Reciprocal Evolutionary Change Research Articles

Inference of host-pathogen interaction matrices from genome-wide polymorphism data.

Host-pathogen coevolution is defined as the reciprocal evolutionary changes in both species due to genotype x genotype (GxG) interactions at the genetic level determining the outcome and severity of infection. While co-analyses of host and pathogen genomes (co-GWAs) allow us to pinpoint the interacting genes, these do not reveal which host genotype(s) is/are resistant to which pathogen genotype(s). The knowledge of this so-called infection matrix is important for agriculture and medicine. Building on established theories of host-pathogen interactions, we here derive four novel indices capturing the characteristics of the infection matrix. These indices can be computed from full genome polymorphism data of randomly sampled uninfected hosts, as well as infected hosts and their pathogen strains. We use these indices in an Approximate Bayesian Computation method to pinpoint loci with relevant GxG interactions and to infer their underlying interaction matrix. In a combined SNP data set of 451 European humans and their infecting Hepatitis C Virus (HCV) strains and 503 uninfected individuals, we reveal a new human candidate gene for resistance to HCV and new virus mutations matching human genes. For two groups of significant human-HCV (GxG) associations, we infer a gene-for-gene infection matrix, which is commonly assumed to be typical of plant-pathogen interactions. Our model-based inference framework bridges theoretical models of GxG interactions with host and pathogen genomic data. It, therefore, paves the way for understanding the evolution of key GxG interactions underpinning HCV adaptation to the European human population after a recent expansion.

Abstract IA006: Co-evolving artificial intelligence and pathology

Abstract A fundamental question in cancer biology is how cancers evolve heterogeneity and treatment resistance. The evolution trajectory of cancer is dictated by selective pressures from treatments and the tumor ecosystem. Artificial intelligence (AI) enables us to directly study geographical patterns of the microenvironment in pathological samples, to infer cancer habitats and niches. Significant challenges and open questions remain: how to establish multidisciplinary platforms, develop reproducible AI tools, and how to leverage pathology, genetic, molecular, and clinical data to improve personalized oncology. Charles Darwin described how the intimate coexistence between flowering plants and insects leads to reciprocal evolutionary changes; this is now known as coevolution. Today, through the demolition of disciplinary barriers, AI and pathology can co-evolve to create evolutionary changes and new paradigms. I will discuss our latest progress on combining AI and experimental technologies for spatial histology and omics data analysis. We aim to understand how cancer evolves within diverse environmental conditions. Our work has revealed a high level of geospatial variation in the tumor microenvironment, with profound implications for early diagnosis, biomarker development, and cancer therapeutics. Citation Format: Yinyin Yuan. Co-evolving artificial intelligence and pathology [abstract]. In: Proceedings of the AACR Special Conference on Rethinking DCIS: An Opportunity for Prevention?; 2022 Sep 8-11; Philadelphia, PA. Philadelphia (PA): AACR; Can Prev Res 2022;15(12 Suppl_1): Abstract nr IA006.

Interacting phenotypes and the coevolutionary process: Interspecific indirect genetic effects alter coevolutionary dynamics.

Coevolution occurs when species interact to influence one another's fitness, resulting in reciprocal evolutionary change. In many coevolving lineages, trait expression in one species is modified by the genotypes and phenotypes of the other, forming feedback loops reminiscent of models of intraspecific social evolution. Here, we adapt the theory of within-species social evolution, characterized by indirect genetic effects and social selection imposed by interacting individuals, to the case of interspecific interactions. In a trait-based model, we derive general expressions for multivariate evolutionary change in two species and the expected between-species covariance in evolutionary change when selection varies across space. We show that reciprocal interspecific indirect genetic effects can dominate the coevolutionary process and drive patterns of correlated evolution beyond what is expected from direct selection alone. In extreme cases, interspecific indirect genetic effects can lead to coevolution when selection does not covary between species or even when one species lacks genetic variance. Moreover, our model indicates that interspecific indirect genetic effects may interact in complex ways with cross-species selection to determine the course of coevolution. Importantly, our model makes empirically testable predictions for how different forms of reciprocal interactions contribute to the coevolutionary process.

Coevolutionary dynamics shape the structure of bacteria-phage infection networks.

Coevolution-reciprocal evolutionary change among interacting species driven by natural selection-is thought to be an important force in shaping biodiversity. This ongoing process takes place within tangled networks of species interactions. In microbial communities, evolutionary change between hosts and parasites occurs at the same time scale as ecological change. Yet, we still lack experimental evidence of the role of coevolution in driving changes in the structure of such species interaction networks. Filling this gap is important because network structure influences community persistence through indirect effects. Here, we quantified experimentally to what extent coevolutionary dynamics lead to contrasting patterns in the architecture of bacteria-phage infection networks. Specifically, we look at the tendency of these networks to be organized in a nested pattern by which the more specialist phages tend to infect only a proper subset of those bacteria infected by the most generalist phages. We found that interactions between coevolving bacteria and phages become less nested over time under fluctuating dynamics, and more nested under arms race dynamics. Moreover, when coevolution results in high average infectivity, phages and bacteria differ more from each other over time under arms race dynamics than under fluctuating dynamics. The tradeoff between the fitness benefits of evolving resistance/infectivity traits and the costs of maintaining them might explain these differences in network structure. Our study shows that the interaction pattern between bacteria and phages at the community level depends on the way coevolutionunfolds.

Rapid diversification of coevolving marine Synechococcus and a virus

Marine viruses impose a heavy mortality on their host bacteria, whereas at the same time the degree of viral resistance in marine bacteria appears to be high. Antagonistic coevolution--the reciprocal evolutionary change of interacting species--might reconcile these observations, if it leads to rapid and dynamic levels of viral resistance. Here we demonstrate the potential for extensive antagonistic coevolution between the ecologically important marine cyanobacterium Synechococcus and a lytic virus. In a 6-mo-long replicated chemostat experiment, Synechococcus sp. WH7803 and the virus (RIM8) underwent multiple coevolutionary cycles, leading to the rapid diversification of both host and virus. Over the course of the experiment, we detected between 4 and 13 newly evolved viral phenotypes (differing in host range) and between 4 and 11 newly evolved Synechococcus phenotypes (differing in viral resistance) in each chemostat. Genomic analysis of isolates identified several candidate genes in both the host and virus that might influence their interactions. Notably, none of the viral candidates were tail fiber genes, thought to be the primary determinants of host range in tailed bacteriophages, highlighting the difficulty in generalizing results from bacteriophage infecting γ-Proteobacteria. Finally, we show that pairwise virus-host coevolution may have broader community consequences; coevolution in the chemostat altered the sensitivity of Synechoccocus to a diverse suite of viruses, as well as the virus' ability to infect additional Synechococcus strains. Our results indicate that rapid coevolution may contribute to the generation and maintenance of Synechococcus and virus diversity and thereby influence viral-mediated mortality of these key marine bacteria.

Geographic isolation trumps coevolution as a driver of yucca and yucca moth diversification

Coevolution is thought to be especially important in diversification of obligate mutualistic interactions such as the one between yuccas and pollinating yucca moths. We took a three-step approach to examine if plant and pollinator speciation events were likely driven by coevolution. First, we tested whether there has been co-speciation between yuccas and pollinator yucca moths in the genus Tegeticula (Prodoxidae). Second, we tested whether co-speciation also occurred between yuccas and commensalistic yucca moths in the genus Prodoxus (Prodoxidae) in which reciprocal evolutionary change is unlikely. Finally, we examined the current range distributions of yuccas in relationship to pollinator speciation events to determine if plant and moth speciation events likely occurred in sympatry or allopatry. Co-speciation analyses of yuccas with their coexisting Tegeticula pollinator and commensalistic Prodoxus lineages demonstrated phylogenetic congruence between both groups of moths and yuccas, even though moth lineages differ in the type of interaction with yuccas. Furthermore, Yucca species within a lineage occur primarily in allopatry rather than sympatry. We conclude that biogeographic factors are the overriding force in plant and pollinator moth speciation and significant phylogenetic congruence between the moth and plant lineages is likely due to shared biogeography rather than coevolution.

Branching Out with Coevolutionary Trees

Coevolution (reciprocal evolutionary change in interacting species) is posited as a major mechanism that creates new species. A challenge has been to understand how coevolution has shaped the patterns of relatedness of interacting species and the traits involved in the interaction. Ongoing advances in the field of molecular phylogenetics have opened exciting avenues to examine both ancient and recent coevolutionary processes. Using plant–insect interactions as examples, I review the predictions of a number of coevolutionary models.

The Coevolving Web of Life(American Society of Naturalists Presidential Address)

Coevolution--reciprocal evolutionary change in interacting species--is one of the central biological processes organizing the web of life, and most species are involved in one or more coevolved interactions. We have learned in recent years that coevolution is a highly dynamic process that continually reshapes interactions among species across ecosystems, creating geographic mosaics over timescales sometimes as short as thousands or even hundreds of years. If we take that as our starting point, what should we now be asking about the coevolutionary process? Here I suggest five major questions that we need to answer if we are to understand how coevolution shapes the web of life. How evolutionarily dynamic is specialization to other species, and what is the role of coevolutionary alternation in driving those dynamics? Does the geographic mosaic of coevolution shape adaptation in fundamentally different ways in different forms of interaction? How does the geographic mosaic of coevolution shape speciation? How does the structure of reciprocal selection change during the assembly of large webs of interacting species? How important are genomic events such as whole-genome duplication (i.e., polyploidy) and whole-genome capture (i.e., hybridization) in generating novel webs of interacting species? I end by suggesting four points about coevolution that we should tell every new student or researcher in biology.

First evidence of regular common cuckoo, Cuculus canorus, parasitism on eastern olivaceous warblers, Hippolais pallida elaeica

Coevolution is defined as specialized relationships between species that lead to a reciprocal evolutionary change. A particularly suitable model system for studying coevolution is the interactions between obligate avian brood parasites and their hosts. The common cuckoo (Cuculus canorus, hereafter cuckoo) is a well-known brood parasite, which utilizes a range of smaller passerines as hosts. However, warblers of the genus Hippolais have rarely been reported as being victims of cuckoos, and furthermore, few data exist on the occurrence of antiparasite defenses in these hosts. In this study, we examined possible host-parasite coevolution between cuckoos and eastern olivaceous warblers (Hippolais pallida elaeica, hereafter olivaceous warblers) in three closely situated areas in northwestern Bulgaria. The olivaceous warbler has never been reported to be a regular cuckoo host. However, the present study, carried out in 2001-2003 shows that the olivaceous warbler is regularly and heavily parasitized by the cuckoo in this area. Parasitism rate was high (26.6%, 34/128) and consistent among years, with some variation between areas. The cuckoo egg mimicry was moderately good, and olivaceous warbler rejection rate of such eggs was 50%. Cuckoo eggs laid in olivaceous warbler nests had a whitish to whitish-green ground color, and the majority appeared to be distinctly different from cuckoo eggs found in other host species in the area. The olivaceous warbler proved to be a rather good host for cuckoos as 20.6% (7/34) of cuckoo eggs laid produced fledglings, a breeding success comparable to other suitable hosts in Europe. This is the first in-depth study of brood parasitism in a warbler of the genus Hippolais, and cuckoos parasitizing olivaceous warblers probably represent a previously unknown gens.

Co-evolution of Firm Strategies and Institutional Setting in Firm-based Late Industrialization — The Case of the Japanese Commercial Aircraft Industry

This paper examines the reciprocal evolutionary changes that occur through mutual interactions between firm strategies and the institutional setting in which the firms are embedded, in a context of firm-based late industrialization (FLI). More specifically, it delineates how such mutual interactions create a “micro-macro loop” and the co-evolutionary structure between (micro-level) firm strategies and (meso/macro-level) institutional setting. We elaborate the concept of a micro-macro loop by identifying the specific aspects in which firm strategies and institutional setting mutually interact in the context of firm-based late industrialization. By focusing on those specific aspects of the micro-macro loop, we then delineate the co-evolution of those two variables during the postwar development of the Japanese commercial aircraft industry. Finally, the empirical part of the paper describes how such a co-evolutionary structure has fostered and/or hindered the FLI of the postwar Japanese commercial aircraft industry.

Trick or treat: the battle of the sexes

Males and females differ in many ways due to theirdistinct roles in reproduction. A fundamental asym-metry, that in fact defines the genders, occurs over initialinvestment in gametes, with males producing many, tinyand females few, large gametes. Another very generalasymmetry concerns the intensity of selection for mul-tiple mating between the sexes: while males can max-imize their reproductive output by obtaining as manypartners as possible, females need fewer partners toachieve their maximum reproductive output (Bateman,1948). That these distinct roles can generate a battle ofthe sexes or sexual conflict and can affect the evolu-tionary dynamics of reproductive traits and behaviourshas been recognized since the 1970s, and has nowdeveloped into an exciting and major area of investiga-tion in evolutionary biology. Evolutionary conflictbetween the sexes, or sexually antagonistic selection,can affect either traits encoded by the same locus in bothsexes (intra-locus conflict), where different phenotypicvalues will be favoured, or male and female traitsgoverned by different loci (inter-locus conflict). Whileintralocus conflict may result in the evolution of sexlimitation and sexual dimorphism (de facto becoming aninterlocus effect), interlocus conflict gives wide scope forcontinual evolution of traits in males that manipulatefemale reproduction, and of female resistance to mani-pulation. The recent rise of interest for this field wasparticularly stimulated by this insight that antagonisticselection on male and female traits can fuel chainreactions of reciprocal evolutionary change, i.e. lead toan intra-specific Red Queen process analogous to coev-olutionary arms races between hosts and parasites (Rice& Holland, 1997).The timely monograph by Arnqvist & Rowe (2005)synthesizes research on sexual conflict, embeds it in thehistorical and conceptual context of sexual selectionresearch, explores many natural history examples acrosstaxa, and questions both the conceptual stringency andthe empirical testability of hypotheses emanating fromthe idea of diverging evolutionary optima in males andfemales, thus paving the way for future directions. Oneof the strengths of this book is the comprehensive lookat studies completed by a wide variety of scientists(on 75 pages, the reference list comprises over one-fifthof the book).As a young field of broad interest to biologists fromdifferent sub-disciplines, sexual conflict is not free ofconceptual heterogeneity. The possible meanings ofmetaphors such as conflict resolution or battle of sexesare fitted into the framework of intraspecific coevolution,where average male and female fitness cannot be inde-pendent of each other. The authors are honest about thefact that there are often identical expectations under asexual selectionandsexual conflict scenario;forexample,correlated male–female evolution. They note the difficul-ties this presents in determining the force at work in anygiven system. However, they also discuss the theoreticalcontributions that sexual conflict theory has made,including the distinction between a male trait experien-cing sexually antagonistic selection vs. sexual selection.Under sexually antagonistic selection, the male trait isadvantageous to the male but simultaneously disadvan-tageous to the female. In contrast, a male trait undertraditional sexual selection is advantageous to both themaleandthefemale.Thus,inthelattercasethemaletraitcan spread by female preference for the trait. Despite thistheoreticaldistinction,therecurrentlyisnogoldenruletodemonstrate conflict in any given system. For empiricists,the authors advocate a combined approach, encompas-sing economic studies to measure costs and benefits ofsexual interactions, phenotypic manipulation, experi-mental tests of optimality modeling, experimental evolu-tion, genetic experiments, and comparative studies. Theyalsodiscusshowtomeasurethestrengthofsexualconflictby the phenotypic selection gradient approach of Shuster& Wade (2003), and through inference of the cost ofsexually antagonistic adaptations to population fitness.The honesty in discussing how far empirical studies candiscriminate among hypotheses, and in identifying whereempirical evidence or theoretical developments arelacking, is one of the strengths of this book. Such honestyboth promotes further thought and discussion amongreaders and avoids the pitfalls of overinterpretation.The conflict between the sexes can affect traitsexpressed both before and after mating. Pre-matingsexual conflict is illustrated by examples as diverse as

The geographic mosaic of coevolution

Coevolution - reciprocal evolutionary change in interacting species driven by natural selection - is one of the most important ecological and genetic processes organizing the earth's biodiversity: most plants and animals require coevolved interactions with other species to survive and reproduce. The Geographic Mosaic of Coevolution analyzes how the biology of species provides the raw material for long-term coevolution, evaluates how local coadaptation forms the basic module of coevolutionary change, and explores how the coevolutionary process reshapes locally coevolving interactions across the earth's constantly changing landscapes. Picking up where his influential The Coevolutionary Process left off, John N. Thompson synthesizes the state of a rapidly developing science that integrates approaches from evolutionary ecology, population genetics, phylogeography, systematics, evolutionary biochemistry and physiology, and molecular biology. Using models, data, and hypotheses to develop a complete conceptual framework, Thompson also draws on examples from a wide range of taxa and environments, illustrating the expanding breadth and depth of research in coevolutionary biology.

The Geographic Mosaic of Coevolution. By J. N. Thompson, pp. 443. University of Chicago Press, USA, 2005. ISBN 0 226 79762 7. £20 (US$28)

It could be argued that much of evolution is really coevolution. Organisms do not exist in an ecological vacuum, but as parts of a network of interacting species. A given species may compete with others for access to prey species used as food, while itself serving as food to predator and parasite species. Natural selection will drive reciprocal evolutionary changes between interacting species. Across its geographical range, a species will encounter different local networks, since the same set of species do not co-occur everywhere. Thus, coevolutionary outcomes will vary in space, forming a geographical mosaic shaped by local adaptation and gene flow. This is the theme of John Thompson's new book, in which the author develops a conceptual framework for the study of coevolution.

Lizards as a plant's 'hired help': letting pollinators in and seeds out

It is well-known that plants utilize many different kinds of animals for pollination and dispersal of their seeds, but an alternative kind of evolutionary relationship has attracted less attention: animals can facilitate pollen and seed transport without acting as a vector. We studied interactions between an epacridaceous plant (the honey bush, Richea scoparia) and a lizard (the snow skink, Niveoscincus microlepidotus) near the summit of Mount Wellington, Tasmania. The lizards gain access to the plant's nectar by tearing the fused petals (the calyptra) from the flower, thus exposing the plant's reproductive organs. Snow skinks forage selectively on flowers with higher-than-average nectar content, suggesting that this behaviour has evolved in response to plant characteristics. Lizard foraging may benefit R. scoparia, because calyptra remain attached unless a lizard tears the flower open. Our experiments demonstrated that the lizard's calyptra removal dramatically increased the plant's seed release. In 60 fruits from flowers with their calyptra intact, no seeds at all were released. However, 57 out of 60 (87%) fruits from flowers with their calyptra removed by the lizards successfully released their seeds. This system appears to involve reciprocal evolutionary changes in the interacting species (behaviour in the lizards and reproductive morphology in the plant). Thus the system seems to provide an unusual case of coevolution.

The Raw Material for Coevolution

Our current understanding of the coevolutionary process has been based upon studies of six aspects of the biology of organisms that shape the potential for ongoing reciprocal evolutionary change in natural communities. These include analyses of the phylogenetic context of coevolving interactions, patterns of specialization of species to one another, the genetic architecture of coevolution and its ecological consequences, the distributed outcomes of interspecific interactions, the rates and forms of selection on interactions within biological communities, and the geographic dynamics of interacting species. These studies of the raw material for coevolution are helping replace the general concept of diffuse coevolution with more testable hypotheses on the structure and ongoing dynamics of reciprocal evolutionary change within natural communities.

Toxicity of Dangerous Prey: Variation of Tetrodotoxin Levels Within and Among Populations of the Newt Taricha granulosa

The ability to identify and accurately measure traits at the phenotypic interface of potential coevolutionary interactions is critical in documenting reciprocal evolutionary change between species. We quantify the defensive chemical trait of a prey species, the newt Taricha granulosa, thought to be part of a coevolutionary arms race. Variation in newt toxicity among populations results from variation in levels of the neurotoxin tetrodotoxin (TTX). Individual variation in TTX levels occurs within populations. Although TTX exists as a family of stereoisomers, only two of these (TTX and 6-epi-TTX) are likely to be sufficiently toxic and abundant to play a role in the defensive ecology of the newt.

The evolution of polyandry I: intragenomic conflict and genetic incompatibility

Why do females across a wide range of taxa mate with more than one male? We suggest that a better understanding of polyandry may be gained by considering the implications of intragenomic conflict for female reproductive success. Here, we revisit the literature on cellular endosymbionts, transposable elements, segregation distorters, maternal-effect lethals and genomically imprinted genes to show that each of these selfish genetic elements can modify maternal and paternal haplotypes in ways that render them incompatible within the developing embryo. We propose that the cumulative threat to female reproductive success of genetic incompatibility arising from intragenomic conflict may be an important force driving the evolution of polyandry. By mating with more than one male, females can potentially exploit post-copulatory mechanisms for minimizing the risk and/or cost of fertilization by genetically incompatible sperm. This hypothesis differs fundamentally from other genetic benefit models of polyandry in that the fitness consequences of intragenomic conflict depend on an interaction between parental genomes and are thus non-additive. Reciprocal evolutionary change between selfish genetic elements and their suppressors, combined with the capacity of these elements for horizontal transfer between species, is likely to ensure the persistence of genetic incompatibility as a threat to female reproductive success.

INTERACTION AND COEVOLUTION.

John Thompson defines coevolution as reciprocal evolutionary change in interacting species. In so doing he confronts the conundrum that muddies the understanding of some of the most fascinating phenomena in nature. Evolutionary biology explores the links between genetic change and variation in form and function, while community ecology seeks to explain the distribution and abundance of species that are tacitly treated as fixed in form and function. The two intellectual traditions simply do not mix easily. To get a grip on such a slippery topic, Thompson gives us a thoughtful and scholarly discussion of a remarkably broad spectrum of coevolutionary phenomena, ranging from the traditional antagonisms of ecological competition, parasitism, and predation to the mutual dependencies found in pollination, seed dispersal, and symbioses. The common theme is a neo-Darwinian interpretation of both antagonistic and mutualistic relationships in light of individual fitness. Interaction and Coevolution is a short book (138 pages of text, plus 556 well-chosen references) consisting of a brief introduction and seven substantive chapters. Organization is thematic rather than taxonomic, and the general approach is that of review and synthesis of empirical work rather than theory per se. The task is challenging, and the result has both important strengths and nagging shortcomings. A major contribution of this book is its broad treatment of ecology and evolutionary biology from a unified and thoroughly critical perspective. Emphasis is where parsimony should have it, on interpretations of evolutionary antagonism and mutualism which are consistent with natural selection on individuals within two or more interacting populations. Antagonisms, in which a victim suffers loss of resources, life, limb, or leaf are grouped together in two chapters covering parasitism, predation, and grazing on the one hand and competition on the other. Mutual dependence among symbionts and between plants and their pollinators or dispersal agents are considered in subsequent chapters, but Thompson makes the central point that any distinction between evolutionary antagonism and mutualism is one of degree rather than kind. For example, the link between antagonism and mutualism is obvious in fig pollination, in which