Evolutionary Biosemiotics and Multilevel Construction Networks

In contrast to the traditional relational semiotics, biosemiotics decisively deviates towards dynamical aspects of signs at the evolutionary and developmental time scales. The analysis of sign dynamics requires constructivism (in a broad sense) to explain how new components such as subagents, sensors, effectors, and interpretation networks are produced by developing and evolving organisms. Semiotic networks that include signs, tools, and subagents are multilevel, and this feature supports the plasticity, robustness, and evolvability of organisms. The origin of life is described here as the emergence of simple self-constructing semiotic networks that progressively increased the diversity of their components and relations. Primitive organisms have no capacity to classify and track objects; thus, we need to admit the existence of proto-signs that directly regulate activities of agents without being associated with objects. However, object recognition and handling became possible in eukaryotic species with the development of extensive rewritable epigenetic memory as well as sensorial and effector capacities. Semiotic networks are based on sequential and recursive construction, where each step produces components (i.e., agents, scaffolds, signs, and resources) that are needed for the following steps of construction. Construction is not limited to repair and reproduction of what already exists or is unambiguously encoded, it also includes production of new components and behaviors via learning and evolution. A special case is the emergence of new levels of organization known as metasystem transition. Multilevel semiotic networks reshape the phenotype of organisms by combining a mosaic of features developed via learning and evolution of cooperating and/or conflicting subagents.     

Intrinsic disorder in scaffold proteins: getting more from less

Regulation, recognition and cell signaling involve the coordinated actions of many players. Signaling scaffolds, with their ability to bring together proteins belonging to common and/or interlinked pathways, play crucial roles in orchestrating numerous events by coordinating specific interactions among signaling proteins. This review examines the roles of intrinsic disorder (ID) in signaling scaffold protein function. Several well-characterized scaffold proteins with structurally and functionally characterized ID regions are used here to illustrate the importance of ID for scaffolding function. These examples include scaffolds that are mostly disordered, only partially disordered or those in which the ID resides in a scaffold partner. Specific scaffolds discussed include RNase, voltage-activated potassium channels, axin, BRCA1, GSK-3beta, p53, Ste5, titin, Fus3, BRCA1, MAP2, D-AKAP2 and AKAP250. Among the mechanisms discussed are: molecular recognition features, fly-casting, ease of encounter complex formation, structural isolation of partners, modulation of interactions between bound partners, masking of intramolecular interaction sites, maximized interaction surface per residue, toleration of high evolutionary rates, binding site overlap, allosteric modification, palindromic binding, reduced constraints for alternative splicing, efficient regulation via posttranslational modification, efficient regulation via rapid degradation, protection of normally solvent-exposed sites, enhancing the plasticity of interaction and molecular crowding. We conclude that ID can enhance scaffold function by a diverse array of mechanisms. In other words, scaffold proteins utilize several ID-facilitated mechanisms to enhance function, and by doing so, get more functionality from less structure.     

Evolution in response to social selection: the importance of interactive effects of traits on fitness

Social interactions have a powerful effect on the evolutionary process. Recent attempts to synthesize models of social selection with equations for indirect genetic effects (McGlothlin et al. 2010) provide a broad theoretical base from which to study selection and evolutionary response in the context of social interactions. However, this framework concludes that social selection will lead to evolution only if the traits carried by social partners are nonrandomly associated. I suggest this conclusion is incomplete, and that traits that do not covary between social partners can nevertheless lead to evolution via interactive effects on fitness. Such effects occur when there are functional interactions between traits, and as an example I use the interplay in water striders (Gerridae) between grasping appendages carried by males and spines by females. Functional interactive effects between traits can be incorporated into both the equations for social selection and the general model of social evolution proposed by McGlothlin et al. These expanded equations would accommodate adaptive coevolution in social interactions, integrate the quantitative genetic approach to social evolution with game theoretical approaches, and stimulate some new questions about the process of social evolution.     

Cost of interacting with sexual partners in a facultative sexual microbe

The widespread occurrence of sexual organisms despite the high costs of sex has long intrigued biologists. The best-known costs are the twofold cost of producing males and the cost associated with producing traits to attract mates and to interact with mating partners, such as exaggerated sexual behaviors and morphological modifications. These costs have been inferred from studies of plants and animals but are thought to be absent in facultative sexual microbes. Here, using the facultative sexual fungus Cryptococcus neoformans, I provide experimental evidence showing that: (i) interactions with active sexual partners can be costly for vegetative fitness in a facultative sexual microbe; (ii) this cost is positively correlated to mating ability; (iii) this cost is composed of at least two distinct components, the cost of producing mating signals that exert effects on mating partners and that associated with responding to active mating partners; and (iv) extended asexual reproduction can reduce both components of the cost. This cost must have been compensated for by the production of zygotes and sexual spores to allow the initial evolution and spread of sexual reproduction in eukaryotes.     

Global patterns of body size evolution are driven by precipitation in legless amphibians

Body size shapes ecological interactions across and within species, ultimately influencing the evolution of large‐scale biodiversity patterns. Therefore, macroecological studies of body size provide a link between spatial variation in selection regimes and the evolution of animal assemblages through space. Multiple hypotheses have been formulated to explain the evolution of spatial gradients of animal body size, predominantly driven by thermal (Bergmann's rule), humidity (‘water conservation hypothesis’) and resource constraints (‘resource rule’, ‘seasonality rule’) on physiological homeostasis. However, while integrative tests of all four hypotheses combined are needed, the focus of such empirical efforts needs to move beyond the traditional endotherm–ectotherm dichotomy, to instead interrogate the role that variation in lifestyles within major lineages (e.g. classes) play in creating neglected scenarios of selection via analyses of largely overlooked environment–body size interactions. Here, we test all four rules above using a global database spanning 99% of modern species of an entire Order of legless, predominantly underground‐dwelling amphibians (Gymnophiona, or caecilians). We found a consistent effect of increasing precipitation (and resource abundance) on body size reductions (supporting the water conservation hypothesis), while Bergmann's, the seasonality and resource rules are rejected. We argue that subterranean lifestyles minimize the effects of aboveground selection agents, making humidity a dominant selection pressure – aridity promotes larger body sizes that reduce risk of evaporative dehydration, while smaller sizes occur in wetter environments where dehydration constraints are relaxed. We discuss the links between these principles with the physiological constraints that may have influenced the tropically‐restricted global radiation of caecilians.     

The importance of fungi in shaping the paleoecosystem

Although fungi have a long geologic history, many aspects regarding their origins and subsequent evolution remain impossible to document from the fossil record. As heterotrophs, fungi must interact with other organisms, and it is here that the fossil record can provide an important source of biological and paleoecological information about fungal interactions. Saprophytic, parasitic and biotrophic interactions among fungi and other organisms are ancient; examples of these interrelationships are discussed as they relate to the establishment and evolution of the biological and physical paleoecosystem.     

Inferring coevolution in a plant–pollinator network

Mutualistic interactions are at the core of community dynamics, determining dispersal, colonization and differential survival and reproduction among individuals and species. Mutualistic interactions therefore affect the fitness of interaction partners, hence modifying their respective evolutionary trajectories reciprocally, potentially leading to coevolution. Although mathematical models predict coevolution in mutualistic interaction networks, no empirical data are available. By taking into account the patterns of interactions and reconstructing evolutionary change in plant and pollinator traits, we tested the hypothesis that coevolution occurs between plants and insects that interact more frequently, or more symmetrically. To test this hypothesis, we built an interaction network with data from five flowering seasons, measured plant and insect morphology, mapped morphology on the plant and insect phylogenies, and reconstructed ancestral character changes based on maximum parsimony. We calculated an index, called the coevolutionary ratio, which represents the amount of correlated change in traits that mediate the interaction between plants and pollinators (i.e. proboscis versus corolla length, and body width and corolla aperture). Our results suggest that high frequency of interaction, i.e. the number of times two species interact, does not lead to coevolution. Instead, symmetry of interaction strength, i.e. the reciprocal similarity in the mutual effect of interaction partners, may lead to coevolution, in spite of a pervasive lack of reciprocal specialization and high interaction frequency. Although the statistical signal is quite weak, our results hold for three statistical tests of very different nature. The most specialized species, expected to be under directional selection, do not show more evolutionary change than do generalist species, expected to be under different, perhaps opposing, selective pressures. By dissecting the complexity of an interaction network we show that coevolution may partially shape functional morphology of interaction partners, thus providing the closest evidence to date of mutualistic adaptation of organisms within a community.     

Hunter-Gatherer Inter-Band Interaction Rates: Implications for Cumulative Culture

Our species exhibits spectacular success due to cumulative culture. While cognitive evolution of social learning mechanisms may be partially responsible for adaptive human culture, features of early human social structure may also play a role by increasing the number potential models from which to learn innovations. We present interview data on interactions between same-sex adult dyads of Ache and Hadza hunter-gatherers living in multiple distinct residential bands (20 Ache bands; 42 Hadza bands; 1201 dyads) throughout a tribal home range. Results show high probabilities (5%–29% per year) of cultural and cooperative interactions between randomly chosen adults. Multiple regression suggests that ritual relationships increase interaction rates more than kinship, and that affinal kin interact more often than dyads with no relationship. These may be important features of human sociality. Finally, yearly interaction rates along with survival data allow us to estimate expected lifetime partners for a variety of social activities, and compare those to chimpanzees. Hadza and Ache men are estimated to observe over 300 men making tools in a lifetime, whereas male chimpanzees interact with only about 20 other males in a lifetime. High intergroup interaction rates in ancestral humans may have promoted the evolution of cumulative culture.     

High-Throughput Ligand Discovery Reveals a Sitewise Gradient of Diversity in Broadly Evolved Hydrophilic Fibronectin Domains

Discovering new binding function via a combinatorial library in small protein scaffolds requires balance between appropriate mutations to introduce favorable intermolecular interactions while maintaining intramolecular integrity. Sitewise constraints exist in a non-spatial gradient from diverse to conserved in evolved antibody repertoires; yet non-antibody scaffolds generally do not implement this strategy in combinatorial libraries. Despite the fact that biased amino acid distributions, typically elevated in tyrosine, serine, and glycine, have gained wider use in synthetic scaffolds, these distributions are still predominantly applied uniformly to diversified sites. While select sites in fibronectin domains and DARPins have shown benefit from sitewise designs, they have not been deeply evaluated. Inspired by this disparity between diversity distributions in natural libraries and synthetic scaffold libraries, we hypothesized that binders resulting from discovery and evolution would exhibit a non-spatial, sitewise gradient of amino acid diversity. To identify sitewise diversities consistent with efficient evolution in the context of a hydrophilic fibronectin domain, >10⁵ binders to six targets were evolved and sequenced. Evolutionarily favorable amino acid distributions at 25 sites reveal Shannon entropies (range: 0.3–3.9; median: 2.1; standard deviation: 1.1) supporting the diversity gradient hypothesis. Sitewise constraints in evolved sequences are consistent with complementarity, stability, and consensus biases. Implementation of sitewise constrained diversity enables direct selection of nanomolar affinity binders validating an efficient strategy to balance inter- and intra-molecular interaction demands at each site.     

Binding properties and evolution of homodimers in protein-protein interaction networks

We demonstrate that protein–protein interaction networks in several eukaryotic organisms contain significantly more self-interacting proteins than expected if such homodimers randomly appeared in the course of the evolution. We also show that on average homodimers have twice as many interaction partners than non-self-interacting proteins. More specifically, the likelihood of a protein to physically interact with itself was found to be proportional to the total number of its binding partners. These properties of dimers are in agreement with a phenomenological model, in which individual proteins differ from each other by the degree of their ‘stickiness’ or general propensity toward interaction with other proteins including oneself. A duplication of self-interacting proteins creates a pair of paralogous proteins interacting with each other. We show that such pairs occur more frequently than could be explained by pure chance alone. Similar to homodimers, proteins involved in heterodimers with their paralogs on average have twice as many interacting partners than the rest of the network. The likelihood of a pair of paralogous proteins to interact with each other was also shown to decrease with their sequence similarity. This points to the conclusion that most of interactions between paralogs are inherited from ancestral homodimeric proteins, rather than established de novo after duplication. We finally discuss possible implications of our empirical observations from functional and evolutionary standpoints.     

Dangerous liaisons: the ecology of private interest and common good

Many ecological interactions that are called mutualistic are in fact mixtures of antagonistic and mutualistic aspects. For example, plasmids exploit their bacterial hosts but also protect them against external threats. In this study, we analyse the conditions for the evolution of what we call 'dangerous liaisons': interactions combining mutualistic and antagonistic aspects. Starting point of our analysis is a model that was proposed as early as 1934. In this model, partners have to form a complex (either temporary or long lasting) in order to interact. Using this model framework we then set out to define and tease apart private interests of the interacting partners from their common good. This dichotomy provides a unifying perspective to classify ecological interactions. We discuss some examples to illustrate how the outcome of the interaction may depend on densities or on other contextual variables. Finally, we note that having a common good is not a necessary condition for partners to have aligned interests. In a dangerous liaison partners may have interest to cooperate even when this does not bolster the common good.     

Structural flexibility of small GTPases. Can it explain their functional versatility?

Multiple interactions with many different partners are responsible for the amazing functional versatility of proteins, especially those participating in cellular regulation. The structural properties that could facilitate multiple interactions are examined for small GTPases. The role of cellular constraints, compartmentation and scaffolds on protein-protein interactions is considered.     

Scanning image correlation spectroscopy

Molecular interactions are at the origin of life. How molecules get at different locations in the cell and how they locate their partners is a major and partially unresolved question in biology that is paramount to signaling. Spatio-temporal correlations of fluctuating fluorescently tagged molecules reveal how they move, interact, and bind in the different cellular compartments. Methods based on fluctuations represent a remarkable technical advancement in biological imaging. Here we discuss image analysis methods based on spatial and temporal correlation of fluctuations, raster image correlation spectroscopy, number and brightness, and spatial cross-correlations that give us information about how individual molecules move in cells and interact with partners at the single molecule level. These methods can be implemented with a standard laser scanning microscope and produce a cellular level spatio-temporal map of molecular interactions.     

Volatile terpenes – mediators of plant-to-plant communication

Plants interact with other organisms employing volatile organic compounds (VOCs). The largest group of plant-released VOCs are terpenes, comprised of isoprene, monoterpenes, and sesquiterpenes. Mono- and sesquiterpenes are well-known communication compounds in plant–insect interactions, whereas the smallest, most commonly emitted terpene, isoprene, is rather assigned a function in combating abiotic stresses. Recently, it has become evident that different volatile terpenes also act as plant-to-plant signaling cues. Upon being perceived, specific volatile terpenes can sensitize distinct signaling pathways in receiver plant cells, which in turn trigger plant innate immune responses. This vastly extends the range of action of volatile terpenes, which not only protect plants from various biotic and abiotic stresses, but also convey information about environmental constraints within and between plants. As a result, plant–insect and plant–pathogen interactions, which are believed to influence each other through phytohormone crosstalk, are likely equally sensitive to reciprocal regulation via volatile terpene cues. Here, we review the current knowledge of terpenes as volatile semiochemicals and discuss why and how volatile terpenes make good signaling cues. We discuss how volatile terpenes may be perceived by plants, what are possible downstream signaling events in receiver plants, and how responses to different terpene cues might interact to orchestrate the net plant response to multiple stresses. Finally, we discuss how the signal can be further transmitted to the community level leading to a mutually beneficial community-scale response or distinct signaling with near kin.     

J domain independent functions of J proteins

Heat shock proteins of 40 kDa (Hsp40s), also called J proteins, are obligate partners of Hsp70s. Via their highly conserved and functionally critical J domain, J proteins interact and modulate the activity of their Hsp70 partners. Mutations in the critical residues in the J domain often result in the null phenotype for the J protein in question. However, as more J proteins have been characterized, it is becoming increasingly clear that a significant number of J proteins do not “completely” rely on their J domains to carry out their cellular functions, as previously thought. In some cases, regions outside the highly conserved J domain have become more important making the J domain dispensable for some, if not for all functions of a J protein. This has profound effects on the evolution of such J proteins. Here we present selected examples of J proteins that perform J domain independent functions and discuss this in the context of evolution of J proteins with dispensable J domains and J-like proteins in eukaryotes.     

The consequences of synthetic auxin herbicide on plant–herbivore interactions

Although herbicide drift is a common side effect of herbicide application in agroecosystems, its effects on the ecology and evolution of natural communities are rarely studied. A recent shift to dicamba, a synthetic auxin herbicide known for ‘drifting’ to nontarget areas, necessitates the examination of drift effects on the plant–insect interactions that drive eco-evo dynamics in weed communities. We review current knowledge of direct effects of synthetic auxin herbicides on plant–insect interactions, focusing on plant herbivory, and discuss potential indirect effects, which are cascading effects on organisms that interact with herbicide-exposed plants. We end by developing a framework for the study of plant–insect interactions given drift, highlighting potential changes to plant developmental timing, resource quantity, quality, and cues.     

Bimolecular fluorescence complementation (BiFC) analysis of protein interactions in Caenorhabditis elegans

Protein interactions are essential components of signal transduction in cells. With the progress in genome-wide yeast two hybrid screens and proteomics analyses, many protein interaction networks have been generated. These analyses have identified hundreds and thousands of interactions in cells and organisms, creating a challenge for further validation under physiological conditions. The bimolecular fluorescence complementation (BiFC) assay is such an assay that meets this need. The BiFC assay is based on the principle of protein fragment complementation, in which two non-fluorescent fragments derived from a fluorescent protein are fused to a pair of interacting partners. When the two partners interact, the two non-fluorescent fragments are brought into proximity and an intact fluorescent protein is reconstituted. Hence, the reconstituted fluorescent signals reflect the interaction of two proteins under study. Over the past six years, the BiFC assay has been used for visualization of protein interactions in living cells and organisms, including our application of the BiFC assay to the transparent nematode Caenorhabditis elegans. We have demonstrated that BiFC analysis in C. elegans provides a direct means to identify and validate protein interactions in living worms and allows visualization of temporal and spatial interactions. Here, we provide a guideline for the implementation of BiFC analysis in living worms and discuss the factors that are critical for BiFC analysis.     

The yeast protein interaction network evolves rapidly and contains few redundant duplicate genes.

In this paper, the structure and evolution of the protein interaction network of the yeast Saccharomyces cerevisiae is analyzed. The network is viewed as a graph whose nodes correspond to proteins. Two proteins are connected by an edge if they interact. The network resembles a random graph in that it consists of many small subnets (groups of proteins that interact with each other but do not interact with any other protein) and one large connected subnet comprising more than half of all interacting proteins. The number of interactions per protein appears to follow a power law distribution. Within approximately 200 Myr after a duplication, the products of duplicate genes become almost equally likely to (1) have common protein interaction partners and (2) be part of the same subnetwork as two proteins chosen at random from within the network. This indicates that the persistence of redundant interaction partners is the exception rather than the rule. After gene duplication, the likelihood that an interaction gets lost exceeds 2.2 x 10(-3)/Myr. New interactions are estimated to evolve at a rate that is approximately three orders of magnitude smaller. Every 300 Myr, as many as half of all interactions may be replaced by new interactions.     

Legacy effects of aboveground-belowground interactions

Root herbivory can greatly affect the performance of aboveground insects via changes in plant chemistry. These interactions have been studied extensively in experiments where aboveground and belowground insects were feeding on the same plant. However, little is known about how aboveground and belowground organisms interact when they feed on plant individuals that grow after each other in the same soil. We show that feeding by aboveground and belowground insect herbivores on ragwort (Jacobaea vulgaris) plants exert unique soil legacy effects, via herbivore-induced changes in the composition of soil fungi. These changes in the soil biota induced by aboveground and belowground herbivores of preceding plants greatly influenced the pyrrolizidine alkaloid content, biomass and aboveground multitrophic interactions of succeeding plants. We conclude that plant-mediated interactions between aboveground and belowground insects are also important when they do not feed simultaneously on the same plant.     

PATHWAYS TO SOCIAL EVOLUTION: RECIPROCITY,RELATEDNESS, AND SYNERGY

Many organisms live in populations structured by space and by class, exhibit plastic responses to their social partners, and are subject to nonadditive ecological and fitness effects. Social evolution theory has long recognized that all of these factors can lead to different selection pressures but has only recently attempted to synthesize how these factors interact. Using models for both discrete and continuous phenotypes, we show that analyzing these factors in a consistent framework reveals that they interact with one another in ways previously overlooked. Specifically, behavioral responses (reciprocity), genetic relatedness, and synergy interact in nontrivial ways that cannot be easily captured by simple summary indices of assortment. We demonstrate the importance of these interactions by showing how they have been neglected in previous synthetic models of social behavior both within and between species. These interactions also affect the level of behavioral responses that can evolve in the long run; proximate biological mechanisms are evolutionarily stable when they generate enough responsiveness relative to the level of responsiveness that exactly balances the ecological costs and benefits. Given the richness of social behavior across taxa, these interactions should be a boon for empirical research as they are likely crucial for describing the complex relationship linking ecology, demography, and social behavior.