Coevolutionary Interactions Research Articles

Association between louse abundance and MHC II supertypes in Galápagos mockingbirds.

Major histocompatibility complex class II (MHC II) is an essential molecule triggering the adaptive immune response by the presentationof pathogens to helper T cells. The association between individual MHC II variants and various parasites has become a frequent finding in studies of vertebrate populations. However, although bird ectoparasites have a significant effect on their host's fitness, and the host's immune system can regulate ectoparasitic infections, no study has yet investigated the association between MHC II polymorphism and ectoparasite infection in the populations of free-living birds. Here, we test whether an association exists between the abundance of a chewing louse (Myrsidea nesomimi) and MHC II polymorphism of its hosts, the Galápagos mockingbirds (Mimus). We have found that the presence of two MHC II supertypes (functionally differentiated clusters) was significantly associated with louse abundance. This pattern supports the theory that a co-evolutionary interaction stands behind the maintenance of MHC polymorphism. Moreover, we have found a positive correlation between louse abundance and heterophil/lymphocyte ratio (an indicator of immunological stress) that serves as an additional piece of evidence that ectoparasite burden is affected by immunological state of Galápagos mockingbirds.

Coevolutionary data-based interaction networks approach highlighting key residues across protein families: The case of the G-protein coupled receptors

We present an approach that, by integrating structural data with Direct Coupling Analysis, is able to pinpoint most of the interaction hotspots (i.e. key residues for the biological activity) across very sparse protein families in a single run. An application to the Class A G-protein coupled receptors (GPCRs), both in their active and inactive states, demonstrates the predictive power of our approach. The latter can be easily extended to any other kind of protein family, where it is expected to highlight most key sites involved in their functional activity.

Retroviruses drive the rapid evolution of mammalian APOBEC3 genes

APOBEC3 (A3) genes are members of the AID/APOBEC gene family that are found exclusively in mammals. A3 genes encode antiviral proteins that restrict the replication of retroviruses by inducing G-to-A mutations in their genomes and have undergone extensive amplification and diversification during mammalian evolution. Endogenous retroviruses (ERVs) are sequences derived from ancient retroviruses that are widespread mammalian genomes. In this study we characterize the A3 repertoire and use the ERV fossil record to explore the long-term history of coevolutionary interaction between A3s and retroviruses. We examine the genomes of 160 mammalian species and identify 1,420 AID/APOBEC-related genes, including representatives of previously uncharacterized lineages. We show that A3 genes have been amplified in mammals and that amplification is positively correlated with the extent of germline colonization by ERVs. Moreover, we demonstrate that the signatures of A3-mediated mutation can be detected in ERVs found throughout mammalian genomes and show that in mammalian species with expanded A3 repertoires, ERVs are significantly enriched for G-to-A mutations. Finally, we show that A3 amplification occurred concurrently with prominent ERV invasions in primates. Our findings establish that conflict with retroviruses is a major driving force for the rapid evolution of mammalian A3 genes.

Coevolution of Snake Venom Toxic Activities and Diet: Evidence that Ecological Generalism Favours Toxicological Diversity.

Snake venom evolution is typically considered to be predominantly driven by diet-related selection pressures. Most evidence for this is based on lethality to prey and non-prey species and on the identification of prey specific toxins. Since the broad toxicological activities (e.g., neurotoxicity, coagulotoxicity, etc.) sit at the interface between molecular toxinology and lethality, these classes of activity may act as a key mediator in coevolutionary interactions between snakes and their prey. Indeed, some recent work has suggested that variation in these functional activities may be related to diet as well, but previous studies have been limited in geographic and/or taxonomic scope. In this paper, we take a phylogenetic comparative approach to investigate relationships between diet and toxicological activity classes on a global scale across caenophidian snakes, using the clinically oriented database at toxinology.com. We generally find little support for specific prey types selecting for particular toxicological effects except that reptile-feeders are more likely to be neurotoxic. We find some support for endothermic prey (with higher metabolic rates) influencing toxic activities, but differently from previous suggestions in the literature. More broadly, we find strong support for a general effect of increased diversity of prey on the diversity of toxicological effects of snake venom. Hence, we provide evidence that selection pressures on the toxicological activities of snake venom has largely been driven by prey diversity rather than specific types of prey. These results complement and extend previous work to suggest that specific matching of venom characteristics to prey may occur at the molecular level and translate into venom lethality, but the functional link between those two is not constrained to a particular toxicological route.

Evolutionary History of the Toll-Like Receptor Gene Family across Vertebrates.

Adaptation to a wide range of pathogenic environments is a major aspect of the ecological adaptations of vertebrates during evolution. Toll-like receptors (TLRs) are ancient membrane-bound sensors in animals and are best known for their roles in detecting and defense against invading pathogenic microorganisms. To understand the evolutionary history of the vertebrate TLR gene family, we first traced the origin of single-cysteine cluster TLRs that share the same protein architecture with vertebrate TLRs in early-branching animals and then analyzed all members of the TLR family in over 200 species covering all major vertebrate clades. Our results indicate that although the emergence of single-cysteine cluster TLRs predates the separation of bilaterians and cnidarians, most vertebrate TLR members originated shortly after vertebrate emergence. Phylogenetic analyses divided 1,726 vertebrate TLRs into 8 subfamilies, and TLR3 may represent the most ancient subfamily that emerged before the branching of deuterostomes. Our analysis reveals that purifying selection predominated in the evolution of all vertebrate TLRs, with mean dN/dS (ω) values ranging from 0.082 for TLR21 in birds to 0.434 for TLR11 in mammals. However, we did observe patterns of positive selection acting on specific codons (527 of 60,294 codons across all vertebrate TLRs, 8.7‰), which are significantly concentrated in ligand-binding extracellular domains and suggest host–pathogen coevolutionary interactions. Additionally, we found stronger positive selection acting on nonviral compared with viral TLRs, indicating the more essential nonredundant function of viral TLRs in host immunity. Taken together, our findings provide comprehensive insight into the complex evolutionary processes of the vertebrate TLR gene family, involving gene duplication, pseudogenization, purification, and positive selection.

Molecular Targets for Coevolutionary Interactions Between Pacific Oyster Larvae and Their Sympatric Vibrios.

Bacteria of the Vibrio genus are the most predominant infectious agents threatening marine wildlife and aquaculture. Due to the large genetic diversity of these pathogens, the molecular determinants of Vibrio virulence are only poorly understood. Furthermore, studies tend to ignore co-evolutionary interactions between different host populations and their locally encountered Vibrio communities. Here, we explore the molecular targets of such co-evolutionary interactions by analyzing the genomes of nine Vibrio strains from the Splendidus-clade showing opposite virulence patterns towards two populations of Pacific oysters introduced into European Wadden Sea. By contrasting Vibrio phylogeny to their host specific virulence patterns, we could identify two core genome genes (OG1907 and OG 3159) that determine the genotype by genotype (G × G) interactions between oyster larvae and their sympatric Vibrio communities. Both genes show positive selection between locations targeting only few amino acid positions. Deletion of each gene led to a loss of the host specific virulence patterns while complementation with OG3159 alleles from both locations could recreate the wild type phenotypes matching the origin of the allele. This indicates that both genes can act as a genetic switch for Vibrio-oyster coevolution demonstrating that local adaptation in distinct Vibrio lineages can rely on only few genes independent of larger pathogenicity islands or plasmids.

Inhibitory and nutrient use phenotypes among coexisting Fusarium and Streptomyces populations suggest local coevolutionary interactions in soil.

Bacteria and fungi are key components of virtually all natural habitats, yet the significance of fungal-bacterial inhibitory interactions for the ecological and evolutionary dynamics of specific bacterial and fungal populations in natural habitats have been overlooked. More specifically, despite the broad consensus that antibiotics play a key role in providing a fitness advantage to competing microbes, the significance of antibiotic production in mediating cross-kingdom coevolutionary interactions has received relatively little attention. Here, we characterize reciprocal inhibition among Streptomyces and Fusarium populations from prairie soil, and explore antibiotic inhibition in relation to niche overlap among sympatric and allopatric populations. We found evidence for local adaptation between Fusarium and Streptomyces populations as indicated by significantly greater inhibition among sympatric than allopatric populations. Additionally, for both taxa, there was a significant positive correlation between the strength of inhibition against the other taxon and the intensity of resource competition from that taxon among sympatric but not allopatric populations. These data suggest that coevolutionary antagonistic interactions between Fusarium and Streptomyces are driven by resource competition, and support the hypothesis that antibiotics act as weapons in mediating bacterial-fungal interactions in soil.

Coevolutionary arms race between a specialist brood parasite, the Screaming Cowbird, and its host, the Grayish Baywing

Interspecific brood parasites exploit the parental care of host species. This exploitation entails fitness costs for the hosts, which favor the evolution of antiparasitic defenses. Host defenses select for counter-defenses in the parasite, which in turn select for improved host defenses; this results in a coevolutionary arms race that may operate at each stage of the nesting cycle of the host. Most studied examples of the coevolutionary arms race in brood parasites are restricted to the egg stage, with relatively few studies showing coevolution between hosts and parasites at the nestling or fledgling stages; studies on the whole set of host defenses and potential parasite counter-defenses at each stage of the breeding cycle are still lacking. Systems in which parasites are host specialists are particularly well suited to an examination of the pairwise coevolutionary interactions before, during and after host egg-laying, and how these interactions have shaped host resistance or tolerance of parasitism. The Screaming Cowbird (Molothrus rufoaxillaris) is one of the most specialized brood parasites, and mainly parasitizes nests of a single host species, the Grayish Baywing (Agelaioides badius). Parasitism rates of Grayish Baywing nests are extremely high, with most nests parasitized several times. Several traits of this host-parasite system suggest ancient coevolutionary relationships encompassing the entire nesting cycle. In this paper we summarize the main results of a long-term study on the costs of Screaming Cowbird parasitism on the Grayish Baywing’s reproductive success and how these costs have favored reciprocal adaptations and counter-adaptations at each stage of the nesting cycle.

Avian Binocularity and Adaptation to Nocturnal Environments: Genomic Insights from a Highly Derived Visual Phenotype.

Typical avian eyes are phenotypically engineered for photopic vision (daylight). In contrast, the highly derived eyes of the barn owl (Tyto alba) are adapted for scotopic vision (dim light). The dramatic modifications distinguishing barn owl eyes from other birds include: 1) shifts in frontal orientation to improve binocularity, 2) rod-dominated retina, and 3) enlarged corneas and lenses. Some of these features parallel mammalian eye patterns, which are hypothesized to have initially evolved in nocturnal environments. Here, we used an integrative approach combining phylogenomics and functional phenotypes of 211 eye-development genes across 48 avian genomes representing most avian orders, including the stem lineage of the scotopic-adapted barn owl. Overall, we identified 25 eye-development genes that coevolved under intensified or relaxed selection in the retina, lens, cornea, and optic nerves of the barn owl. The agtpbp1 gene, which is associated with the survival of photoreceptor populations, was pseudogenized in the barn owl genome. Our results further revealed that barn owl retinal genes responsible for the maintenance, proliferation, and differentiation of photoreceptors experienced an evolutionary relaxation. Signatures of relaxed selection were also observed in the lens and cornea morphology-associated genes, suggesting that adaptive evolution in these structures was essentially structural. Four eye-development genes (ephb1, phactr4, prph2, and rs1) evolved in positive association with the orbit convergence in birds and under relaxed selection in the barn owl lineage, likely contributing to an increased reliance on binocular vision in the barn owl. Moreover, we found evidence of coevolutionary interactions among genes that are expressed in the retina, lens, and optic nerve, suggesting synergetic adaptive events. Our study disentangles the genomic changes governing the binocularity and low-light perception adaptations of barn owls to nocturnal environments while revealing the molecular mechanisms contributing to the shift from the typical avian photopic vision to the more-novel scotopic-adapted eye.

Assessing Specialized Metabolite Diversity in the Cosmopolitan Plant Genus Euphorbia L.

Coevolutionary theory suggests that an arms race between plants and herbivores yields increased plant specialized metabolite diversity and the geographic mosaic theory of coevolution predicts that coevolutionary interactions vary across geographic scales. Consequently, plant specialized metabolite diversity is expected to be highest in coevolutionary hotspots, geographic regions, which exhibit strong reciprocal selection on the interacting species. Despite being well-established theoretical frameworks, technical limitations have precluded rigorous hypothesis testing. Here we aim at understanding how geographic separation over evolutionary time may have impacted chemical differentiation in the cosmopolitan plant genus Euphorbia. We use a combination of state-of-the-art computational mass spectral metabolomics tools together with cell-based high-throughput immunomodulatory testing. Our results show significant differences in specialized metabolite diversity across geographically separated phylogenetic clades. Chemical structural diversity of the highly toxic Euphorbia diterpenoids is significantly reduced in species native to the Americas, compared to Afro-Eurasia. The localization of these compounds to young stems and roots suggest a possible ecological relevance in herbivory defense. This is further supported by reduced immunomodulatory activity in the American subclade as well as herbivore distribution patterns. We conclude that computational mass spectrometric metabolomics coupled with relevant ecological data provide a strong tool for exploring plant specialized metabolite diversity in a chemo-evolutionary framework.

Bacteria from natural populations transfer plasmids mostly towards their kin.

Plasmids play a key role in microbial ecology and evolution, yet the determinants of plasmid transfer rates are poorly understood. Particularly, interactions between donor hosts and potential recipients are understudied. Here, we investigate the importance of genetic similarity between naturally co-occurring Escherichia coli isolates in plasmid transfer. We uncover extensive variability, spanning over five orders of magnitude, in the ability of isolates to donate and receive two different plasmids, R1 and RP4. Overall, transfer is strongly biased towards clone-mates, but not correlated to genetic distance when donors and recipients are not clone-mates. Transfer is limited by the presence of a functional restriction-modification system in recipients, suggesting sharing of strain-specific defence systems contributes to bias towards kin. Such restriction of transfer to kin sets the stage for longer-term coevolutionary interactions leading to mutualism between plasmids and bacterial hosts in natural communities.

Afterword: Tough Questions; Hard Problems; Incremental Progress.

The papers in this issue have specific and focused targets that are essential for making incremental progress on the very difficult problem of identifying the coevolutionary interactions of cognition and culture. The purpose of this paper is to discern the shape of a few of the large problems that loom over these more narrowly focussed papers, and to explain and assess the ways these papers contribute to their solution. The background problems described are (a) the character of the selective interactions between the evolution of culture and of cognition; (b) the special features of cumulative cultural evolution; and (c) the place of language in an account of cognition-culture coevolution. The paper ends with some reflections on the extraordinarily difficult challenge of testing scenarios in this field.

Ecological and Evolutionary Processes Shaping Viral Genetic Diversity.

The contemporary genomic diversity of viruses is a result of the continuous and dynamic interaction of past ecological and evolutionary processes. Thus, genome sequences of viruses can be a valuable source of information about these processes. In this review, we first describe the relevant processes shaping viral genomic variation, with a focus on the role of host–virus coevolution and its potential to give rise to eco-evolutionary feedback loops. We further give a brief overview of available methodology designed to extract information about these processes from genomic data. Short generation times and small genomes make viruses ideal model systems to study the joint effect of complex coevolutionary and eco-evolutionary interactions on genetic evolution. This complexity, together with the diverse array of lifetime and reproductive strategies in viruses ask for extensions of existing inference methods, for example by integrating multiple information sources. Such integration can broaden the applicability of genetic inference methods and thus further improve our understanding of the role viruses play in biological communities.

Evaluating the structure of commensalistic epiphyte–phorophyte networks: a comparative perspective of biotic interactions

Epiphytic vascular plants comprise an essential part of the tropical flora and are a key component for ecosystem functioning. Some recent studies have used a network approach to investigate the interaction of epiphytes with host phorophytes at the community level. However, knowledge on commensalistic epiphyte–phorophyte network structure still lags behind with regard to other biotic interaction networks. Our goal was to provide a more complete overall perspective on commensalistic epiphyte–phorophyte interaction and its placement with respect to other better studied mutualistic interactions. We hypothesized that the intensity of the fitness effect of the different types of biotic interactions would determine the degree of specialization of the interacting organisms. Thus, commensalistic epiphyte–phorophyte interactions would have lower specialization than mutualistic interactions. We compiled and analysed the structural properties (nestedness, network specialization and modularity) of 12 commensalistic epiphyte–phorophyte networks and compared them with the same metrics to 11 ant–myrmecophyte, 86 pollination and 13 seed dispersal mutualistic networks. Epiphyte–phorophyte networks were nested and modular with regard to the corresponding null models and had greater nestedness than mutualistic networks, whereas specialization and modularity were significantly lower. Commensalistic epiphyte–phorophyte networks of interactions are both nested and modular, and hence, are structured in a similar way to most other types of networks that involve co-evolutionary interactions. Nevertheless, the nature and intensity of the ecological processes involved in the generation of these patterns is likely to differ. The lower values of modularity in commensalistic epiphyte–phorophyte networks are probably due to the low levels of specialization and the lack of co-evolutionary processes between the interacting partners.

Potential of Natural-Based Anticancer Compounds for P-Glycoprotein Inhibition.

Medicinal value of natural products comes from symbiotic and competitive evolution in Earth's complex biosphere. Billions of years of co-evolutionary interactions among millions of species have produced a large repertoire of defense molecules effective in fighting bacteria, viral, and fungal pathogens. Each species contains millions of different and useful molecules and new research technologies enabled the screening of molecules and complex mixtures from diverse biological sources. Traditional use of plants and other species led to the discovery of many bioactive compounds with various properties. In the last four decades, a large number of them were evaluated for their potential to treat cancer. Penetration of drugs into the cancer cell is necessary for their lethal pharmacological effect through interaction with intracellular target molecules. Increased activity of membrane efflux pumps reduces the intracellular drug accumulation, thereby preventing drug-target interactions. The discovery of the efflux transporter P-glycoprotein (P-gp) in multidrug resistant (MDR) cancer cells prompted the efforts in overcoming drug resistance by P-gp inhibition. The search for nontoxic anticancer agents from natural sources able to overcome MDR has been imperative in the field of drug design and discovery. Herein, we review various natural compounds from diverse sources emphasizing their potential to inhibit P-gp activity and/or expression.

Egg retrieval versus egg rejection in cuckoo hosts.

Before complex nests evolved, birds laid eggs on the ground, and egg retrieval evolved as an adaptation against accidental displacement of eggs outside the nest. Therefore, egg retrieval is an ancient, and likely ancestral, widespread behaviour in birds. However, it has received little attention in studies of avian brood parasitism, perhaps because most parasitism occurs in species with complex nests, a context in which egg retrieval seems irrelevant. However, for cavity-nesting hosts of avian brood parasites, egg retrieval may still play an important role in the coevolutionary interactions between obligate brood parasites and hosts, because egg retrieval can be considered to be antagonistic to egg rejection behaviour in hosts, yet both may involve cognition to recognize eggs. We hypothesized that (1) cavity-nesting hosts should retrieve misplaced eggs from outside the nest cup, (2) brood parasitism has modulated egg retrieval behaviour in cavity-nesting hosts and (3) hosts use the same visual cues for decision-making during egg recognition in both egg retrieval and egg rejection actions. To test these hypotheses, we performed a series of experiments in a cavity-nesting host, the green-backed tit ( Parus monticolus). Foreign eggs with different levels of mimicry were placed within or outside nest cups of hosts to test their responses. We found that host decisions about whether to retrieve or reject an egg both depended on the degree of mimicry. However, hosts sometimes first retrieved poorly mimetic foreign eggs and then rejected them. Alternatively, hosts sometimes failed to retrieve highly mimetic conspecific eggs. We suggest that egg retrieval in hosts is likely to be a result of the interaction between ancient retrieval behaviour and subsequent adaptation against brood parasitism. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

Development and behavior of Plaintive Cuckoo (Cacomantis merulinus) nestlings and their Common Tailorbird (Orthotomus sutorius) hosts

BackgroundOur knowledge of avian brood parasitism is primarily based on studies of a few selected species. Recently, researchers have targeted a wider range of host–parasite systems, which has allowed further evaluation of hypotheses derived from well-known study systems but also disclosed adaptations that were previously unknown. Here we present developmental and behavioral data on the previously undescribed Plaintive Cuckoo (Cacomantis merulinus) nestling and one of its hosts, the Common Tailorbird (Orthotomus sutorius).MethodsWe discovered more than 80 Common Tailorbird nests within an area of 25 km2, and we recorded nestling characteristics, body mass, tarsus length and begging display every 3 days for both species.ResultsPlaintive Cuckoo nestlings followed a developmental pathway that was relatively similar to that of their well-studied relative, the Common Cuckoo (Cuculus canorus). Tailorbird foster siblings were evicted from the nest rim. The cuckoo nestlings gained weight faster than host nestlings, and required 3–9 days longer time to fledge than host nestlings. Predation was high during the early stages of development, but the nestlings acquired a warning display around 11 days in the nest, after which none of the studied cuckoo nestlings were depredated. The cuckoos’ begging display, which appeared more intense than that of host nestlings, was initially vocally similar with that of the host nestlings but began to diverge from the host sound output after day 9.ConclusionsThe developmental data on Plaintive Cuckoo nestlings and their tailorbird host builds an important foundation for future work on the co-evolutionary interactions in this parasite–host system.

Host use and host shifts in Drosophila.

Over a thousand Drosophila species have radiated onto a wide range of feeding and breeding sites. These radiations involve adaptations for locating, accepting, and growing in hosts with highly differing characteristics. In a number of species, owing to the availability of sequenced genomes, particular steps in host specialization and genes that control them, are being identified. Many cases of specialization involve the ability to detoxify some component of the host. Examples include Drosophila sechellia and the octanoic acid in Morinda citrifolia, alpha-amanitin in mycophagous drosophilids, and the alkaloids in cactophilic species. Owing to the known ecologies of many species for which genomes exist, the Drosophila model system provides an unprecedented opportunity to simultaneously examine the genes underlying HOST LOCATION, HOST ACCEPTANCE and HOST USE, the types of selection acting upon them and any coevolutionary interactions among the genes underlying these steps.

DCA-MOL: A PyMOL Plugin To Analyze Direct Evolutionary Couplings.

Direct coupling analysis (DCA) is a statistical modeling framework designed to uncover relevant molecular evolutionary relationships from biological sequences. Although DCA has been successfully used in several applications, mapping and visualizing of evolutionary couplings and direct information to a particular set of molecules requires multiple steps and could be prone to errors. DCA-MOL extends PyMOL functionality to allow users to interactively analyze and visualize coevolutionary residue-residue interactions between contact maps and structures. True positive rates for the top N pairs can be computed and visualized in real-time to evaluate the quality of residue-residue contact predictions. Different types of interactions in monomeric proteins, RNA, molecular interfaces, and protein conformational dynamics as well as multiple protein complexes can be studied efficiently within one application. DCA-MOL is available for download from http://dca-mol.cent.uw.edu.pl.

Dietary Phytochemicals, Honey Bee Longevity and Pathogen Tolerance.

Continued loss of natural habitats with native prairies and wildflower patches is eliminating diverse sources of pollen, nectar and phytochemicals therein for foraging bees. The longstanding plant-pollinator mutualism reiterates the role of phytochemicals in sustaining plant-pollinator relationship and promoting honey bee health. We studied the effects of four phytochemicals—caffeine, gallic acid, kaempferol and p-coumaric acid, on survival and pathogen tolerance in the European honey bee, Apis mellifera (L.). We recorded longevity of worker bees that were provided ad libitum access to sugar solution supplemented with different concentrations of phytochemicals. We artificially infected worker bees with the protozoan parasite, Nosema ceranae. Infected bees were provided access to the same concentrations of the phytochemicals in the sugar solution, and their longevity and spore load at mortality were determined. Bees supplemented with dietary phytochemicals survived longer and lower concentrations were generally more beneficial. Dietary phytochemicals enabled bees to combat infection as seen by reduced spore-load at mortality. Many of the phytochemicals are plant defense compounds that pollinators have evolved to tolerate and derive benefits from. Our findings support the chemical bases of co-evolutionary interactions and reiterate the importance of diversity in floral nutrition sources to sustain healthy honey bee populations by strengthening the natural mutualistic relationships.