The evolutionary origin of developmental enhancers in vertebrates: Insights from non-model species

How random DNA mutations have established the diverse morphology of extant vertebrates is one of the major challenges in evolutionary biology. Thanks to the recent advancement in DNA sequencing technologies, the genome sequences of many non-model species have been determined, which allows us to address previously inaccessible questions about gene regulatory evolution in vertebrates. In particular, the genome sequences of non-teleost ray-finned fishes and cartilaginous fishes offer clues about when and how vertebrates gained developmental enhancers related to morphological traits that were required for the water-to-land transition. In this review, I examine the evolutionary origin of conserved non-coding elements (CNEs), which often function as tissue-specific developmental enhancers, and discuss how CNEs are related to gene regulatory changes that caused the major morphological transitions of vertebrates.     

A farewell to arms and legs: a review of limb reduction in squamates

Elongated snake-like bodies associated with limb reduction have evolved multiple times throughout vertebrate history. Limb-reduced squamates (lizards and snakes) account for the vast majority of these morphological transformations, and thus have great potential for revealing macroevolutionary transitions and modes of body-shape transformation. Here we present a comprehensive review on limb reduction, in which we examine and discuss research on these dramatic morphological transitions. Historically, there have been several approaches to the study of squamate limb reduction: (i) definitions of general anatomical principles of snake-like body shapes, expressed as varying relationships between body parts and morphometric measurements; (ii) framing of limb reduction from an evolutionary perspective using morphological comparisons; (iii) defining developmental mechanisms involved in the ontogeny of limb-reduced forms, and their genetic basis; (iv) reconstructions of the evolutionary history of limb-reduced lineages using phylogenetic comparative methods; (v) studies of functional and biomechanical aspects of limb-reduced body shapes; and (vi) studies of ecological and biogeographical correlates of limb reduction. For each of these approaches, we highlight their importance in advancing our understanding, as well as their weaknesses and limitations. Lastly, we provide suggestions to stimulate further studies, in which we underscore the necessity of widening the scope of analyses, and of bringing together different perspectives in order to understand better these morphological transitions and their evolution. In particular, we emphasise the importance of investigating and comparing the internal morphology of limb-reduced lizards in contrast to external morphology, which will be the first step in gaining a deeper insight into body-shape variation.     

Evolutionary changes in the timing of gut morphogenesis in larvae of the marine annelid Streblospio benedicti

The planktonic larvae of marine invertebrates are diverse in their nutritional modes, suggesting that evolutionary transitions in larval nutritional mode have been frequent. One approach to identifying the developmental changes that play important roles in such transitions is to compare "intermediate" larval forms to closely related larvae representative of their common ancestor. Here we make such a comparison between obligately planktotrophic and facultatively feeding larvae of the poecilogonous polychaete annelid Streblospio benedicti. We used feeding experiments to show that the derived, facultatively feeding larvae of this species develop the ability to feed at a later developmental stage (five muscle bands) than planktotrophic larvae (two to three muscle bands). This delay in the onset of feeding ability does not appear to be caused by delay in the formation of particle capture structures, but instead by delay in the development of a continuous, functional gut. These observations are consistent with the hypothesis that evolutionary increases in egg size in annelids lead predictably to heterochronic delays in gut development, and hence to transitions in larval nutritional mode.     

Integrating Ontogeny of Echolocation and Locomotion Gives Unique Insights into the Origin of Bats

The evolutionary sequence of events that led to flight and echolocation in bats is a compelling question in biology. Fundamentally lacking from this discussion is the ontogeny of how these two systems become functionally integrated producing an evolutionary developmental model. We build such a model by integrating growth and development of the cochlea, larynx, and sound production with the ontogeny of locomotion in newborn bats. In addition, we use available fossil and molecular data along with patterns of high frequency vocalization in extant mammals to model probable evolutionary transitions in bats. We find clear evidence that the ability to hear high frequency echolocation-like sounds preceded the ability to produce it and that a simple echolocation system was likely inherited from a shrew-like ancestor and was not an in situ evolutionary innovation of bats. Refinement of this system coevolved with sustained flight, both ontogenetically and evolutionarily, leading to the sophisticated echolocation observed today.     

The Radiata and the evolutionary origins of the bilaterian body plan

The apparent conservation of cellular and molecular developmental mechanisms observed in a handful of bilaterian metazoans has spawned a "race" to reconstruct the bilaterian ancestor. Knowledge of this ancestor would permit us to reconstruct the evolutionary changes that have occurred along specific bilaterian lineages. However, comparisons among extant bilaterians provide an unnecessarily limited view of the ancestral bilaterian. Since the original bilaterians are believed by many to be derived from a radially symmetrical ancestor, additional evidence might be obtained by examining present-day radially symmetrical animals. We briefly review pertinent features of the body plans of the extant radial eumetazoan phyla, the Cnidaria, and Ctenophora, in the context of revealing potential evolutionary links to the bilaterians.     

The making of a monster: postnatal ontogenetic changes in craniomandibular shape in the great sabercat Smilodon

Derived sabercats had craniomandibular morphologies that in many respects were highly different from those of extant felids, and this has often been interpreted functionally as adaptations for predation at extreme gape angles with hypertrophied upper canines. It is unknown how much of this was a result of intraspecific postnatal ontogeny, since juveniles of sabercats are rare and no quantitative study has been made of craniomandibular ontogeny. Postnatal ontogenetic craniomandibular shape changes in two morphologically derived sabercats, Smilodon fatalis and S. populator, were analysed using geometric morphometrics and compared to three species of extant pantherines, the jaguar, tiger, and Sunda clouded leopard. Ontogenetic shape changes in Smilodon usually involved the same areas of the cranium and mandible as in extant pantherines, and large-scale modularization was similar, suggesting that such may have been the case for all felids, since it followed the same trends previously observed in other mammals. However, in other respects Smilodon differed from extant pantherines. Their crania underwent much greater and more localised ontogenetic shape changes than did the mandibles, whereas crania and mandibles of extant pantherines underwent smaller, fewer and less localised shape changes. Ontogenetic shape changes in the two species of Smilodon are largely similar, but differences are also present, notably those which may be tied to the presence of larger upper canines in S. populator. Several of the specialized cranial characters differentiating adult Smilodon from extant felids in a functional context, which are usually regarded as evolutionary adaptations for achieving high gape angles, are ontogenetic, and in several instances ontogeny appears to recapitulate phylogeny to some extent. No such ontogenetic evolutionary adaptive changes were found in the extant pantherines. Evolution in morphologically derived sabercats involved greater cranial ontogenetic changes than among extant felids, resulting in greatly modified adult craniomandibular morphologies.     

Frequent nonrandom shifts in the temporal sequence of developmental landmark events during teleost evolutionary diversification

Morphological transformations can be generated by evolutionary changes in the sequence of developmental events. In this study, we examined the evolutionary dynamics of the developmental sequence on a macroevolutionary scale in teleosts. Using the information from previous reports describing the development of 31 species, we extracted the developmental sequences of 19 landmark events involving the formation of phylogenetically conserved body parts; we then inferred ancestral developmental sequences by two different parsimony‐based methods—event‐pairing and continuous analysis. The phylogenetic comparisons of these sequences revealed event‐dependent heterogeneity in the frequency of sequence changes. Most of the sequence changes occurred as exchanges of temporally neighboring events. These heterochronic changes in developmental sequences accumulated along evolutionary time, but the precise distribution of the changes over the teleostean phylogeny remains unclear due to technical limitations.     

Developmental Integration and the Evolution of Pleiotropy

The different forms of morphological integration, developmental,functional, genetic, and evolutionary are defined and theirtheoretical relationships explored. Quantitative genetic modelspredict that the co-selection of traits involved in a commonfunction will lead to pleiotropic effects at the loci affectingthem while functionally-unrelated traits will be affected byseparate sets of loci (Wagner, 1996). The patterns of geneticvariation produced by these pleiotropic mutations and stabilizingselection for functionally and developmentally interacting traitsresults in their specific co-inheritance relative to other traits.This in turn leads to their co-ordinated response to selection.Therefore, functional and developmental integration lead togenetic integration which, in turn leads to evolutionary integration.Three examples of how developmental integration structures pleiotropyand morphological variation in non-human primate crania, artificially-modifiedhuman crania, and for the effects ofindividual genes on murinemandibular morphology are presented.     

Towards a historization of aposematism

Aposematism is one of the oldest phenomena in evolutionary biology and still a major puzzle to biologists. Despite its evolutionary nature, most attempts to understand aposematism are devoid of phylogenetic components. In addition, most studies that do take phylogeny into account need to bring the analysis even further. We argue that in order to fully understand aposematism we must have a clear picture of the evolutionary history behind present behaviours. In this paper we frame aposematism in a phylogenetic context and argue that most studies still are wanting in terms of demonstrating aposematism. Aposematism is not an end product but rather evolutionary scenarios including character transformations as well as prey–predator interactions. Finally, we suggest that, regardless how we restrict the concept of aposematism, knowing the directions of events facilitate all kinds of comparisons with a promise of uniting functional and evolutionary aspects into a historization of aposematism.     

Exploring developmental, functional, and evolutionary aspects of amphioxus sensory cells

Amphioxus has neither elaborated brains nor definitive sensory organs, so that the two may have evolved in a mutually affecting manner and given rise to the forms seen in extant vertebrates. Clarifying the developmental and functional aspects of the amphioxus sensory system is thus pivotal for inferring the early evolution of vertebrates. Morphological studies have identified and classified amphioxus sensory cells; however, it is completely unknown whether the morphological classification makes sense in functional and evolutionary terms. Molecular markers, such as gene expression, are therefore indispensable for investigating the developmental and functional aspects of amphioxus sensory cells. This article reviews recent molecular studies on amphioxus sensory cells. Increasing evidence shows that the non-neural ectoderm of amphioxus can be subdivided into molecularly distinct subdomains by the combinatorial code of developmental cues involving the RA-dependent Hox code, suggesting that amphioxus epithelial sensory cells developed along positional information. This study focuses particularly on research involving the molecular phylogeny and expression of the seven-transmembrane, G protein-coupled receptor (GPCR) genes and discusses the usefulness of this information for characterizing the sensory cells of amphioxus.     

Arabidopsis thaliana leaf form evolved via loss of KNOX expression in leaves in association with a selective sweep

Morphological diversity is often caused by altered gene expression of key developmental regulators. However, the precise developmental trajectories through which morphologies evolved remain poorly understood. It is also unclear to what degree genetic changes contributing to morphological divergence were fixed by natural selection. Here we investigate these problems in the context of evolutionary developmental transitions that produced the simple unlobed leaf of the model species Arabidopsis thaliana. We demonstrate that A. thaliana leaf shape likely derived from a more complex lobed ancestral state that persists in extant Arabidopsis species. We also show that evolution of the unlobed leaf form in A. thaliana involved loss of expression of the knotted1-like homeobox gene SHOOTMERISTEMLESS (STM) in leaves and that cis-regulatory divergence contributed to this process. Further, we provide evidence for a selective sweep at the A. thaliana STM locus, indicating that loss of STM expression in A. thaliana leaves may have been fixed by positive selection. In summary, our data provide key information as to when and how the characteristic leaf form of A. thaliana evolved.     

Does morphological convergence imply functional similarity? A test using the evolution of quadrupedalism in ornithischian dinosaurs

Convergent morphologies are thought to indicate functional similarity, arising because of a limited number of evolutionary or developmental pathways. Extant taxa displaying convergent morphologies are used as analogues to assess function in extinct taxa with similar characteristics. However, functional studies of extant taxa have shown that functional similarity can arise from differing morphologies, calling into question the paradigm that form and function are closely related. We test the hypothesis that convergent skeletal morphology indicates functional similarity in the fossil record using ornithischian dinosaurs. The rare transition from bipedality to quadrupedality occurred at least three times independently in this clade, resulting in a suite of convergent osteological characteristics. We use homology rather than analogy to provide an independent line of evidence about function, reconstructing soft tissues using the extant phylogenetic bracket and applying biomechanical concepts to produce qualitative assessments of muscle leverage. We also optimize character changes to investigate the sequence of character acquisition. Different lineages of quadrupedal ornithischian dinosaur stood and walked differently from each other, falsifying the hypothesis that osteological convergence indicates functional similarity. The acquisition of features correlated with quadrupedalism generally occurs in the same order in each clade, suggesting underlying developmental mechanisms that act as evolutionary constraints.     

Plant growth forms: an ecological and evolutionary perspective

Trees, shrubs, lianas and herbs have widely different mechanical architectures, which can also vary phenotypically with the environment. This review investigates how environmental effects, particularly mechanical perturbation, can influence biomechanical development in self-supporting and climbing growth forms. The bifacial vascular cambium is discussed in terms of its significance to growth form variation, ecology and evolution among extant plants, and during its appearance and early evolution. A key aspect of this developmental innovation concerned its potential for architectural and mechanical variation in response to environmental effects as well as optimizing hydraulic supply before the appearance of laminate leaves. Growth form diversity and its importance to past and present ecosystems are discussed in relation to both evolutionary constraints and ecological factors such as climatic change and atmospheric CO2 concentrations. We discuss how widely ranging growth forms such as climbers show a large range of developmental and phenotypic variation that has much to offer in understanding how the environment can modify plant development, particularly in terms of the bifacial vascular cambium. The broad approach we propose would benefit a wide range of studies from research into wood development to long-term ecological censuses of today's potentially changing ecosystems.     

Evolution and patterning of the ovule in seed plants

The ovule and its developmental successor, the seed, together represent a highly characteristic feature of seed plants that has strongly enhanced the reproductive and dispersal potential of this diverse group of taxa. Ovules encompass multiple tissues that perform various roles within a highly constrained space, requiring a complex cascade of genes that generate localized cell proliferation and programmed cell death during different developmental stages. Many heritable morphological differences among lineages reflect relative displacement of these tissues, but others, such as the second (outer) integuments of angiosperms and Gnetales, represent novel and apparently profound and independent innovations. Recent studies, mostly on model taxa, have considerably enhanced our understanding of gene expression in the ovule. However, understanding its evolutionary history requires a comparative and phylogenetic approach that is problematic when comparing extant angiosperms not only with phylogenetically distant extant gymnosperms but also with taxa known only from fossils. This paper reviews ovule characters across a phylogenetically broad range of seed plants in a dynamic developmental context. It discusses both well-established and recent theories of ovule and seed evolution and highlights potential gaps in comparative data that will usefully enhance our understanding of evolutionary transitions and developmental mechanisms.     

轮藻和陆地植物系统发育及其进化

Charophytic algae and land plants together make up a monophyletic group, streptophytes, which represents one of the main lineages of multicellular eukaryotes and has contributed greatly to the change of the environment on earth in the Phanerozoic Eon. Significant progress has been made to understand phylogenetic relationships among members of this group by phylogenetic studies of morphological and molecular data over the last twenty-five years. Mesostigma viride is now regarded as among the earliest diverging unicellular organisms in streptophytes. Characeae are the sister group to land plants. Liverworts represent the first diverging lineage of land plants. Hornworts and lycophytes are extant representatives of bryophytes and vascular plants, respectively, when early land plants changed from gametophyte to sporophyte as the dominant generation in the life cycle. Equisetum, Psilotaceae, and ferns constitute the monophyletic group of monilophytes, which are sister to seed plants. Gnetales are related to conifers, not to angiosperms as previously thought. Amborella, Nymphaeales, Hydatellaceae, Illiciales, Trimeniaceae, and Austrobaileya represent the earliest diverging lineages of extant angiosperms. These phylogenetic results, together with recent progress on elucidating genetic and developmental aspects of the plant life cycle, multicellularity, and gravitropism, will facilitate evolutionary developmental studies of these key traits, which will help us to gain mechanistic understanding on how plants adapted to environmental challenges when they colonized the land during one of the major transitions in evolution of life.     

Assessing dinosaur growth patterns: a microscopic revolution

Some of the longest standing questions in dinosaur paleontology pertain to their development. Did dinosaurs grow at slow rates similar to extant reptiles or rapidly similar to living birds and mammals? How did some forms attain gigantic proportions? Conversely, how did birds (avian dinosaurs) become miniaturized? New data on dinosaur longevity garnered from bone microstructure (i.e. osteohistology) are making it possible to assess basic life-history parameters of the dinosaurs such as growth rates and timing of developmental events. Analyses of these data in an evolutionary context are enabling the identification of developmental patterns that lead to size changes within the Dinosauria. Furthermore, this rich new database is providing inroads for studying individual and population biology. All in all, paleohistological research is proving to be the most promising avenue towards gaining a comprehensive understanding of dinosaur biology.     

Evolutionary Connectionism: Algorithmic Principles Underlying the Evolution of Biological Organisation in Evo-Devo,Evo-Eco and Evolutionary Transitions

The mechanisms of variation, selection and inheritance, on which evolution by natural selection depends, are not fixed over evolutionary time. Current evolutionary biology is increasingly focussed on understanding how the evolution of developmental organisations modifies the distribution of phenotypic variation, the evolution of ecological relationships modifies the selective environment, and the evolution of reproductive relationships modifies the heritability of the evolutionary unit. The major transitions in evolution, in particular, involve radical changes in developmental, ecological and reproductive organisations that instantiate variation, selection and inheritance at a higher level of biological organisation. However, current evolutionary theory is poorly equipped to describe how these organisations change over evolutionary time and especially how that results in adaptive complexes at successive scales of organisation (the key problem is that evolution is self-referential, i.e. the products of evolution change the parameters of the evolutionary process). Here we first reinterpret the central open questions in these domains from a perspective that emphasises the common underlying themes. We then synthesise the findings from a developing body of work that is building a new theoretical approach to these questions by converting well-understood theory and results from models of cognitive learning. Specifically, connectionist models of memory and learning demonstrate how simple incremental mechanisms, adjusting the relationships between individually-simple components, can produce organisations that exhibit complex system-level behaviours and improve the adaptive capabilities of the system. We use the term “evolutionary connectionism” to recognise that, by functionally equivalent processes, natural selection acting on the relationships within and between evolutionary entities can result in organisations that produce complex system-level behaviours in evolutionary systems and modify the adaptive capabilities of natural selection over time. We review the evidence supporting the functional equivalences between the domains of learning and of evolution, and discuss the potential for this to resolve conceptual problems in our understanding of the evolution of developmental, ecological and reproductive organisations and, in particular, the major evolutionary transitions.     

Supertree analyses of the roles of viviparity and habitat in the evolution of atherinomorph fishes

Using supertree phylogenetic reconstructions, we investigate how livebearing and freshwater adaptations may have shaped evolutionary patterns in the Atherinomorpha, a large clade (approximately 1500 extant species) of ray-finned fishes. Based on maximum parsimony reconstructions, livebearing appears to have evolved at least four times independently in this group, and no reversions to the ancestral state of oviparity were evident. With respect to habitat, at least five evolutionary transitions apparently occurred from freshwater to marine environments, at least two transitions in the opposite direction, and no clear ancestral state was identifiable. All viviparous clades exhibited more extant species than their oviparous sister taxa, suggesting that transitions to viviparity may be associated with cladogenetic diversification. Transitions to freshwater were usually, but not invariably associated with increased species richness, but the trend was, overall, not significant among sister clades. Additionally, we investigated whether livebearing and freshwater adaptations are currently associated with elevated risks of extinction as implied by species' presence on the 2004 IUCN Red List. Despite being correlated with decreased brood size, livebearing has not significantly increased extinction risk in the Atherinomorpha. However, freshwater species were significantly more likely than marine species to be listed as endangered.     

Origin of evolutionary novelty: examples from limbs

Classic hypotheses of vertebrate morphology are being informed by new data and new methods. Long nascent issues, such as the origin of tetrapod limbs, are being explored by paleontologists, molecular biologists, and functional anatomists. Progress in this arena will ultimately come down to knowing how macroevolutionary differences between taxa emerge from the genetic and phenotypic variation that arises within populations. The assembly of limbs over developmental and evolutionary time offers examples of the major processes at work in the origin of novelties. Recent comparative developmental analyses demonstrate that many of the mechanisms used to pattern limbs are ancient. One of the major consequences of this phenomenon is parallelism in the evolution of anatomical structures. Studies of both the fossil record and intrapopulational variation of extant populations reveal regularities in the origin of variation. These examples reveal processes acting at the level of populations that directly affect the patterns of diversity observed at higher taxonomic levels.     

The evolutionary history of the ‘alba’ polymorphism in the butterfly subfamily Coliadinae (Lepidoptera: Pieridae)

Polymorphisms are common in the natural world and have played an important role in our understanding of how selection maintains multiple phenotypes within extant populations. Studying the evolutionary history of polymorphisms has revealed important features of this widespread form of phenotypic diversity, including its role in speciation, niche breadth, and range size. In the present study, we examined the evolutionary history of a ubiquitous colour polymorphism in the sulphur butterflies (subfamily: Coliadinae) termed the ‘alba’ polymorphism. We investigated the origin and stability of the ‘alba’ polymorphism using ancestral state reconstruction analysis. Our results indicate that the ancestor of the Coliadinae was polymorphic and that this polymorphism has undergone repeated transitions to monomorphism. Repeated loss of polymorphism suggests that the ‘alba’ polymorphism may be relatively unstable over evolutionary time. These results provide a framework for future studies on the origin and maintenance of the ‘alba’ polymorphism and guide the direction of future hypotheses. We discuss these results in light of current understandings of how the ‘alba’ polymorphism is maintained in extant populations.