Molecular mechanisms of dominance evolution in Müllerian mimicry

Natural selection acting on dominance between adaptive alleles at polymorphic loci can be sufficiently strong for dominance to evolve. However, the molecular mechanisms underlying such evolution are generally unknown. Here, using Müllerian mimicry as a case‐study for adaptive morphological variation, we present a theoretical analysis of the invasion of dominance modifiers altering gene expression through different molecular mechanisms. Toxic species involved in Müllerian mimicry exhibit warning coloration, and converge morphologically with other toxic species of the local community, due to positive frequency‐dependent selection acting on these colorations. Polymorphism in warning coloration may be maintained by migration–selection balance with fine scale spatial heterogeneity. We modeled a dominance modifier locus altering the expression of the warning coloration locus, targeting one or several alleles, acting in cis or trans, and either enhancing or repressing expression. We confirmed that dominance could evolve when balanced polymorphism was maintained at the color locus. Dominance evolution could result from modifiers enhancing one allele specifically, irrespective of their linkage with the targeted locus. Nonspecific enhancers could also persist in populations, at frequencies tightly depending on their linkage with the targeted locus. Altogether, our results identify which mechanisms of expression alteration could lead to dominance evolution in polymorphic mimicry.     

Are aposematic signals honest? A review

We explore the relevance of honest signalling theory to the evolution of aposematism. We begin with a general consideration of models of signal stability, with a focus on the Zahavian costly signalling framework. Next, we review early models of signalling in the context of aposematism (some that are consistent and some inconsistent with costly honest signalling). We focus on controversies surrounding the idea that aposematic signals are handicaps in a Zahavian framework. Then, we discuss how the alignment of interests between signaller and predator influences the evolution of aposematism, highlight the distinction between qualitative and quantitative honesty and review theory and research relevant to these categories. We also review recent theoretical treatments of the evolution of aposematism that have focused on honest signalling as well as empirical research on a variety of organisms, including invertebrates and frogs. Finally, we discuss future directions for empirical and theoretical research in this area.     

The quantitative genetics of sexual dimorphism: assessing the importance of sex-linkage

Sexual dimorphism (SD) is a defining feature of gonochorous animals and dioecious plants, but the evolution of SD from an initially monomorphic genome presents a conundrum. Theory predicts that the evolution of SD will be facilitated if genes with sex-specific fitness effects occur on sex chromosomes. We review this theory and show that it generates three testable predictions. For organisms with an XX/XY chromosomal system of sex determination: (1) SD should be associated with X-linked effects; (2) X-linked effects should show strong directional dominance for sexually dimorphic traits favored in males but expressed in both sexes; and (3) SD should be associated with a reduction in the between-sex additive genetic covariance and correlation. A literature review reveals that empirical evaluations of the association between sex-linkage and SD have lagged behind theory. Tests for the presence of sex-linked effects have been plagued by the need to make simplifying assumptions, such as the absence of dominance or maternal effects, that greatly weaken their discriminatory power. Further, most have used comparisons between species or populations, whereas the correct level of analysis is within populations. To overcome these problems, we derive a novel pedigree design that permits separate estimation of X-linked, dominance and maternal effects. We suggest that the data from such a design would be most appropriately analyzed using the animal model. This novel protocol will allow quantitative evaluation of the above predictions, and hence should spur progress in understanding the role of sex-linkage in the evolution of SD.     

Quantitative genetic models of sexual selection

Modeling of R.A. Fisher's ideas about the evolution of male ornamentation using quantitative genetics began in the 1980s. Following an initial period of enthusiasm, interest in these models began to wane when theoretical studies seemed to show that the rapid evolution of ornaments would not occur if there were costs associated with female mate choice. Recent theoretical work has shown, however, that runaway evolution and other kinds of extensive diversification of ornaments and preferences can occur, even when female choice is costly. These new models highlight crucial parameters that profoundly influence evolutionary trajectories, but these parameters have been neglected in empirical studies. Here, we review quantitative genetic models of sexual selection with the aim of fostering communication and synergism between theoretical and empirical enterprises. We also point out several areas in which additional empirical work could distinguish between alternative models of evolution.     

基因差异表达与杂种优势形成机制探讨

对杂种优势这一普遍而重要的生物学现象研究虽有百余年的历史, 但其根本机理尚未阐述清楚。继基因组组成差异及基因效应研究之后, 基因表达差异成为探寻杂种优势分子机理新的切入点。旨在通过揭示杂种中等位基因差异表达、杂种与亲本间基因差异表达的调控机制, 来认识杂种优势形成的分子机理, 从而达到指导育种实践的目的。文章概述了杂种等位基因差异表达现象及其产生机理, 总结了杂种与亲本相比所呈现出的加性、显性和超显性等多种差异基因表达模式, 归纳了表达谱研究筛选出的与杂种优势形成有关的基因, 以及某些关键生化代谢途径对杂种优势形成的贡献。但由于杂种优势机理的复杂性, 基因表达研究并没有得出统一的表达模式, 大多数杂种优势基因也不能被归属为同一类别。尽管如此, 基因表达谱研究毕竟迈出了解析杂种优势形成复杂基因表达网络的第一步, 随着表达谱技术和生物信息学的不断更新和发展, 杂种优势形成的分子机理有望在基因表达层面上取得突破。     

On the evolution of dominance modifiers II: a non-equilibrium approach to the evolution of genetic systems

The evolution of dominance is both the simplest and best investigated example of the evolution of genetic systems. Nevertheless, there exists striking empirical material, e.g. industrial melanism, for which no satisfactory explanation could so far be provided. In this paper we take an approach to this classical problem based on a global analysis together with computer simulations. It reveals that during the evolution of dominance one has to distinguish a "nonequilibrium phase" and a "Fisherian phase". The non-equilibrium phase appears to be characterized by the fact that in general the selection intensity at the primary locus does not affect the degree of modifier selection but only the time necessary for passing through this phase. A further essential conclusion is that modifier evolution only obtains a reasonable amount of efficiency if the population reaches the Fisherian phase already with a high modifier frequency. Using these results, predictions on the population genetic prerequisites for the evolution of dominance are derived. From these we conclude that even in populations in which dominance evolution has occurred it cannot be expected that back-crosses into relics of the ancestral population lead to a breakdown of dominance within a few generations. These predictions are in accordance with empirical data on Biston betularia and Odontopera bidentata.     

Genetics of dispersal

Dispersal is a process of central importance for the ecological and evolutionary dynamics of populations and communities, because of its diverse consequences for gene flow and demography. It is subject to evolutionary change, which begs the question, what is the genetic basis of this potentially complex trait? To address this question, we (i) review the empirical literature on the genetic basis of dispersal, (ii) explore how theoretical investigations of the evolution of dispersal have represented the genetics of dispersal, and (iii) discuss how the genetic basis of dispersal influences theoretical predictions of the evolution of dispersal and potential consequences. Dispersal has a detectable genetic basis in many organisms, from bacteria to plants and animals. Generally, there is evidence for significant genetic variation for dispersal or dispersal‐related phenotypes or evidence for the micro‐evolution of dispersal in natural populations. Dispersal is typically the outcome of several interacting traits, and this complexity is reflected in its genetic architecture: while some genes of moderate to large effect can influence certain aspects of dispersal, dispersal traits are typically polygenic. Correlations among dispersal traits as well as between dispersal traits and other traits under selection are common, and the genetic basis of dispersal can be highly environment‐dependent. By contrast, models have historically considered a highly simplified genetic architecture of dispersal. It is only recently that models have started to consider multiple loci influencing dispersal, as well as non‐additive effects such as dominance and epistasis, showing that the genetic basis of dispersal can influence evolutionary rates and outcomes, especially under non‐equilibrium conditions. For example, the number of loci controlling dispersal can influence projected rates of dispersal evolution during range shifts and corresponding demographic impacts. Incorporating more realism in the genetic architecture of dispersal is thus necessary to enable models to move beyond the purely theoretical towards making more useful predictions of evolutionary and ecological dynamics under current and future environmental conditions. To inform these advances, empirical studies need to answer outstanding questions concerning whether specific genes underlie dispersal variation, the genetic architecture of context‐dependent dispersal phenotypes and behaviours, and correlations among dispersal and other traits.     

EVOLUTION OF DOMINANCE IN SPOROPHYTIC SELF-INCOMPATIBILITY SYSTEMS: I. GENETIC LOAD AND COEVOLUTION OF LEVELS OF DOMINANCE IN POLLEN AND PISTIL

Recent theoretical advances have suggested that various forms of balancing selection may promote the evolution of dominance through an increase of the proportion of heterozygote genotypes. We test whether dominance can evolve in the sporophytic self-incompatibility (SSI) system in plants. SSI prevents mating between individuals expressing identical SI phenotypes by recognition of pollen by pistils, which avoids selfing and inbreeding depression. SI phenotypes depend on a complex network of dominance relationships between alleles at the self-incompatibility locus ( S -locus). Empirical studies suggest that these relationships are not random, but the exact evolutionary processes shaping these relationships remain unclear. We investigate the expected patterns of dominance under the hypothesis that dominance is a direct target of natural selection. We follow the fate of a mutant allele at the S -locus whose dominance relationships are changed but whose specificity remains unaltered. We show that strict codominance is not evolutionarily stable in SSI, and that inbreeding depression due to deleterious mutations linked or unlinked to the S -locus exerts strong constraints on changes in relative levels of dominance in pollen and pistil. Our results provide a general adaptive explanation for most patterns of dominance relationships empirically observed in natural plant populations.     

Causes and effects of haploinsufficiency

Haploinsufficiency is a form of genetic dominance and is the underlying mechanism of numerous human inherited conditions in which the causal genes are sensitive to altered dosage. This review examines the poorly understood relationships between haploinsufficiency, dosage sensitivity and genetic dominance, whose common theme is the existence of nonlinear relationships between genotype and phenotype. We present an up‐to‐date account of the bases of haploinsufficiency from the perspective of theoretical and experimental models. We also discuss human conditions caused by haploinsufficiency, including developmental syndromes and cancer. Connections between the understanding of these conditions' genetic mechanisms and advances in treatments are also described.     

Biological applications of the theory of birth-and-death processes

In this review, we discuss applications of the theory of birth-and-death processes to problems in biology, primarily, those of evolutionary genomics. The mathematical principles of the theory of these processes are briefly described. Birth-and-death processes, with some straightforward additions such as innovation, are a simple, natural and formal framework for modeling a vast variety of biological processes such as population dynamics, speciation, genome evolution, including growth of paralogous gene families and horizontal gene transfer and somatic evolution of cancers. We further describe how empirical data, e.g. distributions of paralogous gene family size, can be used to choose the model that best reflects the actual course of evolution among different versions of birth-death-and-innovation models. We conclude that birth-and-death processes, thanks to their mathematical transparency, flexibility and relevance to fundamental biological processes, are going to be an indispensable mathematical tool for the burgeoning field of systems biology.     

The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: maternal effects, sib-social effects, and heterochrony

We discuss the evolutionary origin and elaboration of sociality using an indirect genetic effects perspective. Indirect genetic effects models simultaneously consider zygotic genes, genes expressed in social partners (especially mothers and siblings), and the interactions between them. Incorporation of these diverse genetic effects should lead to more realistic models of social evolution. We first review haplodiploidy as a factor that promotes the evolution of eusociality. Social insect biologists have doubted the importance of relatedness asymmetry caused by haplodiploidy and focused on other predisposing factors such as maternal care. However; indirect effects theory shows that maternal care evolves more readily in haplodiploids, especially with inbreeding and despite multiple mating. Because extended maternal care is believed to be a precondition for the evolution of eusociality, the evolutionary bias towards maternal care in haplodiploids may result in a further bias towards eusociality in these groups. Next, we compare kin selection and parental manipulation and then briefly review additional hypotheses for the evolutionary origin of eusociality. We present a verbal model for the evolutionary origin and elaboration of sib-social care from maternal care based on the modification of the timing of expression of maternal care behaviors. Specifically, heterochrony genes cause maternal care behaviors to be expressed prereproductively towards siblings instead of postreproductively towards offspring. Our review demonstrates that both maternal effect genes (expressed in a parental manipulation manner) and direct effect zygotic genes (expressed in an offspring control manner) are likely involved in the evolution of eusociality. We conclude by describing theoretical and empirical advances with indirect genetic effects and sociogenomics, and we provide specific quantitative genetic and genomic predictions from our heterochrony model for the evolutionary origin and elaboration of eusociality.     

Opsin expression predicts male nuptial color in threespine stickleback

Theoretical models of sexual selection suggest that male courtship signals can evolve through the build‐up of genetic correlations between the male signal and female preference. When preference is mediated via increased sensitivity of the signal characteristics, correlations between male signal and perception/sensitivity are expected. When signal expression is limited to males, we would expect to find signal‐sensitivity correlations in males. Here, we document such a correlation within a breeding population of threespine stickleback mediated by differences in opsin expression. Males with redder nuptial coloration express more long‐wavelength‐sensitive (LWS) opsin, making them more sensitive to orange and red. This correlation is not an artifact of shared tuning to the optical microhabitat. Such correlations are an essential feature of many models of sexual selection, and our results highlight the potential importance of opsin expression variation as a substrate for signal‐preference evolution. Finally, these results suggest a potential sensory mechanism that could drive negative frequency‐dependent selection via male–male competition and thus maintain variation in male nuptial color.     

Comparative methods for the analysis of gene-expression evolution: an example using yeast functional genomic data

Understanding the evolution of gene function is a primary challenge of modern evolutionary biology. Despite an expanding database from genomic and developmental studies, we are lacking quantitative methods for analyzing the evolution of some important measures of gene function, such as gene-expression patterns. Here, we introduce phylogenetic comparative methods to compare different models of gene-expression evolution in a maximum-likelihood framework. We find that expression of duplicated genes has evolved according to a nonphylogenetic model, where closely related genes are no more likely than more distantly related genes to share common expression patterns. These results are consistent with previous studies that found rapid evolution of gene expression during the history of yeast. The comparative methods presented here are general enough to test a wide range of evolutionary hypotheses using genomic-scale data from any organism.     

The resolution of sexual antagonism by gene duplication

Disruptive selection between males and females can generate sexual antagonism, where alleles improving fitness in one sex reduce fitness in the other. This type of genetic conflict arises because males and females carry nearly identical sets of genes: opposing selection, followed by genetic mixing during reproduction, generates a population genetic "tug-of-war" that constrains adaptation in either sex. Recent verbal models suggest that gene duplication and sex-specific cooption of paralogs might resolve sexual antagonism and facilitate evolutionary divergence between the sexes. However, this intuitive proximal solution for sexual dimorphism potentially belies a complex interaction between mutation, genetic drift, and positive selection during duplicate fixation and sex-specific paralog differentiation. The interaction of these processes--within the explicit context of duplication and sexual antagonism--has yet to be formally described by population genetics theory. Here, we develop and analyze models of gene duplication and sex-specific differentiation between paralogs. We show that sexual antagonism can favor the fixation and maintenance of gene duplicates, eventually leading to the evolution of sexually dimorphic genetic architectures for male and female traits. The timescale for these evolutionary transitions is sensitive to a suite of genetic and demographic variables, including allelic dominance, recombination, sex linkage, and population size. Interestingly, we find that female-beneficial duplicates preferentially accumulate on the X chromosome, whereas male-beneficial duplicates are biased toward autosomes, independent of the dominance parameters of sexually antagonistic alleles. Although this result differs from previous models of sexual antagonism, it is consistent with several findings from the empirical genomics literature.     

The adaptive landscape as a conceptual bridge between micro- and macroevolution

An adaptive landscape concept outlined by G.G. Simpson constitutes the major conceptual bridge between the fields of micro- and macroevolutionary study. Despite some important theoretical extensions since 1944, this conceptual bridge has been ignored in many empirical studies. In this article, we review the status of theoretical work and emphasize the importance of models for peak movement. Although much theoretical work has been devoted to evolution on stationary, unchanging landscapes, an important new development is a focus on the evolution of the landscape itself. We also sketch an agenda of empirical issues that is inspired by theoretical developments.     

Pathogens and sex in plants

Summary Extant theories that attribute the evolution of sex to pathogen attack depend on the assumption that pathogens are narrowly specialized, so that high fitness on one host genotype results in poor fitness on hosts with other allele combinations. This assumption is necessary in order for frequency-dependent selection to produce sustained cycling of gametic disequilibrium across the host's disease resistance loci, which makes recombination advantageous. However, a review of numerous genetic studies on plant disease resistance failed to uncover a single example consistent with this assumption. Instead, the empirical results provide strong support for a different pattern of pathogen specificity, in which adaptation by pathogens to one resistance allele does not preclude high fitness on alternate host genotypes lacking that allele. Modification of traditional models for pathogen-mediated evolution of sex showed that for conditions close to the empirical pattern of genotypic specificity, sex is almost never favoured. For plants, these results cast doubt on current theories arguing that pathogens are the primary selective agent responsible for sexual reproduction.     

The evolution of mate choice and mating biases

We review the current status of three well-established models (direct benefits, indirect benefits and sensory drive) and one newcomer (antagonistic chase-away) of the evolution of mate choice and the biases that are expressed during choice. We highlight the differences and commonalities in the underlying genetics and evolutionary dynamics of these models. We then argue that progress in understanding the evolution of mate choice is currently hampered by spurious distinctions among models and a misguided tendency to test the processes underlying each model as mutually exclusive alternatives. Finally, we suggest potentially fruitful directions for future theoretical and empirical research.     

Adaptive protein evolution and regulatory divergence in Drosophila

Two recent studies demonstrated a positive correlation between divergence in gene expression and protein sequence in Drosophila. This correlation could be driven by positive selection or variation in functional constraint. To distinguish between these alternatives, we compared patterns of molecular evolution for 1,862 genes with two previously reported estimates of expression divergence in Drosophila. We found a slight negative trend (nonsignificant) between positive selection on protein sequence and divergence in expression levels between Drosophila melanogaster and Drosophila simulans. Conversely, shifts in expression patterns during Drosophila development showed a positive association with adaptive protein evolution, though as before the relationship was weak and not significant. Overall, we found no strong evidence for an increase in the incidence of positive selection on protein-coding regions in genes with divergent expression in Drosophila, suggesting that the previously reported positive association between protein and regulatory divergence primarily reflects variation in functional constraint.