Using zebrafish to investigate cypriniform evolutionary novelties: functional development and evolutionary diversification of the kinethmoid

Although the zebrafish has become a popular model organism for biomedical studies, we propose that the wealth of morphological novelties that characterize this cypriniform fish makes it well suited for investigating the development of evolutionary innovations. Morphological novelties associated with feeding in cypriniform fishes include: a unique structure of the pharyngeal jaws in which the lower pharyngeal jaws are enlarged and opposed to a pad on the basioccipital process; a palatal organ found on the roof of the buccal chamber that is thought to help process detrital food within the buccal chamber; and, the kinethmoid, a novel ossification that effects a unique means of premaxillary protrusion. We present new morphological and developmental data and review functional data regarding the role of the kinethmoid in premaxillary protrusion in the zebrafish. Premaxillary protrusion plays an important role in effective prey acquisition in teleosts and the evolution of a unique means of premaxillary protrusion within Cypriniformes may have led to a number of trophic radiations within this clade. Ontogenetic data from zebrafish show that substantial premaxillary protrusion is not seen until these fish have undergone metamorphosis at which point the adductor mandibulae musculature becomes divided and all ligamentous attachments become established. A comparative study of families within Cypriniformes shows diverse morphologies of the kinethmoid. The morphological diversification that characterizes the kinethmoid suggests that this feeding structure has played a role in trophic radiations within Cypriniformes, since the morphology of this feature is correlated with feeding habits.     

The contribution of pseudouridine to stabilities and structure of RNAs

Thermodynamic data are reported revealing that pseudouridine (Ψ) can stabilize RNA duplexes when replacing U and forming Ψ-A, Ψ-G, Ψ-U and Ψ-C pairs. Stabilization is dependent on type of base pair, position of Ψ within the RNA duplex, and type and orientation of adjacent Watson–Crick pairs. NMR spectra demonstrate that for internal Ψ-A, Ψ-G and Ψ-U pairs, the N3 imino proton is hydrogen bonded to the opposite strand nucleotide and the N1 imino proton may also be hydrogen bonded. CD spectra show that general A-helix structure is preserved, but there is some shifting of peaks and changing of intensities. Ψ has two hydrogen donors (N1 and N3 imino protons) and two hydrogen bond acceptors because the glycosidic bond is C-C rather than C-N as in uridine. This greater structural potential may allow Ψ to behave as a kind of structurally driven universal base because it can enhance stability relative to U when paired with A, G, U or C inside a double helix. These structural and thermodynamic properties may contribute to the biological functions of Ψ.     

Cyclical parthenogenesis and viviparity in aphids as evolutionary novelties

Evolutionary novelties represent challenges to biologists, particularly those who would like to understand the developmental and genetic changes responsible for their appearance. Most modern aphids possess two apparent evolutionary novelties: cyclical parthenogenesis (a life cycle with both sexual and asexual phases) and viviparity (internal development and live birth of progeny) in their asexual phase. Here I discuss the evolution of these apparent novelties from a developmental standpoint. Although a full understanding of the evolution of cyclical parthenogenesis and viviparity in aphids can seem a daunting task, these complex transitions can at least be broken down into a handful of steps. I argue that these should include the following: a differentiation of two developmentally distinct oocytes; de novo synthesis of centrosomes and modification of meiosis during asexual oogenesis; a loss or bypass of any cell cycle arrest and changes in key developmental events during viviparous oogenesis; and a change in how mothers specify the sexual vs. asexual fates of their progeny. Grappling with the nature of such steps and the order in which they occurred ought to increase our understanding and reduce the apparent novelty of complex evolutionary transitions. J. Exp. Zool. (Mol. Dev. Evol.) 318B:448-459, 2012. ? 2012 Wiley Periodicals, Inc.     

The contribution of statistical physics to evolutionary biology

Evolutionary biology shares many concepts with statistical physics: both deal with populations, whether of molecules or organisms, and both seek to simplify evolution in very many dimensions. Often, methodologies have undergone parallel and independent development, as with stochastic methods in population genetics. Here, we discuss aspects of population genetics that have embraced methods from physics: non-equilibrium statistical mechanics, travelling waves and Monte-Carlo methods, among others, have been used to study polygenic evolution, rates of adaptation and range expansions. These applications indicate that evolutionary biology can further benefit from interactions with other areas of statistical physics; for example, by following the distribution of paths taken by a population through time.     

The contribution of developmental palaeontology to extensions of evolutionary theory

Evo‐devo is featuring prominently in current discussion to extend evolutionary theory. Developmental palaeontology, the study of life history evolution and ontogeny in fossils, remains an area of investigation that could benefit from, but also illuminate, the discourse and research agenda of evo‐devo. Understanding how and why evolution proceeds in phenotypic space is an important goal of evo‐devo and one that can be significantly enriched through the examination of development in the fossil record (Palaeo‐evo‐devo). Such an approach permits developmental pathways to be extended into the past, constraining hypotheses of developmental evolution in ways that cannot be predicted by patterns observed from extant taxa alone. The comparison of developmental dynamics among extant and extinct taxa yields a more complete understanding of the temporal persistence of factors that shape evolution in phenotypic space. As more data are compiled that document ‘fossilized ontogenies’, a stage will emerge from which insights into the evolution of development can begin to appraise those phenotypes that are inaccessible to evo‐devo.     

The evolutionary history of small RNAs in Solanaceae

The Solanaceae or “nightshade” family is an economically important group with remarkable diversity. To gain a better understanding of how the unique biology of the Solanaceae relates to the family’s small RNA (sRNA) genomic landscape, we downloaded over 255 publicly available sRNA data sets that comprise over 2.6 billion reads of sequence data. We applied a suite of computational tools to predict and annotate two major sRNA classes: (1) microRNAs (miRNAs), typically 20- to 22-nucleotide (nt) RNAs generated from a hairpin precursor and functioning in gene silencing and (2) short interfering RNAs (siRNAs), including 24-nt heterochromatic siRNAs typically functioning to repress repetitive regions of the genome via RNA-directed DNA methylation, as well as secondary phased siRNAs and trans-acting siRNAs generated via miRNA-directed cleavage of a polymerase II-derived RNA precursor. Our analyses described thousands of sRNA loci, including poorly understood clusters of 22-nt siRNAs that accumulate during viral infection. The birth, death, expansion, and contraction of these sRNA loci are dynamic evolutionary processes that characterize the Solanaceae family. These analyses indicate that individuals within the same genus share similar sRNA landscapes, whereas comparisons between distinct genera within the Solanaceae reveal relatively few commonalities.

Analysis of over 255 publicly available small RNA data sets enabled characterization of the small RNA landscape for the Solanaceae family.     

Plasticity of ontogenetic trajectories in cyprinids: a source of evolutionary novelties

Research in evolutionary developmental (evo‐devo) biology is making an increasingly important contribution to our understanding of the molecular mechanisms underlying the establishment of complex morphological traits. Deciphering the ontogenetic trajectories leading to the differentiation of sister species (and the existence of hybrids) is a new challenge in our understanding of speciation processes. In the present study, we characterized the ontogenetic trajectory of lower lip morphology in two cyprinid species and their hybrids. Chondrostoma toxostoma has an arched lower lip and a generalist diet. Chondrostoma nasus has a straight lower lip and a specialist diet. An analysis of 99 C. toxostoma, 99 C. nasus and 25 first‐generation (F₁) hybrid individuals demonstrated that the difference between arched and straight lip morphology was found to depend strongly on the height/width ratio of the lower lip. A comparison of the ontogenetic trajectories of these morphometric traits showed that the height of the lower lip was isometric to body length in both species, whereas developmental changes involving an acceleration and a hypermorphosis of the widening of the lower lip led to a straight lip morphology in C. nasus. F₁ hybrids were characterized by an extreme phenotype resulting from a rate of lower lip widening slower than that in the two parent species. Therefore, we rejected a codominance hypothesis and concluded that the first stage of hybridization provides the foundations of evolutionary novelty. These results have important evolutionary implications because lower lip shape is linked to dietary behaviour in many fish species. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 342–355.     

The contribution of recombination to heterozygosity differs among plant evolutionary lineages and life-forms

Background  

Despite its role as a generator of haplotypic variation, little is known about how the rates of recombination evolve across taxa. Recombination is a very labile force, susceptible to evolutionary and life trait related processes, which have also been correlated with general levels of genetic diversity. For example, in plants, it has been shown that long-lived outcrossing taxa, such as trees, have higher heterozygosity (H _e) at SSRs and allozymes than selfing or annual species. However, some of these tree taxa have surprisingly low levels of nucleotide diversity at the DNA sequence level, which points to recombination as a potential generator of genetic diversity in these organisms. In this study, we examine how genome-wide and within-gene rates of recombination evolve across plant taxa, determine whether such rates are influenced by the life-form adopted by species, and evaluate if higher genome-wide rates of recombination translate into higher H _e values, especially in trees.     

Functional evolutionary developmental biology (evo-devo) of morphological novelties in plants

The origin of morphological and ecological novelties is a long-standing problem in evolutionary biology.Understanding these processes requires investigation from both the development and evolution standpoints,which promotes a new research field called evolutionary developmental biology (evo-devo).The fundamental mechanism for the origin of a novel structure may involve heterotopy,heterochrony,ectopic expression,or loss of an existing regulatory factor.Accordingly,the morphological and ecological traits cont...     

Conserved developmental processes and the formation of evolutionary novelties: examples from butterfly wings

The origin and diversification of evolutionary novelties-lineage-specific traits of new adaptive value-is one of the key issues in evolutionary developmental biology. However, comparative analysis of the genetic and developmental bases of such traits can be difficult when they have no obvious homologue in model organisms. The finding that the evolution of morphological novelties often involves the recruitment of pre-existing genes and/or gene networks offers the potential to overcome this challenge. Knowledge about shared developmental processes obtained from extensive studies in model organisms can then be used to understand the origin and diversification of lineage-specific structures. Here, we illustrate this approach in relation to eyespots on the wings of Bicyclus anynana butterflies. A number of spontaneous mutations isolated in the laboratory affect eyespots, lepidopteran-specific features, and also processes that are shared by most insects. We discuss how eyespot mutants with disturbed embryonic development may help elucidate the genetic pathways involved in eyespot formation, and how venation mutants with altered eyespot patterns might shed light on mechanisms of eyespot development.     

Small regulatory RNAs controlled by genomic imprinting and their contribution to human disease

More than a hundred protein-coding genes are controlled by genomic imprinting in humans. These atypical genes are organized in chromosomal domains, each of which is controlled by a differentially methylated "imprinting control region" (ICR). How ICRs mediate the parental allele-specific expression of close-by genes is now becoming understood. At several imprinted domains, this epigenetic mechanism involves the action of long non-coding RNAs. It is less well appreciated that imprinted gene domains also transcribe hundreds of microRNA and small nucleolar RNA genes and that these represent the densest clusters of small RNA genes in mammalian genomes. The evolutionary reasons for this remarkable enrichment of small regulatory RNAs at imprinted domains remain unclear. However, recent studies show that imprinted small RNAs modulate specific functions in development and metabolism and also are frequently perturbed in cancer. Here, we review our current understanding of imprinted small RNAs in the human genome and discuss how perturbation of their expression contributes to disease.     

Small regulatory RNAs controlled by genomic imprinting and their contribution to human disease

More than a hundred protein-coding genes are controlled by genomic imprinting in humans. These atypical genes are organized in chromosomal domains, each of which is controlled by a differentially methylated "imprinting control region" (ICR). How ICRs mediate the parental allele-specific expression of close-by genes is now becoming understood. At several imprinted domains, this epigenetic mechanism involves the action of long non-coding RNAs. It is less well appreciated that imprinted gene domains also transcribe hundreds of microRNA and small nucleolar RNA genes and that these represent the densest clusters of small RNA genes in mammalian genomes. The evolutionary reasons for this remarkable enrichment of small regulatory RNAs at imprinted domains remain unclear. However, recent studies show that imprinted small RNAs modulate specific functions in development and metabolism and also are frequently perturbed in cancer. Here, we review our current understanding of imprinted small RNAs in the human genome and discuss how perturbation of their expression contributes to disease.     

Functional evolutionary developmental biology (evo‐devo) of morphological novelties in plants

Abstract The origin of morphological and ecological novelties is a long‐standing problem in evolutionary biology. Understanding these processes requires investigation from both the development and evolution standpoints, which promotes a new research field called “evolutionary developmental biology” (evo‐devo). The fundamental mechanism for the origin of a novel structure may involve heterotopy, heterochrony, ectopic expression, or loss of an existing regulatory factor. Accordingly, the morphological and ecological traits controlled by the regulatory genes may be gained, lost, or regained during evolution. Floral morphological novelties, for example, include homeotic alterations (related to organ identity), symmetric diversity, and changes in the size and morphology of the floral organs. These gains and losses can potentially arise through modification of the existing regulatory networks. Here, we review current knowledge concerning the origin of novel floral structures, such as “evolutionary homeotic mutated flowers”, floral symmetry in various plant species, and inflated calyx syndrome (ICS) within Solanaceae. Functional evo‐devo of the morphological novelties is a central theme of plant evolutionary biology. In addition, the discussion is extended to consider agronomic or domestication‐related traits, including the type, size, and morphology of fruits (berries), within Solanaceae.     

Homology of the internal sac components in the leaf beetle subfamily criocerinae and evolutionary novelties related to the extremely elongated flagellum

Extremely elongated intromittent organs are found in a wide range of taxa, especially among insects. This phenomenon is generally thought to result from sexual selection, but it is predicted that limited storage space in the body cavity and the difficulty of using the elongated organs should have constrained the evolution of extreme elongation, neutralizing any selective advantage. Therefore, in groups with long intromittent organs, features that overcome these constraints may have evolved or coevolved together with intromittent organ elongation. Using a comparative morphological approach and outgroup comparisons, we identified potential constraints and key novelties that may neutralize such constraints in the leaf beetle subfamily Criocerinae. Observations of the internal sac structure throughout Criocerinae were performed. Comparing the results with preceding studies from outgroups, a ground plan of the criocerine internal sac was constructed. Our analysis also identified specific features that are always correlated with extreme elongation: the rotation of whole internal‐sac sclerites and the possession of a pocket in which to store the elongated flagellum. The pocket is thought to be formed by the rotation of the sclerites, markedly altering internal sac shape from the criocerine ground plan. Onlythe clades that have acquired this derived state contain species with an elongated flagellum that distinctly exceeds the median lobe length. It is presumed that these character correlations evolved independently three times. The detected character correlations corroborate the hypothesis that there are latent adaptive constraints for the evolution of extremely elongated intromittent organs. The constraints may have been neutralized by the alteration from the criocerine ground plan resulting in the formation of a storage pocket. In conclusion, deviation from the criocerine ground plan isconsidered to be the evolutionary innovation that neutralized the latent adaptive constraints of flagellum elongation in the subfamily Criocerinae. J. Morphol., 2012. © 2011 Wiley Periodicals, Inc.     

Environmental sensing by chromatin: an epigenetic contribution to evolutionary change

Chromatin structure and function are regulated by families of protein-modifying enzymes that are sensitive to a variety of metabolic and environmental agents. These enzymes, and proteins that read the modifications they maintain, constitute a system by which environmental agents, such as chemical toxins and dietary components, can directly regulate patterns of gene expression. This review describes this environmental sensing system from an evolutionary perspective. It is proposed that persistent environmentally-induced changes in gene expression patterns can cause changes in phenotype that are acted upon by natural selection, and that epigenetic processes can potentially play central roles in evolution.     

Paired sequence difference in ribosomal RNAs: evolutionary and phylogenetic implications

Ribosomal RNAs have secondary structures that are maintained by internal Watson-Crick pairing. Through analysis of chordate, arthropod, and plant 5S ribosomal RNA sequences, we show that Darwinian selection operates on these nucleotide sequences to maintain functionally important secondary structure. Insect phylogenies based on nucleotide positions involved in pairing and the production of secondary structure are incongruent with those constructed on the basis of positions that are not. Furthermore, phylogeny reconstruction using these nonpairing bases is concordant with other, morphological data.