Ploidally antagonistic selection maintains stable genetic polymorphism

Understanding the maintenance of genetic variation in the face of selection remains a key issue in evolutionary biology. One potential mechanism for the maintenance of genetic variation is opposing selection during the diploid and haploid stages of biphasic life cycles universal among eukaryotic sexual organisms. If haploid and diploid gene expression both occur, selection can act in each phase, potentially in opposing directions. In addition, sex-specific selection during haploid phases is likely simply because male and female gametophytes/gametes tend to have contrasting life histories. We explored the potential for the maintenance of a stable polymorphism under ploidally antagonistic as well as sex-specific selection. Furthermore, we examined the role of the chromosomal location of alleles (autosomal or sex-linked). Our analyses show that the most permissible conditions for the maintenance of polymorphism occur under negative ploidy-by-sex interactions, where stronger selection for an allele in female than male diploids is coupled with weaker selection against the allele in female than male haploids. Such ploidy-by-sex interactions also promote allele frequency differences between the sexes. With constant fitness, ploidally antagonistic selection can maintain stable polymorphisms for autosomal and X-linked genes but not for Y-linked genes. We discuss the implications of our results and outline a number of biological settings where the scenarios modeled may apply.     

Microhabitat variation and sexual selection can maintain male color polymorphisms

Male color polymorphism may be an important precursor to sympatric speciation by sexual selection, but the processes maintaining such polymorphisms are not well understood. Here, we develop a formal model of the hypothesis that male color polymorphisms may be maintained by variation in the sensory environment resulting in microhabitat-specific selection pressures. We analyze the evolution of two male color morphs when color perception (by females and predators) is dependent on the microhabitat in which natural and sexual selection occur. We find that an environment of heterogeneous microhabitats can lead to the maintenance of color polymorphism despite asymmetries in the strengths of natural and sexual selection and in microhabitat proportions. We show that sexual selection alone is sufficient for polymorphism maintenance over a wide range of parameter space, even when female preferences are weak. Polymorphisms can also be maintained by natural selection acting alone, but the conditions for polymorphism maintenance by natural selection will usually be unrealistic for the case of microhabitat variation. Microhabitat variation and sexual selection for conspicuous males may thus provide a situation particularly favorable to the maintenance of male color polymorphisms. These results are important both because of the general insight they provide into a little appreciated mechanism for the maintenance of variation in natural populations and because such variation is an important prerequisite for sympatric speciation.     

Disentangling the causes of heterogeneity in male fecundity in gynodioecious Beta vulgaris ssp. maritima

Variation among individuals in reproductive success is advocated as a major process driving evolution of sexual polymorphisms in plants, such as gynodioecy where females and hermaphrodites coexist. In gynodioecious Beta vulgaris ssp. maritima, sex determination involves cytoplasmic male sterility (CMS) genes and nuclear restorers of male fertility. Both restored CMS and non-CMS hermaphrodites co-occur. Genotype-specific differences in male fitness are theoretically expected to explain the maintenance of cytonuclear polymorphism. Using genotypic information on seedlings and flowering plants within two metapopulations, we investigated whether male fecundity was influenced by ecological, phenotypic and genetic factors, while taking into account the shape and scale of pollen dispersal. Along with spatially restricted pollen flow, we showed that male fecundity was affected by flowering synchrony, investment in reproduction, pollen production and cytoplasmic identity of potential fathers. Siring success of non-CMS hermaphrodites was higher than that of restored CMS hermaphrodites. However, the magnitude of the difference in fecundity depended on the likelihood of carrying restorer alleles for non-CMS hermaphrodites. Our results suggest the occurrence of a cost of silent restorers, a condition supported by scarce empirical evidence, but theoretically required to maintain a stable sexual polymorphism in gynodioecious species.     

The potential for sexually antagonistic polymorphism in different genome regions

Sex differences in the fitness effects of alleles at a single locus (intralocus sexual antagonism, or SA) have several evolutionary consequences. Among the consequences of SA, polymorphisms at genes partially linked to the sex-determining region of the sex chromosome pair potentially drive the evolution of suppressed recombination between the sex chromosomes. Understanding the conditions under which SA polymorphism can exist at such pseudo-autosomal (or PAR) loci should increase understanding of the evolution of recombination between sex chromosome pairs, and can help predict when we may expect potentially empirically detectable allele frequency differences between the sexes. Models so far published have concluded that PAR genes can maintain SA polymorphisms over a wider range of selection coefficients than autosomal ones, but have used restrictive assumptions. We expand the modeling of SA alleles at a single locus with the full range of degrees of linkage to the male-specific region, to include strong or weak selection and the possibility of different dominance coefficients in the two sexes. We confirm the previous major conclusion that SA polymorphisms are generally maintained in a larger region of parameter space if the locus is in the PAR than if it is autosomal.     

Colour polymorphism is likely to be disadvantageous to some populations and species due to genetic architecture and morph interactions

Polymorphism describes two or more distinct, genetically determined, phenotypes that co‐occur in the same population, where the rarest morph is maintained at a frequency above the mutation rate (Ford 1945; Huxley 1955). In a recent opinion piece, we explored a new idea regarding the role of genetic architectures and morph interactions in colour polymorphisms and how this can negatively affect population performance (Bolton et al. 2015). In this issue of Molecular Ecology, Forsman (2016) thoroughly discusses the current evidence for polymorphisms enhancing population performance and critiques the validity of the definitions of polymorphism we use in our original paper. We respond by clarifying that the negative consequences of polymorphisms that we discussed are likely to be most pertinent in species that have a particular set of characteristics, such as strong sexual or social interactions between morphs and discrete genetic architectures. Although it was not our intention to redefine polymorphism, we do believe that there should be further discussion about refining or characterizing balanced polymorphisms with respect to the degree of morph sympatry, discreteness of traits and their underlying genetic architecture, and the types of selection that drive and maintain the variation. The latter describes whether polymorphism is primarily maintained by external factors such as predation pressure or internal factors such as interactions with members of the same species. The contribution of Forsman (2016) is useful to this discussion, and we hope that our exchange of opinions will inspire new empirical and theoretical ideas on the origin and maintenance of colour polymorphisms.     

Linking color polymorphism maintenance and speciation

Here, we review the recently burgeoning literature on color polymorphisms, seeking to integrate studies of the maintenance of genetic variation and the evolution of reproductive isolation. Our survey reveals that several mechanisms, some operating between populations and others within them, can contribute to both color polymorphism persistence and speciation. As expected, divergent selection clearly can couple with gene flow to maintain color polymorphism and mediate speciation. More surprisingly, recent evidence suggests that diverse forms of within-population sexual selection can generate negative frequency dependence and initiate reproductive isolation. These findings deserve additional study, particularly concerning the roles of heterogeneous visual environments and correlational selection. Finally, comparative studies and more comprehensive approaches are required to elucidate when color polymorphism evolves, persists, or leads to speciation.     

Maintenance of a genetic polymorphism by fluctuating selection on sex‐limited traits

Fluctuating selection is often thought to be ineffective in maintaining a genetic polymorphism except when generations overlap, for example when a seed bank causes a storage effect. Here, I demonstrate that fluctuating selection on sex‐limited traits automatically includes such a ‘storage effect’ because sex‐limited alleles are shielded from selection in the sex where they are not expressed. With analytical calculations and numerical simulations I show that fluctuating selection can maintain a genetic polymorphism in sex‐limited traits. Such a protected polymorphism can reduce the cost of sex when female‐limited traits are involved. But, this effect will probably be small compared to the two‐fold advantage of asexual reproduction unless many polymorphic loci interact or exceptionally strong environmental fluctuations are present. It is argued that genetic polymorphisms maintained by fluctuating selection on sex‐limited traits may partly explain the large genetic variance of traits under strong sexual selection.     

Selection with gene-cytoplasm interactions. I. Maintenance of cytoplasm polymorphisms

General conditions for the protectedness of gene-cytoplasm polymorphisms are considered for a biallelic model with two cytoplasm types and under the assumption that nuclear polymorphisms cannot be maintained in the presence of only one cytoplasm type. Analytical results involving male fertilities, female fertilities, viabilities and selfing rates are obtained, and numerical results show spiral and cyclic behavior of population trajectories. It is shown that a maternally inherited cytoplasmic polymorphism cannot be maintained in the absence of a nuclear polymorphism, and that a gene-cytoplasm polymorphism can only be maintained if the population shows sexual asymmetry, i.e. , if the ratio of male to female fertility varies among genotypes. Thus, the classical viability selection model does not allow gene-cytoplasm polymorphisms.     

DNA polymorphisms amplified by arbitrary primers are useful as genetic markers.

Molecular genetic maps are commonly constructed by analyzing the segregation of restriction fragment length polymorphisms (RFLPs) among the progeny of a sexual cross. Here we describe a new DNA polymorphism assay based on the amplification of random DNA segments with single primers of arbitrary nucleotide sequence. These polymorphisms, simply detected as DNA segments which amplify from one parent but not the other, are inherited in a Mendelian fashion and can be used to construct genetic maps in a variety of species. We suggest that these polymorphisms be called RAPD markers, after Random Amplified Polymorphic DNA.     

The maintenance (or not) of polygenic variation by soft selection in heterogeneous environments

On the basis of single-locus models, spatial heterogeneity of the environment coupled with strong population regulation within each habitat (soft selection) is considered an important mechanism maintaining genetic variation. We studied the capacity of soft selection to maintain polygenic variation for a trait determined by several additive loci, selected in opposite directions in two habitats connected by dispersal. We found three main types of stable equilibria. Extreme equilibria are characterized by extreme specialization to one habitat and loss of polymorphism. They are analogous to monomorphic equilibria in singe-locus models and are favored by similar factors: high dispersal, weak selection, and low marginal average fitness of intermediate genotypes. At the remaining two types of equilibria the population mean is intermediate but variance is very different. At fully polymorphic equilibria all loci are polymorphic, whereas at low-variance equilibria at most one locus remains polymorphic. For most parameters only one type of equilibrium is stable; the transition between the domains of fully polymorphic and low-variance equilibria is typically sharp. Low-variance equilibria are favored by high marginal average fitness of intermediate genotypes, in contrast to single-locus models, in which marginal overdominance is particularly favorable for maintenance of polymorphism. The capacity of soft selection to maintain polygenic variation is thus more limited than extrapolation from single-locus models would suggest, in particular if dispersal is high and selection weak. This is because in a polygenic model, variance can evolve independently of the mean, whereas in the single-locus two-allele case, selection for an intermediate mean automatically leads to maintenance of polymorphism.     

Antagonistic pleiotropy in species with separate sexes,and the maintenance of genetic variation in life‐history traits and fitness

Antagonistic pleiotropy (AP)—where alleles of a gene increase some components of fitness at a cost to others—can generate balancing selection, and contribute to the maintenance of genetic variation in fitness traits, such as survival, fecundity, fertility, and mate competition. Previous theory suggests that AP is unlikely to maintain variation unless antagonistic selection is strong, or AP alleles exhibit pronounced differences in genetic dominance between the affected traits. We show that conditions for balancing selection under AP expand under the likely scenario that the strength of selection on each fitness component differs between the sexes. Our model also predicts that the vast majority of balanced polymorphisms have sexually antagonistic effects on total fitness, despite the absence of sexual antagonism for individual fitness components. We conclude that AP polymorphisms are less difficult to maintain than predicted by prior theory, even under our conservative assumption that selection on components of fitness is universally sexually concordant. We discuss implications for the maintenance of genetic variation, and for inferences of sexual antagonism that are based on sex‐specific phenotypic selection estimates—many of which are based on single fitness components.     

The contribution of haploids, diploids and clones to fine-scale population structure in the seaweed Cladophoropsis membranacea (Chlorophyta)

Local populations of Cladophoropsis membranacea exist as mats of coalesced thalli composed of free-living haploid and diploid plants including clonally reproduced plants of either phase. None of the phases are morphologically distinguishable. We used eight microsatellite loci to explore clonality and fine-scale patch structure in C. membranacea at six sites on the Canary Islands. Mats were always composites of many individuals; not single, large clones. Haploids outnumbered diploids at all sites (from 2:1 to 10:1). In both haploid and diploid plants, genetic diversity was high and there was no significant difference in allele frequencies. Significant heterozygote deficiencies were found in the diploid plants at five out of six sites and linkage disequilibrium was associated with the haploid phase at all sites. Short dispersal distances of gametes/spores and small effective population sizes associated with clonality probably contribute to inbreeding. Spatial autocorrelation analysis revealed that most clones were found within a radius of approximately 60 cm and rarely further than 5 m. Dominance of the haploid phase may reflect seasonal shifts in the relative frequencies of haploids and diploids, but may alternatively reflect superiority of locally adapted and competitively dominant, haploid clones; a strategy that is theoretically favoured in disturbed environments. Although sexual reproduction may be infrequent in C. membranacea, it is sufficient to maintain both life history phases and supports theoretical modelling studies that show that haploid-diploid life histories are an evolutionarily stable strategy.     

Interactions between spatial and temporal scales in the evolution of dispersal rate

The evolution of dispersal rate is studied with a model of several local populations linked by dispersal. Three dispersal strategies are considered where all, half or none of the offspring disperse. The spatial scale (number of patches) and the temporal scale (probability of local extinction) of the environment are critical in determining the selective advantage of the different dispersal strategies. The results from the simulations suggest that an interaction between group selection and individual selection results in a different outcome in relation to the spatial and temporal scales of the environment. Such an interaction is able to maintain a polymorphism in dispersal strategies. The maintenance of this polymorphism is also scale-dependent. This study suggests a mechanism for the short-term evolution of dispersal, and provides a testable prediction of this hypothesis, namely that loss of dispersal abilities should be more frequent in spatially more continuous environments, or in temporally more stable environments. This revised version was published online in July 2006 with corrections to the Cover Date.     

A quasispecies approach to the evolution of sexual replication in unicellular organisms

This study develops a simplified model describing the evolutionary dynamics of a population composed of obligate sexually and asexually reproducing, unicellular organisms. The model assumes that the organisms have diploid genomes consisting of two chromosomes, and that the sexual organisms replicate by first dividing into haploid intermediates, which then combine with other haploids, followed by the normal mitotic division of the resulting diploid into two new daughter cells. We assume that the fitness landscape of the diploids is analogous to the single-fitness-peak approach often used in single-chromosome studies. That is, we assume a master chromosome that becomes defective with just one point mutation. The diploid fitness then depends on whether the genome has zero, one, or two copies of the master chromosome. We also assume that only pairs of haploids with a master chromosome are capable of combining so as to produce sexual diploid cells, and that this process is described by second-order kinetics. We find that, in a range of intermediate values of the replication fidelity, sexually reproducing cells can outcompete asexual ones, provided the initial abundance of sexual cells is above some threshold value. The range of values where sexual reproduction outcompetes asexual reproduction increases with decreasing replication rate and increasing population density. We critically evaluate a common approach, based on a group selection perspective, used to study the competition between populations and show its flaws in addressing the evolution of sex problem.     

Constraints on the origin and maintenance of genetic kin recognition

Kin-recognition mechanisms allow helping behaviors to be directed preferentially toward related individuals, and could be expected to evolve in many cases. However, genetic kin recognition requires a genetic polymorphism on which recognition is based, and kin discriminating behaviors will affect the evolution of such polymorphism. It is unclear whether genetic polymorphisms used in kin recognition should be maintained by extrinsic selection pressures or not, as opposite conclusions have been reached by analytical one-locus models and simulations exploring different population structures. We analyze a two-locus model in a spatially subdivided population following the island model of dispersal between demes of finite size. We find that in the absence of mutation, selection eliminates polymorphism in most cases, except with extreme spatial structure and low recombination. With mutation, the population may reach a stable limit cycle over which both loci are polymorphic; however, the average frequency of conditional helping can be high only under strong structure and low recombination. Finally, we review evidence for extrinsic selection maintaining polymorphism on which kin recognition is based.     

Polymorphisms for purely cytoplasmically inherited traits in bisexual plants

It is shown that cytoplasm polymorphisms transmitted only by the ovules can be maintained without gene-cytoplasmic interactions. The necessary prerequisites are asymmetry of the plasmotypes in production of ovules and pollen (sexual asymmetry), incomplete and frequency-dependent fertilization efficiency and differential selfing rates. These factors can generate the negative frequency dependence of cytoplasmic fitnesses required for a stable polymorphism. The model considered allows also for facultative fixation of either of two plasmotypes and, thus, may produce all of the dynamical characteristics known for nuclear selection with two alleles at one locus.

Strong sexual asymmetry, which probably occurs frequently in bisexual plants, may facilitate stable cytoplasmic polymorphisms. However, these polymorphisms may also endanger survival of the whole population in the absence of nuclear interactions. Gene-cytoplasmic interactions avoid this risk and, at the same time, utilize the advantages of sexual asymmetry in maintaining genetic polymorphisms.

     

Sexual conflict and the maintenance of genetic variation in natural populations

Understanding the factors that maintain genetic variation in natural populations is a foundational goal of evolutionary biology. To this end, population geneticists have developed a variety of models that can produce stable polymorphisms. In one of the earliest models, Owen ( 1953 ) demonstrated that differences in selection pressures acting on males and females could maintain multiple alleles of a gene at a stable equilibrium. If the selection pressures act in opposite directions in males and females, we refer to this as (inter‐) sexual conflict or sexual antagonism (Arnqvist & Rowe, 2005 ). Testing if sexual conflict maintains genetic variation in natural populations is a tremendous challenge—it requires both identifying loci that harbor sexually antagonistic alleles and determining whether those alleles are maintained as stable polymorphisms (Mank, 2017 ). Doing so genome‐wide is even harder because it is not tractable to identify sexually antagonistic alleles and test for stable polymorphisms at all loci. Dutoit et al. ( 2018 ) confront this challenge in a paper published in this issue of Molecular Ecology. Using gene expression and population genomic data from the collared flycatcher, Dutoit et al. ( 2018 ) identify associations and correlations between genomic signatures of balanced polymorphisms and sexual conflict.     

Evolution of haploid–diploid life cycles when haploid and diploid fitnesses are not equal

Many organisms spend a significant portion of their life cycle as haploids and as diploids (a haploid–diploid life cycle). However, the evolutionary processes that could maintain this sort of life cycle are unclear. Most previous models of ploidy evolution have assumed that the fitness effects of new mutations are equal in haploids and homozygous diploids, however, this equivalency is not supported by empirical data. With different mutational effects, the overall (intrinsic) fitness of a haploid would not be equal to that of a diploid after a series of substitution events. Intrinsic fitness differences between haploids and diploids can also arise directly, for example because diploids tend to have larger cell sizes than haploids. Here, we incorporate intrinsic fitness differences into genetic models for the evolution of time spent in the haploid versus diploid phases, in which ploidy affects whether new mutations are masked. Life‐cycle evolution can be affected by intrinsic fitness differences between phases, the masking of mutations, or a combination of both. We find parameter ranges where these two selective forces act and show that the balance between them can favor convergence on a haploid–diploid life cycle, which is not observed in the absence of intrinsic fitness differences.     

Revisiting santa rosalia to unfold a degeneracy of classic models of speciation

Abstract Many classic models of speciation incorporate assortative mating based on mating groups, such as plants with different flowering times, and they investigate whether an ecological trait under disruptive natural selection becomes genetically associated with the selectively neutral mating trait. It is well known that this genetic association is potently destroyed by recombination. In this note, we point out a more fundamental difficulty: if a "knife-edge" symmetry assumption of previous models is violated, then the mating trait is no longer neutral and sexual selection eliminates the polymorphism in the mating locus. This result strengthens the growing consensus that magic traits are the more likely route to nonallopatric speciation. We expand the model assuming also ecological selection on the mating trait and investigate the conditions for natural selection to overcome sexual selection and maintain mating polymorphism; we find that the combination of natural and sexual selection can cause also bistability of allele frequencies.