Conservation of sex chromosomes in lacertid lizards

Sex chromosomes are believed to be stable in endotherms, but young and evolutionary unstable in most ectothermic vertebrates. Within lacertids, the widely radiated lizard group , sex chromosomes have been reported to vary in morphology and heterochromatinization, which may suggest turnovers during the evolution of the group. We compared the partial gene content of the Z‐specific part of sex chromosomes across major lineages of lacertids and discovered a strong evolutionary stability of sex chromosomes. We can conclude that the common ancestor of lacertids, living around 70 million years ago (Mya), already had the same highly differentiated sex chromosomes. Molecular data demonstrating an evolutionary conservation of sex chromosomes have also been documented for iguanas and caenophidian snakes. It seems that differences in the evolutionary conservation of sex chromosomes in vertebrates do not reflect the distinction between endotherms and ectotherms, but rather between amniotes and anamniotes, or generally, the differences in the life history of particular lineages.     

The genomic legacy from the extinct Lepus timidus to the three hare species of Iberia: contrast between mtDNA, sex chromosomes and autosomes

Extensive interspecific genetic introgression is often reported, and appraising its genomic impact can serve to determine whether it results from selection on specific loci or from demographic processes affecting the whole genome. The three species of hares present in the Iberian Peninsula harbour high frequencies of mitochondrial DNA (mtDNA) from Lepus timidus, an arctic/boreal species now extinct in the region. This could result from the invasive replacement of L. timidus by the temperate species during deglaciation but should then have left traces in the nuclear genome. We typed single nucleotide polymorphisms (SNPs) discovered by sequencing 10 autosomal loci, two X-linked and one Y-linked in species-wide samples of the four taxa. Based on lineage-diagnostic SNPs, we detected no trace of L. timidus sex chromosomes in Iberia. From the frequencies of inferred haplotypes, autosomal introgression into L. granatensis appeared mostly sporadic but always widespread instead of restricted to the north as mtDNA. Autosomal introgression into Iberian L. europaeus , inhabiting the Pyrenean foothills, was hardly detectable, despite quasi-fixation of L. timidus mtDNA. L. castroviejoi , endemic to the Cantabrian Mountains and fixed for L. timidus mtDNA, showed little traces of autosomal introgression. The absence of sex-chromosome introgression presumably resulted from X-linked hybrid male unfitness. The contrasting patterns between the autosomes and mtDNA could reflect general gender asymmetric processes such as frequency-dependent female assortative mating, lower mtDNA migration and higher male dispersal, but adaptive mtDNA introgression cannot be dismissed. Additionally, we document reciprocal introgression between L. europaeus and both L. granatensis in Iberia and L. timidus outside Iberia.     

Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals

In theory, parthenogenetic lineages have low evolutionary potential because they inexorably accumulate deleterious mutations and do not generate much genotypic diversity. As a result, most parthenogenetic taxa occupy the terminal nodes of phylogenetic trees. The rate and mode of development of parthenogenesis are important factors to consider when assessing its costs and benefits since they determine both the level of genetic diversity and the ecological adaptability of the resulting lineages. The origin of parthenogenesis is polyphyletic in many taxa, suggesting that genetic systems maintaining sexuality are often labile. In addition, the loss of sex may be achieved in several ways, leading to parthenogenetic lineages with distinct genetic profiles. This could then influence not only the fate of such lineages in the long term, but also the outcome of competition with their sexual counterparts in the short term. In this paper, we review the possible evolutionary routes to parthenogenesis based on a survey of the phylogenetic relationships between sexual and parthenogenetic lineages in a broad range of animals. We also examine the different mechanisms by which parthenogenetic lineages could arise, and discuss the influence of these mechanisms on both the genetic properties and the ecological life styles of the resulting lineages.  © 2003 The Linnean Society of London. Biological Journal of the Linnean Society , 2003, 79 , 151–163.     

Waves of parthenogenesis in the desert: evidence for the parallel loss of sex in a grasshopper and a gecko from Australia

The rarity of parthenogenesis, reproduction without sex, is a major evolutionary puzzle. To understand why sexual genetic systems are so successful in nature, we must understand why parthenogenesis sometimes evolves and persists. Here we use DNA sequence data to test for similarities in the tempo and mode of the evolution of parthenogenesis in a grasshopper and a lizard from the Australian desert. We find spectacular congruence between genetic and geographic patterns of parthenogenesis in these distantly related organisms. In each species, parthenogenesis evolved twice and appears to have expanded in parallel waves across the desert, suggesting a highly general selective force against sex.     

Transfer of a parasitic sex factor to the nuclear genome of the host: A hypothesis on the evolution of sex-determining mechanisms in the terrestrial Isopod Armadillidium vulgare Latr.

In A. vulgare sex is usually determined either by a cytoplasmic feminizing factor (F symbiotic bacteria) or by another feminizing factor (f) which behaves like a mobile element of DNA and which seems to correspond to a fragment of bacterial DNA. By inhibiting the expression of male genes carried by the Z heterochromosome, these feminizing factors induce differentiation of neo-females [ZZ(+F) or ZZ(+f)]. Such a mechanism leads to the production of progenies whose sex ratio is highly female biased. In some populations in which F and/or f factors are present, genetic females (WZ) have disappeared and all individuals (males and females) are genetic males. However in other populations, cohabitation of ZZ(+f) neo-females and females in all points similar to genetic females is observed. Such a situation may be unstable and is not likely to be explainable only by migrations of individuals from distinct populations. Owing to certain types of crosses, in particular those which involve an artificial neo-male ( = female reversed into a functional male by an implant of androgenic gland) we show here that the f factor can be transmitted as a Mendelian gene. In these progenies Z_fZ females may appear: like WZ females, they breed broods whose sex ratio is unbiased. The hypothesis that the “F bacteria—A. vulgare” symbiosis may have led, after a complex co-evolutive process (F bacteria → f mobile element → insertion of f on Z heterochromosome), to the creation (from a male genotype) of a female genotype, is put forward. The consequences of such a phenomenon on the composition and the evolution of A. vulgare populations are examined.     

The rates of introgression and barriers to genetic exchange between hybridizing species: sex chromosomes vs autosomes

Interspecific crossing experiments have shown that sex chromosomes play a major role in reproductive isolation between many pairs of species. However, their ability to act as reproductive barriers, which hamper interspecific genetic exchange, has rarely been evaluated quantitatively compared to Autosomes. This genome-wide limitation of gene flow is essential for understanding the complete separation of species, and thus speciation. Here, we develop a mainland-island model of secondary contact between hybridizing species of an XY (or ZW) sexual system. We obtain theoretical predictions for the frequency of introgressed alleles, and the strength of the barrier to neutral gene flow for the two types of chromosomes carrying multiple interspecific barrier loci. Theoretical predictions are obtained for scenarios where introgressed alleles are rare. We show that the same analytical expressions apply for sex chromosomes and autosomes, but with different sex-averaged effective parameters. The specific features of sex chromosomes (hemizygosity and absence of recombination in the heterogametic sex) lead to reduced levels of introgression on the X (or Z) compared to autosomes. This effect can be enhanced by certain types of sex-biased forces, but it remains overall small (except when alleles causing incompatibilities are recessive). We discuss these predictions in the light of empirical data comprising model-based tests of introgression and cline surveys in various biological systems.     

The relationship between gene dosage,gene expression,and sex in Drosophila

In Drosophila, the ratio of the number of X chromosomes to sets of other chromosomes initiates a series of events which result in sexual differentiation. In addition, this ratio establishes dosage compensation, a mechanism which equalizes the products of X-linked genes in males and females. The present review discusses possible genetic entities responsible for the interpretation of chromosomal sex and subsequent sex-mediated regulation during development.     

A supernumerary “B-sex” chromosome drives male sex determination in the Pachón cavefish,Astyanax mexicanus

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A genetic method to resolve gender complements investigations on sex ratios in Rumex acetosa

The perennial dioecious weed, Rumex acetosa, possesses sex chromosomes (XX in females, XY1Y2 in males). Yet, the operational sex ratios are female-biased. Until now, sex ratio studies in R. acetosa, as in most plants, have relied on data obtained at sexual maturity. To resolve gender among the seeds and nonflowering plants of R. acetosa, a genetic method involving a DNA marker located on both Y chromosomes has now been developed and applied. The results suggest that the sex ratios are about 1 : 1 in the whole seed pool, but that a significant female bias develops by the time of flowering. Since the age of sexually mature plants is two years or more, the time frame during which the female bias present at sexual maturity develops can be several years. It appears that male seeds germinate at a lower rate and males suffer from a greater mortality during the years-long lifespan of R. acetosa. However, there are no considerable sex-related differences in vegetative vigour.     

Counterselection on sex chromosomes in the Mus musculus European hybrid zone

The extent to which alleles can disperse across a hybrid zone depends on the selection they are subjected to in the hybrid genetic background or, for those that are selectively neutral, on their ability to escape from the unfavourable environment by recombination. Three markers spanning a 45 cM segment in the center of the X chromosome were used to investigate the degree to which selection against X chromosome linked genes helps to maintain the barrier to gene flow in the hybrid zone between Mus musculus domesticus and M. m. musculus in Denmark. The introgression of all the sex chromosome specific markers was more limited than that of the autosomal enzymes (Idh1, Amy, Gpd1, Pgm1, Es1, Es2, Mpi, Np1, Es10, Sod1) and the mitochondrial DNA. The cline for DXPas2, which is in the center of the X chromosome, is extremely steep and shows that certain genes located in this region are strongly selected against in the hybrid background. The clines of the other two X-linked markers, Hprt and DXPas1, and of the Y chromosome are not as abrupt and all three have similar asymmetric introgression patterns. Although the musculus variants appear to behave in much the same way as those of the autosomal genes, the domesticus variants do not introgress. The results show that X-linked and to a lesser extent Y-linked genes are more strongly selected against in the hybrid genome than the mitochondrial genome or the different autosomal loci. This suggests that co-adapted gene systems involving the sex chromosomes may play an important role in the hybrid breakdown between the two subspecies.     

The contrasting role of heterochromatin in the differentiation of sex chromosomes: an overview from Neotropical fishes

During the evolutionary process of the sex chromosomes, a general principle that arises is that cessation or a partial restriction of recombination between the sex chromosome pair is necessary. Data from phylogenetically distinct organisms reveal that this phenomenon is frequently associated with the accumulation of heterochromatin in the sex chromosomes. Fish species emerge as excellent models to study this phenomenon because they have much younger sex chromosomes compared to higher vertebrates and many other organisms making it possible to follow their steps of differentiation. In several Neotropical fish species, the heterochromatinization, accompanied by amplification of tandem repeats, represents an important step in the morphological differentiation of simple sex chromosome systems, especially in the ZZ/ZW sex systems. In contrast, multiple sex chromosome systems have no additional increase of heterochromatin in the chromosomes. Thus, the initial stage of differentiation of the multiple sex chromosome systems seems to be associated with proper chromosomal rearrangements, whereas the simple sex chromosome systems have an accumulation of heterochromatin. In this review, attention has been drawn to this contrasting role of heterochromatin in the differentiation of simple and multiple sex chromosomes of Neotropical fishes, highlighting their surprising evolutionary dynamism.     

Genetic diversity and the origins of parthenogenesis in the teiid lizard Aspidoscelis laredoensis

Unisexual vertebrates typically form through hybridization events between sexual species in which reproductive mode transitions occur in the hybrid offspring. This evolutionary history is thought to have important consequences for the ecology of unisexual lineages and their interactions with congeners in natural communities. However, these consequences have proven challenging to study owing to uncertainty about patterns of population genetic diversity in unisexual lineages. Of particular interest is resolving the contribution of historical hybridization events versus post formational mutation to patterns of genetic diversity in nature. Here we use restriction site associated DNA genotyping to evaluate genetic diversity and demographic history in Aspidoscelis laredoensis, a diploid unisexual lizard species from the vicinity of the Rio Grande River in southern Texas and northern Mexico. The sexual progenitor species from which one or more lineages are derived also occur in the Rio Grande Valley region, although patterns of distribution across individual sites are quite variable. Results from population genetic and phylogenetic analyses resolved the major axes of genetic variation in this species and highlight how these match predictions based on historical patterns of hybridization. We also found discordance between results of demographic modelling using different statistical approaches with the genomic data. We discuss these insights within the context of the ecological and evolutionary mechanisms that generate and maintain lineage diversity in unisexual species. As one of the most dynamic, intriguing, and geographically well investigated groups of whiptail lizards, these species hold substantial promise for future studies on the constraints of diversification in unisexual vertebrates.     

Postzygotic incompatibilities between the pupfishes, Cyprinodon elegans and Cyprinodon variegatus: hybrid male sterility and sex ratio bias

I examined the intrinsic postzygotic incompatibilities between two pupfishes, Cyprinodon elegans and Cyprinodon variegatus. Laboratory hybridization experiments revealed evidence of strong postzygotic isolation. Male hybrids have very low fertility, and the survival of backcrosses into C. elegans was substantially reduced. In addition, several crosses produced female-biased sex ratios. Crosses involving C. elegans females and C. variegatus males produced only females, and in backcrosses involving hybrid females and C. elegans males, males made up approximately 25% of the offspring. All other crosses produced approximately 50% males. These sex ratios could be explained by genetic incompatibilities that occur, at least in part, on sex chromosomes. Thus, these results provide strong albeit indirect evidence that pupfish have XY chromosomal sex determination. The results of this study provide insight on the evolution of reproductive isolating mechanisms, particularly the role of Haldane's rule and the 'faster-male' theory in taxa lacking well-differentiated sex chromosomes.     

Rapid assessment of the sex of codling moth Cydia pomonella (Linnaeus) (Lepidoptera: Tortricidae) eggs and larvae

Two different methods were tested to identify the sex of the early developmental stages of the codling moth Cydia pomonella (Linnaeus) (Lepidoptera: Tortricidae) with a WZ/ZZ (female/male) sex chromosome system. First, it was shown that the sex of all larval stages can be easily determined by the presence or absence of sex chromatin, which is formed by the female‐specific W chromosome in interphase nuclei. This trait can also be used to identify the sex of newly hatched larvae but it does require care and accuracy. Secondly, a new sexing technique was developed based on a molecular marker of the codling moth W chromosome. Flanking regions of an earlier described W‐specific sequence (CpW2) were isolated and sequenced and a 2.74 kb sequence (CpW2‐EcoRI), specific for the W chromosome, was obtained. Several PCR tests were conducted, which confirmed that the CpW2‐EcoRI sequence is a reliable marker for the sex identification in codling moth samples of different geographical origin. In addition, a fragment of a codling moth gene, period (Cpper) was isolated and sequenced. Results of southern hybridization of the Cpper probe with female and male genomic DNA suggested that the Cpper gene is located on the Z chromosome. Then a multiplex PCR assay was developed, which co‐amplified the CpW2‐EcoRI sequence to identify the W chromosome and the Z‐linked Cpper sequence, which served as a positive control of accurate processing of tested samples. The multiplex PCR provides an easy and rapid identification of the sex of embryos and early larval instars of the codling moth.     

Review. Meiotic drive and sex determination: molecular and cytological mechanisms of sex ratio adjustment in birds

Differences in relative fitness of male and female offspring across ecological and social environments should favour the evolution of sex-determining mechanisms that enable adjustment of brood sex ratio to the context of breeding. Despite the expectation that genetic sex determination should not produce consistent bias in primary sex ratios, extensive and adaptive modifications of offspring sex ratio in relation to social and physiological conditions during reproduction are often documented. Such discordance emphasizes the need for empirical investigation of the proximate mechanisms for modifying primary sex ratios, and suggests epigenetic effects on sex-determining mechanisms as the most likely candidates. Birds, in particular, are thought to have an unusually direct opportunity to modify offspring sex ratio because avian females are heterogametic and because the sex-determining division in avian meiosis occurs prior to ovulation and fertilization. However, despite evidence of strong epigenetic effects on sex determination in pre-ovulatory avian oocytes, the mechanisms behind such effects remain elusive. Our review of molecular and cytological mechanisms of avian meiosis uncovers a multitude of potential targets for selection on biased segregation of sex chromosomes, which may reflect the diversity of mechanisms and levels on which such selection operates in birds. Our findings indicate that pronounced differences between sex chromosomes in size, shape, size of protein bodies, alignment at the meiotic plate, microtubule attachment and epigenetic markings should commonly produce biased segregation of sex chromosomes as the default state, with secondary evolution of compensatory mechanisms necessary to maintain unbiased meiosis. We suggest that it is the epigenetic effects that modify such compensatory mechanisms that enable context-dependent and precise adjustment of primary sex ratio in birds. Furthermore, we highlight the features of avian meiosis that can be influenced by maternal hormones in response to environmental stimuli and may account for the precise and adaptive patterns of offspring sex ratio adjustment observed in some species.     

Context-dependent sex allocation: constraints on the expression and evolution of maternal effects

Despite decades of research, whether vertebrates can and do adaptively adjust the sex ratio of their offspring is still highly debated. However, this may have resulted from the failure of empirical tests to identify large and predictable fitness returns to females from strategic adjustment. Here, we test the effect of diet quality and maternal condition on facultative sex ratio adjustment in the color polymorphic Gouldian finch (Erythrura gouldiae), a species that exhibits extreme maternal allocation in response to severe and predictable (genetically-determined) fitness costs. On high-quality diets, females produced a relatively equal sex ratio, but over-produced sons in poor dietary conditions. Despite the lack of sexual size dimorphism, nutritionally stressed foster sons were healthier, grew faster, and were more likely to survive than daughters. Although these findings are in line with predictions from sex allocation theory, the extent of adjustment is considerably lower than previously reported for this species. Females therefore have strong facultative control over sex allocation, but the extent of adjustment is likely determined by the relative magnitude of fitness gains and the ability to reliably predict sex-specific benefits from environmental (vs. genetic) variables. These findings may help explain the often inconsistent, weak, or inconclusive empirical evidence for adaptive sex ratio adjustment in vertebrates.     

Variation in the cranium shape of wall lizards (Podarcis spp.): effects of phylogenetic constraints, allometric constraints and ecology

We used geometric morphometrics to explore the influence of phylogenetic and allometric constraints as well as ecology on variation in cranium shape in five species of monophyletic, morphologically similar Podarcis lizards (Podarcis erhardii, Podarcis melisellensis, Podarcis muralis, Podarcis sicula and Podarcis taurica). These species belong to different clades, they differ in their habitat preferences and can be classified into two distinct morphotypes: saxicolous and terrestrial. We found (i) no phylogenetic signal in cranium shape, (ii) diverging allometric slopes among species, and (iii) a significant effect of habitat on cranium shape. The saxicolous species (P. erhardii and P. muralis) had crania with elongated parietals, elongated cranium bases, shortened anterior parts of the dorsal cranium, reduced chambers of the jaw adductor muscles and larger subocular foramina. These cranial features are adaptations that compensate for a flattened cranium, dwelling on vertical surfaces and seeking refuge in crevices. The crania of the terrestrial species (P. melisellensis, P. sicula and P. taurica) tended to be more elongate and robust, with enlarged chambers of the jaw adductor muscle, reduced skull bases and shortened parietals. Terrestrial species exhibited more variation in cranium shape than saxicolous species. Our study suggests that shape variation in Podarcis sp. lizards is largely influenced by ecology, which likely affects species-specific patterns of static allometry.