Evolutionary Novelty and the Evo-Devo Synthesis: Field Notes

Accounting for the evolutionary origins of morphological novelty is one of the core challenges of contemporary evolutionary biology. A successful explanatory framework requires the integration of different biological disciplines, but the relationships between developmental biology and standard evolutionary biology remain contested. There is also disagreement about how to define the concept of evolutionary novelty. These issues were the subjects of a workshop held in November 2009 at the University of Alberta. We report on the discussion and results of this workshop, addressing questions about (i) how to define evolutionary novelty and understand its significance, (ii) how to interpret evolutionary developmental biology as a synthesis and its relation to neo-Darwinian evolutionary theory, and (iii) how to integrate disparate biological approaches in general.     

Evolutionary Developmental Biology (Evo-Devo): Past, Present, and Future

Evolutionary developmental biology (evo–devo) is that part of biology concerned with how changes in embryonic development during single generations relate to the evolutionary changes that occur between generations. Charles Darwin argued for the importance of development (embryology) in understanding evolution. After the discovery in 1900 of Mendel’s research on genetics, however, any relationship between development and evolution was either regarded as unimportant for understanding the process(es) of evolution or as a black box into which it was hard to see. Research over the past two decades has opened that black box, revealing how studies in evo–devo highlight the mechanisms that link genes (the genotype) with structures (the phenotype). This is vitally important because genes do not make structures. Developmental processes make structures using road maps provided by genes, but using many other signals as well—physical forces such as mechanical stimulation, temperature of the environment, and interaction with chemical products produced by other species—often species in entirely different kingdoms as in interactions between bacteria and squid or between leaves and larvae (Greene Science 243:643–666, 1989). Not only do genes not make structures (the phenotype), but new properties and mechanisms emerge during embryonic development: genes are regulated differentially in different cells and places; aggregations of similar cells provide the cellular resources (modules) from which tissues and organs arise; modules and populations of differently differentiated cells interact to set development along particular tracks; and organisms interact with their environment and create their niche in that environment. Such interactions are often termed “epigenetic,” meaning that they direct gene activity using mechanisms that are not encoded in the DNA of the genes. This paper reviews the origins of evo–devo, how the field has changed over the past 30 years, evaluates the recognition of the importance for development and evolution of mechanisms that are not encoded in DNA, and evaluates what the future might bring for evo–devo. Although impossible to know, history tells us that we might expect more of the same; expansion of evo–devo into other areas of biology (ecology, physiology, behavior); absorption of evo–devo by evolution or a unification of biology in which evo–devo plays a major role.     

Predicting Phenotypic Diversity and the Underlying Quantitative Molecular Transitions

During development, signaling networks control the formation of multicellular patterns. To what extent quantitative fluctuations in these complex networks may affect multicellular phenotype remains unclear. Here, we describe a computational approach to predict and analyze the phenotypic diversity that is accessible to a developmental signaling network. Applying this framework to vulval development in C. elegans, we demonstrate that quantitative changes in the regulatory network can render ~500 multicellular phenotypes. This phenotypic capacity is an order-of-magnitude below the theoretical upper limit for this system but yet is large enough to demonstrate that the system is not restricted to a select few outcomes. Using metrics to gauge the robustness of these phenotypes to parameter perturbations, we identify a select subset of novel phenotypes that are the most promising for experimental validation. In addition, our model calculations provide a layout of these phenotypes in network parameter space. Analyzing this landscape of multicellular phenotypes yielded two significant insights. First, we show that experimentally well-established mutant phenotypes may be rendered using non-canonical network perturbations. Second, we show that the predicted multicellular patterns include not only those observed in C. elegans, but also those occurring exclusively in other species of the Caenorhabditis genus. This result demonstrates that quantitative diversification of a common regulatory network is indeed demonstrably sufficient to generate the phenotypic differences observed across three major species within the Caenorhabditis genus. Using our computational framework, we systematically identify the quantitative changes that may have occurred in the regulatory network during the evolution of these species. Our model predictions show that significant phenotypic diversity may be sampled through quantitative variations in the regulatory network without overhauling the core network architecture. Furthermore, by comparing the predicted landscape of phenotypes to multicellular patterns that have been experimentally observed across multiple species, we systematically trace the quantitative regulatory changes that may have occurred during the evolution of the Caenorhabditis genus.     

Evo-Devo: the long and winding road

Evolutionary developmental biology (Evo-Devo) aims to unveil how developmental processes and mechanisms become modified during evolution and how from these changes the past and present biodiversity arose. The first wave of Evo-Devo identified a conserved set of toolkits common to most metazoans. The present second wave has changed gear and aims to identify how genes and modules were used differently through evolution to build the past and present morphological diversity. The burgeoning third wave is introducing experimental testing of predictions drawn from the first and second waves. Here we review some of the hottest topics, contributions and insights of present Evo-Devo related to basic concepts and paradigms of evolutionary research. Future directions of Evo-Devo are also highlighted; in other words, Quo Vadis, Evo-Devo?     

The Evolution of Integration of Biological Systems: An Evolutionary Perspective through Studies on Cells, Tissues, and Organs

Biologists are integrating studies of morphology, development,physiology,and other disciplines in order to understand howspecies and lineages diversify and cope with their environments.An evolutionary perspective in such studies, including thoseof cells, tissues, and organs, is potentially useful for thestructure and analysis of such problems. Evolutionary biologyis the study of the history of evolution and the elucidationof its mechanisms. Comparative biology is the comparison ofa trait or traits in selected taxa, and may be, but need notbe, evolutionary in approach. A phylogenetic hypothesis is necessaryfor reconstruction of pattern in morphology, ecology, behavior,and other areas. Acquaintance with evolutionary and phylogeneticperspectives can guide selection of taxa for study and opennew approaches to analysis of data. Such an approach is notalways appropriate to problems in biology, but it could be utilizedbeneficially more frequently than is currently practiced. Studiesof cells, tissues, and organs may contribute to the constructionof new phylogenetic hypotheses and to analysis of patterns andmechanisms of change when pursued from an evolutionary perspective     

Biological Evolution on Display: an Approach to Evolutionary Issues Through a Museum

Biological museums can promote interest in evolution and contribute to its understanding. Modern exhibitions generally emphasize the main concepts of evolutionary theory: biodiversity and adaptation. In 2009 at the Zoological Museum of Rome, to celebrate Charles Darwin, a pilot didactic project was carried out for schools and the general public in order to involve people in evolutionary issues, to stimulate interest and at constructing knowledge about evolution. An exhibition consisting of exhibits and laboratory settings was created. The thematic contexts of the exhibition and the practical experiences were aimed at facing some epistemological obstacles that influence the understanding of evolution and at constructing some “framing concepts” that, on the contrary, could facilitate it. The communicative and didactic strategies were all participative and interactive, based on the personal questioning and restructuring of preexisting knowledge. Behaviors, conversations, and comments by the participants were monitored in order to record any possible change of ideas, interests, attitudes, and learning.     

Evolutionary Transitions Among Dinosaurs: Examples from the Jurassic of China

Dinosaurs have captured the popular imagination more than any other extinct group of organisms and are therefore a powerful tool in teaching evolutionary biology. Most students are familiar with a wide variety of dinosaurs and the relative suddenness of their extinction, but few are aware of the tremendous longevity of their time on Earth and the richness of their fossil record. We first review some of the best-known groups of dinosaurs and discuss how their less-specialized relatives elucidate the path through which each evolved. We then discuss our recent discovery of Yinlong downsi, a distant relative of Triceratops, and other fossils from Jurassic deposits in China to exemplify how the continuing discovery of fossils is filling out the dinosaur family tree.     

Evolutionary Transitions in the Fossil Record of Terrestrial Hoofed Mammals

In the past few decades, many new discoveries have provided numerous transitional fossils that show the evolution of hoofed mammals from their primitive ancestors. We can now document the origin of the odd-toed perissodactyls, their early evolution when horses, brontotheres, rhinoceroses, and tapirs can barely be distinguished, and the subsequent evolution and radiation of these groups into distinctive lineages with many different species and interesting evolutionary transformations through time. Similarly, we can document the evolution of the even-toed artiodactyls from their earliest roots and their great radiation into pigs, peccaries, hippos, camels, and ruminants. We can trace the complex family histories in the camels and giraffes, whose earliest ancestors did not have humps or long necks and looked nothing like the modern descendants. Even the Proboscidea and Sirenia show many transitional fossils linking them to ancient ancestors that look nothing like modern elephants or manatees. All these facts show that creationist attacks on the fossil record of horses and other hoofed mammals are completely erroneous and deceptive. Their critiques of the evidence of hoofed mammal evolution are based entirely on reading trade books and quoting them out of context, not on any firsthand knowledge or training in paleontology or looking at the actual fossils.     

Mapping Biological Transmission: An Empirical,Dynamical, and Evolutionary Approach

The current debate over extending inheritance and its evolutionary impact has focused on adding new categories of non-genetic factors to the classical transmission of DNA, and on trying to redefine inheritance. Transmitted factors have been mainly characterized by their directions of transmission (vertical, horizontal, or both) and the way they store variations. In this paper, we leave aside the issue of defining inheritance. We rather try to build an evolutionary conceptual framework that allows for tracing most, if not all forms of transmission and makes sense of their different tempos and modes. We discuss three key distinctions that should in particular be the targets of theoretical and empirical investigation, and try to assess the interplay among them and evolutionary dynamics. We distinguish two channels of transmission (channel 1 and channel 2), two measurements of the temporal dynamics of transmission, respectively across and within generations (durability and residency), and two types of transmitted factors according to their evolutionary relevance (selectively relevant and neutral stable factors). By implementing these three distinctions we can then map different forms of transmission over a continuous space describing the combination of their varying dynamical features. While our aim is not to provide yet another model of inheritance, putting together these distinctions and crossing them, we manage to offer an inclusive conceptual framework of transmission, grounded in empirical observation, and coherent with evolutionary theory. This interestingly opens possibilities for qualitative and quantitative analyses, and is a necessary step, we argue, in order to question the interplay between the dynamics of evolution and the dynamics of multiple forms of transmission.     

Evolutionary Divergence of the Genetic Architecture Underlying Photoperiodism in the Pitcher-Plant Mosquito, Wyeomyia Smithii

We determine the contribution of composite additive, dominance, and epistatic effects to the genetic divergence of photoperiodic response along latitudinal, altitudinal, and longitudinal gradients in the pitcher-plant mosquito, Wyeomyia smithii. Joint scaling tests of crosses between populations showed wide-spread epistasis as well as additive and dominance differences among populations. There were differences due to epistasis between an alpine population in North Carolina and populations in Florida, lowland North Carolina, and Maine. Longitudinal displacement resulted in differences due to epistasis between Florida and Alabama populations separated by 300 km but not between Maine and Wisconsin populations separated by 2000 km. Genetic differences between New Jersey and Ontario did not involve either dominance or epistasis and we estimated the minimum number of effective factors contributing to a difference in mean critical photoperiod of 5 SD between them as n(E) = 5. We propose that the genetic similarity of populations within a broad northern region is due to their more recent origin since recession of the Laurentide Ice Sheet and that the unique genetic architecture of each population is the result of both mutation and repeated migration-founder-flush episodes during the dispersal of W. smithii in North America. Our results suggest that differences in composite additive and dominance effects arise early in the genetic divergence of populations while differences due to epistasis accumulate after more prolonged isolation.     

Metabolic Interrelations Underlying the Physiological and Evolutionary Advantages of Genetic Diversity

Past findings have established how the faster growth, greaterreproductive output and/or longer survival that are associatedwith heterosis and genomic diversity measured as multi-locusheterozygosity stem from slower intensities with which proteinsare renewed and replaced (=protein turnover). Slower turnoverresults in lower energy requirements and reduced metabolic sensitivityto environmental change, representing a mechanistic basis forevolutionary consequences of genetic polymorphism. To determinethe genetic and functional basis of differences in whole-bodyprotein turnover, we have begun to resolve different proteolyticpathways, searching for genetic polymorphisms with a directeffect upon proteolysis, and assessing the metabolic and physiologicalconsequences of those genetic influences in the mussel Mytilusedulis. Our recent work has established the physiological importanceof lysosomal enzymes under normal conditions of basal proteolysis,and shown that associated effects on energy flux may vary accordingto functional differences between separate enzymes. Data arepresented here which compare metabolic consequences of polymorphismin the lysosomal aminopeptidases Lap-1 and Lap-2. Findings establishthat metabolic and phenotypic effects of genetic polymorphismresult directly from genetic variation at the loci coding forthese peptidases, rather than from linked loci. They also illustratethe complexity of interrelations that ultimately influence theevolutionary consequences of genomic diversity, including associatedinfluences of both Lap-1 and Lap-2 on energy requirements andanimal condition. We impress that energy requirements for proteinturnover may represent a functional basis for epistasis, includingassociations whereby advantages of genetic polymorphism aregreatest at loci that code for enzymes acting in both proteincatabolism and energy provision.     

Neutrality and Robustness in Evo-Devo: Emergence of Lateral Inhibition

Embryonic development is defined by the hierarchical dynamical process that translates genetic information (genotype) into a spatial gene expression pattern (phenotype) providing the positional information for the correct unfolding of the organism. The nature and evolutionary implications of genotype–phenotype mapping still remain key topics in evolutionary developmental biology (evo-devo). We have explored here issues of neutrality, robustness, and diversity in evo-devo by means of a simple model of gene regulatory networks. The small size of the system allowed an exhaustive analysis of the entire fitness landscape and the extent of its neutrality. This analysis shows that evolution leads to a class of robust genetic networks with an expression pattern characteristic of lateral inhibition. This class is a repertoire of distinct implementations of this key developmental process, the diversity of which provides valuable clues about its underlying causal principles.     

Epistemic, Evolutionary, and Physical Conditions for Biological Information

The necessary but not sufficient conditions for biological informational concepts like signs, symbols, memories, instructions, and messages are (1) an object or referent that the information is about, (2) a physical embodiment or vehicle that stands for what the information is about (the object), and (3) an interpreter or agent that separates the referent information from the vehicle’s material structure, and that establishes the stands-for relation. This separation is named the epistemic cut, and explaining clearly how the stands-for relation is realized is named the symbol-matter problem. (4) A necessary physical condition is that all informational vehicles are material boundary conditions or constraints acting on the lawful dynamics of local systems. It is useful to define a dependency hierarchy of information types: (1) syntactic information (i.e., communication theory), (2) heritable information acquired by variation and natural selection, (3) non-heritable learned or creative information, and (4) measured physical information in the context of natural laws. High information storage capacity is most reliably implemented by discrete linear sequences of non-dynamic vehicles, while the execution of information for control and construction is a non-holonomic dynamic process. The first epistemic cut occurs in self-replication. The first interpretation of base sequence information is by protein folding; the last interpretation of base sequence information is by natural selection. Evolution has evolved senses and nervous systems that acquire non-heritable information, and only very recently after billions of years, the competence for human language. Genetic and human languages are the only known complete general purpose languages. They have fundamental properties in common, but are entirely different in their acquisition, storage and interpretation.