Tasks and perspectives of development of evolutionary physiology

The paper considers the main tasks facing evolutionary physiology as well as the methods that allow these tasks to be solved. It is shown that alongside with traditional, classical methods (phylogenetic, ontogenetic, experimental, clinical), there developed and got recognition in the present-day evolutionary physiology principally new methodological approaches important for solution of actual problems of this discipline. It is the method of mathematical modeling of functions, which makes it possible not only to study on the model, in temporary scales convenient for analysis, evolution of the given functions under the given actions, but also to model the evolutionary process itself in its different manifestations. It is the method of gene engineering that allows studying processes of formation of specific functional systems, their interaction and “mutual adjustment” at the organism level. It is lastly the method of tissue cultures allowing reconstruction under artificial conditions various systems of organism and study of regularities and mechanisms of morphogenesis and formation of functions. The paper discusses trends of development of evolutionary physiology for the last few years, considers perspective directions of studies, using specific examples, and shows possible ways for practical applications of fundamental investigations in the field of evolutionary physiology. Journal variant of the report published in the Collection of Papers “Tendency of Development of Physiological Sciences,” St. Petersburg, 2000.     

Evolution of evolutionary physiology

In 19th century and at the beginning 20th century, reports appeared in the field of comparative and ontogenetic physiology and the value of these methods for understanding of evolution of functions. The term "evolutionary physiology" was suggested by A. N. Severtsov in 1914. In the beginning of 30s, in the USSR, laboratories for researches in problems of evolutionary physiology were created, the results of these researches having been published. In 1956 in Leningrad, the Institute of Evolutionary Physiology was founded by L. A. Orbeli. He formulates the goals and methods of evolutionary physiology. In the following half a century, the evolutionary physiology was actively developed. The evolutionary physiology solves problems of evolution of function of functions evolution, often involving methods of adjacent sciences, including biochemistry, morphology, molecular biology.     

Charles Darwin,evolutionary physiology,and origin of life

In the first half of the 19th century investigations began in the field of comparative and ontogenetic physiology, and the publication of On the Origin of Species by Charles Darwin became a further stimulus for the development of problems of evolutionary physiology. The term evolutionary physiology was coined by A.N. Severtzov in 1914, in the early 1930s the USSR created laboratories for the development of problems of evolutionary physiology. In 1956 L.A. Orbeli organized the Sechenov Institute of Evolutionary Physiology (Academy of Sciences of the USSR) in Leningrad. This paper discusses the problems of physiological paleontology, principles of the evolution of functions, regularities in functional evolution, and physiologic approaches to the origin of cell and life.     

Physiological regulatory networks: ecological roles and evolutionary constraints

Ecological and evolutionary physiology has traditionally focused on one aspect of physiology at a time. Here, we discuss the implications of considering physiological regulatory networks (PRNs) as integrated wholes, a perspective that reveals novel roles for physiology in organismal ecology and evolution. For example, evolutionary response to changes in resource abundance might be constrained by the role of dietary micronutrients in immune response regulation, given a particular pathogen environment. Because many physiological components impact more than one process, organismal homeostasis is maintained, individual fitness is determined and evolutionary change is constrained (or facilitated) by interactions within PRNs. We discuss how PRN structure and its system-level properties could determine both individual performance and patterns of physiological evolution.     

Trade-offs in thermal adaptation: the need for a molecular to ecological integration

Through functional analyses, integrative physiology is able to link molecular biology with ecology as well as evolutionary biology and is thereby expected to provide access to the evolution of molecular, cellular, and organismic functions; the genetic basis of adaptability; and the shaping of ecological patterns. This paper compiles several exemplary studies of thermal physiology and ecology, carried out at various levels of biological organization from single genes (proteins) to ecosystems. In each of those examples, trade-offs and constraints in thermal adaptation are addressed; these trade-offs and constraints may limit species' distribution and define their level of fitness. For a more comprehensive understanding, the paper sets out to elaborate the functional and conceptual connections among these independent studies and the various organizational levels addressed. This effort illustrates the need for an overarching concept of thermal adaptation that encompasses molecular, organellar, cellular, and whole-organism information as well as the mechanistic links between fitness, ecological success, and organismal physiology. For this data, the hypothesis of oxygen- and capacity-limited thermal tolerance in animals provides such a conceptual framework and allows interpreting the mechanisms of thermal limitation of animals as relevant at the ecological level. While, ideally, evolutionary studies over multiple generations, illustrated by an example study in bacteria, are necessary to test the validity of such complex concepts and underlying hypotheses, animal physiology frequently is constrained to functional studies within one generation. Comparisons of populations in a latitudinal cline, closely related species from different climates, and ontogenetic stages from riverine clines illustrate how evolutionary information can still be gained. An understanding of temperature-dependent shifts in energy turnover, associated with adjustments in aerobic scope and performance, will result. This understanding builds on a mechanistic analysis of the width and location of thermal windows on the temperature scale and also on study of the functional properties of relevant proteins and associated gene expression mechanisms.     

An integrative model of evolutionary covariance: a symposium on body shape in fishes

A major direction of current and future biological research is to understand how multiple, interacting functional systems coordinate in producing a body that works. This understanding is complicated by the fact that organisms need to work well in multiple environments, with both predictable and unpredictable environmental perturbations. Furthermore, organismal design reflects a history of past environments and not a plan for future environments. How complex, interacting functional systems evolve, then, is a truly grand challenge. In accepting the challenge, an integrative model of evolutionary covariance is developed. The model combines quantitative genetics, functional morphology/physiology, and functional ecology. The model is used to convene scientists ranging from geneticists, to physiologists, to ecologists, to engineers to facilitate the emergence of body shape in fishes as a model system for understanding how complex, interacting functional systems develop and evolve. Body shape of fish is a complex morphology that (1) results from many developmental paths and (2) functions in many different behaviors. Understanding the coordination and evolution of the many paths from genes to body shape, body shape to function, and function to a working fish body in a dynamic environment is now possible given new technologies from genetics to engineering and new theoretical models that integrate the different levels of biological organization (from genes to ecology).     

Heterotachy, an important process of protein evolution.

Because of functional constraints, substitution rates vary among the positions of a protein but are usually assumed to be constant at a given site during evolution. The distribution of the rates across the sequence positions generally fits a Gamma distribution. Models of sequence evolution were accordingly designed and led to improved phylogenetic reconstruction. However, it has been convincingly demonstrated that the evolutionary rate of a given position is not always constant throughout time. We called such within-site rate variations heterotachy (for "different speed" in Greek). Yet, heterotachy was found among homologous sequences of distantly related organisms, often with different functions. In such cases, the functional constraints are likely different, which would explain the different distribution of variable sites. To evaluate the importance of heterotachy, we focused on amino acid sequences of mitochondrial cytochrome b, for which the function is likely the same in all vertebrates. Using 2,038 sequences, we demonstrate that 95% of the variable positions are heterotachous, i.e., underwent dramatic variations of substitution rate among vertebrate lineages. Heterotachy even occurs at small evolutionary scale, and in these cases it is very unlikely to be related to functional changes. Since a large number of sequences are required to efficiently detect heterotachy, the extent of this phenomenon could not be estimated for all proteins yet. It could be as large as for cytochrome b, since this protein is not a peculiar case. The observations made here open several new avenues of research, such as the understanding of the evolution of functional constraints or the improvement of phylogenetic reconstruction methods.     

Whole-organism studies of adhesion in pad-bearing lizards: creative evolutionary solutions to functional problems

Understanding the evolution of complex functional traits is a challenge for evolutionary physiology. Here we investigate the evolution of subdigital toepads in lizards, which have arisen independently at least three times, although with subtle anatomical differences. Some designs (anole, gecko) appear functionally equivalent, whereas other designs (skink) are inferior. The functional equivalence of geckos and anoles highlights the creative aspect of the evolutionary process in that these two groups have arrived at the same functional endpoint along very different trajectories. However, this functional equivalence does not result in equivalence for performance at whole-organism tasks (e.g., running uphill), as the evolution of behavior (e.g., toe-furling) has enabled geckos to be superior climbers than anoles. We also show that adaptive increases in the toepad size within a closely related lizard genus (Anolis) has resulted in concomitant evolution of enhanced clinging ability and increased perch heights. A third insight is that pad-bearing geckos are capable of carrying tremendous loads (up to 250% of body weight) up smooth surfaces, and that the toepad itself does not appear limiting. This comparative and whole-organism approach to lizard toepads underscores how organisms can evolve multiple solutions to evolutionary problems.     

An evolutionary treatment of the morphology and physiology of circulatory organs in insects

An overview from an evolutionary perspective is presented on the research of the past 2 decades on insect circulatory organs. Based on various functional morphology it is clear that the flow mode of the dorsal vessel ('heart') has changed during the evolution of hexapods. In all apterygotes and mayflies the flow is bidirectional. In most pterygote insects, however, it is unidirectional. In some endopterygote insects, the direction of the flow alternates. This is achieved by heartbeat reversal, which may have various physiological functions and is a derived condition that probably occurred several times during the course of insect evolution. Special attention is given to the hemolymph flow in body appendages. In ancestral hexapods, they are supplied by arteries, whereas circulation in appendages of higher insects is accomplished by accessory pulsatile organs. These auxiliary hearts are autonomous pumps and exhibit a great diversity in their functional morphology. They represent evolutionary innovations which evolved by recruitment of building blocks from various organ systems and were assembled into new functional units. Almost all pulsatile circulatory organs in insects investigated exhibit a myogenic automatism with a superimposed neuronal control. The neuroanatomy of insect circulatory organs has been investigated only in a small number of species but in considerable detail. Numerous potential peptidergic and a few aminergic mediators could be demonstrated by immunocytochemical and biochemical methods. The cardiotropic effectiveness of these mediators may vary among species and it can be stated that there is no uniform picture of the control of the various circulatory organs in insects. A possible explanation for the differences may lie in the different evolutionary origins of the muscular components. Furthermore, insect circulatory organs may represent important neurohemal releasing sites.     

Scientific schools: traditions, dogmas, progress in the study of the brain evolution

The role of traditions, revision of dogmatic concepts, and emergence of novel theories in the investigations of the vertebrate brain evolution on the bases of modern neuroscientific data represent the objective of the present paper. Problems of homology, encephalization, recapitulation, dissolution, and the significance of their revision for understanding the brain evolution are considered. Arguments for equal importance in studying consequences of both phylogenetic and divergent adaptive evolution are presented. Comparative study of functional mechanisms is suggested as a perspective trend of the evolutionary physiology. It will be a valuable tool both for understanding the brain evolution and for applied investigations in neurobiology and medicine.     

Motifs,modules and games in bacteria

Global explorations of regulatory network dynamics, organization and evolution have become tractable thanks to high-throughput sequencing and molecular measurement of bacterial physiology. From these, a nascent conceptual framework is developing, that views the principles of regulation in term of motifs, modules and games. Motifs are small, repeated, and conserved biological units ranging from molecular domains to small reaction networks. They are arranged into functional modules, genetically dissectible cellular functions such as the cell cycle, or different stress responses. The dynamical functioning of modules defines the organism's strategy to survive in a game, pitting cell against cell, and cell against environment. Placing pathway structure and dynamics into an evolutionary context begins to allow discrimination between those physical and molecular features that particularize a species to its surroundings, and those that provide core physiological function. This approach promises to generate a higher level understanding of cellular design, pathway evolution and cellular bioengineering.     

Modular evolution and increase of functional complexity in replicating RNA molecules

At early stages of biochemical evolution, the complexity of replicating molecules was limited by unavoidably high mutation rates. In an RNA world, prior to the appearance of cellular life, an increase in molecular length, and thus in functional complexity, could have been mediated by modular evolution. We describe here a scenario in which short, replicating RNA sequences are selected to perform a simple function. Molecular function is represented through the secondary structure corresponding to each sequence, and a given target secondary structure yields the optimal function in the environment where the population evolves. The combination of independently evolved populations may have facilitated the emergence of larger molecules able to perform more complex functions (including RNA replication) that could arise as a combination of simpler ones. We quantitatively show that modular evolution has relevant advantages with respect to the direct evolution of large functional molecules, among them the allowance of higher mutation rates, the shortening of evolutionary times, and the very possibility of finding complex structures that could not be otherwise directly selected.     

Questioning the Ubiquity of Neofunctionalization

Gene duplication provides much of the raw material from which functional diversity evolves. Two evolutionary mechanisms have been proposed that generate functional diversity: neofunctionalization, the de novo acquisition of function by one duplicate, and subfunctionalization, the partitioning of ancestral functions between gene duplicates. With protein interactions as a surrogate for protein functions, evidence of prodigious neofunctionalization and subfunctionalization has been identified in analyses of empirical protein interactions and evolutionary models of protein interactions. However, we have identified three phenomena that have contributed to neofunctionalization being erroneously identified as a significant factor in protein interaction network evolution. First, self-interacting proteins are underreported in interaction data due to biological artifacts and design limitations in the two most common high-throughput protein interaction assays. Second, evolutionary inferences have been drawn from paralog analysis without consideration for concurrent and subsequent duplication events. Third, the theoretical model of prodigious neofunctionalization is unable to reproduce empirical network clustering and relies on untenable parameter requirements. In light of these findings, we believe that protein interaction evolution is more persuasively characterized by subfunctionalization and self-interactions.     

A bigger mouse? The rat genome unveiled

Rattus norvegicus is an important experimental organism and interesting to evolutionary biologists. The recently published draft rat genome sequence provides us with insights into both the rat's evolution and its physiology. We learn more about genome evolution and, in particular, the adaptive significance of gene family expansions and the evolution of rodent genomes, which appears to have decelerated since the divergence of mouse and rat. An important observation is that some regions of genomes, many in noncoding regions, show very high sequence conservation, while others show unexpectedly fast evolution. Both of these may be pointers to functional significance.     

Acanthamoeba is an evolutionary ancestor of macrophages: A myth or reality?

Given the remarkable similarities in cellular structure (morphological and ultra-structural features), molecular motility, biochemical physiology, ability to capture prey by phagocytosis and interactions with microbial pathogens, here we pose the question whether Acanthamoeba and macrophages are evolutionary related. This is discussed in the light of evolution and functional aspects such as the astonishing resemblance of many bacteria to infect and multiply inside human macrophages and amoebae in analogous ways. Further debate and studies will determine if Acanthamoeba is an evolutionary ancestor of macrophages. Is this a myth or reality?     

High evolutionary and functional distinctiveness of endemic monocots in world islands

Functionally and evolutionarily distinct species have traits or an evolutionary history that are shared by few others in a given set, which make them priority species for biodiversity conservation. On islands, life in isolation has led to the evolution of many distinct forms and functions as well as to a high level of endemism. The aim of this study is to assess the evolutionary and functional distinctiveness of insular monocotyledons and their distribution across 126 islands worldwide. We show that evolutionary and functional distinctiveness are decoupled but that both are higher on islands than on continental areas. Anagenesis on islands followed by extinctions and/or diversification on the mainland may have led to highly evolutionarily distinct species while functionally distinct species may have arisen from ecological niche shift or niche expansion. Insular endemic species with high evolutionary distinctiveness but not with high functional distinctiveness are significantly range-restricted compared to less distinct species, possibly indicating differences in dispersal potential. By showing that distinctiveness is high on islands and that the most distinct species are range-restricted, our study has important conservation implications. Indeed, islands are among the most threatened systems of the world, and extinctions of the most distinct species could lead to significant loss of phylogenetic and functional diversity.

     

Coiled-Coil Proteins Facilitated the Functional Expansion of the Centrosome

Repurposing existing proteins for new cellular functions is recognized as a main mechanism of evolutionary innovation, but its role in organelle evolution is unclear. Here, we explore the mechanisms that led to the evolution of the centrosome, an ancestral eukaryotic organelle that expanded its functional repertoire through the course of evolution. We developed a refined sequence alignment technique that is more sensitive to coiled coil proteins, which are abundant in the centrosome. For proteins with high coiled-coil content, our algorithm identified 17% more reciprocal best hits than BLAST. Analyzing 108 eukaryotic genomes, we traced the evolutionary history of centrosome proteins. In order to assess how these proteins formed the centrosome and adopted new functions, we computationally emulated evolution by iteratively removing the most recently evolved proteins from the centrosomal protein interaction network. Coiled-coil proteins that first appeared in the animal–fungi ancestor act as scaffolds and recruit ancestral eukaryotic proteins such as kinases and phosphatases to the centrosome. This process created a signaling hub that is crucial for multicellular development. Our results demonstrate how ancient proteins can be co-opted to different cellular localizations, thereby becoming involved in novel functions.     

Processes of fungal proteome evolution and gain of function: gene duplication and domain rearrangement

During evolution, organisms have gained functional complexity mainly by modifying and improving existing functioning systems rather than creating new ones ab initio. Here we explore the interplay between two processes which during evolution have had major roles in the acquisition of new functions: gene duplication and protein domain rearrangements. We consider four possible evolutionary scenarios: gene families that have undergone none of these event types; only gene duplication; only domain rearrangement, or both events. We characterize each of the four evolutionary scenarios by functional attributes. Our analysis of ten fungal genomes indicates that at least for the fungi clade, species significantly appear to gain complexity by gene duplication accompanied by the expansion of existing domain architectures via rearrangements. We show that paralogs gaining new domain architectures via duplication tend to adopt new functions compared to paralogs that preserve their domain architectures. We conclude that evolution of protein families through gene duplication and domain rearrangement is correlated with their functional properties. We suggest that in general, new functions are acquired via the integration of gene duplication and domain rearrangements rather than each process acting independently.     

Evolution of protein phosphorylation for distinct functional modules in vertebrate genomes

Recent publications have revealed that the evolution of phosphosites is influenced by the local protein structures and whether the phosphosites have characterized functions or not. With knowledge of the wide functional range of phosphorylation, we attempted to clarify whether the evolutionary conservation of phosphosites is different among distinct functional modules. We grouped the phosphosites in the human genome into the modules according to the functional categories of KEGG (Kyoto Encyclopedia of Genes and Genomes) and investigated their evolutionary conservation in vertebrate genomes from mouse to zebrafish. We have found that the phosphosites in the vertebrate-specific functional modules (VFMs), such as cellular signaling processes and responses to stimuli, are evolutionarily more conserved than those in the basic functional modules (BFMs), such as metabolic and genetic processes. The phosphosites in the VFMs are also significantly more conserved than their flanking regions, whereas those in the BFMs are not. These results hold for both serine/threonine and tyrosine residues, although the fraction of phosphorylated tyrosine residues is increased in the VFMs. Moreover, the difference in the evolutionary conservation of the phosphosites between the VFMs and BFMs could not be explained by the difference in the local protein structures. There is also a higher fraction of phosphosites with known functions in the VFMs than BFMs. Based on these findings, we have concluded that protein phosphorylation may play more dominant roles for the VFMs than BFMs during the vertebrate evolution. As phosphorylation is a quite rapid biological reaction, the VFMs that quickly respond to outer stimuli and inner signals might heavily depend on this regulatory mechanism. Our results imply that phosphorylation may have an essential role in the evolution of vertebrates.