosomes, others exhibit rapid sex chromosome evolution, including transitions between male and female heterogamety, and turnover in the chromosome pair recruited to determine sex. These turnover events have important consequences for multiple facets of evolution, as sex chromosomes are predicted to play a central role in adaptation, sexual dimorphism, and speciation. However, our understanding of the processes driving the formation and turnover of sex chromosome systems is limited, in part because we lack a complete understanding of interspecific variation in the mechanisms by which sex is determined. New bioinformatic methods are making it possible to identify and characterize sex chromosomes in a diverse array of non‐model species, rapidly filling in the numerous gaps in our knowledge of sex chromosome systems across the tree of life. In turn, this growing data set is facilitating and fueling efforts to address many of the unanswered questions in sex chromosome evolution. Here, we synthesize the available bioinformatic approaches to produce a guide for characterizing sex chromosome system and identity simultaneously across clades of organisms. Furthermore, we survey our current understanding of the processes driving sex chromosome turnover, and highlight important avenues for future research.     

Genetic evidence for co-occurrence of chromosomal and thermal sex-determining systems in a lizard

An individual's sex depends upon its genes (genotypic sex determination or GSD) in birds and mammals, but reptiles are more complex: some species have GSD whereas in others, nest temperatures determine offspring sex (temperature-dependent sex determination). Previous studies suggested that montane scincid lizards (Bassiana duperreyi, Scincidae) possess both of these systems simultaneously: offspring sex is determined by heteromorphic sex chromosomes (XX-XY system) in most natural nests, but sex ratio shifts suggest that temperatures override chromosomal sex in cool nests to generate phenotypically male offspring even from XX eggs. We now provide direct evidence that incubation temperatures can sex-reverse genotypically female offspring, using a DNA sex marker. Application of exogenous hormone to eggs also can sex-reverse offspring (oestradiol application produces XY as well as XX females). In conjunction with recent work on a distantly related lizard taxon, our study challenges the notion of a fundamental dichotomy between genetic and thermally determined sex determination, and hence the validity of current classification schemes for sex-determining systems in reptiles.     

Two sexes,one genome: the evolutionary dynamics of intralocus sexual conflict

As the evolutionary interests of males and females are frequently divergent, a trait value that is optimal for the fitness of one sex is often not optimal for the other. A shared genome also means that the same genes may underlie the same trait in both sexes. This can give rise to a form of sexual antagonism, known as intralocus sexual conflict (IASC). Here, a tug‐of‐war over allelic expression can occur, preventing the sexes from reaching optimal trait values, thereby causing sex‐specific reductions in fitness. For some traits, it appears that IASC can be resolved via sex‐specific regulation of genes that subsequently permits sexual dimorphism; however, it seems that whole‐genome resolution may be impossible, due to the genetic architecture of certain traits, and possibly due to the changing dynamics of selection. In this review, we explore the evolutionary mechanisms of, and barriers to, IASC resolution. We also address the broader consequences of this evolutionary feud, the possible interactions between intra‐ and interlocus sexual conflict (IRSC: a form of sexual antagonism involving different loci in each sex), and draw attention to issues that arise from using proxies as measurements of conflict. In particular, it is clear that the sex‐specific fitness consequences of sexual dimorphism require characterization before making assumptions concerning how this relates to IASC. Although empirical data have shown consistent evidence of the fitness effects of IASC, it is essential that we identify the alleles mediating these effects in order to show IASC in its true sense, which is a “conflict over shared genes.”     

A test of three hypotheses for ovariole number determination in the grasshopper Romalea microptera

Ovariole number in insects determines potential fecundity and can be influenced by genes, environmental conditions during development and parental effects. In the present study, three hypotheses are tested for ovariole number determination in the grasshopper Romalea microptera (Beauvois), which exhibits both intra‐ and interpopulation variation in ovariole number. In hypothesis 1, variation in ovariole number is a result of genetic variation. In hypothesis 2, ovariole number is influenced by nutrition during development. In hypothesis 3, ovariole number is influenced by maternal nutritional status. Females from four treatments are compared: low‐food, high‐food, daughters of low‐food, and daughters of high‐food. There is a relationship between parent and offspring ovariole number despite different environments, supporting hypothesis 1. Also, ovariole numbers are slightly, but significantly lower in individuals fed a low‐food diet compared with a high‐food diet, supporting hypothesis 2. Hypothesis 3 is not supported: starved and well‐fed females produce eggs of similar mass, as well as offspring with similar numbers of ovarioles, suggesting that the nutritional status of mothers does not influence offspring mass or offspring ovariole number. The results imply that genetic variation and developmental conditions determine ovariole number in this species but maternal environment does not. These results conflict with previous studies of ovariole determination in grasshoppers and locusts.