Evo-devo and the evolution of social behavior

The integration of evolutionary biology with developmental genetics into the hybrid field of 'evo-devo' resulted in major advances in understanding multicellular development and morphological evolution. Here we show how insights from evo-devo can be applied to study the evolution of social behavior. We develop this idea by reviewing studies that suggest that molecular pathways controlling feeding behavior and reproduction in solitary insects are part of a 'genetic toolkit' underlying the evolution of a particularly complex form of social behavior, division of labor among workers in honeybee colonies. The evo-devo approach, coupled with advances in genomics for non-model genetic organisms, including the recent sequencing of the honeybee genome, promises to advance our understanding of the evolution of social behavior.     

Evidence for repeated acquisition and loss of complex body-form characters in an insular clade of Southeast Asian semi-fossorial skinks

Evolutionary simplification, or loss of complex characters, is a major theme in studies of body-form evolution. The apparently infrequent evolutionary reacquisition of complex characters has led to the assertion (Dollo's Law) that once lost, complex characters may be impossible to re-evolve, at least via the exact same evolutionary process. Here, we provide one of the most comprehensive, fine-scale analyses of squamate body-form evolution to date, introducing a new model system of closely related, morphologically variable, lizards. Our phylogenetic results support independent instances of complete limb loss as well as multiple instances of digit and external ear opening loss and re-acquisition. Even more striking, we find strong statistical support for the re-acquisition of a pentadactyl body form from a digit-reduced ancestor. Our study reveals that species of the genus Brachymeles exemplify regions of morphospace (body plans) previously undocumented in squamates. Our findings have broad, general implications for body-form evolution in burrowing vertebrates: whatever constraints have shaped trends in morphological evolution among other squamate groups (excluding Bipes) have been lost in this one exemplary clade. The results of our study join a nascent body of literature showing strong statistical support for character loss, followed by evolutionary re-acquisition of complex structures associated with a generalized pentadactyl body form.     

The great escape: do parasites break Dollo's law?

A long-held assumption in evolutionary studies is that a character that changes from a complex to a simple state is unlikely to return to the same complex state. The extreme version of this assumption has been codified as Dollo's law. Unfortunately, this paradigm has supported the idea that simple and complex traits are qualitatively different, when it is more sensible to suggest that there is a quantitative difference. Dollo's law has been the predominant paradigm in parasitology, where a move from a free-living state to parasitism has been considered a unidirectional pathway or 'one-way trip' because organisms lose the structures required to return to the free-living state. Several recent studies have suggested that complex structures can be regained from simple traits, and we suggest that this is also possible for parasites.     

On phylogenetic tests of irreversible evolution

"Dollo's law" states that, following loss, a complex trait cannot reevolve in an identical manner. Although the law has previously fallen into disrepute, it has only recently been challenged with statistical phylogenetic methods. We employ simulation studies of an irreversible binary character to show that rejections of Dollo's law based on likelihood-ratio tests of transition rate constraints or on reconstructions of ancestral states are frequently incorrect. We identify two major causes of errors: incorrect assignment of root state frequencies, and neglect of the effect of the character state on rates of speciation and extinction. Our findings do not necessarily overturn the conclusions of phylogenetic studies claiming reversals, but we demonstrate devastating flaws in the methods that are the foundation of all such studies. Furthermore, we show that false rejections of Dollo's law can be reduced by the use of appropriate existing models and model selection procedures. More powerful tests of irreversibility require data beyond phylogenies and character states of extant taxa, and we highlight empirical work that incorporates additional information.     

Limpets break Dollo's Law

A new molecular phylogeny of the limpet molluscs (Calyptraeidae) reveals that coiled shells have independently re-evolved at least once in this family, which is a violation of Dollo's Law that complex ancestral states, once lost, are never reacquired. Reacquisition of the coiled ancestral state is remarkable in that uncoiled shells have been the most recent ancestral state for 20 million-100 million years. Adult coiling might have re-evolved by the mechanism of prolonging the period during which genes for coiling are expressed in larvae. This and other developmental mechanisms could provide general routes for maintaining the potential to produce traits lost in distant ancestors.     

Evolutionary developmental biology and genomics

Reciprocal questions often frame studies of the evolution of developmental mechanisms. How can species share similar developmental genetic toolkits but still generate diverse life forms? Conversely, how can similar forms develop from different toolkits? Genomics bridges the gap between evolutionary and developmental biology, and can help answer these evo-devo questions in several ways. First, it informs us about historical relationships, thus orienting the direction of evolutionary diversification. Second, genomics lists all toolkit components, thereby revealing contraction and expansion of the genome and suggesting mechanisms for evolution of both developmental functions and genome architecture. Finally, comparative genomics helps us to identify conserved non-coding elements and their relationship to genome architecture and development.     

Re-evolution of lost mandibular teeth in frogs after more than 200 million years, and re-evaluating Dollo's law

Dollo's law states that structures that are evolutionarily lost will not be regained. Recent phylogenetic studies have revealed several potential examples in which Dollo's law seems to be violated, where lost structures appear to have been regained over evolutionary time. However, these examples have recently been questioned and suggested to be methodological artifacts. In this article, I document a striking and incontrovertible phylogenetic example of the re-evolution of a lost, complex structure: mandibular teeth in the frog genus Gastrotheca. I use a time-calibrated phylogeny for 170 amphibian species to show that mandibular teeth were lost in the ancestor of modern frogs at least 230 million years ago (Mya) and have been regained in the last ～ 5-17 My. I review recent studies on trait re-evolution and show that this long period of trait absence prior to re-acquisition is largely unprecedented. I also argue that there are several methodological issues that may cause trait re-evolution to be hardest to detect under those conditions when it is most likely to occur, leading to erroneous failures to reject Dollo's law. Finally, I discuss a mechanism that may facilitate trait re-evolution, and the evolution of mandibular teeth in frogs as an example of developmental constraint.     

Dollo's law and the re-evolution of shell coiling

Gastropods have lost the quintessential snail feature, the coiled shell, numerous times in evolution. In many cases these animals have developed a limpet morphology with a cap-shaped shell and a large foot. Limpets thrive in marginal habitats such as hydrothermal vents, the high-energy rocky intertidal areas and fresh water, but they are considered to be evolutionary dead-ends, unable to re-evolve a coiled shell and therefore unable to give rise to the diversity seen among coiled snails. The re-evolution of a coiled shell, or any complex character, is considered unlikely or impossible (Dollo's law) because the loss of the character is followed by the loss of the genetic architecture and developmental mechanisms that underlie that character. Here, we quantify the level of coiling in calyptraeids, a family of mostly uncoiled limpets, and show that coiled shells have re-evolved at least once within this family. These results are the first demonstration, to our knowledge, of the re-evolution of coiling in a gastropod, and show that the developmental features underlying coiling have not been lost during 20-100 Myr of uncoiled evolutionary history. This is the first example of the re-evolution of a complex character via a change in developmental timing (heterochrony) rather than a change in location of gene expression (heterotopy).     

Studies of threespine stickleback developmental evolution: progress and promise

A promising route for understanding the origin and diversification of organismal form is through studies at the intersection of evolution and development (evo-devo). While much has been learned over the last two decades concerning macroevolutionary patterns of developmental change, a fundamental gap in the evo-devo synthesis is the integration of mathematical population and quantitative genetics with studies of how genetic variation in natural populations affects developmental processes. This micro-evo-devo synthesis requires model organisms with which to ask empirical questions. Threespine stickleback fish (Gasterosteus aculeatus), long a model for studying behavior, ecology and evolution, is emerging as a prominent model micro-evo-devo system. Research on stickleback over the last decade has begun to address the genetic basis of morphological variation and sex determination, and much of this work has important implications for understanding the genetics of speciation. In this paper we review recent threespine stickleback micro-evo-devo results, and outline the resources that have been developed to make this synthesis possible. The prospects for stickleback research to speed the micro-(and macro-) evo-devo syntheses are great, and this workhorse model system is well situated to continue contributing to our understanding of the generation of diversity in organismal form for many more decades.     

The Body Plan Concept and Its Centrality in Evo-Devo

A body plan is a suite of characters shared by a group of phylogenetically related animals at some point during their development. The concept of bauplane, or body plans, has played and continues to play a central role in the study of evolutionary developmental biology (evo-devo). Despite the importance of the body plan concept in evo-devo, many researchers may not be familiar with the progression of ideas that have led to our current understanding of body plans, and/or current research on the origin and maintenance of body plans. This lack of familiarity, as well as former ties between the body plan concept and metaphysical ideology is likely responsible for our underappreciation of the body plan concept in its own right, as well as its role in evo-devo. My aim in this review is to outline how we have arrived at our modern definition of body plan, the controversies associated with the concept, its role in evo-devo, and how current research is informing us on body plans. To this end, I integrate concepts such as the nature of phyla, the Cambrian explosion, constraint, evolvability, and results from recent research on gene regulatory networks with the much older concept of the body plan.     

Evolutionary Developmental Biology: the Interaction of Developmental Biology,Evolutionary Biology,Paleontology, and Genomics

Paleontological Journal - Evolutionary developmental biology (evo-devo) formed due to the interactions of evolutionary biology, paleontology, and comparative genomics, analyzes the interrelations...     

In search of evolutionary developmental mechanisms: the 30-year gap between 1944 and 1974

The approach I have elected in this retrospective of how I became a student of evo-devo is both biographical and historical, a case study along the lines of Waddington's The Evolution of an Evolutionist ('75), although in my case it is the Evolution of an Evo-devoist. What were the major events that brought me to developmental biology and from there to evo-devo? They were, of course, specific to my generation, to the state of knowledge at the time, and to my own particular circumstances. Although exposed to evolution and embryology as an undergraduate in the 1960s, my PhD and post-PhD research programme lay within developmental biology until the early 1970s. An important formative influence on my studies as an undergraduate was the work of Conrad Hal Waddington (1905-1975), whose writings made me aware of genetic assimilation and gave me an epigenetic approach to my developmental studies. The switch to evo-devo (and my discovery of the existence of the neural crest), I owe to an ASZ (now SICB) symposium held in 1973.     

Evo-devo: extending the evolutionary synthesis

Evolutionary developmental biology (evo-devo) explores the mechanistic relationships between the processes of individual development and phenotypic change during evolution. Although evo-devo is widely acknowledged to be revolutionizing our understanding of how the development of organisms has evolved, its substantial implications for the theoretical basis of evolution are often overlooked. This essay identifies major theoretical themes of current evo-devo research and highlights how its results take evolutionary theory beyond the boundaries of the Modern Synthesis.     

Equine clinical cytogenetics: the past and future

Cytogenetic analyses of horses have benefited the horse industry by identifying chromosomal aberrations causing congenital abnormalities, embryonic loss and infertility. Technical advances in cytogenetics enabled the identification of chromosome specific aberrations. More recently, advances in genomic tools have been used to more precisely define chromosome abnormalities. In this report we review the history of equine clinical cytogenetics, identify historical landmarks for equine clinical cytogenetics, discuss how the current use of genomic tools has benefited this area, and how future genomics tools may enhance clinical cytogenetic studies in the horse.     

Beyond Arabidopsis. Translational biology meets evolutionary developmental biology

Developmental processes shape plant morphologies, which constitute important adaptive traits selected for during evolution. Identifying the genes that act in developmental pathways and determining how they are modified during evolution is the focus of the field of evolutionary developmental biology, or evo-devo. Knowledge of genetic pathways in the plant model Arabidopsis serves as the starting point for investigating how the toolkit of developmental pathways has been used and reused to form different plant body plans. One productive approach is to identify genes in other species that are orthologous to genes known to control developmental pathways in Arabidopsis and then determine what changes have occurred in the protein coding sequence or in the gene's expression to produce an altered morphology. A second approach relies on natural variation among wild populations or crop plants. Natural variation can be exploited to identify quantitative trait loci that underlie important developmental traits and, thus, define those genes that are responsible for adaptive changes. The possibility of applying comparative genomics approaches to Arabidopsis and related species promises profound new insights into the interplay of evolution and development.     

Supernumerary teeth in Lynx lynx and the irreversibility of evolution

Supernumerary dental elements have been reported in Lynx lynx by several authors. These features have been given different evolutionary interpretations by different commentators. I note here that, since these features are absent in the plesiomorphic sister-groups of L. lynx , they represent a true evolutionary reversal. If they were simply a retention of an evolutionarily older phenotype, we should expect to see them developed in at least one plesiomorphic sister-group. Such development of a previously hidden character can occur if it is genetically linked to features selected for, until it becomes phenotypically expressed, whereupon selection can act on the character itself. Since Dollo's law, which is the theoretical issue behind the present discussion, is not a law, but a rule, and, like all rules based on probabilities, we should expect to find exceptions in the fossil record. Such exceptions are not rare, but few are as spectacular as the present one, in which the redeveloped feature is at least phenotypically identical with one which has been lost in the Felidae since the Miocene.     

Empowering plant evo-devo: virus induced gene silencing validates new and emerging model systems

It is increasingly recognized that current established model systems are not sufficient to understand the evolution of biodiversity. The main limitation in developing additional model systems is the difficulty or inability to perform functional studies of target genes. Evolutionary developmental (evo-devo) biologists have adopted a transient transgenic technique, developed over the last decade for agricultural applications, which is allowing functional studies in the most disparate plant lineages. From monocots to dicots and from herbs to trees, virus-induced gene silencing (VIGS) has opened up a world of opportunities in plant evo-devo.     

Population genomics for wildlife conservation and management

Biodiversity is under threat worldwide. Over the past decade, the field of population genomics has developed across nonmodel organisms, and the results of this research have begun to be applied in conservation and management of wildlife species. Genomics tools can provide precise estimates of basic features of wildlife populations, such as effective population size, inbreeding, demographic history and population structure, that are critical for conservation efforts. Moreover, population genomics studies can identify particular genetic loci and variants responsible for inbreeding depression or adaptation to changing environments, allowing for conservation efforts to estimate the capacity of populations to evolve and adapt in response to environmental change and to manage for adaptive variation. While connections from basic research to applied wildlife conservation have been slow to develop, these connections are increasingly strengthening. Here we review the primary areas in which population genomics approaches can be applied to wildlife conservation and management, highlight examples of how they have been used, and provide recommendations for building on the progress that has been made in this field.     

Odonata (dragonflies and damselflies) as a bridge between ecology and evolutionary genomics

Odonata (dragonflies and damselflies) present an unparalleled insect model to integrate evolutionary genomics with ecology for the study of insect evolution. Key features of Odonata include their ancient phylogenetic position, extensive phenotypic and ecological diversity, several unique evolutionary innovations, ease of study in the wild and usefulness as bioindicators for freshwater ecosystems worldwide. In this review, we synthesize studies on the evolution, ecology and physiology of odonates, highlighting those areas where the integration of ecology with genomics would yield significant insights into the evolutionary processes that would not be gained easily by working on other animal groups. We argue that the unique features of this group combined with their complex life cycle, flight behaviour, diversity in ecological niches and their sensitivity to anthropogenic change make odonates a promising and fruitful taxon for genomics focused research. Future areas of research that deserve increased attention are also briefly outlined.