A comparison of the Trojan Y Chromosome and daughterless carp eradication strategies

Two autocidal genetic biocontrol methods have been proposed as a means to eliminate invasive fish by changing the sex ratio of the population: the Trojan Y Chromosome (TYC) strategy and the Daughterless Carp (DC) strategy. Both strategies were modeled using ordinary differential equations that allow the kinetics of female decline to be assessed under identical modeling conditions. When compared directly in an ordinary differential equation (ODE) model, the TYC strategy was found to result in female extinction more rapidly than a DC strategy (in each of three models tested in which the Daughterless autocidal fish contained an aromatase inhibitor gene in either two or eight copies). The TYC strategy additionally required the introduction of fewer autocidal fish to the target population to achieve local extinction of females as compared to the DC approach. The results suggest that the relatively lower efficiency of female reduction associated with the DC approach is a consequence of a greater capacity to produce females and also a reduced capacity to produce males as compared to the TYC system.     

Analysis of the Trojan Y chromosome model for eradication of invasive species in a dendritic riverine system

The use of Trojan Y chromosomes has been proposed as a genetic strategy for the eradication of invasive species. The strategy is particularly relevant to invasive fish species that have XY sex determination system and are amenable to sex-reversal. In this paper we study the dynamics of an invasive fish population occupying a dendritic domain in which Trojan individuals bearing multiple Y chromosomes have been released as a means of eradication. We demonstrate the existence of a bounded absorbing set that represents extinction of the invasive species irrespective of the dendritic configuration. The method of analysis used to obtain global estimates could be applied to other population problems and other geometries.     

Analysis of the Trojan Y-Chromosome eradication strategy for an invasive species

The Trojan Y-Chromosome (TYC) strategy, an autocidal genetic biocontrol method, has been proposed to eliminate invasive alien species. In this work, we analyze the dynamical system model of the TYC strategy, with the aim of studying the viability of the TYC eradication and control strategy of an invasive species. In particular, because the constant introduction of sex-reversed trojan females for all time is not possible in practice, there arises the question: What happens if this injection is stopped after some time? Can the invasive species recover? To answer that question, we perform a rigorous bifurcation analysis and study the basin of attraction of the recovery state and the extinction state in both the full model and a certain reduced model. In particular, we find a theoretical condition for the eradication strategy to work. Additionally, the consideration of an Allee effect and the possibility of a Turing instability are also studied in this work. Our results show that: (1) with the inclusion of an Allee effect, the number of the invasive females is not required to be very low when the introduction of the sex-reversed trojan females is stopped, and the remaining Trojan Y-Chromosome population is sufficient to induce extinction of the invasive females; (2) incorporating diffusive spatial spread does not produce a Turing instability, which would have suggested that the TYC eradication strategy might be only partially effective, leaving a patchy distribution of the invasive species.     

A model describing the effect of sex-reversed YY fish in an established wild population: The use of a Trojan Y chromosome to cause extinction of an introduced exotic species

A novel means of inducing extinction of an exotic fish population is proposed using a genetic approach to shift the ratio of male to females within a population. In the proposed strategy, sex-reversed fish containing two Y chromosomes are introduced into a normal fish population. These YY fish result in the production of a disproportionate number of male fish in subsequent generations. Mathematical modeling of the system following introduction of YY fish at a constant rate reveals that female fish decline in numbers over time, leading to eventual extinction of the population.     

Stochastic models for the Trojan Y-Chromosome eradication strategy of an invasive species

The Trojan Y-Chromosome (TYC) strategy, an autocidal genetic biocontrol method, has been proposed to eliminate invasive alien species. In this work, we develop a Markov jump process model for this strategy, and we verify that there is a positive probability for wild-type females going extinct within a finite time. Moreover, when sex-reversed Trojan females are introduced at a constant population size, we formulate a stochastic differential equation (SDE) model as an approximation to the proposed Markov jump process model. Using the SDE model, we investigate the probability distribution and expectation of the extinction time of wild-type females by solving Kolmogorov equations associated with these statistics. The results indicate how the probability distribution and expectation of the extinction time are shaped by the initial conditions and the model parameters.     

Selective trade-offs and sex-chromosome evolution in Silene latifolia

Alleles of sexually antagonistic genes (i.e., genes with alleles affecting fitness in opposite directions in the two sexes) can avoid expression in the sex to which they are detrimental via two processes: they are subsumed into the nonrecombining, sex-determining portion of the sex chromosomes or they evolve sex-limited expression. The former is considered more likely and leads to Y-chromosome degeneration. We mapped quantitative trait loci of major effect for sexually dimorphic traits of Silene latifolia to the recombining portions of the sex chromosomes and found them to exhibit sex-specific expression, with the Y chromosome in males controlling a relatively larger proportion of genetic variance than the X in females and the average autosome. Both reproductive and ecophysiological traits map to the recombining region of the sex chromosomes. We argue that genetic correlations among traits maintain recombination and polymorphism for these genes because of balancing selection in males, whereas sex-limited expression represses detrimental alleles in females. Our data suggest that the Y chromosome of S. latifolia plays a major role in the control of key metabolic activities beyond reproductive functions.     

Sex reversal and primary sex ratios in the common frog (Rana temporaria)

Sex reversal has been suggested to have profound implications for the evolution of sex chromosomes and population dynamics in ectotherms. Occasional sex reversal of genetic males has been hypothesized to prevent the evolutionary decay of nonrecombining Y chromosomes caused by the accumulation of deleterious mutations. At the same time, sex reversals can have a negative effect on population growth rate. Here, we studied phenotypic and genotypic sex in the common frog (Rana temporaria) in a subarctic environment, where strongly female‐biased sex ratios have raised the possibility of frequent sex reversals. We developed two novel sex‐linked microsatellite markers for the species and used them with a third, existing marker and a Bayesian modelling approach to study the occurrence of sex reversal and to determine primary sex ratios in egg clutches. Our results show that a significant proportion (0.09, 95% credible interval: 0.04–0.18) of adults that were genetically female expressed the male phenotype, but there was no evidence of sex reversal of genetic males that is required for counteracting the degeneration of Y chromosome. The primary sex ratios were mostly equal, but three clutches consisted only of genetic females and three others had a significant female bias. Reproduction of the sex‐reversed genetic females appears to create all‐female clutches potentially skewing the population level adult sex‐ratio consistent with field observations. However, based on a simulation model, such a bias is expected to be small and transient and thus does not fully explain the observed female‐bias in the field.     

Sex reversal in Nile tilapia (Oreochromis niloticus) using a nonsteroidal aromatase inhibitor

Several studies have demonstrated that steroid hormones can influence sex differentiation in nonmammalian vertebrates and it has been hypothesized that male and female sex differentiation are driven by androgen and estrogen hormones, respectively. Estrogen biosynthesis is mediated by the steroidogenic enzyme cytochrome P450 aromatase, which converts androgens to estrogens. In the present study we examined the efficacy of a potent nonsteroidal aromatase inhibitor incorporated into the food, on sex reversal of Nile tilapia (Oreochromis niloticus) larvae. Nile tilapia larvae were divided in seven groups, which were fed with diets containing different amounts of the aromatase inhibitor Fadrozole (0, 50, 75 and 100 mg/kg) during 15 and 30 days, starting 9 days after hatching. Independent of the period, the proportion of males was significantly higher in the treated groups. Treatment with the highest doses (75 and 100 mg/kg) for 30 days produced 100% males. Histological examination revealed no differences in gonadal tissues between control males and treated fish. Furthermore, one intersex fish was identified in the group treated with 50 mg Fadrozole/kg for 30 days. This study reports that a 100% Nile tilapia male population can be obtained by suppressing aromatase activity and suggests that besides steroid hormones, nonsteroidal compounds, such as aromatase inhibitors, have potential for production of monosex population in tilapia. J. Exp. Zool. 290:177-181, 2001.     

Two Tests of Y Chromosomal Variation in Male Fertility of Drosophila Melanogaster

Deficiency mapping with Y autosome translocations has shown that the Y chromosome of Drosophila melanogaster carries genes that are essential to male fertility. While the qualitative behavior of these lesions provides important insight into the physiological importance of the Y chromosome, quantitative variation in effects on male fertility among extant Y chromosomes in natural populations may have a significant effect on the evolution of the Y chromosome. Here a series of 36 Y chromosome replacement lines were tested in two ways designed to detect subtle variation in effects on male fertility and total male fitness. The first test involved crossing males from the 36 lines to an excess of females in an attempt to measure differences in male mating success (virility) and male fecundity. The second test challenged males bearing each of the 36 Y chromosomes to competition in populations with males bearing a standard, phenotypically marked (BsY) chromosome. These tests indicated that the Y chromosome lines did not differ significantly in either male fertility or total fitness, but that interactions with autosomes approached significance. A deterministic population genetic model was developed allowing Y autosome interaction in fertility, and it is shown that, consistent with the experimental observations, this model cannot protect Y-linked polymorphism.     

ASSOCIATION BETWEEN SEX RATIO DISTORTION AND SEXUALLY ANTAGONISTIC FITNESS CONSEQUENCES OF FEMALE CHOICE

Genetic variation can be beneficial to one sex yet harmful when expressed in the other—a condition referred to as sexual antagonism. Because X chromosomes are transmitted from fathers to daughters, and sexually antagonistic fitness variation is predicted to often be X-linked, mates of relatively low-fitness males might produce high-fitness daughters whereas mates of high-fitness males produce low-fitness daughters. Such fitness consequences have been predicted to influence the evolution of female mating biases and the offspring sex ratio. Females might evolve to prefer mates that provide good genes for daughters or might adjust offspring sex ratios in favor of the sex with the highest relative fitness. We test these possibilities in a laboratory-adapted population of Drosophila melanogaster , and find that females preferentially mate with males carrying genes that are deleterious for daughters. Preferred males produce equal numbers of sons and daughters, whereas unpreferred males produce female-biased sex ratios. As a consequence, mean offspring fitness of unpreferred males is higher than offspring fitness of preferred males. This observation has several interesting implications for sexual selection and the maintenance of population genetic variation for fitness.     

Analysis of repetitive DNA sequences in the sex chromosomes of Oreochromis niloticus

In the Nile tilapia, Oreochromis niloticus, sex determination is primarily genetic, with XX females and XY males. While the X and Y chromosomes (the largest pair) cannot be distinguished in mitotic chromosome spreads, analysis of comparative hybridization of X and Y chromosome derived probes (produced, by microdissection and DOP-PCR, from XX and YY genotypes, respectively) to different genotypes (XX, XY and YY) has demonstrated that sequence differences exist between the sex chromosomes. Here we report the characterization of these probes, showing that a significant proportion of the amplified sequences represent various transposable elements. We further demonstrate that concentrations of a number of these individual elements are found on the sex chromosomes and that the distribution of two such elements differs between the X and Y chromosomes. These findings are discussed in relation to sex chromosome differentiation in O. niloticus and to the changes expected during the early stages of sex chromosome evolution.     

Environmental sex reversal,Trojan sex genes,and sex ratio adjustment: conditions and population consequences

The great diversity of sex determination mechanisms in animals and plants ranges from genetic sex determination (GSD, e.g. mammals, birds, and most dioecious plants) to environmental sex determination (ESD, e.g. many reptiles) and includes a mixture of both, for example when an individual’s genetically determined sex is environmentally reversed during ontogeny (ESR, environmental sex reversal, e.g. many fish and amphibia). ESD and ESR can lead to widely varying and unstable population sex ratios. Populations exposed to conditions such as endocrine‐active substances or temperature shifts may decline over time due to skewed sex ratios, a scenario that may become increasingly relevant with greater anthropogenic interference on watercourses. Continuous exposure of populations to factors causing ESR could lead to the extinction of genetic sex factors and may render a population dependent on the environmental factors that induce the sex change. However, ESR also presents opportunities for population management, especially if the Y or W chromosome is not, or not severely, degenerated. This seems to be the case in many amphibians and fish. Population growth or decline in such species can potentially be controlled through the introduction of so‐called Trojan sex genes carriers, individuals that possess sex chromosomes or genes opposite from what their phenotype predicts. Here, we review the conditions for ESR, its prevalence in natural populations, the resulting physiological and reproductive consequences, and how these may become instrumental for population management.     

Excessive variation in Y chromosomal DNA in Rumex acetosa (Polygonaceae)

Rumex acetosa is one of the few angiosperms that possesses sex chromosomes. The same types of abundant repetitive sequences cover both heterochromatic Y chromosomes present in males. The aim of this study was to investigate genetic variation in paternally inherited Y chromosomal DNA and in maternally inherited cpDNA, and to find out whether the examined genomic regions are suited to a phylogeographic study in R. acetosa. DNA sequence polymorphisms present in the 850-bp heterochromatic segment on the Y chromosomes were compared to variation in the 409-bp long chloroplast section (trnL- trnF spacer) in R. acetosa originating from several European locations and from the Altai mountains in Russia. A great amount of genetic variation was detected within the Y chromosomal region while only four chloroplast genotypes were detected. Although the chloroplast haplotypes possessed some geographic pattern, no clear phylogeographic pattern was detected based on the variable Y chromosomes. The mean Y chromosomal nucleotide diversity among all samples equaled 6.6 %, and the mean proportion of polymorphic sites per individual equaled 8.2 % among SNP sites and 1.7 % among all sites investigated. The high number of substitutions detected in the Y chromosomal DNA shows that this heterochromatic sequence has a high mutation rate. The diversity pattern indicates that gene flow via pollen is extensive and it blurs any geographical pattern in the Y chromosomal variation. The high number of repeats and uncertainty concerning the extent of recombination between the two Y chromosomes impair the usability of the Y chromosomal segment for phylogeographic or population genetic studies.     

The effect of 2n gametes on sex ratios in Actinidia

Sex can sometimes lead to complications. In some crops, 2n gametes have been exploited by plant breeders to transfer genetic variation between taxa of different ploidy levels. However, their role and use in dioecious genera have received relatively little attention. In the dioecious genus Actinidia (kiwifruit), seedling populations usually segregate equally for females and males as sex is determined by an XX female/XY male system. While fertilization involving 2n egg cells is not expected to affect the sex ratios of progenies, fertilization involving 2n pollen is likely to produce progenies with excess males. The extent of sex ratio distortion will depend on the relative contributions of first and second division restitution, and the frequency and location of cross-overs in meiosis. In this study, seedlings recovered from crosses between females of hexaploid Actinidia deliciosa and males of two diploid species, Actinidia chinensis and Actinidia eriantha, included a proportion of pentaploid hybrids presumably derived from fertilization involving 2n pollen. Most of these pentaploids were male, and a proportion of them were likely to be carrying two Y chromosomes. If used as parents in further crosses, males with multiple Y chromosomes are likely to cause distorted sex ratios in their immediate progenies. In dioecious genera such as Actinidia, the effects on sex ratios of different mechanisms of ploidy change need to be taken into account when considering the evolution of polyploidy and the design of breeding strategies involving ploidy manipulation.     

High level of male-biased Scandinavian admixture in Greenlandic Inuit shown by Y-chromosomal analysis

We have used binary markers and microsatellites on the Y chromosome to analyse diversity in a sample of Greenlandic Inuit males. This sample contains Y chromosomes typical of those found in European populations. Because the Y chromosome has a unique and robust phylogeny of a time depth that precedes the split between European and Native American populations, it is possible to assign chromosomes in an admixed population to either continental source. On this basis, 58+/-6% of these Y chromosomes have been assigned to a European origin. The high proportion of European Y chromosomes contrasts with a complete absence of European mitochondrial DNA and indicates strongly male-biased European admixture into Inuit. Comparison of the European component of Inuit Y chromosomes with European population data suggests that they have their origins in Scandinavia. There are two potential source populations: Norse settlers from Iceland, who may have been assimilated 500 years ago, and the Danish-Norwegian colonists of the eighteenth century. Insufficient differentiation between modern Icelandic and Danish Y chromosomes means that a choice between these cannot be made on the basis of diversity analysis. However, the extreme sex bias in the admixture makes the later event more likely as the source.     

Causes and consequences of reciprocal translocations on sex chromosomes

Under XY sex determination, the Y chromosome is only inherited via males, whereas the X chromosome is predominantly found in females. Thus, it is favourable when alleles with high male fitness become associated with the Y chromosome and when alleles with high female fitness become associated with the X chromosome. These favourable associations can be strengthened through linkage. Rearrangements, such as inversions and sex chromosome–autosome fusions, can increase linkage and thereby become favoured (Charlesworth, 2017). In a From the Cover article in this issue of Molecular Ecology, Toups, Rodrigues, Perrin, and Kirkpatrick (2019) present the first genomic analysis of a sex chromosome reciprocal translocation, a particularly dramatic chromosomal rearrangement that modifies linkage with the sex chromosome. As a result of reciprocal translocation, one studied population of the common frog (Rana temporaria, Figure 1) displays a remarkable sex‐determining system in which there are two physically unlinked sex chromosomes that are exclusively cotransmitted (Figure 2a).     

Polymorphism and differentiation of rainbow trout Y chromosomes.

Most fish species show little morphological differentiation in the sex chromosomes. We have coupled molecular and cytogenetic analyses to characterize the male-determining region of the rainbow trout (Oncorhynchus mykiss) Y chromosome. Four genetically diverse male clonal lines of this species were used for genetic and physical mapping of regions in the vicinity of the sex locus. Five markers were genetically mapped to the Y chromosome in these male lines, indicating that the sex locus was located on the same linkage group in each of the lines. We also confirmed the presence of a Y chromosome morphological polymorphism among these lines, with the Y chromosomes from two of the lines having the more common heteromorphic Y chromosome and two of the lines having Y chromosomes morphologically similar to the X chromosome. The fluorescence in situ hybridization (FISH) pattern of two probes linked to sex suggested that the sex locus is physically located on the long arm of the Y chromosome. Fishes appear to be an excellent group of organisms for studying sex chromosome evolution and differentiation in vertebrates because they show considerable variability in the mechanisms and (or) patterns involved in sex determination.     

Sex chromosomes in the spiny eel (Mastacembelus aculeatus) revealed by mitotic and meiotic analysis

Lower vertebrates like fish exhibit tremendous diversity in sex determination. There are wide interplays between environment-dependent sex differentiation ranging from natural hermaphroditism to sex reversal and genetic sex determination. Diverse systems of male and female heterogamety coexist in fish and sex chromosomes are rarely distinguishable in morphology. Here we show that the spiny eel ((Mastacembelus aculeatus) of the Perciformes, has evolved highly heteromorphic X and Y chromosomes. The metacentric X and Y chromosomes are the largest among 24 homologous pairs, differ from each other in size and morphology, and become distinct after C-banding because of conspicuous heterochromatin blocks which exhibit alternate distribution around the centromeric region. Chromosome painting using probes from the microdissected X chromosome revealed sequence homology between X and Y. During the pachytene stage of meiosis the X and Y form a bivalent. However, their synapsis is delayed which is particularly evident in one terminus. Therefore, the X and Y have resulted from a pericentric inversion in the Y. We conclude that M. aculeatus represents an example of a highly advanced stage of sex chromosome evolution in fish.     

Diploid male production correlates with genetic diversity in the parasitoid wasp Venturia canescens: a genetic approach with new microsatellite markers

Sex determination is ruled by haplodiploidy in Hymenoptera, with haploid males arising from unfertilized eggs and diploid females from fertilized eggs. However, diploid males with null fitness are produced under complementary sex determination (CSD), when individuals are homozygous for this locus. Diploid males are expected to be more frequent in genetically eroded populations (such as islands and captive populations), as genetic diversity at the csd locus should be low. However, only a few studies have focused on the relation between population size, genetic diversity, and the proportion of diploid males in the field. Here, we developed new microsatellite markers in order to assess and compare genetic diversity and diploid male proportion (DMP) in populations from three distinct habitat types – mainland, island, or captive –, in the parasitoid wasp Venturia canescens. Eroded genetic diversity and higher DMP were found in island and captive populations, and habitat type had large effect on genetic diversity. Therefore, DMP reflects the decreasing genetic diversity in small and isolated populations. Thus, Hymenopteran populations can be at high extinction risk due to habitat destruction or fragmentation.     

Sex‐antagonistic genes,XY recombination and feminized Y chromosomes

The canonical model of sex‐chromosome evolution predicts that sex‐antagonistic (SA) genes play an instrumental role in the arrest of XY recombination and ensuing Y chromosome degeneration. Although this model might account for the highly differentiated sex chromosomes of birds and mammals, it does not fit the situation of many lineages of fish, amphibians or nonavian reptiles, where sex chromosomes are maintained homomorphic through occasional XY recombination and/or high turnover rates. Such situations call for alternative explanatory frameworks. A crucial issue at stake is the effect of XY recombination on the dynamics of SA genes and deleterious mutations. Using individual‐based simulations, we show that a complete arrest of XY recombination actually benefits females, not males. Male fitness is maximized at different XY recombination rates depending on SA selection, but never at zero XY recombination. This should consistently favour some level of XY recombination, which in turn generates a recombination load at sex‐linked SA genes. Hill–Robertson interferences with deleterious mutations also impede the differentiation of sex‐linked SA genes, to the point that males may actually fix feminized phenotypes when SA selection and XY recombination are low. We argue that sex chromosomes might not be a good localization for SA genes, and sex conflicts seem better solved through the differential expression of autosomal genes.