Evolutionary Conflict Research Articles

Sexual selection modulates genetic conflicts and patterns of genomic imprinting.

Recent years have seen a surge of interest in linking the theories of kin selection and sexual selection. In particular, there is a growing appreciation that kin selection, arising through demographic factors such as sex‐biased dispersal, may modulate sexual conflicts, including in the context of male–female arms races characterized by coevolutionary cycles. However, evolutionary conflicts of interest need not only occur between individuals, but may also occur within individuals, and sex‐specific demography is known to foment such intragenomic conflict in relation to social behavior. Whether and how this logic holds in the context of sexual conflict—and, in particular, in relation to coevolutionary cycles—remains obscure. We develop a kin‐selection model to investigate the interests of different genes involved in sexual and intragenomic conflict, and we show that consideration of these conflicting interests yields novel predictions concerning parent‐of‐origin specific patterns of gene expression and the detrimental effects of different classes of mutation and epimutation at loci underpinning sexually selected phenotypes.

Divalent Cations Increase DNA Repair Activities of Bacterial (6-4) Photolyases.

The (6-4) photolyases of the FeS-BCP group can be considered as the most ancient type among the large family of cryptochrome and photolyase flavoproteins. In contrast to other photolyases, they contain an Fe-S cluster of unknown function, a DMRL chromophore, an interdomain loop, which could interact with DNA, and a long C-terminal extension. We compared DNA repair and photoreduction of two members of the FeS-BCP family, Agrobacterium fabrum PhrB and Rhodobacter sphaeroides RsCryB, with a eukaryotic (6-4) photolyase from Ostreococcus, OsCPF, and a member of the class III CPD photolyases, PhrA from A.fabrum. We found that the low DNA repair effectivity of FeS-BCP proteins is largely stimulated by Mg2+ and other divalent cations, whereas no effect of divalent cations was observed in OsCPF and PhrA. The (6-4) repair activity in the presence of Mg2+ is comparable with the repair activities of the other two photolyases. The photoreduction, on the other hand, is negatively affected by Mg2+ in PhrB, but stimulated by Mg2+ in PhrA. A clear relationship of Mg2+ dependency on DNA repair with the evolutionary position conflicts with Mg2+ dependency of photoreduction. We discuss the Mg2+ effect in the context of structural data and DNA binding.

Artificial selection on ant female caste ratio uncovers a link between female-biased sex ratios and infection by Wolbachia endosymbionts.

Social insect sex and caste ratios are well-studied targets of evolutionary conflicts, but the heritable factors affecting these traits remain unknown. To elucidate these factors, we carried out a short-term artificial selection study on female caste ratio in the ant Monomorium pharaonis. Across three generations of bidirectional selection, we observed no response for caste ratio, but sex ratios rapidly became more female-biased in the two replicate high selection lines and less female-biased in the two replicate low selection lines. We hypothesized that this rapid divergence for sex ratio was caused by changes in the frequency of infection by the heritable bacterial endosymbiont Wolbachia, because the initial breeding stock varied for Wolbachia infection, and Wolbachia is known to cause female-biased sex ratios in other insects. Consistent with this hypothesis, the proportions of Wolbachia-infected colonies in the selection lines changed rapidly, mirroring the sex ratio changes. Moreover, the estimated effect of Wolbachia on sex ratio (~13% female bias) was similar in colonies before and during artificial selection, indicating that this Wolbachia effect is likely independent of the effects of artificial selection on other heritable factors. Our study provides evidence for the first case of endosymbiont sex ratio manipulation in a social insect.

An Evolutionary Genetic Perspective on Cancer Biology

Cancer biology can be better understood by drawing upon methods and concepts from evolutionary genetics. Cancer progression proceeds through somatic evolution, being driven by selection on clonal lineages via the differential survival and proliferation of cell lines. This within-patient evolution can be modeled and analyzed using population genetic and phylogenetic tools to identify mutations and genotypes that are under directional selection during tumor growth, spatial differentiation, and metastasis. Evolutionary genetics can also explain the persistence of cancer within populations. A minority of cancers are associated with inherited risk alleles, which are maintained in populations through genetic drift or antagonistic pleiotropy. Finally, cancer biology can be understood from a macroevolutionary perspective as a case study of evolutionary cooperation and conflict between different levels of biological organization.

Transposable elements: Self-seekers of the germline, team-players of the soma.

The germ track is the cellular path by which genes are transmitted to future generations whereas somatic cells die with their body and do not leave direct descendants. Transposable elements (TEs) evolve to be silent in somatic cells but active in the germ track. Thus, the performance of most bodily functions by a sequestered soma reduces organismal costs of TEs. Flexible forms of gene regulation are permissible in the soma because of the self-imposed silence of TEs, but strict licensing of transcription and translation is maintained in the germ track to control proliferation of TEs. Delayed zygotic genome activation (ZGA) and maternally inherited germ granules are adaptations that enhance germ-track security. Mammalian embryos exhibit very early ZGA associated with extensive mobilization of retroelements. This window of vulnerability to retrotransposition in early embryos is an indirect consequence of evolutionary conflicts within the mammalian genome over postzygotic maternal provisioning.

Cooperation-mediated plasticity in dispersal and colonization.

Kin selection theory predicts that costly cooperative behaviors evolve most readily when directed toward kin. Dispersal plays a controversial role in the evolution of cooperation: dispersal decreases local population relatedness and thus opposes the evolution of cooperation, but limited dispersal increases kin competition and can negate the benefits of cooperation. Theoretical work has suggested that plasticity of dispersal, where individuals can adjust their dispersal decisions according to the social context, might help resolve this paradox and promote the evolution of cooperation. Here, we experimentally tested the hypothesis that conditional dispersal decisions are mediated by a cooperative strategy: we quantified the density-dependent dispersal decisions and subsequent colonization efficiency from single cells or groups of cells among six genetic strains of the unicellular Tetrahymena thermophila that differ in their aggregation level (high, medium, and low), a behavior associated with cooperation strategy. We found that the plastic reaction norms of dispersal rate relative to density differed according to aggregation level: highly aggregative genotypes showed negative density-dependent dispersal, whereas low-aggregation genotypes showed maximum dispersal rates at intermediate density, and medium-aggregation genotypes showed density-independent dispersal with intermediate dispersal rate. Dispersers from highly aggregative genotypes had specialized long-distance dispersal phenotypes, contrary to low-aggregation genotypes; medium-aggregation genotypes showing intermediate dispersal phenotype. Moreover, highly aggregation genotypes showed evidence for beneficial kin-cooperation during dispersal. Our experimental results should help to resolve the evolutionary conflict between cooperation and dispersal: cooperative individuals are expected to avoid kin-competition by dispersing long distances, but maintain the benefits of cooperation by dispersing in small groups.

Nuclear-mitochondrial epistasis: a gene's eye view of genomic conflict.

We use population genetic models to investigate the cooperative and conflicting synergistic fitness effects between genes from the nucleus and the mitochondrion. By varying fitness parameters, we examine the scope for conflict relative to cooperation among genomes and the utility of the “gene's eye view” analytical approach, which is based on the marginal average fitness of specific alleles. Because sexual conflict can maintain polymorphism of mitochondrial haplotypes, we can explore two types of evolutionary conflict (genomic and sexual) with one epistatic model. We find that the nuclear genetic architecture (autosomal, X‐linked, or Z‐linked) and the mating system change the regions of parameter space corresponding to the evolution by sexual and genomic conflict. For all models, regardless of conflict or cooperation, we find that population mean fitness increases monotonically as evolution proceeds. Moreover, we find that the process of gene frequency change with positive, synergistic fitnesses is self‐accelerating, as the success of an allele in one genome or in one sex increases the frequency of the interacting allele upon which its success depends. This results in runaway evolutionary dynamics caused by the positive intergenomic associations generated by selection. An inbreeding mating system tends to further accelerate these runaway dynamics because it maintains favorable host–symbiont or male–female gene combinations. In contrast, where conflict predominates, the success of an allele in one genome or in one sex diminishes the frequency of the corresponding allele in the other, resulting in considerably slower evolutionary dynamics. The rate of change of mean fitness is also much faster with positive, synergistic fitnesses and much slower where conflict is predominant. Consequently, selection rapidly fixes cooperative gene combinations, while leaving behind a slowing evolving residue of conflicting gene combinations at mutation–selection balance. We discuss how an emphasis on marginal fitness averages may obscure the interdependence of allelic fitness across genomes, making the evolutionary trajectories appear independent of one another when they are not.

Evolutionary Conflict Between Maternal and Paternal Interests: Integration with Evolutionary Endocrinology.

Conflict between mates, as well as conflict between parents and offspring are due to divergent evolutionary interests of the interacting individuals. Hormone systems provide genetically based proximate mechanisms for mediating phenotypic adaptation and maladaptation characteristic of evolutionary conflict between individuals. Testosterone (T) is among the most commonly studied hormones in evolutionary biology, and as such, its role in shaping sexually dimorphic behaviors and physiology is relatively well understood, but its role in evolutionary conflict is not as clear. In this review, we outline the genomic conflicts arising within the family unit, and incorporate multiple lines of evidence from the bank vole (Myodes glareolus) system to outline how T impacts traits associated with reproduction and survival, resulting in a sexually antagonistic genetic trade-off in fitness. A major prediction arising from this work is that lower T is favored in females, whereas the optimal T level in males fluctuates in relation to social and ecological factors. We additionally discuss future directions to further integrate endocrinology into the study of sexual and parent-offspring conflicts.

Antimicrobial Functions of Lactoferrin Promote Genetic Conflicts in Ancient Primates and Modern Humans.

Lactoferrin is a multifunctional mammalian immunity protein that limits microbial growth through sequestration of nutrient iron. Additionally, lactoferrin possesses cationic protein domains that directly bind and inhibit diverse microbes. The implications for these dual functions on lactoferrin evolution and genetic conflicts with microbes remain unclear. Here we show that lactoferrin has been subject to recurrent episodes of positive selection during primate divergence predominately at antimicrobial peptide surfaces consistent with long-term antagonism by bacteria. An abundant lactoferrin polymorphism in human populations and Neanderthals also exhibits signatures of positive selection across primates, linking ancient host-microbe conflicts to modern human genetic variation. Rapidly evolving sites in lactoferrin further correspond to molecular interfaces with opportunistic bacterial pathogens causing meningitis, pneumonia, and sepsis. Because microbes actively target lactoferrin to acquire iron, we propose that the emergence of antimicrobial activity provided a pivotal mechanism of adaptation sparking evolutionary conflicts via acquisition of new protein functions.

Parents face quantity-quality trade-offs between reproduction and investment in offspring in Iceland.

How to optimally allocate time, energy and investment in an effort to maximize one's reproductive success is a fundamental problem faced by all organisms. This effort is complicated when the production of each additional offspring dilutes the total resources available for parental investment. Although a quantity–quality trade-off between producing and investing in offspring has long been assumed in evolutionary biology, testing it directly in humans is difficult, partly owing to the long generation time of our species. Using data from an Icelandic genealogy (Íslendingabók) over two centuries, I address this issue and analyse the quantity–quality trade-off in humans. I demonstrate that the primary impact of parents on the fitness of their children is the result of resources and or investment, but not genes. This effect changes significantly across time, in response to environmental conditions. Overall, increasing reproduction has negative fitness consequences on offspring, such that each additional sibling reduces an individual's average lifespan and lifetime reproductive success. This analysis provides insights into the evolutionary conflict between producing and investing in children while also shedding light on some of the causes of the demographic transition.

Interspecific Interactions and the Scope for Parent-Offspring Conflict: High Mite Density Temporarily Changes the Trade-Off between Offspring Size and Number in the Burying Beetle, Nicrophorus vespilloides.

Parents have a limited amount of resources to invest in reproduction and commonly trade-off how much they invest in offspring size (or quality) versus brood size. A negative relationship between offspring size and number has been shown in numerous taxa and it underpins evolutionary conflicts of interest between parents and their young. For example, previous work on vertebrates shows that selection favours mothers that produce more offspring, at the expense of individual offspring size, yet favours offspring that have relatively few siblings and therefore attain a greater size at independence. Here we analyse how this trade-off is temporarily affected by stochastic variation in the intensity of interspecific interactions. We examined the effect of the mite Poecilochirus carabi on the relationship between offspring size and number in the burying beetle, Nicrophorus vespilloides. We manipulated the initial number of mites in the reproductive event (by introducing either no mites, 4 mites, 10 mites, or 16 mites), and assessed the effect on the brood. We found a similar trade-off between offspring size and number in all treatments, except in the '16 mite' treatment where the correlation between offspring number and size flattened considerably. This effect arose because larvae in small broods failed to attain a high mass by dispersal. Our results show that variation in the intensity of interspecific interactions can temporarily change the strength of the trade-off between offspring size and number. In this study, high densities of mites prevented individual offspring from attaining their optimal weight, thus potentially temporarily biasing the outcome of parent-offspring conflict in favour of parents.

Contrasting effects of intralocus sexual conflict on sexually antagonistic coevolution

Evolutionary conflict between the sexes can induce arms races in which males evolve traits that are detrimental to the fitness of their female partners, and vice versa. This interlocus sexual conflict (IRSC) has been proposed as a cause of perpetual intersexual antagonistic coevolution with wide-ranging evolutionary consequences. However, theory suggests that the scope for perpetual coevolution is limited, if traits involved in IRSC are subject to pleiotropic constraints. Here, we consider a biologically plausible form of pleiotropy that has hitherto been ignored in treatments of IRSC and arrive at drastically different conclusions. Our analysis is based on a quantitative genetic model of sexual conflict, in which genes controlling IRSC traits have side effects in the other sex, due to incompletely sex-limited gene expression. As a result, the genes are exposed to intralocus sexual conflict (IASC), a tug-of-war between opposing male- and female-specific selection pressures. We find that the interaction between the two forms of sexual conflict has contrasting effects on antagonistic coevolution: Pleiotropic constraints stabilize the dynamics of arms races if the mating traits are close to evolutionary equilibrium but can prevent populations from ever reaching such a state. Instead, the sexes are drawn into a continuous cycle of arms races, causing the buildup of IASC, alternated by phases of IASC resolution that trigger the next arms race. These results encourage an integrative perspective on the biology of sexual conflict and generally caution against relying exclusively on equilibrium stability analysis.

Coevolution of the Organization and Structure of Prokaryotic Genomes.

The cytoplasm of prokaryotes contains many molecular machines interacting directly with the chromosome. These vital interactions depend on the chromosome structure, as a molecule, and on the genome organization, as a unit of genetic information. Strong selection for the organization of the genetic elements implicated in these interactions drives replicon ploidy, gene distribution, operon conservation, and the formation of replication-associated traits. The genomes of prokaryotes are also very plastic with high rates of horizontal gene transfer and gene loss. The evolutionary conflicts between plasticity and organization lead to the formation of regions with high genetic diversity whose impact on chromosome structure is poorly understood. Prokaryotic genomes are remarkable documents of natural history because they carry the imprint of all of these selective and mutational forces. Their study allows a better understanding of molecular mechanisms, their impact on microbial evolution, and how they can be tinkered in synthetic biology.

A Biological "Arms Race": APOBEC3F Diversity and its Influence on Lentiviral Resistance

Restriction factors are implemented in long-term evolutionary "arms races," in which viral antagonists drive the evolution of host proteins, and vice versa. Consequently, restriction factors are remarkably variable, displaying polymorphism within species and divergence between species as a result of positive selection. This paper investigates diversity in the APOBEC3F (A3F) restriction factors of Old World primates in order to determine whether they display evidence of involvement in an evolutionary "arms race." We speculated that genetic variability in A3F could reflect evolutionary conflict with the VIF proteins of primate lentiviruses, which are known to enhance viral replication by binding and degrading host A3 proteins. A3Fs of several Old World primate species were genotyped, and the sequences revealed both intra-spcies diversity and inter-species divergence. Representative rhesus macaque (<em>macaca mulatta</em>) sequences were cloned and tested for sensitivity to VIFs from various simin immunodeficiency viruses (SIVs). Evolution of A3F in the rhesus lineage is not due to selection by SIVs, but may reflect antagonism by another retrovirus.

Control of parental investment changes plastically over time with residual reproductive value.

Evolutionary conflict between parents and offspring over parental resource investment is a significant selective force on the traits of both parents and offspring. Empirical studies have shown that for some species, the amount of parental investment is controlled by the parents, whereas in other species, it is controlled by the offspring. The main difference between these two strategies is the residual reproductive value of the parents or opportunities for future reproduction. Therefore, this could explain the patterns of control of parental investment at the species level. However, the residual reproductive value of the parents will change during their lifetime; therefore, parental influence on the amount of investment can be expected to change plastically. Here, we investigated control of parental investment when parents were young and had a high residual reproductive value, compared to when they were old and had a low residual reproductive value using a cross-fostering experiment in the burying beetle Nicrophorus quadripunctatus. We found that parents exert greater control over parental investment when they are young, but parental control is weakened as the parents age. Our results demonstrate that control of parental investment is not fixed, but changes plastically during the parent's lifetime.

The constant philopater hypothesis: a new life history invariant for dispersal evolution.

Surprising invariance relationships have emerged from the study of social interaction, whereby a cancelling‐out of multiple partial effects of genetic, ecological or demographic parameters means that they have no net impact upon the evolution of a social behaviour. Such invariants play a pivotal role in the study of social adaptation: on the one hand, they provide theoretical hypotheses that can be empirically tested; and, on the other hand, they provide benchmark frameworks against which new theoretical developments can be understood. Here we derive a novel invariant for dispersal evolution: the ‘constant philopater hypothesis’ (CPH). Specifically, we find that, irrespective of variation in maternal fecundity, all mothers are favoured to produce exactly the same number of philopatric offspring, with high‐fecundity mothers investing proportionally more, and low‐fecundity mothers investing proportionally less, into dispersing offspring. This result holds for female and male dispersal, under haploid, diploid and haplodiploid modes of inheritance, irrespective of the sex ratio, local resource availability and whether mother or offspring controls the latter's dispersal propensity. We explore the implications of this result for evolutionary conflict of interests – and the exchange and withholding of contextual information – both within and between families, and we show that the CPH is the fundamental invariant that underpins and explains a wider family of invariance relationships that emerge from the study of social evolution.

Intergenomic interactions between mitochondrial and Y-linked genes shape male mating patterns and fertility in Drosophila melanogaster.

Under maternal inheritance, mitochondrial genomes are prone to accumulate mutations that exhibit male-biased effects. Such mutations should, however, place selection on the nuclear genome for modifier adaptations that mitigate mitochondrial-incurred male harm. One gene region that might harbor such modifiers is the Y-chromosome, given the abundance of Y-linked variation for male fertility, and because Y-linked modifiers would not exert antagonistic effects in females because they would be found only in males. Recent studies in Drosophila revealed a set of nuclear genes whose expression is sensitive to allelic variation among mtDNA- and Y-haplotypes, suggesting these genes might be entwined in evolutionary conflict between mtDNA and Y. Here, we test whether genetic variation across mtDNA and Y haplotypes, sourced from three disjunct populations, interacts to affect male mating patterns and fertility across 10 days of early life in D. melanogaster. We also investigate whether coevolved mito-Y combinations outperform their evolutionarily novel counterparts, as predicted if the interacting Y-linked variance is comprised of modifier adaptations. Although we found no evidence that coevolved mito-Y combinations outperformed their novel counterparts, interactions between mtDNA and Y-chromosomes affected male mating patterns. These interactions were dependent on male age; thus male reproductive success was shaped by G × G × E interactions.

Rumbling Orchids: How To Assess Divergent Evolution Between Chloroplast Endosymbionts and the Nuclear Host.

Phylogenetic relationships inferred from multilocus organellar and nuclear DNA data are often difficult to resolve because of evolutionary conflicts among gene trees. However, conflicting or "outlier" associations (i.e., linked pairs of "operational terminal units" in two phylogenies) among these data sets often provide valuable information on evolutionary processes such as chloroplast capture following hybridization, incomplete lineage sorting, and horizontal gene transfer. Statistical tools that to date have been used in cophylogenetic studies only also have the potential to test for the degree of topological congruence between organellar and nuclear data sets and reliably detect outlier associations. Two distance-based methods, namely ParaFit and Procrustean Approach to Cophylogeny (PACo), were used in conjunction to detect those outliers contributing to conflicting phylogenies independently derived from chloroplast and nuclear sequence data. We explored their efficiency of retrieving outlier associations, and the impact of input data (unit branch length and additive trees) between data sets, by using several simulation approaches. To test their performance using real data sets, we additionally inferred the phylogenetic relationships within Neotropical Catasetinae (Epidendroideae, Orchidaceae), which is a suitable group to investigate phylogenetic incongruence because of hybridization processes between some of its constituent species. A comparison between trees derived from chloroplast and nuclear sequence data reflected strong, well-supported incongruence within Catasetum, Cycnoches, and Mormodes. As a result, outliers among chloroplast and nuclear data sets, and in experimental simulations, were successfully detected by PACo when using patristic distance matrices obtained from phylograms, but not from unit branch length trees. The performance of ParaFit was overall inferior compared to PACo, using either phylograms or unit branch lengths as input data. Because workflows for applying cophylogenetic analyses are not standardized yet, we provide a pipeline for executing PACo and ParaFit as well as displaying outlier associations in plots and trees by using the software R. The pipeline renders a method to identify outliers with high reliability and to assess the combinability of the independently derived data sets by means of statistical analyses.

Friend or foe: inter-specific interactions and conflicts of interest within the family.

1. Interactions between species can vary from mutually beneficial to evolutionarily neutral to antagonistic, even when the same two species are involved. Similarly, social interactions between members of the same species can lie on a spectrum from conflict to cooperation.2. The aim of the present study was to investigate whether variation in the two types of social behaviour are interconnected. Is the fitness of the various classes of social partner within species (such as parent and offspring, or male and female) differently affected by interactions with a second species? Moreover, can inter‐specific interactions influence the outcome of social interactions within species?3. The present experiments focus on the interactions between the burying beetle Nicrophorus vespilloides Herbst and the phoretic mite Poecilochirus carabi G. Canestrini & R. Canestrini. The approach was to measure the fitness of burying beetle mothers, fathers, and offspring after reproduction, which took place either in the presence or absence of mites.4. We found that male, female, and larval burying beetles derive contrasting fitness costs and benefits from their interactions with the mite, despite sharing a common family environment. From the mite's perspective, its relationship with the burying beetle can, therefore, be simultaneously antagonistic, neutral, and possibly even mutualistic, depending on the particular family member involved. We also found that mites can potentially change the outcome of evolutionary conflicts within the family.5. We conclude that inter‐specific interactions can explain some of the variation in social interactions seen within species. It is further suggested that intra‐specific interactions might contribute to variation in the outcome of interactions between species.

Reproductive mode and the shifting arenas of evolutionary conflict.

In sexually reproducing organisms, the genetic interests of individuals are not perfectly aligned. Conflicts among family members are prevalent since interactions involve the transfer of limited resources between interdependent players. Intrafamilial conflict has traditionally been considered along three major axes: between the sexes, between parents and offspring, and between siblings. In these interactions, conflict is expected over traits in which the resulting phenotypic value is determined by multiple family members who have only partially overlapping fitness optima. We focus on four major categories of animal reproductive mode (broadcast spawning, egg laying, live bearing, and live bearing with matrotrophy) and identify the shared phenotypes or traits over which conflict is expected, and then review the empirical literature for evidence of their occurrence. Major transitions among reproductive mode, such as a shift from external to internal fertilization, an increase in egg-retention time, modifications of embryos and mothers for nutrient transfer, the evolution of postnatal parental care, and increased interaction with the kin network, mark key shifts that both change and expand the arenas in which conflict is played out.