EDITORIAL
Current Approaches in Evolution: From Molecules to Cells and Organisms MUKUND THATTAI1* AND SERGIO G. PEISAJOVICH2 1 National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India 2 Department of Cell and Systems Biology, University of Toronto, Toronto, Ontario, Canada
ABSTRACT
J. Exp. Zool. (Mol. Dev. Evol.) 322B:465–467, 2014
This is an exciting time to be an evolutionary biologist. Indeed, it is difficult to keep up with all the studies that fall under the broad category of “Evolution” since they span species, traits, and scales of organization. This special issue gives a flavor of exciting new approaches in evolutionary biology, but also emphasizes universal themes. The reviews contained here discuss important aspects of molecular evolution at multiple scales, from individual proteins to complex regulatory networks, as well as from unicellular organisms to macroscopic traits in animals. Though the model systems are diverse, the issues addressed are fundamental: the origin of evolutionary novelties, and the forces that drive them to fixation. J. Exp. Zool. (Mol. Dev. Evol.) 322B:465–467, 2014. © 2014 Wiley Periodicals, Inc. How to cite this article: Thattai M, Peisajovich SG. 2014. Current approaches in evolution: From molecules to cells and organisms. J. Exp. Zool. (Mol. Dev. Evol.) 322B:465–467.
For a time, Darwin's theory of evolution appeared to be a victim of its own success. To any practicing biologist, evolution by natural selection may seem a tautology: some evolutionary trajectory must underlay the state of an organism in the present day, and it is easy enough to imagine plausible scenarios for almost any observed pattern. However, to move from a series of anecdotes to a global quantitative understanding of how processes from the micro to the macroscale interact, to actually generate and shape diversity, has proven to be much more difficult. One ultimate goal of evolutionary biology is to develop falsifiable, even predictive, theories of potential evolutionary trajectories. The key problem is one of timescales: evolution rarely operates at rates that can be observed in the laboratory under controlled conditions. As this issue highlights, there are many ways to surmount this obstacle. In essence, the idea is always to collect and interpret data spanning long evolutionary trajectories, either by comparing distantly related organisms, or by accelerating mutation rates in laboratory evolution experiments. In this way, the results of experimental measurements can be extrapolated to the required timescales. Among the many novel approaches that are constantly being added to the toolkit of twenty‐first century evolutionary biologists, we can mention for instance the expanding set of model organisms, the ability to sample across
a broad range of species, the development of new phylogenetic techniques, which rely on the explosion of sequence data, and the integration of directed evolution and synthetic biology strategies to mimic relevant evolutionary processes in the laboratory. Directed evolution studies, which are based on the selection of large libraries of mutant genotypes under laboratory‐controlled conditions, have shed light on important aspects of protein evolution. Synthetic biology is now drastically expanding the scope of directed evolution studies, by shifting the focus from the
Conflicts of interest: None. Correspondences to: Mukund Thattai, National Centre for Biological Sciences, Tata Institute of Fundamental Research, GKVK Campus, Bellary Road, Bangalore 560065, India. E‐mail: [email protected] Correspondences to: Sergio G. Peisajovich, Department of Cell and Systems Biology, University of Toronto, 25 Harbord Street, Toronto, ON, Canada M5S 3G5. E‐mail: [email protected] Received 9 June 2014; Revised 18 June 2014; Accepted 18 June 2014 DOI: 10.1002/jez.b.22586 Published online 16 July 2014 in Wiley Online Library (wileyonlinelibrary.com).
© 2014 WILEY PERIODICALS, INC.
466 individual gene to the network. Using synthetic biology approaches, it is now possible to mimic in the laboratory evolutionary processes that re‐wire regulatory networks, unraveling the nature of intermediate steps, as well as possible complex trajectories, as discussed in detail in a recent review in this journal (Di Roberto and Peisajovich, 2014). The reviews presented in this special issue are testimony to the success of these novel conceptual, computational, and experimental approaches. The review by Kaltenbach and Tokuriki discusses how constraints in enzyme evolution affect evolutionary trajectories, in particular highlighting laboratory evolution studies that mimic natural evolution under precisely defined conditions. In particular, Kaltenback and Tokuriki argue that, while enzyme promiscuity provides the starting point for new enzymatic activities to evolve along a fitness landscape, two important features of fitness landscapes may actually impose constraints to evolution. First, rugged fitness landscapes could trap enzymes in suboptimal fitness peaks. Second, because evolutionary trajectories need to proceed through functional intermediate steps, the evolution of a catalytic activity characterized by a given fitness landscape, into a second activity defined by a different landscape, apparently could only occur when the fitness peaks of both activities (at least partially) overlap. The review by Diss et al. focuses on the role that paralog genes have in robustness against environmental or genetic perturbations. In particular, they discuss molecular mechanisms responsible for functional compensation between paralogs. These include: (i) passive compensation, for example, when the original expression and functional levels of one of the paralogs suffices to compensate for the loss of the other paralog; and (ii) the far more interesting active mechanisms of compensation, which require an element that senses the loss of a paralog and in consequence modifies some aspects of the expression, function, or localization of the other paralog, resulting in the compensation of the initial loss. Specifically, they present examples illustrating how active compensation can result from transcriptional reprogramming, the re‐wiring of protein interaction networks, or protein re‐localization. The reviews of Briguglio and Turkewitz on the membrane traffic system of a complex unicellular eukaryote, and of Agashe and Shankar on the base composition of bacterial genomes, highlight many contrasting ideas. Briguglio and Turkewitz forcefully argue that the tyranny of “model organisms” has prevented the discovery of new modes of evolutionary innovation. They provide a valuable and timely review on the fascinating biology of ciliates, using the free‐living protist Tetrahymena thermopila as a model. In particular, they focus on the intracellular traffic network of this organism. Most studies of membrane traffic have focused on fungi and animals, which are rather closely related on the scale of eukaryotic diversity. Tetrahymena is only distantly related to animals, and provides an opportunity to look at truly universal features of J. Exp. Zool. (Mol. Dev. Evol.)
THATTAI AND PEISAJOVICH eukaryotes, as well as lineage‐specific innovations. Cell biological studies of proteins such as Rab GTPases, vesicle coats and cytoskeletal proteins, when combined with phylogenetic approaches, reveal how ancient molecules have been adapted for novel functions. Though these studies all focus on a single species, its place on the tree of life (far from other model organisms) gives the results a long lever arm, allowing us to discern broad evolutionary trends. Agashe and Shankar consider a trait that, on its face, appears much simpler than the membrane traffic apparatus: the base composition of bacterial genomes. Because this quantity is relatively easy to measure, it has been a staple of microbiological inquiry for decades. Surprisingly, we still do not have a satisfactory theory to explain the range of observed genomic GC contents. Agashe and Shankar discuss various potential expiations for why different bacterial species might have different GC contents, ranging from non‐adaptive explanations such as mutation bias, to adaptive selection‐based ideas, and most intriguingly, potential environmental explanations such as temperature and nutrient limitation. They emphasize new approaches in which the global GC content of a genome might be the result of very local pressures acting at the level of individual genes, hypotheses of this kind are amenable to experimental investigation, though recent experiments seem to have generated more questions than answers. The review by Hauser, van Hazel, and Chang is a great example of how the integration of experimental and computational approaches can shed light on evolutionary innovations, while, remarkably, informing us about ecology and animal behavior. Specifically, they focus their attention on visual pigments that mediate vision in the ultraviolet range of the spectrum, as ultraviolet vision plays important roles in aspects of behavior, such as courtship, that are central to evolution. Hauser, van Hazel, and Chang connect experimental studies that have determined how spectral sensitivities depend on specific amino acid sequences in visual proteins, with comparative sequence analysis in different animals. They argue that in birds spectral tuning mechanisms are consistent and therefore behavioral inferences based on the amino acid sequences of visual pigments are reasonable. In contrast, experimental studies have shown that the spectral sensitivity of mammalian visual pigments seems to be affected by more complex inter‐residue interactions, and thus predictions based solely on sequence comparisons is far more difficult in this group. Finally, the review by Freitas, Gomez‐Skarmeta, and Rodriguez highlights recent findings that have shed light on the evolution of fin development in vertebrates. In particular, they first discuss molecular events that may have guided the evolutionary transition from animals with only unpaired dorsal midline finfolds to animals with paired latero‐ventral fins. In the second part, they move on to discuss the molecular changes that facilitated the evolution of tetrapod limbs from fish paired fins.
CURRENT APPROACHES IN EVOLUTION In the end, we must employ a diversity of approaches if we are to understand how universal the dynamics of evolutionary processes are, and how they play out in detail. These reviews show that we must study “traits” which are both experimentally tractable, and which are sufficiently varied across molecules, species, or lineages. By examining the series of events, leading to the present‐day distribution of such traits, we can better understand evolutionary
467 dynamics; until eventually, broad patterns begin to emerge. Thus, even narrowly defined traits can reveal universal truths.
LITERATURE CITED Di Roberto RB, Peisajovich SG. 2014. The role of domain shuffling in the evolution of signaling networks. J Exp Zool B Mol Dev Evol 322:65–72.
J. Exp. Zool. (Mol. Dev. Evol.)
Current Approaches in Evolution: From Molecules to Cells and Organisms MUKUND THATTAI1* AND SERGIO G. PEISAJOVICH2 1 National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India 2 Department of Cell and Systems Biology, University of Toronto, Toronto, Ontario, Canada
ABSTRACT
J. Exp. Zool. (Mol. Dev. Evol.) 322B:465–467, 2014
This is an exciting time to be an evolutionary biologist. Indeed, it is difficult to keep up with all the studies that fall under the broad category of “Evolution” since they span species, traits, and scales of organization. This special issue gives a flavor of exciting new approaches in evolutionary biology, but also emphasizes universal themes. The reviews contained here discuss important aspects of molecular evolution at multiple scales, from individual proteins to complex regulatory networks, as well as from unicellular organisms to macroscopic traits in animals. Though the model systems are diverse, the issues addressed are fundamental: the origin of evolutionary novelties, and the forces that drive them to fixation. J. Exp. Zool. (Mol. Dev. Evol.) 322B:465–467, 2014. © 2014 Wiley Periodicals, Inc. How to cite this article: Thattai M, Peisajovich SG. 2014. Current approaches in evolution: From molecules to cells and organisms. J. Exp. Zool. (Mol. Dev. Evol.) 322B:465–467.
For a time, Darwin's theory of evolution appeared to be a victim of its own success. To any practicing biologist, evolution by natural selection may seem a tautology: some evolutionary trajectory must underlay the state of an organism in the present day, and it is easy enough to imagine plausible scenarios for almost any observed pattern. However, to move from a series of anecdotes to a global quantitative understanding of how processes from the micro to the macroscale interact, to actually generate and shape diversity, has proven to be much more difficult. One ultimate goal of evolutionary biology is to develop falsifiable, even predictive, theories of potential evolutionary trajectories. The key problem is one of timescales: evolution rarely operates at rates that can be observed in the laboratory under controlled conditions. As this issue highlights, there are many ways to surmount this obstacle. In essence, the idea is always to collect and interpret data spanning long evolutionary trajectories, either by comparing distantly related organisms, or by accelerating mutation rates in laboratory evolution experiments. In this way, the results of experimental measurements can be extrapolated to the required timescales. Among the many novel approaches that are constantly being added to the toolkit of twenty‐first century evolutionary biologists, we can mention for instance the expanding set of model organisms, the ability to sample across
a broad range of species, the development of new phylogenetic techniques, which rely on the explosion of sequence data, and the integration of directed evolution and synthetic biology strategies to mimic relevant evolutionary processes in the laboratory. Directed evolution studies, which are based on the selection of large libraries of mutant genotypes under laboratory‐controlled conditions, have shed light on important aspects of protein evolution. Synthetic biology is now drastically expanding the scope of directed evolution studies, by shifting the focus from the
Conflicts of interest: None. Correspondences to: Mukund Thattai, National Centre for Biological Sciences, Tata Institute of Fundamental Research, GKVK Campus, Bellary Road, Bangalore 560065, India. E‐mail: [email protected] Correspondences to: Sergio G. Peisajovich, Department of Cell and Systems Biology, University of Toronto, 25 Harbord Street, Toronto, ON, Canada M5S 3G5. E‐mail: [email protected] Received 9 June 2014; Revised 18 June 2014; Accepted 18 June 2014 DOI: 10.1002/jez.b.22586 Published online 16 July 2014 in Wiley Online Library (wileyonlinelibrary.com).
© 2014 WILEY PERIODICALS, INC.
466 individual gene to the network. Using synthetic biology approaches, it is now possible to mimic in the laboratory evolutionary processes that re‐wire regulatory networks, unraveling the nature of intermediate steps, as well as possible complex trajectories, as discussed in detail in a recent review in this journal (Di Roberto and Peisajovich, 2014). The reviews presented in this special issue are testimony to the success of these novel conceptual, computational, and experimental approaches. The review by Kaltenbach and Tokuriki discusses how constraints in enzyme evolution affect evolutionary trajectories, in particular highlighting laboratory evolution studies that mimic natural evolution under precisely defined conditions. In particular, Kaltenback and Tokuriki argue that, while enzyme promiscuity provides the starting point for new enzymatic activities to evolve along a fitness landscape, two important features of fitness landscapes may actually impose constraints to evolution. First, rugged fitness landscapes could trap enzymes in suboptimal fitness peaks. Second, because evolutionary trajectories need to proceed through functional intermediate steps, the evolution of a catalytic activity characterized by a given fitness landscape, into a second activity defined by a different landscape, apparently could only occur when the fitness peaks of both activities (at least partially) overlap. The review by Diss et al. focuses on the role that paralog genes have in robustness against environmental or genetic perturbations. In particular, they discuss molecular mechanisms responsible for functional compensation between paralogs. These include: (i) passive compensation, for example, when the original expression and functional levels of one of the paralogs suffices to compensate for the loss of the other paralog; and (ii) the far more interesting active mechanisms of compensation, which require an element that senses the loss of a paralog and in consequence modifies some aspects of the expression, function, or localization of the other paralog, resulting in the compensation of the initial loss. Specifically, they present examples illustrating how active compensation can result from transcriptional reprogramming, the re‐wiring of protein interaction networks, or protein re‐localization. The reviews of Briguglio and Turkewitz on the membrane traffic system of a complex unicellular eukaryote, and of Agashe and Shankar on the base composition of bacterial genomes, highlight many contrasting ideas. Briguglio and Turkewitz forcefully argue that the tyranny of “model organisms” has prevented the discovery of new modes of evolutionary innovation. They provide a valuable and timely review on the fascinating biology of ciliates, using the free‐living protist Tetrahymena thermopila as a model. In particular, they focus on the intracellular traffic network of this organism. Most studies of membrane traffic have focused on fungi and animals, which are rather closely related on the scale of eukaryotic diversity. Tetrahymena is only distantly related to animals, and provides an opportunity to look at truly universal features of J. Exp. Zool. (Mol. Dev. Evol.)
THATTAI AND PEISAJOVICH eukaryotes, as well as lineage‐specific innovations. Cell biological studies of proteins such as Rab GTPases, vesicle coats and cytoskeletal proteins, when combined with phylogenetic approaches, reveal how ancient molecules have been adapted for novel functions. Though these studies all focus on a single species, its place on the tree of life (far from other model organisms) gives the results a long lever arm, allowing us to discern broad evolutionary trends. Agashe and Shankar consider a trait that, on its face, appears much simpler than the membrane traffic apparatus: the base composition of bacterial genomes. Because this quantity is relatively easy to measure, it has been a staple of microbiological inquiry for decades. Surprisingly, we still do not have a satisfactory theory to explain the range of observed genomic GC contents. Agashe and Shankar discuss various potential expiations for why different bacterial species might have different GC contents, ranging from non‐adaptive explanations such as mutation bias, to adaptive selection‐based ideas, and most intriguingly, potential environmental explanations such as temperature and nutrient limitation. They emphasize new approaches in which the global GC content of a genome might be the result of very local pressures acting at the level of individual genes, hypotheses of this kind are amenable to experimental investigation, though recent experiments seem to have generated more questions than answers. The review by Hauser, van Hazel, and Chang is a great example of how the integration of experimental and computational approaches can shed light on evolutionary innovations, while, remarkably, informing us about ecology and animal behavior. Specifically, they focus their attention on visual pigments that mediate vision in the ultraviolet range of the spectrum, as ultraviolet vision plays important roles in aspects of behavior, such as courtship, that are central to evolution. Hauser, van Hazel, and Chang connect experimental studies that have determined how spectral sensitivities depend on specific amino acid sequences in visual proteins, with comparative sequence analysis in different animals. They argue that in birds spectral tuning mechanisms are consistent and therefore behavioral inferences based on the amino acid sequences of visual pigments are reasonable. In contrast, experimental studies have shown that the spectral sensitivity of mammalian visual pigments seems to be affected by more complex inter‐residue interactions, and thus predictions based solely on sequence comparisons is far more difficult in this group. Finally, the review by Freitas, Gomez‐Skarmeta, and Rodriguez highlights recent findings that have shed light on the evolution of fin development in vertebrates. In particular, they first discuss molecular events that may have guided the evolutionary transition from animals with only unpaired dorsal midline finfolds to animals with paired latero‐ventral fins. In the second part, they move on to discuss the molecular changes that facilitated the evolution of tetrapod limbs from fish paired fins.
CURRENT APPROACHES IN EVOLUTION In the end, we must employ a diversity of approaches if we are to understand how universal the dynamics of evolutionary processes are, and how they play out in detail. These reviews show that we must study “traits” which are both experimentally tractable, and which are sufficiently varied across molecules, species, or lineages. By examining the series of events, leading to the present‐day distribution of such traits, we can better understand evolutionary
467 dynamics; until eventually, broad patterns begin to emerge. Thus, even narrowly defined traits can reveal universal truths.
LITERATURE CITED Di Roberto RB, Peisajovich SG. 2014. The role of domain shuffling in the evolution of signaling networks. J Exp Zool B Mol Dev Evol 322:65–72.
J. Exp. Zool. (Mol. Dev. Evol.)
