Sex chromosome-autosome translocations in the leaf-nosed bats, family Phyllostomidae. II. Meiotic analyses of the subfamilies Stenodermatinae and Phyllostominae

Analyses of meiotic pairing and synaptonemal complexes of the composite sex chromosomes of male phyllostomid bats with X-autosome or X- and Y-autosome translocations were performed using Giemsa and silver staining procedures. Typical mammalian sex vesicles were absent in all species analyzed. Stenodermatine species with X-autosome translocations possessed an open ring and tail configuration of the XY1Y2 trivalent. Species with both X- and Y-autosome translocations possessed a closed ring and tail configuration of the neo-XY bivalent. In both cases, the tail represented the autosomal short arm of the X paired with its homologue, either the Y2 in XY1Y2 species or the autosomal arm of the composite Y in neo-XY species. Autosomal pairing of the composite sex bivalent in neo-XY species replaced an association between the original X and Y in late prophase I. The absence of a sex vesicle, the unusual pairing configurations of the composite sex chromosomes, and the presumed absence of meiotic nondisjunction in these species is discussed in light of current hypotheses of sex chromosome behavior in male gametogenesis in mammals.     

Y Fuse? Sex Chromosome Fusions in Fishes and Reptiles

Chromosomal fusion plays a recurring role in the evolution of adaptations and reproductive isolation among species, yet little is known of the evolutionary drivers of chromosomal fusions. Because sex chromosomes (X and Y in male heterogametic systems, Z and W in female heterogametic systems) differ in their selective, mutational, and demographic environments, those differences provide a unique opportunity to dissect the evolutionary forces that drive chromosomal fusions. We estimate the rate at which fusions between sex chromosomes and autosomes become established across the phylogenies of both fishes and squamate reptiles. Both the incidence among extant species and the establishment rate of Y-autosome fusions is much higher than for X-autosome, Z-autosome, or W-autosome fusions. Using population genetic models, we show that this pattern cannot be reconciled with many standard explanations for the spread of fusions. In particular, direct selection acting on fusions or sexually antagonistic selection cannot, on their own, account for the predominance of Y-autosome fusions. The most plausible explanation for the observed data seems to be (a) that fusions are slightly deleterious, and (b) that the mutation rate is male-biased or the reproductive sex ratio is female-biased. We identify other combinations of evolutionary forces that might in principle account for the data although they appear less likely. Our results shed light on the processes that drive structural changes throughout the genome.     

Synaptonemal complexes in Gerbillidae: probable role of intercalated heterochromatin in gonosome-autosome translocations

A study of sex chromosomes and synaptonemal complexes in male specimens of Gerbillus chiesmani, G. nigeriae, G. hoogstrali, and Taterillus pygargus is reported. In each of these Gerbillidae species there are two or three translocations of autosomes with X and Y chromosomes. Analysis of mitotic chromosomes consistently shows the presence of constitutive heterochromatin on the der t(X;autosome) at the X-autosome junction and on the der t(Y;autosome). Analysis of the synaptonemal complexes shows the existence of an unusual structure, lightly stained, at the X-autosome junction and at the Y-autosome junction, which is probably heterochromatic in nature, thus corresponding to the mitotic patterns. This heterochromatin separates the autosomal and gonosomal segments, which behave independently and normally. By analogy with findings from humans and other mammals, a general hypothesis is proposed on the role of intercalated heterochromatin between translocated gonosomes and autosomes. This hypothesis explains why the pathological consequences of these translocations may be very different in males and females. The role of intercalated heterochromatin would be to avoid the pathological consequences of gonosome-autosome translocations resulting from inactivation of the sex chromosomes in female somatic cells and male germinal cells.     

Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study

X-autosome translocations are highly deleterious chromosomal rearrangements due to meiotic disruption, the effects of X-inactivation on the autosome, and the necessity of maintaining different replication timing patterns between the two segments. In spite of this, X-autosome translocations are not uncommon. We here focus on the genus Taterillus (Rodentia, Gerbillinae) which provides two sister lineages differing by two autosome–gonosome translocations. Despite the recent and dramatic chromosomal repatterning characterising these lineages, the X-autosome translocated species all display intercalary heterochromatic blocks (IHBs) between the autosomal and the ancestral sexual segments. These blocks, composed of highly amplified telomeric repeats and rDNA clusters, are not observed on the chromosomes of the non-translocated species, nor the Y1 and Y2 of the translocated species. Such IHBs are found in all mammals documented for X-autosome translocation. We propose an epigenomic hypothesis which explains the viability of X-autosome translocations in mammals. This posits that constitutive heterochromatin is probably selected for in X-autosome translocations since it may (1) prevent facultative heterochromatinization of the inactivated X from spreading to the autosomal part, and (2) allow for the independent regulation of replication timing of the sex and autosomal segments.     

Recombination between homologous autosomes in medfly (Ceratitis capitata) males: type-1 recombination and the implications for the stability of genetic sexing strains

The sterile insect technique (SIT) is an environmentally safe technology to control insect pests. To improve this technology, genetic sexing strains (GSS) have been developed for the Mediterranean fruit fly, Ceratitis capitata. Such strains are based on Y-autosome translocations linking a selectable marker to the male sex and their long-term stability, especially under large-scale mass rearing conditions, is threatened by genetic recombination in the heterozygous males. We have measured male recombination in order to be able to construct GSS that are more stable. Our results show that male recombination occurs at very low frequencies, that is, below 1% per generation. Furthermore, recombination in medfly males occurs premeiotically. By selecting strains where the Y-autosome translocation breakpoint and the selectable marker are closely linked, the deleterious effects of recombination on the stability of GSS can be minimized. In such strains recombination is reduced by ca. 80% as compared to previously studied GSS. Although recombinants still occur at very low frequencies they still pose a threat to the integrity of the sexing system if they possess a selective advantage. Under mass rearing condition such recombinants will accumulate according to their relative fitness and additional measures, such as improved mass rearing strategies, are required to preserve the accuracy of the sexing system. As a conclusion it is shown that current GSS are stable enough to allow mass rearing at levels exceeding 1000 million male medflies per week.     

Speciation by Reinforcement: A Model Derived from Studies of Drosophila

Reinforcement is an increase in premating reproductive isolation between taxa resulting from selection against hybrids. We present a model of reinforcement with a novel type of selection on female mating behavior. Previous models of reinforcement have focused on the divergence of female mating preferences between nascent species. We suggest that an increase in the level of female mating discrimination can yield reinforcement without further divergence of either male characters or female preferences. This model indicates that selection on mating discrimination is a viable mechanism for reinforcement and may allow speciation under less stringent conditions than selection on female preference. This model also incorporates empirical results from genetic studies of hybrid fitness determination in Drosophila species. We find that the details of inheritance, which include sex-linked transmission, sex-limited fertility reduction, and X-autosome epistasis, have important effects on the likelihood of reinforcement. In particular, X-autosome epistasis for hybrid fitness determination facilitates reinforcement when hybrid fertility reduction occurs in males, but hinders the process when it occurs in females. HALDANE's rule indicates that hybrid sterility will generally evolve in males prior to females within nascent species. Thus, HALDANE's rule and X-autosome epistasis provide conditions that are surprisingly favorable for reinforcement in Drosophila.     

Mate-search efficiency can determine the evolution of separate sexes and the stability of hermaphroditism in animals

Limited availability of mating partners has been proposed as an explanation for the occurrence of simultaneous hermaphroditism in animals with pair mating. When low population density or low mobility of a species limits the number of potential mates, simultaneous hermaphrodites may have a selective advantage because, first, they are able to adjust the allocation of resources between male and female functions in order to maximize fitness; second, in a hermaphroditic population the likelihood of meeting a partner is higher because all individuals are potential mates; and, third, in the absence of mating partners, many simultaneously hermaphroditic animals have the option of reproducing through self-fertilization. Recognizing that mate availability is central to the existing theory of hermaphroditism in animals, it is important to examine the effects of mate search on predictions of the stability of hermaphroditism. Many hermaphroditic animals can increase the number of potential mates they contact by active searching. However, since mate search has costs in terms of time and energy, the increased number of potential mates will be traded off against the amount of resources that can be allocated to the production of gametes. We explore the consequences of this trade-off to the evolution of mating strategies and to the selective advantage of self-fertilization. We show that in low and moderate population densities, poor mate-search efficiency and high costs of searching stabilize hermaphroditism and bias sex allocation toward female function. In addition, in very low population densities, there is strong selective advantage for self-fertilization, but this advantage decreases considerably in species with high mate-search efficiency. Most important, however, we present a novel evolutionary prediction: when mate search is efficient, disruptive frequency-dependent selection on time allocation to mate search leads to the evolution of searching and nonsearching phenotypes and, ultimately, to the evolution of males and females.     

Evolutionarily stable mixed mating in a variety of genetic systems

Many species display a mixture of close inbreeding and outbreeding which is referred to as mixed mating. For selfing species, models predict that such mixed mating systems can be stable. Conversely, models considering separate sex species have not been able to explain mixed mating systems. This failure may be a result of the unrealistic assumption that recurrent inbreeding does not increase the inbreeding coefficient. Here we show that mixed mating is expected in separate sex systems when recurrent inbreeding is taken into account. A female that allows her brother to sibmate with her gives an extra mating opportunity to said brother. This kin selective advantage should be strongest in genetic systems where the male is more related to the female. In support of this idea, we find that inbreeding evolves most easily in selfers, followed by diploid sibmating, followed by haplodiploid sibmating. Consideration of published values for the regression of fitness on inbreeding coefficient suggests that many species fall in a range where some selfing/sibmating is optimal.     

Discrete Clutch Sizes, Local Mate Competition, and the Evolution of Precise Sex Allocation

Optimal sex allocation under a population structure with local mate competition has been studied mainly in deterministic models that are based on the assumption of continuous clutch sizes; Hamilton's (1967) model is the classic example. When clutch sizes are small, however, this assumption is not appropriate. When taking the discrete nature of eggs into account it becomes critically important whether females control only the mean sex ratio (“binomial” females) or the variance as well (“precise” females). As both types of sex ratio control have been found, it is of interest to investigate their evolutionary stability. In particular, it may be questioned whether perfect control of the sex ratio is always favoured by natural selection when mating groups are small. Models based on discrete clutch sizes are developed to determine evolutionarily stable (ES) sex ratios. It is predicted that when all females are of the binomial type they should produce a lower proportion of daughters than predicted by Hamilton's model, especially when clutch size and foundress number are small. When all females are of the precise type, the ES number of sons should generally be either a stable mixed strategy or a pure strategy, but there are special cases (for two foundresses and particular clutch sizes) where the ES number of sons lies in a trajectory of neutrally stable mixed strategies; the predicted mean sex ratios can be either higher or lower than predicted by Hamilton's model. The existence of ES mixed strategies implies that individual females do not necessarily have to produce sex ratios with perfect precision; some level of imperfection can be tolerated (i.e., will not be selected against). When the population consists of both binomial and precise females, the latter always have a selective advantage. This advantage of precision does not disappear when precision approaches fixation in the population. The latter result contradicts the conclusions of Taylor and Sauer (1980) which is due to their way of expressing selective advantage; they define selective advantage as the between-generation increase per allele, which will always become vanishingly small when an allele reaches fixation, irrespective of fitness differences.     

EVOLUTION OF CONDITION-DEPENDENT SEX ORNAMENTS AND MATING PREFERENCES: SEXUAL SELECTION BASED ON VIABILITY DIFFERENCES

The possibility that the evolution of mating preferences and secondary sex traits can be based on heritable differences in viability is examined with a three-locus model. Earlier genetic models suggested that viability-based processes alone cannot explain the evolution of mate choice and sex ornaments that reduce survival; a Fisherian mating advantage seemed necessary. The present model is based on a monogamous mating system that precludes such a mating advantage. A key assumption is that ornament development depends on the phenotypic condition and overall genotype of the possessor; there is evidence that secondary sex traits often mirror nutritional status and health, sometimes through hormonal mediation. Ornament and preference can then hitchhike slowly to high frequency with alleles that confer a slight survival advantage, provided that such alleles become available often enough. The evolution of mating preferences and secondary sex traits that reflect overall genotypic constitution therefore can be based solely on viability differences, no Fisherian mating advantage being required. In practice, these and several other mechanisms of sexual selection may occur together.     

A two-sex polygenic model for the evolution of premating isolation. I. Deterministic theory for natural populations

It is proposed that mating behavior is normally determined by independent genetic systems in the male and female. A specific model is put forward in which mating behavior is determined by additive gene contributions in both sexes, and the strength of mating attraction is maximized when mating "scores" in the two sexes are equalized. This type of model, which may be described as a "facilitation" model, is related to models proposed by a number of authors. It is pointed out that a second class of models exists, "avoidance" models, and that these, although less tractable analytically, could be more realistic.-An organism is assumed to be divided into two strains, and selection is introduced through lethality or sterility of the hybrid (postmating isolation). The selective tendency for divergence of mating behavior in one sex is then shown to be proportional to the amount of divergence that already exists in the opposite sex, multiplied by a quantity that can be described as the heritability of mating attraction. The situation in which no initial divergence exists in either sex constitutes an equilibrium that is unstable, but one that requires substantial deviations before any selective progress can be made. Thus, the evolution of premating isolation to reinforce postmating isolation may be an inefficient process. The process would occur much more efficiently if some initial chance divergence in mating behavior occurred during the period in which postmating isolation evolved.     

A comparison of sexual and asexual replication strategies in a simplified model based on the yeast life cycle

This paper develops simplified mathematical models describing the mutation-selection balance for the asexual and sexual replication pathways in Saccharomyces cerevisiae, or Baker’s yeast. The simplified models are based on the single-fitness-peak approximation in quasispecies theory. We assume diploid genomes consisting of two chromosomes, and we assume that each chromosome is functional if and only if its base sequence is identical to some master sequence. The growth and replication of the yeast cells is modeled as a first-order process, with first-order growth rate constants that are determined by whether a given genome consists of zero, one, or two functional chromosomes. In the asexual pathway, we assume that a given diploid cell divides into two diploids. For the sake of generality, our model allows for mitotic recombination and asymmetric chromosome segregation. In the sexual pathway, we assume that a given diploid cell divides into two diploids, each of which then divide into two haploids. The resulting four haploids enter a haploid pool, where they grow and replicate until they meet another haploid with which to fuse. In the sexual pathway, we consider two mating strategies: (1) a selective strategy, where only haploids with functional chromosomes can fuse with one another; (2) a random strategy, where haploids randomly fuse with one another. When the cost for sex is low, we find that the selective mating strategy leads to the highest mean fitness of the population, when compared to all of the other strategies. When the cost for sex is low, sexual replication with random mating also has a higher mean fitness than asexual replication without mitotic recombination or asymmetric chromosome segregation. We also show that, at low replication fidelities, sexual replication with random mating has a higher mean fitness than asexual replication, as long as the cost for sex is low. If the fitness penalty for having a defective chromosome is sufficiently high and the cost for sex sufficiently low, then at low replication fidelities the random mating strategy has a mean fitness that is a factor of larger than the asexual mean fitness. We argue that for yeast, the selective mating strategy is the one that is closer to reality, which if true suggests that sex may provide a selective advantage under considerably more relaxed conditions than previous research has indicated. The results of this paper also suggest that S. cerevisiae switches from asexual to sexual replication when stressed, because stressful growth conditions provide an opportunity for the yeast to clear out deleterious mutations from their genomes. That being said, our model does not contradict theories for the evolution of sex that argue that sex evolved because it allows a population to more easily adapt to changing conditions.     

Differential sex chromosome replication and dosage compensation in polytene trichogen cells of Lucilia cuprina (Diptera: Calliphoridae)

Non banded sex chromosome elements have been identified in polytene trichogen cells of Lucilia cuprina using Y-autosome translocations, C-banding and Quinacrine fluorescence. The X chromosome is an irregular granular structure while the much smaller Y chromosome has both a dense darkly stained and a loosely organised segment. The X and Y chromosomes are underreplicated in polytene cells but comparison of C- and Q-banding characteristics of sex chromosomes in diploid and polytene tissues indicates that selective replication of non C-banding material occurs in both the sex chromosomes. Brightly fluorescing material in the Y chromosome is replicated to such an extent that it consists of half the polytene element, while the C-banding material, which makes up most of the diploid X chromosome, is virtually unreplicated. Differential replication also occurs in autosomes. In XXY males, and in males carrying a duplication of the X euchromatic region, a short uniquely banded polytene chromosome is formed. It is suggested that in males carrying two doses of X euchromatin a dosage compensation mechanism operates in which genes in one copy are silenced by forming a banded polytene chromosome.     

The evolution of leks through female choice

It is generally acknowledged that female preferences for mating in large groups of displaying males could cause the evolution of leks. Recent hypotheses differ on what selective advantage would accrue to females with such preferences, but they agree on the need for some such advantage if these preferences are to select for larger lek sizes. A model developed here, adapted from models of female preferences for individual male traits, shows that female preferences for larger leks can evolve and be maintained without any direct selective advantage. Like the individual choice models, it also demonstrates a number of arbitrary or non-adaptive features inherent in such systems. Most notably, instead of a single optimal outcome, there may exist a curve of possible equilibria. These equilibria can be stable or unstable depending on the nature of the female preferences.     

Evolution of sexual asymmetry

Background

The clear dominance of two-gender sex in recent species is a notorious puzzle of evolutionary theory. It has at least two layers: besides the most fundamental and challenging question why sex exists at all, the other part of the problem is equally perplexing but much less studied. Why do most sexual organisms use a binary mating system? Even if sex confers an evolutionary advantage (through whatever genetic mechanism), why does it manifest that advantage in two, and exactly two, genders (or mating types)? Why not just one, and why not more than two?

Results

Assuming that sex carries an inherent fitness advantage over pure clonal multiplication, we attempt to give a feasible solution to the problem of the evolution of dimorphic sexual asymmetry as opposed to monomorphic symmetry by using a spatial (cellular automaton) model and its non-spatial (mean-field) approximation. Based on a comparison of the spatial model to the mean-field approximation we suggest that spatial population structure must have played a significant role in the evolution of mating types, due to the largely clonal (self-aggregated) spatial distribution of gamete types, which is plausible in aquatic habitats for physical reasons, and appears to facilitate the evolution of a binary mating system.

Conclusions

Under broad ecological and genetic conditions the cellular automaton predicts selective removal from the population of supposedly primitive gametes that are able to mate with their own type, whereas the non-spatial model admits coexistence of the primitive type and the mating types. Thus we offer a basically ecological solution to a theoretical problem that earlier models based on random gamete encounters had failed to resolve.

     

Sexually antagonistic coevolution in a mating system: combining experimental and comparative approaches to address evolutionary processes

We combined experimental and comparative techniques to study the evolution of mating behaviors within in a clade of 15 water striders (Gerris spp.). Superfluous multiple mating is costly to females in this group, and consequently there is overt conflict between the sexes over mating. Two alternative hypotheses that could generate interspecific variation in mating behaviors are tested: interspecific variation in optimal female mating rate versus sexually antagonistic coevolution of persistence and resistance traits. These potentially coevolving traits include male grasping and female antigrasping structures that further the interests of one sex over the other during premating struggles. Both processes are known to play a role in observed behavioral variation within species. We used two large sets of experiments to quantify behavioral differences among species, as well as their response to an environmentally (sex-ratio) induced change in optimal female mating rate. Our analysis revealed a large degree of continuous interspecific variation in all 20 quantified behavioral variables. Nevertheless, species shared the same set of behaviors, and each responded in a qualitatively similar fashion to sex-ratio alterations. A remarkably large proportion (> 50%) of all interspecific variation in the magnitude of behaviors, including their response to sex ratio, could be captured by a single multivariate axis. These data suggest tight coevolution of behaviors within a shared mating system. The pattern of correlated evolution was best accounted for by antagonistic coevolution in the relative abilities of each sex to control the outcome of premating struggles. In species where males have a relative advantage, mating activity is high, and the opposite is found in species where females have gained a relative advantage. Our analyses also suggested that evolution has been unconstrained by history, with no consistent evolutionary tendency toward or away from male or female relative advantage.     

Chromosome banding in Amphibia. XXVI. Coexistence of homomorphic XY sex chromosomes and a derived Y-autosome translocation in Eleutherodactylus maussi (Anura,Leptodactylidae)

A 15-year cytogenetic survey on one population of the leaf litter frog Eleutherodactylus maussi in northern Venezuela confirmed the existence of multiple XXAA male symbol /XAA(Y) female symbol sex chromosomes which originated by a centric (Robertsonian) fusion between the original Y chromosome and an autosome. 95% of the male individuals in this population are carriers of this Y-autosome fusion. In male meiosis the XAA(Y) sex chromosomes pair in the expected trivalent configuration. In the same population, 5% of the male animals still possess the original, free XY sex chromosomes. In a second population of E. maussi analyzed, all male specimens are characterized by these ancestral XY chromosomes which form normal bivalents in meiosis. E. maussi apparently represents the first vertebrate species discovered in which a derived Y-autosome fusion still coexists with the ancestral free XY sex chromosomes. The free XY sex chromosomes, as well as the multiple XA(Y) sex chromosomes are still in a very primitive (homomorphic) stage of differentiation. With no banding technique applied it is possible to distinguish the Y from the X. DNA flow cytometric measurements show that the genome of E. maussi is among the largest in the anuran family Leptodactylidae. The present study also supplies further data on differential chromosome banding and fluorescence in situ hybridization experiments in this amphibian species.     

Classic predictions about sex change do not hold under all types of size advantage

Theory predicts that the ‘size advantage’ (rate of increase in male and female fitness with age or size) determines the direction and the timing of sex change in sequential hermaphrodites. Whereas the size advantage is generated by the mating system and would be expected to vary within and between species, the shape or form of the size advantage has rarely been estimated directly. Here, we ask whether theoretical predictions about the timing of sex change hold under different types of size advantage. We model two biological scenarios representing different processes generating the size advantage and find that different types of size advantage can produce patterns that qualitatively differ from classic predictions. Our results demonstrate that a good understanding of sequentially hermaphroditic mating systems, and specifically, a direct assessment of the processes underlying the size advantage is crucial to reliably predict and explain within‐species patterns of the timing of sex change.     

Evolution of polyandry by reduction in progeny number variance in structured populations

When there is a variation in the quality of males in a population, multiple mating can lead to an increase in the genetic fitness of a female by reducing the variance of the progeny number. The extent of selective advantage obtainable by this process is investigated for a population subdivided into structured demes. It is seen that for a wide range of model parameters (deme size, distribution of male quality, local resource level), multiple mating leads to a considerable increase in the fitness. Frequency-dependent selection or a stable coexistence between polyandry and monandry can also result when the possible costs involved in multiple mating are taken into account.