A General Model to Explain Repeated Turnovers of Sex Determination in the Salicaceae

Dioecy, the presence of separate sexes on distinct individuals, has evolved repeatedly in multiple plant lineages. However, the specific mechanisms by which sex systems evolve and their commonalities among plant species remain poorly understood. With both XY and ZW sex systems, the family Salicaceae provides a system to uncover the evolutionary forces driving sex chromosome turnovers. In this study, we performed a genome-wide association study to characterize sex determination in two Populus species, P. euphratica and P. alba. Our results reveal an XY system of sex determination on chromosome 14 of P. euphratica, and a ZW system on chromosome 19 of P. alba. We further assembled the corresponding sex-determination regions, and found that their sex chromosome turnovers may be driven by the repeated translocations of a Helitron-like transposon. During the translocation, this factor may have captured partial or intact sequences that are orthologous to a type-A cytokinin response regulator gene. Based on results from this and other recently published studies, we hypothesize that this gene may act as a master regulator of sex determination for the entire family. We propose a general model to explain how the XY and ZW sex systems in this family can be determined by the same RR gene. Our study provides new insights into the diversification of incipient sex chromosomes in flowering plants by showing how transposition and rearrangement of a single gene can control sex in both XY and ZW systems.     

Phylogeny of sex‐determining mechanisms in squamate reptiles: are sex chromosomes an evolutionary trap?

Squamate reptiles possess two general modes of sex determination: (1) genotypic sex determination (GSD), where the sex of an individual is determined by sex chromosomes, i.e. by sex‐specific differences in genotype; and (2) temperature‐dependent sex determination (TSD), where sex chromosomes are absent and sex is determined by nongenetic factors. After gathering information about sex‐determining mechanisms for more than 400 species, we employed comparative phylogenetic analyses to reconstruct the evolution of sex determination in Squamata. Our results suggest relative uniformity in sex‐determining mechanisms in the majority of the squamate lineages. Well‐documented variability is found only in dragon lizards (Agamidae) and geckos (Gekkota). Polarity of the sex‐determining mechanisms in outgroups identified TSD as the ancestral mode for Squamata. After extensive review of the literature, we concluded that to date there is no known well‐documented transition from GSD to TSD in reptiles, although transitions in the opposite direction are plentiful and well corroborated by cytogenetic evidence. We postulate that the evolution of sex‐determining mechanisms in Squamata was probably restricted to the transitions from ancestral TSD to GSD. In other words, transitions were from the absence of sex chromosomes to the emergence of sex chromosomes, which have never disappeared and constitute an evolutionary trap. This evolutionary trap hypothesis could change the understanding of phylogenetic conservatism of sex‐determining systems in many large clades such as butterflies, snakes, birds, and mammals. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 156 , 168–183.     

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.     

Ancestral state reconstruction analysis of hymenopteran sex determination mechanisms

We provide the first phylogenetic evidence supporting complementary sex determination (CSD) as the ancestral mechanism for haplodiploidy in the Hymenoptera. It is currently not possible, however, to distinguish the evolutionary polarity of single locus (sl) CSD and multiple‐locus (ml) CSD given the available data. In this light, we discuss the seemingly maladaptive hypothesis of ml‐CSD ancestry, suggesting that collapse from ml‐CSD to sl‐CSD should remain a viable evolutionary hypothesis based on (i) likely weakening of frequency‐dependent selection on sex alleles under ml‐CSD and (ii) recent findings with respect to the evolutionary novelty of the complementary sex determiner gene in honeybees. Our findings help provide a phylogenetically informed blueprint for future sampling of sex determination mechanisms in the Hymenoptera, as they yield hypotheses for many unsampled or ambiguous taxa and highlight taxa whose further sampling will influence reconstruction of the evolutionary polarity of sex determination mechanisms in major clades.     

CONSERVED SEX CHROMOSOMES ACROSS ADAPTIVELY RADIATED ANOLIS LIZARDS

Vertebrates possess diverse sex‐determining systems, which differ in evolutionary stability among particular groups. It has been suggested that poikilotherms possess more frequent turnovers of sex chromosomes than homoiotherms, whose effective thermoregulation can prevent the emergence of the sex reversals induced by environmental temperature. Squamate reptiles used to be regarded as a group with an extensive variability in sex determination; however, we document how the rather old radiation of lizards from the genus Anolis, known for exceptional ecomorphological variability, was connected with stability in sex chromosomes. We found that 18 tested species, representing most of the phylogenetic diversity of the genus, share the gene content of their X chromosomes. Furthermore, we discovered homologous sex chromosomes in species of two genera (Sceloporus and Petrosaurus) from the family Phrynosomatidae, serving here as an outgroup to Anolis. We can conclude that the origin of sex chromosomes within iguanas largely predates the Anolis radiation and that the sex chromosomes of iguanas remained conserved for a significant part of their evolutionary history. Next to therian mammals and birds, Anolis lizards therefore represent another adaptively radiated amniote clade with conserved sex chromosomes. We argue that the evolutionary stability of sex‐determining systems may reflect an advanced stage of differentiation of sex chromosomes rather than thermoregulation strategy.     

Effective heritability of targets of sex-ratio selection under environmental sex determination

Selection is expected to maintain primary sex ratios at an evolutionary equilibrium. In organisms with temperature-dependent sex determination (TSD), targets of sex-ratio selection include the thermal sensitivity of the sex-determining pathway (hereafter, sex determination threshold) and nest-site choice. However, offspring sex may be canalized for nests located in thermally extreme environments; thus, genetic variance for the sex determination threshold is not expressed and is invisible to direct selection. The concept of 'effective heritability' accounts for this dependence and provides a more realistic prediction of the expected evolutionary response to selection in the wild. Past estimates of effective heritability of the sex determination threshold, which were derived from laboratory data, suggested that the potential for the sex determination threshold to evolve in the wild was extremely low. We re-evaluated original estimates of this parameter by analysing field-collected measures of nest temperatures, vegetation cover and clutch sex ratios from nests in a population of painted turtles (Chrysemys picta). We coupled these data with measurements of broad-sense heritability of the sex determination threshold in C. picta, using an experiment that splits clutches of eggs between a constant temperature (i.e. typical laboratory incubation) and a daily fluctuating temperature (i.e. similar to natural nests) with the same mean. We found that (i) the effective heritability of the sex determination threshold appears to have been historically underestimated and the effective heritability of nest-site choice has been overestimated and (ii) significant family-by-incubation treatment interaction exists for sex for C. picta between constant- and fluctuating-temperature regimes. Our results suggest that the thermal sensitivity of the sex-determining pathway may play a larger, more complex role in the microevolution of TSD than traditionally thought.     

Evolution of Sex Determination and Sex Chromosomes: A Novel Alternative Paradigm

Sex chromosomes can differ between species as a result of evolutionary turnover, a process that can be driven by evolution of the sex determination pathway. Canonical models of sex chromosome turnover hypothesize that a new master sex determining gene causes an autosome to become a sex chromosome or an XY chromosome pair to switch to a ZW pair (or vice versa). Here, a novel paradigm for the evolution of sex determination and sex chromosomes is presented, in which there is an evolutionary transition in the master sex determiner, but the X chromosome remains unchanged. There are three documented examples of the novel paradigm, and it is hypothesized that a similar process could happen in a ZW sex chromosome system. Three other taxa are also identified where the novel paradigm may have occurred, and how it could be distinguished from canonical trajectories in these and additional taxa is also described.     

Pleistocene divergence in the absence of gene flow among populations of a viviparous reptile with intraspecific variation in sex determination

Polymorphisms can lead to genetic isolation if there is differential mating success among conspecifics divergent for a trait. Polymorphism for sex‐determining system may fall into this category, given strong selection for the production of viable males and females and the low success of heterogametic hybrids when sex chromosomes differ (Haldane''s rule). Here we investigated whether populations exhibiting polymorphism for sex determination are genetically isolated, using the viviparous snow skink Carinascincus ocellatus. While a comparatively high elevation population has genotypic sex determination, in a lower elevation population there is an additional temperature component to sex determination. Based on 11,107 SNP markers, these populations appear genetically isolated. “Isolation with Migration” analysis also suggests these populations diverged in the absence of gene flow, across a period encompassing multiple Pleistocene glaciations and likely greater geographic proximity of populations. However, further experiments are required to establish whether genetic isolation may be a cause or consequence of differences in sex determination. Given the influence of temperature on sex in one lineage, we also discuss the implications for the persistence of this polymorphism under climate change.     

Segregating variation for temperature-dependent sex determination in a lizard

Temperature-dependent sex determination (TSD) was first reported in 1966 in an African lizard. It has since been shown that TSD occurs in some fish, several lizards, tuataras, numerous turtles and all crocodilians. Extreme temperatures can also cause sex reversal in several amphibians and lizards with genotypic sex determination. Research in TSD species indicates that estrogen signaling is important for ovary development and that orthologs of mammalian genes have a function in gonad differentiation. Nevertheless, the mechanism that actually transduces temperature into a biological signal for ovary versus testis development is not known in any species. Classical genetics could be used to identify the loci underlying TSD, but only if there is segregating variation for TSD. Here, we use the ‘animal model'' to analyze inheritance of sexual phenotype in a 13-generation pedigree of captive leopard geckos, Eublepharis macularius, a TSD reptile. We directly show genetic variance and genotype-by-temperature interactions for sex determination. Additive genetic variation was significant at a temperature that produces a female-biased sex ratio (30 °C), but not at a temperature that produces a male-biased sex ratio (32.5 °C). Conversely, dominance variance was significant at the male-biased temperature (32.5 °C), but not at the female-biased temperature (30 °C). Non-genetic maternal effects on sex determination were negligible in comparison with additive genetic variance, dominance variance and the primary effect of temperature. These data show for the first time that there is segregating variation for TSD in a reptile and consequently that a quantitative trait locus analysis would be practicable for identifying the genes underlying TSD.     

Exploring the evolution of environmental sex determination, especially in reptiles

Environmental sex determination has been documented in a variety of organisms for many decades and the adaptive significance of this unusual sex-determining mechanism has been clarified empirically in most cases. In contrast, temperature-dependent sex determination (TSD) in amniote vertebrates, first noted 40 years ago in a lizard, has defied a general satisfactory evolutionary explanation despite considerable research effort. After briefly reviewing relevant theory and prior empirical work, we draw attention to recent comparative analyses that illuminate the evolutionary history of TSD in amniote vertebrates and point to clear avenues for future research on this challenging topic. To that end, we then highlight the latest empirical findings in lizards and turtles, as well as promising experimental results from a model organism, that portend an exciting future of progress in finally elucidating the evolutionary cause(s) and significance of TSD.     

Sex-chromosome differentiation and ‘sex races’ in the common frog (Rana temporaria)

Sex-chromosome differentiation was recently shown to vary among common frog populations in Fennoscandia, suggesting a trend of increased differentiation with latitude. By rearing families from two contrasted populations (respectively, from northern and southern Sweden), we show this disparity to stem from differences in sex-determination mechanisms rather than in XY-recombination patterns. Offspring from the northern population display equal sex ratios at metamorphosis, with phenotypic sexes that correlate strongly with paternal LG₂ haplotypes (the sex chromosome); accordingly, Y haplotypes are markedly differentiated, with male-specific alleles and depressed diversity testifying to their smaller effective population size. In the southern population, by contrast, a majority of juveniles present ovaries at metamorphosis; only later in development do sex ratios return to equilibrium. Even at these later stages, phenotypic sexes correlate only mildly with paternal LG₂ haplotypes; accordingly, there are no recognizable Y haplotypes. These distinct patterns of gonadal development fit the concept of ‘sex races’ proposed in the 1930s, with our two populations assigned to the ‘differentiated’ and ‘semi-differentiated’ races, respectively. Our results support the suggestion that ‘sex races’ differ in the genetic versus epigenetic components of sex determination. Analysing populations from the ‘undifferentiated race’ with high-density genetic maps should help to further test this hypothesis.     

What was the ancestral sex‐determining mechanism in amniote vertebrates?

Amniote vertebrates, the group consisting of mammals and reptiles including birds, possess various mechanisms of sex determination. Under environmental sex determination (ESD), the sex of individuals depends on the environmental conditions occurring during their development and therefore there are no sexual differences present in their genotypes. Alternatively, through the mode of genotypic sex determination (GSD), sex is determined by a sex‐specific genotype, i.e. by the combination of sex chromosomes at various stages of differentiation at conception. As well as influencing sex determination, sex‐specific parts of genomes may, and often do, develop specific reproductive or ecological roles in their bearers. Accordingly, an individual with a mismatch between phenotypic (gonadal) and genotypic sex, for example an individual sex‐reversed by environmental effects, should have a lower fitness due to the lack of specialized, sex‐specific parts of their genome. In this case, evolutionary transitions from GSD to ESD should be less likely than transitions in the opposite direction. This prediction contrasts with the view that GSD was the ancestral sex‐determining mechanism for amniote vertebrates. Ancestral GSD would require several transitions from GSD to ESD associated with an independent dedifferentiation of sex chromosomes, at least in the ancestors of crocodiles, turtles, and lepidosaurs (tuataras and squamate reptiles). In this review, we argue that the alternative theory postulating ESD as ancestral in amniotes is more parsimonious and is largely concordant with the theoretical expectations and current knowledge of the phylogenetic distribution and homology of sex‐determining mechanisms.     

EVOLUTION OF SEX DETERMINATION SYSTEMS WITH HETEROGAMETIC MALES AND FEMALES IN SILENE

The plant genus Silene has become a model for evolutionary studies of sex chromosomes and sex‐determining mechanisms. A recent study performed in Silene colpophylla showed that dioecy and the sex chromosomes in this species evolved independently from those in Silene latifolia, the most widely studied dioecious Silene species. The results of this study show that the sex‐determining system in Silene otites, a species related to S. colpophylla, is based on female heterogamety, a sex determination system that is unique among the Silene species studied to date. Our phylogenetic data support the placing of S. otites and S. colpophylla in the subsection Otites and the analysis of ancestral states suggests that the most recent common ancestor of S. otites and S. colpophylla was most probably dioecious. These observations imply that a switch from XX/XY sex determination to a ZZ/ZW system (or vice versa) occurred in the subsection Otites. This is the first report of two different types of heterogamety within one plant genus of this mostly nondioecious plant family.     

Ecological genetics of sex ratios in plant populations

In many angiosperm species, populations are reproductively subdivided into distinct sexual morphs including females, males and hermaphrodites. Sexual polymorphism is maintained by frequency-dependent selection, leading to predictable sex ratios at equilibrium. Charles Darwin devoted much of his book ‘The Different Forms of Flowers on Plants of the Same Species’ (1877) to investigating plant sexual polymorphisms and laid the foundation for many problems addressed today by integrating theory with empirical studies of the demography and genetics of populations. Here, we summarize our recent work on the ecological and genetic mechanisms influencing variation in sex ratios and their implications for evolutionary transitions among sexual systems. We present the results of a survey of sex ratios from 126 species from 47 angiosperm families and then address two general problems using examples from diverse angiosperm taxa: (i) the mechanisms governing biased sex ratios in dioecious species; (ii) the origins and maintenance of populations composed of females, males and hermaphrodites. Several themes are emphasized, including the importance of non-equilibrium conditions, the role of life history and demography in affecting sex ratios, the value of theory for modelling the dynamics of sex ratio variation, and the utility of genetic markers for investigating evolutionary processes in sexually polymorphic plant populations.     

BioEssays 10/2020

Frequent independent origins of environmental sex determination (ESD) are assumed within amniotes. However, the phylogenetic distribution of sex-determining modes suggests that ESD is likely very ancient and may be homologous across ESD groups. Sex chromosomes are demonstrated to be old and stable in endothermic (mammals and birds) and many ectothermic (non-avian reptiles) lineages, but they are mostly non-homologous between individual amniote lineages. The phylogenetic pattern may be explained by ancestral ESD with multiple transitions to later evolutionary stable genotypic sex determination. It is pointed out here that amniote ESD shares several key aspects with sequential hermaphroditism of fishes such as a lack of sex differences in genomes, biased population sex ratios, and potentially also molecular mechanism related to general stress responses. Here, it is speculated that ESD evolves via a heterochronic shift of the sensitive period of sex change from the adult to the embryonic stage in a hermaphroditic amniote ancestor. Also see the video abstract here https://youtu.be/q2mjtlCefu4 .     

木本植物性别决定基因研究进展

雌雄异株植物是研究性别决定遗传机制及性染色体起源与进化的理想材料,而克隆性别决定基因是解析性别决定遗传机制的关键。木本植物中有丰富的雌雄异株植物,且包括2种相反的性别决定系统：XY型(雌株为同配型的XX,雄株为异配型的XY)和ZW型(雌株为异配型的ZW,雄株为同配型的ZZ)。此外,不同性别植株的经济价值也有所不同。在木...     

Multigenerational response to artificial selection for biased clutch sex ratios in Tigriopus californicus populations

Polygenic sex determination (PSD) is relatively rare and theoretically evolutionary unstable, yet has been reported across a range of taxa. Evidence for multilocus PSD is provided by (i) large between‐family variance in sex ratio, (ii) paternal and maternal effects on family sex ratio and (iii) response to selection for family sex ratio. This study tests the polygenic hypothesis of sex determination in the harpacticoid copepod Tigriopus californicus using the criterion of response to selection. We report the first multigenerational quantitative evidence that clutch sex ratio responds to artificial selection in both directions (selection for male‐ and female‐biased families) and in multiple populations of T. californicus. In the five of six lines that showed a response to selection, realized heritability estimated by multigenerational analysis ranged from 0.24 to 0.58. Divergence of clutch sex ratio between selection lines is rapid, with response to selection detectable within the first four generations of selection.