Time's arrow: heterochrony and the evolution of development

The concept of heterochrony, which denotes a change in the relative timing of developmental events and processes in evolution, has accompanied attempts to link evolution and development for well over a century. During this time the definition of heterochrony and the application of the concept have varied and by the late 1990's, many questioned the usefulness of the concept. However, in the past decade studies of heterochrony have been revitalized by a new focus on developmental sequence, an examination of heterochrony in explicit phylogenetic contexts and increasing tendencies to examine the heterochrony of many kinds of events, including cellular, molecular and genetic events. Examples of such studies are reviewed in this paper and it is argued that this new application of heterochrony provides an extraordinarily rich opportunity for understanding the developmental basis of evolutionary change.     

Heterochrony revisited: the evolution of developmental sequences

The concept of heterochrony is a persistent component of discussions about the way that evolution and development interact. Since the late 1970s heterochrony has been defined largely as developmental changes in the relationship of size and shape. This approach to heterochrony, here termed growth heterochrony, is limited in the way it can analyse change in the relative timing of developmental events in a number of respects. In particular, analytical techniques do not readily allow the study of changes in developmental events not characterized by size and shape parameters, or of many kinds of events in many taxa. I discuss here an alternative approach to heterochrony, termed sequence heterochrony, in which a developmental trajectory is conceptualized as a series of discrete events. Heterochrony is demonstrated when the sequence position of an event changes relative to other events in that sequence. I summarize several analytical techniques that allow the investigation of sequence heterochrony in phylogenetic contexts and also quantitatively. Finally, several examples of how this approach may be used to test hypotheses on the way development evolves are summarized.     

Estimating evolution of temporal sequence changes: a practical approach to inferring ancestral developmental sequences and sequence heterochrony

Developmental biology often yields data in a temporal context. Temporal data in phylogenetic systematics has important uses in the field of evolutionary developmental biology and, in general, comparative biology. The evolution of temporal sequences, specifically developmental sequences, has proven difficult to examine due to the highly variable temporal progression of development. Issues concerning the analysis of temporal sequences and problems with current methods of analysis are discussed. We present here an algorithm to infer ancestral temporal sequences, quantify sequence heterochronies, and estimate pseudoreplicate consensus support for sequence changes using Parsimov-based genetic inference [PGi]. Real temporal developmental sequence data sets are used to compare PGi with currently used approaches, and PGi is shown to be the most efficient, accurate, and practical method to examine biological data and infer ancestral states on a phylogeny. The method is also expandable to address further issues in developmental evolution, namely modularity.     

Homology and heterochrony: the evolutionary embryologist Gavin Rylands de Beer (1899-1972)

The evolutionary embryologist Gavin Rylands de Beer can be viewed as one of the forerunners of modern evolutionary developmental biology in that he posed crucial questions and proposed relevant answers about the causal relationship between ontogeny and phylogeny. In his developmental approach to the phylogenetic phenomenon of homology, he emphasized that homology of morphological structures is to be identified neither with the sameness of the underlying developmental processes nor with the homology of the genes that are involved in the development of the structures. De Beer's work on developmental evolution focused on the notion of heterochrony, arguing that paedomorphosis increases morphological evolvability and is thereby an important mode of evolution that accounts for the origin of many taxa, including higher taxa.     

Macroevolution of plant defense strategies

Theories of plant defense expression are typically based on the concepts of tradeoffs among traits and of phylogenetic conservatism within clades. Here, I review recent developments in phylogenetic approaches to understanding the evolution of plant defense strategies and plant-herbivore coevolutionary interactions. I focus particularly on multivariate defense against insect herbivores, which is the simultaneous deployment of multiple traits, often arranged as convergently evolved defense syndromes. Answering many of the outstanding questions in the biology of plant defense will require generating broad hypotheses that can be explicitly tested by using comparative approaches and interpreting phylogenetic patterns. The comparative approach has wide-spread potential to reinvigorate tests of classic hypotheses about the evolution of interspecific interactions.     

An integrative approach identifies developmental sequence heterochronies in freshwater basommatophoran snails

Adopting an integrative approach to the study of sequence heterochrony, we compared the timing of developmental events encompassing a mixture of developmental stages and functional traits in the embryos of 12 species of basommatophoran snails in an explicit phylogenetic framework. PARSIMOV analysis demonstrated clear functional heterochronies associated both with basal branches within the phylogeny and with terminal speciation events. A consensus of changes inferred under both accelerated transformation and delayed transformation optimizations identified four heterochronies where the direction of movement was known plus six twin heterochronies where the relative movements of the two events could not be assigned. On average, 0.5 and 0.58 events were inferred to have changed their position in the developmental sequence on internal and terminal branches of the phylogeny, respectively; these values are comparable with frequencies of sequence heterochrony reported in mammals. Directional heterochronies such as the early occurrence of body flexing in relation to the ontogeny of the eye spots, heart beat, and free swimming events occurred convergently and/or at different levels (i.e., familial, generic, and species) within the phylogeny. Such a functional approach to the study of developmental sequences has highlighted the possibility that heterochrony may have played a prominent role in the evolution of this group of invertebrates.     

Phylogeny and evo-devo: characters, homology, and the historical analysis of the evolution of development

The concept of homology continues to attract more and more commentary. In systematic and evolutionary biology the meaning of homology as synapomorphic similarity inherited from a common ancestor has gained wide acceptance over the last three or four decades. In recent years, however, developmental biologists, in particular, have argued for a new approach to, and new definition for, homology that revolves around the desire to make it more process-oriented and more mechanistic. These efforts raise questions about the relationship between developmental and evolutionary biology as well as how the evolution of development is to be studied. It is argued in this paper that this new approach to homology seemingly decouples developmental biology from the study of the evolution of development rather than to facilitate that study. In contrast, applying the notion of historical, phylogenetic homology to developmental data is inherently comparative and therefore evolutionary.     

INTEGRATING FOSSILS WITH MOLECULAR PHYLOGENIES IMPROVES INFERENCE OF TRAIT EVOLUTION

Comparative biologists often attempt to draw inferences about tempo and mode in evolution by comparing the fit of evolutionary models to phylogenetic comparative data consisting of a molecular phylogeny with branch lengths and trait measurements from extant taxa. These kinds of approaches ignore historical evidence for evolutionary pattern and process contained in the fossil record. In this article, we show through simulation that incorporation of fossil information dramatically improves our ability to distinguish among models of quantitative trait evolution using comparative data. We further suggest a novel Bayesian approach that allows fossil information to be integrated even when explicit phylogenetic hypotheses are lacking for extinct representatives of extant clades. By applying this approach to a comparative dataset comprising body sizes for caniform carnivorans, we show that incorporation of fossil information not only improves ancestral state estimates relative to those derived from extant taxa alone, but also results in preference of a model of evolution with trend toward large body size over alternative models such as Brownian motion or Ornstein–Uhlenbeck processes. Our approach highlights the importance of considering fossil information when making macroevolutionary inference, and provides a way to integrate the kind of sparse fossil information that is available to most evolutionary biologists.     

Considering the zebrafish in a comparative context

This article introduces a special issue on zebrafish biology that attempts to integrate developmental genetics with comparative studies of other fish species. For zebrafish researchers, comparative work offers a better understanding of the evolutionary history of their model system. Comparative biologists can gain many insights from the developmental and genetic mechanisms revealed in zebrafish that have contributed to the huge range of morphological variation among fishes that has arisen over millions of years. These ideas are considered here in various contexts, including systematics, genome organization and the development of the nervous system, pigmentation, craniofacial skeleton and dentition. Studies of the zebrafish in phylogenetic context provide an opportunity for synergy between communities using these two fundamentally different approaches.     

Eyespot evolution: phylogenetic insights from Junonia and related butterfly genera (Nymphalidae: Junoniini)

SUMMARY Butterfly eyespots have been the focus of a number of developmental and evolutionary studies. However, a phylogenetic component has rarely been explicitly incorporated in these studies. In this study, I utilize a phylogeny to trace the evolution of eyespot number and position on the wing in a group of nymphalid butterflies, the subtribe Junoniini. These butterflies have two kinds of eyespot arrangements which I refer to as Serial and Individual . In the Serial arrangement, eyespots are placed in a series on compartments 1−6 (counting from the anterior wing margin). In the Individual arrangement, eyespots are isolated on specific compartments, ranging from 1 to 4 in number. This can be divided into four subtypes based on the number and positions of eyespots. I map the evolution of these five arrangements over a phylogeny of Junoniini reconstructed with ca. 3000 base pairs of sequence data from three genes. The results show that almost all arrangements have evolved at least twice, with multiple shifts between them by addition and deletion of eyespots. I propose a model involving genetic or developmental coupling between eyespots in specific compartments to explain these shifts. I discuss their evolution in light of existing knowledge about their development. I also discuss potential explanations for functional significance of the eyespot patterns found in the group. Differential selection for and against eyespots, both at different times over the phylogeny and in different regions, have driven the evolution of eyespot arrangements. The study throws open many questions about the adaptive significance of eyespots and the developmental underpinnings of the various arrangements.     

Life history evolution and comparative developmental biology of echinoderms

Evolutionary biologists studying life history variation have used echinoderms in experimental, laboratory, and field studies of life history evolution. This focus on echinoderms grew originally from the tradition of comparative embryology, in which echinoderms were central. The tools for obtaining and manipulating echinoderm gametes and larvae were taken directly from comparative embryological research. In addition, the comparative embryologists employed a diverse array of echinoderms, not a few model species, and this diversity has led to a broad understanding of the development, function, and evolution of echinoderm larvae. As a result, this branch of life history evolution has deep roots in comparative developmental biology of echinoderms. Here two main aspects of this relationship are reviewed. The first is a broad range of studies of fertilization biology, dispersal, population genetics, functional morphology, and asexual reproduction in which developmental biologists might take a keen interest because of the historical origins of this research in echinoderm comparative embryology. The second is a similarly broad variety of topics in life history research in which evolutionary biologists require techniques or data from developmental biology in order to make progress on understanding patterns of life history variation among echinoderm species and higher taxa. Both sets of topics provide opportunities for interaction and collaboration.     

Heterochrony: Developmental mechanisms and evolutionary results

The concept of heterochrony, that the relative timing of ontogenetic events can shift during evolution, has been a major paradigm for understanding the role of developmental processes in evolution. In this paper we consider heterochrony from the perspective of developmental biology. Our objective is to redefine heterochrony more broadly so that the concept becomes readily applicable to the evolution of the full range of ontogenetic processes, from embryogenesis through the adult. Throughout, we stress the importance of considering heterochrony from a hierarchical perspective. Thus, we recognize that a heterochronic change at one level of organization may be the result of non-heterochronic events at an underlying level. As such, heterochrony must be studied using a combination of genetic, molecular, cellular, and morphological approaches.     

Haeckel's ABC of evolution and development

One of the central, unresolved controversies in biology concerns the distribution of primitive versus advanced characters at different stages of vertebrate development. This controversy has major implications for evolutionary developmental biology and phylogenetics. Ernst Haeckel addressed the issue with his Biogenetic Law, and his embryo drawings functioned as supporting data. We re-examine Haeckel's work and its significance for modern efforts to develop a rigorous comparative framework for developmental studies. Haeckel's comparative embryology was evolutionary but non-quantitative. It was based on developmental sequences, and treated heterochrony as a sequence change. It is not always clear whether he believed in recapitulation of single characters or entire stages. The Biogenetic Law is supported by several recent studies -- if applied to single characters only. Haeckel's important but overlooked alphabetical analogy of evolution and development is an advance on von Baer. Haeckel recognized the evolutionary diversity in early embryonic stages, in line with modern thinking. He did not necessarily advocate the strict form of recapitulation and terminal addition commonly attributed to him. Haeckel's much-criticized embryo drawings are important as phylogenetic hypotheses, teaching aids, and evidence for evolution. While some criticisms of the drawings are legitimate, others are more tendentious. In opposition to Haeckel and his embryo drawings, Wilhelm His made major advances towards developing a quantitative comparative embryology based on morphometrics. Unfortunately His's work in this area is largely forgotten. Despite his obvious flaws, Haeckel can be seen as the father of a sequence-based phylogenetic embryology.     

Origins of multicellular complexity: Volvox and the volvocine algae

The collection of evolutionary transformations known as the ‘major transitions’ or ‘transitions in individuality’ resulted in changes in the units of evolution and in the hierarchical structure of cellular life. Volvox and related algae have become an important model system for the major transition from unicellular to multicellular life, which touches on several fundamental questions in evolutionary biology. The Third International Volvox Conference was held at the University of Cambridge in August 2015 to discuss recent advances in the biology and evolution of this group of algae. Here, I highlight the benefits of integrating phylogenetic comparative methods and experimental evolution with detailed studies of developmental genetics in a model system with substantial genetic and genomic resources. I summarize recent research on Volvox and its relatives and comment on its implications for the genomic changes underlying major evolutionary transitions, evolution and development of complex traits, evolution of sex and sexes, evolution of cellular differentiation and the biophysics of motility. Finally, I outline challenges and suggest future directions for research into the biology and evolution of the volvocine algae.     

Heterochrony and allometry: the analysis of evolutionary change in ontogeny

The connection between development and evolution has become the focus of an increasing amount of research in recent years, and heterochrony has long been a key concept in this relation. Heterochrony is defined as evolutionary change in rates and timing of developmental processes; the dimension of time is therefore an essential part in studies of heterochrony. Over the past two decades, evolutionary biologists have used several methodological frameworks to analyse heterochrony, which differ substantially in the way they characterize evolutionary changes in ontogenies and in the resulting classification, although they mostly use the same terms. This review examines how these methods compare ancestral and descendant ontogenies, emphasizing their differences and the potential for contradictory results from analyses using different frameworks. One of the two principal methods uses a clock as a graphical display for comparisons of size, shape and age at a particular ontogenic stage, whereas the other characterizes a developmental process by its time of onset, rate, and time of cessation. The literature on human heterochrony provides particularly clear examples of how these differences produce apparent contradictions when applied to the same problem. Developmental biologists recently have extended the concept of heterochrony to the earliest stages of development and have applied it at the cellular and molecular scale. This extension brought considerations of developmental mechanisms and genetics into the study of heterochrony, which previously was based primarily on phenomenological characterizations of morphological change in ontogeny. Allometry is the pattern of covariation among several morphological traits or between measures of size and shape; unlike heterochrony, allometry does not deal with time explicitly. Two main approaches to the study of allometry are distinguished, which differ in the way they characterize organismal form. One approach defines shape as proportions among measurements, based on considerations of geometric similarity, whereas the other focuses on the covariation among measurements in ontogeny and evolution. Both are related conceptually and through the use of similar algebra. In addition, there are close connections between heterochrony and changes in allometric growth trajectories, although there is no one-to-one correspondence. These relationships and outline links between different analytical frameworks are discussed.     

Kowalevsky, comparative evolutionary embryology, and the intellectual lineage of evo-devo

Alexander Kowalevsky was one of the most significant 19th century biologists working at the intersection of evolution and embryology. The reinstatement of the Alexander Kowalevsky Medal by the St. Petersburg Society of Naturalists for outstanding contributions to understanding evolutionary relationships in the animal kingdom, evolutionary developmental biology, and comparative zoology is timely now that Evo-devo has emerged as a major research discipline in contemporary biology. Consideration of the intellectual lineage of comparative evolutionary embryology explicitly forces a reconsideration of some current conceptions of the modern emergence of Evo-devo, which has tended to exist in the shadow of experimental embryology throughout the 20th century, especially with respect to the recent success of developmental biology and developmental genetics. In particular we advocate a sharper distinction between the heritage of problems and the heritage of tools for contemporary Evo-devo. We provide brief overviews of the work of N. J. Berrill and D. T. Anderson to illustrate comparative evolutionary embryology in the 20th century, which provides an appropriate contextualization for a conceptual review of our research on the sea urchin genus Heliocidaris over the past two decades. We conclude that keeping research questions rather than experimental capabilities at the forefront of Evo-devo may be an antidote to any repeat of the stagnation experienced by the first group of evolutionary developmental biologists over one hundred years ago and acknowledges Kowalevsky's legacy in evolutionary embryology.     

The phylogenetic placement of Chondrichthyes: inferences from analysis of multiple genes and implications for comparative studies

Elasmobranch fishes (sharks and rays) have proven valuable for inferring general and specific properties of molecular evolution through comparative studies with crown group vertebrates because they are the most ancient group of gnathostomes. Recent studies have questioned the conventional phylogenetic placement of sharks in the vertebrate tree, however. In this paper I review the importance of the basal position of Chondrichthyes for comparative biology and compile evidence from multiple, independent genes to evaluate the phylogenetic placement of sharks. The results suggests that alternative phylogenetic hypotheses of the relationships among the Chondrichthyes, Actinopterygii and Sarcopterygii can not be refuted with available data, implying that the assumption of the basal placement of sharks in the vertebrate tree is suspect. Resolving the phylogeny of basal vertebrates is important for testing hypotheses about the evolution of vertebrates, and the current lack of a robust phylogeny limits evolutionary inferences that can be gained from comparative studies that include sharks and rays.     

Comparative methods in developmental biology

The need for a phylogenetic framework is becoming appreciated in many areas of biology. Such a framework has found limited use in developmental studies. Our current research program is therefore directed to applying comparative and phylogenetic methods to developmental data. In this paper, we examine the concepts underlying this work, discuss potential difficulties, and identify some solutions. While developmental biologists frequently make cross-species comparisons, they usually adopt a phenetic approach, whereby degrees of overall similarity in development are sought. Little emphasis is placed on reconstructing the evolutionary divergence in developmental characters. Indeed, developmental biologists have historically concentrated on apparently ‘conserved’ or ‘universal’ developmental mechanisms. Thus, there has been little need for phylogenetic methodologies which analyse specialised features shared only within a subset of species (i.e., synapomorphies). We discuss the potential value of such methodologies, and argue that difficulties in adapting them to developmental studies fall into three interlinked areas: One concerns the nature and definition of developmental characters. Another is the difficulty of identifying equivalent developmental stages in different species. Finally the phylogenetic non-independence of developmental characters presents real problems under some protocols. These problems are not resolved. However, it is clear that the application of phylogenetic methodology to developmental data is both necessary and fundamental to research into the relationship between evolution and development.