Evolutionary Conflict Research Articles

The resolution of evolutionary conflicts within species.

Evolutionary conflicts of interest occur at all levels, scales and forms of biological organization. They are a fundamental component of the living world and range from conflicts between genetic elements and cells, to conflicts between the sexes and between competing individuals. Yet, the existence of admirably well functioning genomes, bodies, mating pairs and societies suggests that processes must exist to resolve or mitigate such conflicts. We organized this special feature 'The resolution of evolutionary conflicts within species' to encourage the flow of knowledge between fields that traditionally have often taken different approaches to study evolutionary conflicts. Contributed papers discuss data from bacteria, plants and animals (including humans) and present theory, molecular mechanisms and population dynamics of how conflicts are resolved in nature. Together, they contribute to a synthetic theory of conflict resolution.

The role of conflict in the formation and maintenance of variant sex chromosome systems in mammals.

The XX/XY sex chromosome system is deeply conserved in therian mammals, as is the role of Sry in testis determination, giving the impression of stasis relative to other taxa. However, the long tradition of cytogenetic studies in mammals documents sex chromosome karyotypes that break this norm in myriad ways, ranging from fusions between sex chromosomes and autosomes to Y chromosome loss. Evolutionary conflict, in the form of sexual antagonism or meiotic drive, is the primary predicted driver of sex chromosome transformation and turnover. Yet conflict-based hypotheses are less considered in mammals, perhaps because of the perceived stability of the sex chromosome system. To address this gap, we catalogue and characterize all described sex chromosome variants in mammals, test for family-specific rates of accumulation, and consider the role of conflict between the sexes or within the genome in the evolution of these systems. We identify 152 species with sex chromosomes that differ from the ancestral state and find evidence for different rates of ancestral to derived transitions among families. Sex chromosome-autosome fusions account for 80% of all variants whereas documented sex chromosome fissions are limited to three species. We propose that meiotic drive and drive suppression provide viable explanations for the evolution of many of these variant systems, particularly those involving autosomal fusions. We highlight taxa particularly worthy of further study and provide experimental predictions for testing the role of conflict and its alternatives in generating observed sex chromosome diversity.

The roles of gene duplications in the dynamics of evolutionary conflicts.

Evolutionary conflicts occur when there is antagonistic selection between different individuals of the same or different species, life stages or between levels of biological organization. Remarkably, conflicts can occur within species or within genomes. In the dynamics of evolutionary conflicts, gene duplications can play a major role because they can bring very specific changes to the genome: changes in protein dose, the generation of novel paralogues with different functions or expression patterns or the evolution of small antisense RNAs. As we describe here, by having those effects, gene duplication might spark evolutionary conflict or fuel arms race dynamics that takes place during conflicts. Interestingly, gene duplication can also contribute to the resolution of a within-locus evolutionary conflict by partitioning the functions of the gene that is under an evolutionary trade-off. In this review, we focus on intraspecific conflicts, including sexual conflict and illustrate the various roles of gene duplications with a compilation of examples. These examples reveal the level of complexity and the differences in the patterns of gene duplications within genomes under different conflicts. These examples also reveal the gene ontologies involved in conflict and the genomic location of the elements of the conflict. The examples provide a blueprint for the direct study of these conflicts or the exploration of the presence of similar conflicts in other lineages.

Hybridization constrains the evolution of mimicry complexes in woodpeckers

The evolution of interspecific mimicry does not always result in perfect resemblance between mimics and models. Differences between members of a mimicry complex can be explained by genetic or developmental constraints. Alternatively, imperfect mimicry might be the outcome of a tradeoff between multiple selective pressures. In this study, we explored the evolutionary conflict between mimicry and hybridization in woodpeckers. Based on the selective tradeoff hypothesis, we expected that mimicry complexes will start to evolve once the constraint of maladaptive hybridization is relaxed. Hence, we predicted limited overlap in the divergence times between hybridizing species pairs and members of a mimicry complex. This prediction was supported by clear tipping point in the probability of hybridization and mimicry at ca 9 million years of divergence. Around this timepoint, the probability of hybridization approaches zero while the probability of belonging to a mimicry complex increases. This finding is only correlational and remains to be confirmed in other taxonomic groups. Nonetheless, our results suggest a selective tradeoff between evolving interspecific mimicry and avoiding maladaptive hybridization in woodpeckers.

The nuclear pore protein NUP98 impedes LTR-driven basal gene expression of HIV-1, viral propagation, and infectivity.

Nucleoporins (NUPs) are cellular effectors of human immunodeficiency virus-1 (HIV-1) replication that support nucleocytoplasmic trafficking of viral components. However, these also non-canonically function as positive effectors, promoting proviral DNA integration into the host genome and viral gene transcription, or as negative effectors by associating with HIV-1 restriction factors, such as MX2, inhibiting the replication of HIV-1. Here, we investigated the regulatory role of NUP98 on HIV-1 as we observed a lowering of its endogenous levels upon HIV-1 infection in CD4+ T cells. Using complementary experiments in NUP98 overexpression and knockdown backgrounds, we deciphered that NUP98 negatively affected HIV-1 long terminal repeat (LTR) promoter activity and lowered released virus levels. The negative effect on promoter activity was independent of HIV-1 Tat, suggesting that NUP98 prevents the basal viral gene expression. ChIP-qPCR showed NUP98 to be associated with HIV-1 LTR, with the negative regulatory element (NRE) of HIV-1 LTR playing a dominant role in NUP98-mediated lowering of viral gene transcription. Truncated mutants of NUP98 showed that the attenuation of HIV-1 LTR-driven transcription is primarily contributed by its N-terminal region. Interestingly, the virus generated from the producer cells transiently expressing NUP98 showed lower infectivity, while the virus generated from NUP98 knockdown CD4+ T cells showed higher infectivity as assayed in TZM-bl cells, corroborating the anti-HIV-1 properties of NUP98. Collectively, we show a new non-canonical function of a nucleoporin adding to the list of moonlighting host factors regulating viral infections. Downregulation of NUP98 in a host cell upon HIV-1 infection supports the concept of evolutionary conflicts between viruses and host antiviral factors.

The spectre of chloroquine—evolutionary conflict at the molecular level in a Plasmodium falciparum multidrug resistance protein

The spectre of chloroquine—evolutionary conflict at the molecular level in a Plasmodium falciparum multidrug resistance protein

Journalistic Practices in Difficult Times: The Cases of Fictional Television Series Borgen and El Caso in Denmark and Spain

This study sets out to understand how journalism is represented in the Danish fiction series Borgen and the Spanish series El Caso: Crónica de Sucesos. The aim is to provide an understanding of how journalism is conceptualized in non-American fiction. Through textual analysis, we found out that Borgen (years 2010 and up) represents a generational and evolutionary conflict in which journalistic values are restrained by political and commercial imperatives reflecting challenges in Danish journalism. As such, this series criticizes the free press myth—commonly found in American fiction series. El Caso (1960s) also engages with this myth through the representation of journalism practices embedded in Spain’s Francoist regime that balance public and political-religious interests. However, El Caso smooths over this conflict to illustrate how journalists cleverly overcame the censorship of the Catholic church. Both series explore the gendered and cultural obstacles of their respective contexts and eras.

Uncloaking the viral glycocalyx: How do viruses exploit glycoimmune checkpoints?

The surfaces of cells and enveloped viruses alike are coated in carbohydrates that play multifarious roles in infection and immunity. Organisms across all kingdoms of life make use of a diverse set of monosaccharide subunits, glycosidic linkages, and branching patterns to encode information within glycans. Accordingly, sugar-patterning enzymes and glycan binding proteins play integral roles in cell and organismal biology, ranging from glycoprotein quality control within the endoplasmic reticulum to lymphocyte migration, coagulation, inflammation, and tissue homeostasis. Unsurprisingly, genes involved in generating and recognizing oligosaccharide patterns are playgrounds for evolutionary conflicts that abound in cross-species interactions, exemplified by the myriad plant lectins that function as toxins. In vertebrates, glycans bearing acidic nine-carbon sugars called sialic acids are key regulators of immune responses. Various bacterial and fungal pathogens adorn their cells in sialic acids that either mimic their hosts' or are stolen from them. Yet, how viruses commandeer host sugar-patterning enzymes to thwart immune responses remains poorly studied. Here, we review examples of viruses that interact with sialic acid-binding immunoglobulin-like lectins (Siglecs), a family of immune cell receptors that regulate toll-like receptor signaling and govern glycoimmune checkpoints, while highlighting knowledge gaps that merit investigation. Efforts to illuminate how viruses leverage glycan-dependent checkpoints may translate into new clinical treatments that uncloak viral antigens and infected cell surfaces by removing or masking immunosuppressive sialoglycans, or by inhibiting viral gene products that induce their biosynthesis. Such approaches may hold the potential to unleash the immune system to clear long intractable chronic viral infections.

ORPA: a fast and efficient phylogenetic analysis method for constructing genome-wide alignments of organelle genomes

Creating a multi-gene alignment matrix for phylogenetic analysis using organelle genomes involves aligning single-gene datasets manually, a process that can be time-consuming and prone to errors. The HomBlocks pipeline has been created to eliminate the inaccuracies arising from manual operations. The processing of a large number of sequences, however, remains a time-consuming task. To conquer this challenge, we develop a speedy and efficient method called Organelle Genomes for Phylogenetic Analysis (ORPA). ORPA can quickly generate multiple sequence alignments for whole-genome comparisons by parsing the result files of NCBI BLAST, completing the task just in 1 min. With increasing data volume, the efficiency of ORPA is even more pronounced, over 300 times faster than HomBlocks in aligning 60 high-plant chloroplast genomes. The phylogenetic tree outputs from ORPA are equivalent to HomBlocks, indicating its outstanding efficiency. Due to its speed and accuracy, ORPA can identify species-level evolutionary conflicts, providing valuable insights into evolutionary cognition.

Competitive interference among rhizobia reduces benefits to hosts.

The capacity of beneficial microbes to compete for host infection-and the ability of hosts to discriminate among them-introduces evolutionary conflict that is predicted to destabilize mutualism. We investigated fitness outcomes in associations between legumes and their symbiotic rhizobia to characterize fitness impacts of microbial competition. Diverse Bradyrhizobium strains varying in their capacity to fix nitrogen symbiotically with a common host plant, Acmispon strigosus, were tested in full-factorial coinoculation experiments involving 28 pairwise strain combinations. We analyzed the effects of interstrain competition and host discrimination on symbiotic-interaction outcomes by relativizing fitness proxies to clonally infected and uninfected controls. More than one thousand root nodules of coinoculated plants were genotyped to quantify strain occupancy, and the Bradyrhizobium strain genome sequences were analyzed to uncover the genetic bases of interstrain competition outcomes. Strikingly, interstrain competition favored a fast-growing, minimally beneficial rhizobia strain. Host benefits were significantly diminished in coinoculation treatments relative to expectations from clonally inoculated controls, consistent with competitive interference among rhizobia that reduced both nodulation and plant growth. Competition traits appear polygenic, linked with inter-strain allelopathic interactions in the rhizosphere. This study confirms that competition among strains can destabilize mutualism by favoring microbes that are superior in colonizing host tissues but provide minimal benefits to host plants. Moreover, our findings help resolve the paradox that despite efficient host control post infection, legumes nonetheless encounter rhizobia that vary in their nitrogen fixation.

Seasonal specialization drives divergent population dynamics in two closely related butterflies

Seasons impose different selection pressures on organisms through contrasting environmental conditions. How such seasonal evolutionary conflict is resolved in organisms whose lives span across seasons remains underexplored. Through field experiments, laboratory work, and citizen science data analyses, we investigate this question using two closely related butterflies (Pieris rapae and P. napi). Superficially, the two butterflies appear highly ecologically similar. Yet, the citizen science data reveal that their fitness is partitioned differently across seasons. Pieris rapae have higher population growth during the summer season but lower overwintering success than do P. napi. We show that these differences correspond to the physiology and behavior of the butterflies. Pieris rapae outperform P. napi at high temperatures in several growth season traits, reflected in microclimate choice by ovipositing wild females. Instead, P. rapae have higher winter mortality than do P. napi. We conclude that the difference in population dynamics between the two butterflies is driven by seasonal specialization, manifested as strategies that maximize gains during growth seasons and minimize harm during adverse seasons, respectively.

Adaptation in the face of internal conflict: the paradox of the organism revisited.

The paradox of the organism refers to the observation that organisms appear to function as coherent purposeful entities, despite the potential for within-organismal components like selfish genetic elements and cancer cells to erode them from within. While it is commonly accepted that organisms may pursue fitness maximisation and can be thought to hold particular agendas, there is a growing recognition that genes and cells do so as well. This can lead to evolutionary conflicts between an organism and the parts that reside within it. Here, we revisit the paradox of the organism. We first outline its conception and relationship to debates about adaptation in evolutionary biology. Second, we review the ways selfish elements may exploit organisms, and the extent to which this threatens organismal integrity. To this end, we introduce a novel classification scheme that distinguishes between selfish elements that seek to distort transmission versus those that seek to distort phenotypic traits. Our classification scheme also highlights how some selfish elements elude a multi-level selection decomposition using the Price equation. Third, we discuss how the organism can retain its status as the primary fitness-maximising agent in the face of selfish elements. The success of selfish elements is often constrained by their strategy and further limited by a combination of fitness alignment and enforcement mechanisms controlled by the organism. Finally, we argue for the need for quantitative measures of both internal conflicts and organismality.

Cheating leads to the evolution of multipartite viruses.

In multipartite viruses, the genome is split into multiple segments, each of which is transmitted via a separate capsid. The existence of multipartite viruses poses a problem, because replication is only possible when all segments are present within the same host. Given this clear cost, why is multipartitism so common in viruses? Most previous hypotheses try to explain how multipartitism could provide an advantage. In so doing, they require scenarios that are unrealistic and that cannot explain viruses with more than 2 multipartite segments. We show theoretically that selection for cheats, which avoid producing a shared gene product, but still benefit from gene products produced by other genomes, can drive the evolution of both multipartite and segmented viruses. We find that multipartitism can evolve via cheating under realistic conditions and does not require unreasonably high coinfection rates or any group-level benefit. Furthermore, the cheating hypothesis is consistent with empirical patterns of cheating and multipartitism across viruses. More broadly, our results show how evolutionary conflict can drive new patterns of genome organisation in viruses and elsewhere.

Volatiles of fungal cultivars act as cues for host-selection in the fungus-farming ambrosia beetle Xylosandrus germanus.

Many wood-boring insects use aggregation pheromones during mass colonization of host trees. Bark beetles (Curculionidae: Scolytinae) are a model system, but much less is known about the role of semiochemicals during host selection by ambrosia beetles. As an ecological clade within the bark beetles, ambrosia beetles are obligately dependent on fungal mutualists for their sole source of nutrition. Mass colonization of trees growing in horticultural settings by exotic ambrosia beetles can occur, but aggregation cues have remained enigmatic. To elucidate this mechanism, we first characterized the fungal associates of the exotic, mass-aggregating ambrosia beetle Xylosandrus germanus in Southern Germany. Still-air olfactometer bioassays documented the attraction of X. germanus to its primary nutritional mutualist Ambrosiella grosmanniae and to a lesser extent another common fungal isolate (Acremonium sp.). During two-choice bioassays, X. germanus was preferentially attracted to branch sections (i.e., bolts) that were either pre-colonized by conspecifics or pre-inoculated with A. grosmanniae. Subsequent analyses identified microbial volatile organic compounds (MVOCs) that could potentially function as aggregation pheromones for X. germanus. To our knowledge, this is the first evidence for fungal volatiles as attractive cues during host selection by X. germanus. Adaptive benefits of responding to fungal cues associated with an infestation of conspecifics could be a function of locating a suitable substrate for cultivating fungal symbionts and/or increasing the likelihood of mating opportunities with the flightless males. However, this requires solutions for evolutionary conflict arising due to potential mixing of vertically transmitted and horizontally acquired symbiont strains, which are discussed.

Evolution of parental roles in phase portraits of bimatrix asymmetric games

In this paper, we address the evolutionary dynamic of parental roles using game theory. The main purpose of the article was to expand a classical list of evolutionary dynamic parental conflicts by adding some important cases which hitherto have not been intensively studied. Our models are apt to deliver some novel insights into the evolution of parental care. We also introduced several hypothetical events that served as illustrations of an arising alteration in cost-benefits for both parents and simulated a subsequent evolutionary endpoint. Our models revealed that evolutionary outcomes for reproductive decisions of both parents could be completely predicted by certain payoff matrices, which serve as proxies for a Darwinian fitness gain. In this sense, the result of a frequency-dependent selection on reproductive traits would inevitably depend on fitness costs and benefits arising for both parents in various circumstances. We demonstrated that population division could be a plausible evolutionary consequence for any human mating game where ‘reproductive defection’ represents the best response to any action by the reproductive opponent. We conclude that future evolutionary studies of human reproductive behavior should be more oriented on estimating a sex-biased asymmetry in potential fitness gains obtained by cooperative and deceptive parents in diverse environments and cultures.

Females adopt sexual catalepsy to facilitate mating.

Theory predicts that males and females of dioecious species typically engage in an evolutionary sexual conflict over the frequency and choice of mating partner. Female sexual cannibalism, a particularly dramatic illustration of this conflict, is widespread in certain animal taxa including spiders. Nevertheless, females of some funnel weaving spiders that are generally aggressive to conspecifics enter a cataleptic state after male courtship, ensuring the males can mate without risk of attack. In this study, we demonstrated that the physical posture and duration, metabolites, and central neurotransmitters of females of Aterigena aculeata in sexual catalepsy closely resemble females in thanatosis but are distinct from those in anesthesia, indicating that the courted females feign death to eliminate the risk of potentially aggressive responses and thereby allow preferred males to mate. Unlike the taxonomically widespread thanatosis, which generally represents a deceptive visual signal that acts against the interest of the receivers, sexual catalepsy of females in the funnel weaving spiders may deliver a sexual-receptive signal to the courting males and thereby benefit both the signal senders and receivers. Therefore, sexual catalepsy in A. aculeata may not reflect a conflict but rather a confluence of interest between the sexes.

The geometry of evolutionary conflict

Conflicts of interest abound not only in human affairs but also in the biological realm. Evolutionary conflict occurs over multiple scales of biological organization, from genetic outlawry within genomes, to sibling rivalry within nuclear families, to collective-action disputes within societies. However, achieving a general understanding of the dynamics and consequences of evolutionary conflict remains an outstanding challenge. Here, we show that a development of R. A. Fisher's classic 'geometric model' of adaptation yields novel and surprising insights into the dynamics of evolutionary conflict and resulting maladaptation, including the discoveries that: (i) conflict can drive evolving traits arbitrarily far away from all parties' optima and, indeed, if all mutations are equally likely then contested traits are more often than not driven outwith the zone of actual conflict (hyper-maladaptation); (ii) evolutionary conflicts drive persistent maladaptation of orthogonal, non-contested traits (para-maladaptation); and (iii) modular design greatly ameliorates conflict-driven maladaptation, thereby facilitating major transitions in individuality.

Testing evolutionary conflict theories for sexual and physical intimate partner violence in Sub-Saharan Africa.

Intimate partner violence (IPV) refers to physical, sexual and psychological violence. Here an evolutionary approach is used to compare risk factors for male-to-female IPV perpetration, analysing physical and sexual IPV separately. Two hypotheses based on sexual conflict theory have been applied to IPV perpetration, but they remain largely untested using empirical data: (a) men perpetrate IPV in response to a perceived threat to their paternity certainty; and (b) IPV is caused by men pursuing a higher fertility optima than their partners, either within marriage (reproductive coercion) or outside marriage (paternal disinvestment). Demographic Health Survey data from couples in 12 sub-Saharan African countries (n = 25,577) were used to test these evolutionary hypotheses, using multilevel models and controlling for potential social and environmental confounds. The results show that evolutionary theory provides important insight into different risk factors by IPV type. Indicators of paternity concern are associated with an increased risk of both physical and sexual IPV, indicators of paternal disinvestment are associated with an increased risk of physical IPV only, while reproductive coercion is not associated with either IPV type. The risk factors identified here correspond with proximate-level explanations for IPV perpetration, but an evolutionary interpretation explains why these particular factors may motivate IPV in certain contexts.

Adaptive duplication and genetic diversification of protein kinase R contribute to the specificity of bat-virus interactions.

Several bat species act as asymptomatic reservoirs for many viruses that are highly pathogenic in other mammals. Here, we have characterized the functional diversification of the protein kinase R (PKR), a major antiviral innate defense system. Our data indicate that PKR has evolved under positive selection and has undergone repeated genomic duplications in bats in contrast to all studied mammals that have a single copy of the gene. Functional testing of the relationship between PKR and poxvirus antagonists revealed how an evolutionary conflict with ancient pathogenic poxviruses has shaped a specific bat host-virus interface. We determined that duplicated PKRs of the Myotis species have undergone genetic diversification, allowing them to collectively escape from and enhance the control of DNA and RNA viruses. These findings suggest that viral-driven adaptations in PKR contribute to modern virus-bat interactions and may account for bat-specific immunity.

Flexible embryonic shell allies large offspring size and anti-predatory protection in viviparous snails

The evolutionary conflicts between viviparous reproductive mode and skeleton shape may occur whenever the space available for embryo development or delivery is limited by hard inflexible structures of a parent (bones, shell, etc.). In tetrapods, offspring size is at odds with female locomotion efficiency, which results in obstetric selection. We suggest a similar relationship for viviparous gastropods, where spacious canal needed for embryo delivery may interfere with anti-predatory role of narrow and toothed shell aperture. We explored this hypothesis in the group of viviparous land snails (Clausiliidae, subfamily Phaedusinae), known for complex apertural barriers protecting the shell interior. Most of the shell structure modifications we recorded facilitate the delivery of embryos but simultaneously reduce the safeguard of a narrow shell opening. However, we also observed highly flexible embryonic shells that may withstand squeezing between apertural barriers during birth. We investigated the microstructure of these flexible embryonic shells, compared to the typical hard shells of clausiliid embryos, which are rigid and unpliable already in the genital tract of the parent. Our results suggest that the unusual flexibility, which is related to a low number of organomineral layers in the shell, evolved in two phylogenetically distant lineages of Phaedusinae. This adaptation reduces mechanical constraints for birth of the neonates but allows to maintain the protective function of the apertural barriers.