A pluralist approach to sex and recombination

One of the greatest challenges for evolutionary biology is explaining the widespread occurrence of sexual reproduction and the associated process of genetic recombination. A large number of theories have been developed that provide a sufficient short-term advantage for sex to offset its two-fold cost. These theories can be broadly classified into environmental (or ecological) and mutation-based models. Traditionally, the different theories have been viewed as competing, and empirical work has attempted to distinguish between them. Here we highlight the advantages that may be gained from considering that multiple mechanisms (environmental and mutational) may be at work, and that interactions between the theories may be very important.     

Recombination and the evolution of mutational robustness

Mutational robustness is the degree to which a phenotype, such as fitness, is resistant to mutational perturbations. Since most of these perturbations will tend to reduce fitness, robustness provides an immediate benefit for the mutated individual. However, robust systems decay due to the accumulation of deleterious mutations that would otherwise have been cleared by selection. This decay has received very little theoretical attention. At equilibrium, a population or asexual lineage is expected to have a mutation load that is invariant with respect to the selection coefficient of deleterious alleles, so the benefit of robustness (at the level of the population or asexual lineage) is temporary. However, previous work has shown that robustness can be favoured when robustness loci segregate independently of the mutating loci they act upon. We examine a simple two-locus model that allows for intermediate rates of recombination and inbreeding to show that increasing the effective recombination rate allows for the evolution of greater mutational robustness.     

The effect of mutational robustness on the evolvability of multicellular organisms and eukaryotic cells

Canalization involves mutational robustness, the lack of phenotypic change as a result of genetic mutations. Given the large divergence in phenotype across species, understanding the relationship between high robustness and evolvability has been of interest to both theorists and experimentalists. Although canalization was originally proposed in the context of multicellular organisms, the effect of multicellularity and other classes of hierarchical organization on evolvability has not been considered by theoreticians. We address this issue using a Boolean population model with explicit representation of an environment in which individuals with explicit genotype and a hierarchical phenotype representing multicellularity evolve. Robustness is described by a single real number between zero and one which emerges from the genotype–phenotype map. We find that high robustness is favoured in constant environments, and lower robustness is favoured after environmental change. Multicellularity and hierarchical organization severely constrain robustness: peak evolvability occurs at an absolute level of robustness of about 0.99 compared with values of about 0.5 in a classical neutral network model. These constraints result in a sharp peak of evolvability in which the maximum is set by the fact that the fixation of adaptive mutations becomes more improbable as robustness decreases. When robustness is put under genetic control, robustness levels leading to maximum evolvability are selected for, but maximal relative fitness appears to require recombination.     

A heuristic model on the role of plasticity in adaptive evolution: plasticity increases adaptation,population viability and genetic variation

An ongoing new synthesis in evolutionary theory is expanding our view of the sources of heritable variation beyond point mutations of fixed phenotypic effects to include environmentally sensitive changes in gene regulation. This expansion of the paradigm is necessary given ample evidence for a heritable ability to alter gene expression in response to environmental cues. In consequence, single genotypes are often capable of adaptively expressing different phenotypes in different environments, i.e. are adaptively plastic. We present an individual-based heuristic model to compare the adaptive dynamics of populations composed of plastic or non-plastic genotypes under a wide range of scenarios where we modify environmental variation, mutation rate and costs of plasticity. The model shows that adaptive plasticity contributes to the maintenance of genetic variation within populations, reduces bottlenecks when facing rapid environmental changes and confers an overall faster rate of adaptation. In fluctuating environments, plasticity is favoured by selection and maintained in the population. However, if the environment stabilizes and costs of plasticity are high, plasticity is reduced by selection, leading to genetic assimilation, which could result in species diversification. More broadly, our model shows that adaptive plasticity is a common consequence of selection under environmental heterogeneity, and hence a potentially common phenomenon in nature. Thus, taking adaptive plasticity into account substantially extends our view of adaptive evolution.     

Studies on chiasma distribution and chiasma movement in Zoniopoda tarsata (Orthoptera: Romaleidae)

A sample of 27 males of Zoniopoda tarsata from Argentina was studied cytologically. The three largest autosomal pairs and the X were characterized by the presence of interstitial C-bands. Chiasma position relative to the bands was analyzed at diplotene and diakinesis. The frequency of interstitial, terminal and total chiasmata per cell was studied for the whole autosomal bivalent set, analysing the variations between stages and among individuals. The comparison of interstitial chiasma frequencies between stages and among individuals and the study of chiasma position relative to the bands in pairs 1, 2 and 3 indicated that chiasma distribution varied from diplotene to diakinesis. Therefore, terminalization does exist in this species and the movement may occur towards the centromere. The frequency of terminal associations at diplotene showed a high negative correlation (r=-0.89; p<10^-5) with the number of interstitial chiasmata. This correlation would not be expected if the two kinds of association were produced by different (independent) mechanisms. Consequently, terminal associations were considered genuine chiasmata. The correlation between interstitial and total chiasmata was very much lower then the former (r=0.39; p=0.04). This fact, besides the relatively low variation for chiasma number, observed among individuals suggests that in this species the number of interestitial chiasmata, which are the most important in controlling the genetical recombination, is mainly regulated by changes in chiasma distribution, while variations in total chiasma frequency are of much lower magnitude.Member of Carrera del Investigador del Consejo Nacional de Investigaciones Cientificas y Técnicas (CONICET)     

The opportunity for canalization and the evolution of genetic networks

There has been a recent revival of interest in how genetic interactions evolve, spurred on by an increase in our knowledge of genetic interactions at the molecular level. Empirical work on genetic networks has revealed a surprising amount of robustness to perturbations, suggesting that robustness is an evolved feature of genetic networks. Here, we derive a general model for the evolution of canalization that can incorporate any form of perturbation. We establish an upper bound to the strength of selection on canalization that is approximately equal to the fitness load in the system. This method makes it possible to compare different forms of perturbation, including genetic, developmental, and environmental effects. In general, load that arises from mutational processes is low because the mutation rate is itself low. Mutation load can create selection for canalization in a small network that can be achieved through dominance evolution or gene duplication, and in each case selection for canalization is weak at best. In larger genetic networks, selection on genetic canalization can be reasonably strong because larger networks have higher mutational load. Because load induced through migration, segregation, developmental noise, and environmental variance is not mutation limited, each can cause strong selection for canalization.     

Recombination Modification in a Fluctuating Environment

This paper examines the theory of the evolution of increased recombination between two loci subjected to interactive selection in a temporally fluctuating environment. Both cyclical and stochastic environments are considered. It is shown that temporal variation in the linkage disequilibrium coefficient for the pair of selected loci, due to fluctuations in the selective values of the genotypes at these loci, can give rise to selection in favor of modifier genes increasing recombination. The equilibrium level of recombination established in a given population depends on several factors; it is highest for intermediate values of the environmental periodicity or autocorrelation, for cases when the modifier genes are themselves linked to the selected loci, and for high levels of environmental variation. In general, it seems that the rate of modification of recombination values by this process will be low except when the modifiers are tightly linked to the selected loci. The possible evolutionary significance of this process is discussed in relation to observations on genetic systems of plants and animals.     

Symbiosis versus competition in plant virus evolution

Darwin's theory of evolution by natural selection has been supported by molecular evidence and by experimental evolution of viruses. However, it might not account for the evolution of all life, and an alternative model of evolution through symbiotic relationships also has gained support. In this review, the evolution of plant viruses has been reinterpreted in light of these two seemingly opposing theories by using evidence from the earliest days of plant virology to the present. Both models of evolution probably apply in different circumstances, but evolution by symbiotic association (symbiogenesis) is the most likely model for many evolutionary events that have resulted in rapid changes or the formation of new species. In viruses, symbiogenesis results in genomic reassortment or recombination events among disparate species. These are most noticeable by phylogenetic comparisons of extant viruses from different taxonomic groups.     

Reducing mutation load through sexual selection on males

Mutation load is a key parameter in evolutionary theories, but relatively little empirical information exists on the mutation load of populations, or the elimination of this load through selection. We manipulated the opportunity for sexual selection within a mutation accumulation divergence experiment to determine how sexual selection on males affected the accumulation of mutations contributing to sexual and nonsexual fitness. Sexual selection prevented the accumulation of mutations affecting male mating success, the target trait, as well as reducing mutation load on productivity, a nonsexual fitness component. Mutational correlations between mating success and productivity (estimated in the absence of sexual selection) were positive. Sexual selection significantly reduced these fitness component correlations. Male mating success significantly diverged between sexual selection treatments, consistent with the fixation of genetic differences. However, the rank of the treatments was not consistent across assays, indicating that the mutational effects on mating success were conditional on biotic and abiotic context. Our experiment suggests that greater insight into the genetic targets of natural and sexual selection can be gained by focusing on mutational rather than standing genetic variation, and on the behavior of trait variances rather than means.     

A meta-analysis of the heritability of developmental stability

The existence of additive genetic variance in developmental stability has important implications for our understanding of morphological variation. The heritability of individual fluctuating asymmetry and other measures of developmental stability have frequently been estimated from parent-offspring regressions, sib analyses, or from selection experiments. Here we review by meta-analysis published estimates of the heritability of developmental stability, mainly the degree of individual fluctuating asymmetry in morphological characters. The overall mean effect size of heritabilities of individual fluctuating asymmetry was 0.19 from 34 studies of 17 species differing highly significantly from zero (P < 0.0001). The mean heritability for 14 species was 0.27. This indicates that there is a significant additive genetic component to developmental stability. Effect size was larger for selection experiments than for studies based on parent-offspring regression or sib analyses, implying that genetic estimates were unbiased by maternal or common environment effects. Additive genetic coefficients of variation for individual fluctuating asymmetry were considerably higher than those for character size per se. Developmental stability may be significantly heritable either because of strong directional selection, or fluctuating selection regimes which prevent populations from achieving a high degree of developmental stability to current environmental and genetic conditions.     

Extent of adaptation is not limited by unpredictability of the environment in laboratory populations of Escherichia coli

Environmental variability is on the rise in different parts of the earth, and the survival of many species depends on how well they cope with these fluctuations. Our current understanding of how organisms adapt to unpredictably fluctuating environments is almost entirely based on studies that investigate fluctuations among different values of a single environmental stressor such as temperature or pH . How would unpredictability affect adaptation when the environment fluctuates between qualitatively very different kinds of stresses? To answer this question, we subjected laboratory populations of Escherichia coli to selection over ~ 260 generations. The populations faced predictable and unpredictable environmental fluctuations across qualitatively different selection environments, namely, salt and acidic pH . We show that predictability of environmental fluctuations does not play a role in determining the extent of adaptation, although the extent of ancestral adaptation to the chosen selection environments is of key importance.     

Sex differences in recombination

One of the stronger empirical generalizations to emerge from the study of genetic systems is that achiasmate meiosis, which has evolved 25–30 times, is always restricted to the heterogametic sex in dioecious species, usually the male. Here we collate data on quantitative sex differences in chiasma frequency from 54 species (4 hermaphroditic flatworms, 18 dioecious insects and vertebrates and 32 hermaphroditic plants) to test whether similar trends hold. Though significant sex differences have been observed within many species, only the Liliaceae show a significant sexual dimorphism in chiasma frequency across species, with more crossing over in embryo mother cells than in pollen mother cells; chiasma frequencies are unrelated to sex and gamety in all other higher taxa studied. Further, the magnitude of sexual dimorphism, independent of sign, does not differ among the three main ecological groups (dioecious animals, plants, and hermaphroditic animals), contrary to what would be expected if it reflected sex-specific selection on recombination. These results indicate that the strong trends for achiasmate meiosis do not apply to quantitative sex differences in recombination, and contradict theories of sex-specific costs and benefits. An alternative hypothesis suggests that sex differences may be more-or-less neutral, selection determining only the mean rate of recombination. While male and female chiasma frequencies are more similar than would be expected under complete neutrality, a less absolute form of the hypothesis is more difficult to falsify. In female mice the sex bivalent has more chiasmata for its length than the autosomes, perhaps compensating for the absence of recombination in males. Finally, we observe that chiasma frequencies in males and females are positively correlated across species, validating the use of only one sex in comparative studies of recombination.     

How do genetic correlations affect species range shifts in a changing environment?

Species may be able to respond to changing environments by a combination of adaptation and migration. We study how adaptation affects range shifts when it involves multiple quantitative traits evolving in response to local selection pressures and gene flow. All traits develop clines shifting in space, some of which may be in a direction opposite to univariate predictions, and the species tracks its environmental optimum with a constant lag. We provide analytical expressions for the local density and average trait values. A species can sustain faster environmental shifts, develop a wider range and greater local adaptation when spatial environmental variation is low (generating low migration load) and multitrait adaptive potential is high. These conditions are favoured when nonlinear (stabilising) selection is weak in the phenotypic direction of the change in optimum, and genetic variation is high in the phenotypic direction of the selection gradient.     

Role of chromosomes in evolution: a new interpretation

The number of possible meiotic segregations of paternal and maternal chromosomes is 2N (N = haploid chromosome number). In eutherian Mammals, where large variations of N exist, 2N may be very different in related species, genes, or families. For instance, in Cercopithecidae, species with the highest value (N = 36) make 2(15) = 32,768 more gametic chromosome combinations than those with the lowest value (N = 21). It is also shown that the number of chiasmata varies from species to species and is proportional to the haploid number of arms NF/2 of the karyotype. Thus, increase or decrease of both N and NF/2, often concomitant, both increase or decrease genetic mixing. The chromosomal phylogeny of Primates, Carnivora and Rodentia shows that pure dichotomic evolution is rare, at contrast with populational (non dichotomic) evolution which seems most frequent. In these Mammals, the few examples of dichotomic evolution are observed in groups with low values of N and NF/2. It is concluded that dichotomic evolution, which should be favoured by the transmission of groups of linked mutant alleles, is prevented, in most instances, by the high recombination rate in karyotypes with high values of N and NF/2. Thus the mode of speciation would depend on karyotype modifications by long term effects on population genetics, in addition to the immediate effects of gametic barriers due to chromosomal rearrangements in the heterozygous state.     

Environmental variation, fluctuating selection and genetic drift in subdivided populations

Although there have many studies of the population genetical consequences of environmental variation, little is known about the combined effects of genetic drift and fluctuating selection in structured populations. Here we use diffusion theory to investigate the effects of temporally and spatially varying selection on a population of haploid individuals subdivided into a large number of demes. Using a perturbation method for processes with multiple time scales, we show that as the number of demes tends to infinity, the overall frequency converges to a diffusion process that is also the diffusion approximation for a finite, panmictic population subject to temporally fluctuating selection. We find that the coefficients of this process have a complicated dependence on deme size and migration rate, and that changes in these demographic parameters can determine both the balance between the dispersive and stabilizing effects of environmental variation and whether selection favors alleles with lower or higher fitness variance.     

Environmental Noise,Genetic Diversity and the Evolution of Evolvability and Robustness in Model Gene Networks

The ability of organisms to adapt and persist in the face of environmental change is accepted as a fundamental feature of natural systems. More contentious is whether the capacity of organisms to adapt (or “evolvability”) can itself evolve and the mechanisms underlying such responses. Using model gene networks, I provide evidence that evolvability emerges more readily when populations experience positively autocorrelated environmental noise (red noise) compared to populations in stable or randomly varying (white noise) environments. Evolvability was correlated with increasing genetic robustness to effects on network viability and decreasing robustness to effects on phenotypic expression; populations whose networks displayed greater viability robustness and lower phenotypic robustness produced more additive genetic variation and adapted more rapidly in novel environments. Patterns of selection for robustness varied antagonistically with epistatic effects of mutations on viability and phenotypic expression, suggesting that trade-offs between these properties may constrain their evolutionary responses. Evolution of evolvability and robustness was stronger in sexual populations compared to asexual populations indicating that enhanced genetic variation under fluctuating selection combined with recombination load is a primary driver of the emergence of evolvability. These results provide insight into the mechanisms potentially underlying rapid adaptation as well as the environmental conditions that drive the evolution of genetic interactions.     

A Darwinian evolutionary system. I. Definition and basic properties

Biological evolution as conceived by the present synthetic theory of evolution is modelled by a mathematical system which consists of three arrays: the genotype and phenotype population and their environment, and four operators: selection, mutation, recombination, and alteration (describing the change of the environment by the population). An evolutionary process then could be represented as the cyclic iteration of these operations on the respective arrays. Some simple versions of this system were investigated by computer simulation. They exhibited the following properties. (i) Population fitness increased with the generation number. (ii) The evolutionary rate increased with variance of fitness. (iii) The evolutionary rate increased with the number of individuals, and decreased with the number of loci. (iv) The evolutionary rate increased with the selection pressure. (v) For a given system in a given state there existed an optimal mutation rate. (vi) Free recombination was optimal. (vii) The mutational load of fitness increased with the mutation rate, but was independent of the selection pressure; contrary to this, the mutational load of the population “morph” decreased with the selection pressure, i.e. one could compensate for the deleterious effect of mutation by strong selection. These rules applied to haploids with equal, unequal, non-epistatic, and epistatic gene effect, and also to diploids. It was found that epistatic gene effect for relatively low mutation rates slows down evolution, whereas unequal gene effect enhances it. Diploids were not found to be superior to haploids in evolutionary terms, except in the case of diploids with dominant gene action for very small population sizes. The results are discussed with regard to their applicability to the simulation of more complex evolutionary phenomena.     

Lampbrush Chromosomes in the Japanese Quail Coturnix coturnix japonica: Cytological Map of Macrochromosomes and Meiotic Crossing-over Frequency in Females

Cytological map of lampbrush macrobivalents of the Japanese quail (Coturnix coturnix japonica) were constructed. Investigation of chiasmata allowed to estimate the frequency of reciprocal genetic recombination (crossing over) in Japanese quail female meiosis. The total chiasma number in bivalents of Japanese quail oocyte nuclei was determined to be 53–58. Macrobivalents 1–5 and Z of the Japanese quail had on average 3.3 chiasmata per bivalent, and microbivalents, 1.0–1.1 chiasmata per bivalent. The chiasmata (crossover) frequency in Japanese quail females was lower than in chicken. In macrochromosomes of Japanese quail females, one crossover occurred per 43.9 Mb, and in chicken, per 30.0 Mb. Judging from chiasma frequency, the genetic length of the Japanese quail genome is likely to be 2650–2900 cM. Crossover frequency in the species was 0.023 per Mb in macrobivalents and 0.07–0.08 Mb in microbivalents and for the total genome, 0.041 crossing over per Mb. The genetic length of one Mb (recombination rate ) in female Japanese quails was 1.14 cM in macrochromosomes, 3.60–4.12 cM in microchromosomes, and about 1.96–2.15 cM averaged over the genome.     

MUTATION LOAD AND THE SURVIVAL OF SMALL POPULATIONS

Previous attempts to model the joint action of selection and mutation in finite populations have treated population size as being independent of the mutation load. However, the accumulation of deleterious mutations is expected to cause a gradual reduction in population size. Consequently, in small populations random genetic drift will progressively overpower selection making it easier to fix future mutations. This synergistic interaction, which we refer to as a mutational melt-down, ultimately leads to population extinction. For many conditions, the coefficient of variation of extinction time is less than 0.1, and for species that reproduce by binary fission, the expected extinction time is quite insensitive to population carrying capacity. These results are consistent with observations that many cultures of ciliated protozoans and vertebrate fibroblasts have characteristic extinction times. The model also predicts that clonal lineages are unlikely to survive more than 10⁴ to 10⁵ generations, which is consistent with existing data on parthenogenetic animals. Contrary to the usual view that Muller's ratchet does more damage when selection is weak, we show that the mean extinction time declines as mutations become more deleterious. Although very small sexual populations, such as self-fertilized lines, are subject to mutational meltdowns, recombination effectively eliminates the process when the effective population size exceeds a dozen or so. The concept of the effective mutation load is developed, and several procedures for estimating it are described. It is shown that this load can be reduced substantially when mutational effects are highly variable.     

Lampbrush chromosomes in the japanese quail Coturnix coturnix japonica: cytological maps of macro chromosomes and meiotic crossover frequency in females

Cytological maps of lampbrush macrobivalents of the Japanese quail (Coturnix coturnix japonica) were constructed. Investigation of chiasmata allowed determination of the meiotic frequency of reciprocal genetic recombination (crossing over) in Japanese quail females. The total chiasma number in bivalents of Japanese quail oocyte nuclei was determined to be 53-58. Macrobivalents 1-5 and Z of the Japanese quail had on average 3.3 chiasmata per bivalent, and microbivalents, 1.0-1.1 chiasmata per bivalent. The chiasmata (crossover) frequency in Japanese quail females was lower than in chicks. In macrochromosomes of Japanese quail females, one crossover occurred per 43.9 Mb, and in chicken, per 30.0 Mb. Judging from chiasma frequency, the genetic length of the Japanese quail genome is likely to be 2650-2900 cM. Crossover frequency in the species was 0.023 per Mb in macrobivalents and 0.07-0.08 Mb in microbivalents and for the total genome, 0.041 crossovers per Mb. The genetic length of one Mb (theta) in female Japanese quails was 1.14 cM in macrochromosomes, 3.60-4.12 cM in microchromosomes, and about 1.96-2.15 cM averaged over the genome.