Testing heterochrony: Connecting skull shape ontogeny and evolution of feeding adaptations in baleen whales

Ontogeny plays a key role in the evolution of organisms, as changes during the complex processes of development can allow for new traits to arise. Identifying changes in ontogenetic allometry—the relationship between skull shape and size during growth—can reveal the processes underlying major evolutionary transformations. Baleen whales (Mysticeti, Cetacea) underwent major morphological changes in transitioning from their ancestral raptorial feeding mode to the three specialized filter-feeding modes observed in extant taxa. Heterochronic processes have been implicated in the evolution of these feeding modes, and their associated specialized cranial morphologies, but their role has never been tested with quantitative data. Here, we quantified skull shapes ontogeny and reconstructed ancestral allometric trajectories using 3D geometric morphometrics and phylogenetic comparative methods on sample representing modern mysticetes diversity. Our results demonstrate that Mysticeti, while having a common developmental trajectory, present distinct cranial shapes from early in their ontogeny corresponding to their different feeding ecologies. Size is the main driver of shape disparity across mysticetes. Disparate heterochronic processes are evident in the evolution of the group: skim feeders present accelerated growth relative to the ancestral nodes, while Balaenopteridae have overall slower growth, or pedomorphosis. Gray whales are the only taxon with a relatively faster rate of growth in this group, which might be connected to its unique benthic feeding strategy. Reconstructed ancestral allometries and related skull shapes indicate that extinct taxa used less specialized filter-feeding modes, a finding broadly in line with the available fossil evidence.     

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.     

Levels of diversity in endomycorrhizal fungi (Glomales,Zygomycetes) and their role in defining taxonomic and non-taxonomic groups

Diversity in glomalean fungi is manifested at the molecular, morphological, and ecological levels. Characters at any of these levels can be ordered into hierarchical patterns defining taxonomic groups if they are conserved enough to be heritable through geologic time in all descendants of a common ancestor. At present, only morphological characters associated with mode of spore formation and in subcellular structure of spores are sufficiently stable and diverse to recognize at least 150 species. Ontogenetic comparisons indicate that species integrity, despite asexual reproduction, is the result of rigid internal constraints imposed on variation during the process of spore subcellular differentiation. Epigenetic factors dominate because the differentiation sequence is linear and each new stage is causally linked to preceding stages. Some morphological characters of the fungal mycelium also exist, but they define more inclusive groups at the family level and above. Most diversity in the mycorrhizae consists of life-history traits associated with abundance and architecture of fungal components, their rate of formation and longevity, and their cost in the symbiosis. These characters participate in processes at the molecular and ecological levels, so they are autonomous from morphological determinants. They often are labile or affected by external environmental conditions, so fewer stable taxonomic characters are likely to be discovered. Instead, molecular and ecological diversity has greater potential to define; (a) niche specificity of organisms/populations and (b) causal processes linked to host-fungus compatibility and mycorrhizal efficiency. Any taxonomic characters that relate to mycorrhizal functions will come only from comparative studies involving organisms from shared habitats rather than those having shared spore morphologies.     

A Genomic and Molecular View of Wood Formation

Wood formation is a process derived from plant secondary growth. Different from primary growth, plant secondary growth is derived from cambium meristem cells in the vascular and cork cambia and leads to the girth increase of the plant trunk. In the secondary growth process, plants convert most of photosynthesized products into various biopolymers for use in the formation of woody tissues. This article summarizes the new developments of genomic and genetic characterization of wood formation in herbaceous model plant and tree plant systems. Genomic studies have categorized a collection of the genes for which expression is associated with secondary growth. During wood formation, the expression of many genes is regulated in a stage-specific manner. The function of many genes involved in wood biosyntheses and xylem differentiation has been characterized. Although great progress has been achieved in the molecular and genomic understanding of plant secondary growth in recent years, the profound genetic mechanisms underlying this plant development remain to be investigated. Completion of the first tree genome sequence (Populus genome) provides a valuable genomic resource for characterization of plant secondary growth.     

Constraints in the ligament ontogeny and evolution of pteriomorphian Bivalvia

A study of ligaments of larval, postlarval and adult shells of fossil and recent pteriomorphian bivalves leads to the following observations and hypotheses: (1) Ligament growth passively follows the general growth pattern of the mantle margin. No independent genetic information fixes the anterior, ventral, or posterior growth direction of the ligament. Further growth constraints relate to physical availability of space on the ligament area and to heterochronic processes. (2) The disjunct ligament and the repetition of fibrous or lamellar sublayers are phenotypic aspects of the same derived ligament Bauplan 1. All Pteriomorphia possess the ability to produce repetitive ligaments. This ability and space reductions of the ligament area in independent phylogenetic lineages are responsible for the iterative evolution of ligament grades. (3) Spondylidae and Plicatulidae are duplivincular, and the Ostreoidea are plesiomorphically multivincular. (4) Larval anterior-helical growth of the soft tissue produces opisthogyrate shells and possibly caused the evolution of the alivincular-multivincular grade. Duplivincular-alivincular and multivincular-alivincular grades can be distinguished if larval shell characters are known. (5) The taxonomic distribution of ligament grades as amended in this paper is largely consistent with modern phylogeny hypotheses based on genetic or morphologic or combined character sets. However, the resolution of early phylogenetic nodes requires more data on larval shells of Lower Palaeozoic taxa.     

Spatiotemporal reorganization of growth rates in the evolution of ontogeny

Abstract. Heterochrony, evolutionary changes in rate or timing of development producing parallelism between ontogeny and phylogeny, is viewed as the most common type of evolutionary change in development. Alternative hypotheses such as heterotopy, evolutionary change in the spatial patterning of development, are rarely entertained. We examine the evidence for heterochrony and heterotopy in the evolution of body shape in two clades of piranhas. One of these is the sole case of heterochrony previously reported in the group; the others were previously interpreted as cases of heterotopy. To compare ontogenies of shape, we computed ontogenetic trajectories of shape by multivariate regression of geometric shape variables (i.e., partial warp scores and shape coordinates) on centroid size. Rates of development relative to developmental age and angles between the trajectories were compared statistically. We found a significant difference in developmental rate between species of Serrasalmus , suggesting that heterochrony is a partial explanation for the evolution of body shape, but we also found a significant difference between their ontogenetic transformations; the direction of the difference between them suggests that heterotopy also plays a role in this group. In Pygocentrus we found no difference in developmental rate among species, but we did find a difference in the ontogenies, suggesting that heterotopy, but not heterochrony, is the developmental basis for shape diversification in this group. The prevalence of heterotopy as a source of evolutionary novelty remains largely unexplored and will not become clear until the search for developmental explanations looks beyond heterochrony.     

The role of two LEAFY paralogs from Idahoa scapigera (Brassicaceae) in the evolution of a derived plant architecture

Idahoa scapigera produces solitary flowers in the axils of rosette leaves without elongation of the shoot axis, a rosette-flowering architecture. Previous work with one of the two I. scapigera LFY paralogs, IscLFY1, showed that this gene caused aerial flowering rosettes in Arabidopsis thaliana. In this paper, we report that after three generations IscLFY1 transgenic lines are phenotypically indistinguishable from wild-type Arabidopsis, indicating that IscLFY1 protein is able to replace normal LFY function. Additionally, we found that ectopic LFY expression late in development can phenocopy aspects of the aerial rosette phenotype, suggesting that shoot compression caused by IscLFY1 could be caused by localized overexpression of a functional IscLFY protein. We also characterized the expression and function of the second I. scapigera LFY paralog, IscLFY2, in A. thaliana. In contrast to IscLFY1, this paralog was expressed in floral meristems and the shoot apical meristem (SAM). In I. scapigera, LFY-specific antibodies detected high protein levels in developing flowers but not in the apex, suggesting trans-regulatory differences between I. scapigera and A. thaliana. Most IscLFY2 transgenic A. thaliana plants were indistinguishable from wild type, but in a minority of lines the SAM was converted to a terminal flower as would be expected from the reporter-expression pattern. Taken together these results show that both I. scapigera paralogs have conserved LFY function, both proteins can rescue lfy and both can modify inflorescence architecture in an A. thaliana background: either by affecting internode elongation (IscLFY1) or by causing homeotic conversion of shoots into flowers (IscLFY2).     

The effects of island ontogeny on species diversity and phylogeny

A major goal of island biogeography is to understand how island communities are assembled over time. However, we know little about the influence of variable area and ecological opportunity on island biotas over geological timescales. Islands have limited life spans, and it has been posited that insular diversity patterns should rise and fall with an island''s ontogeny. The potential of phylogenies to inform us of island ontogenetic stage remains unclear, as we lack a phylogenetic framework that focuses on islands rather than clades. Here, we present a parsimonious island-centric model that integrates phylogeny and ontogeny into island biogeography and can incorporate a negative feedback of diversity on species origination. This framework allows us to generate predictions about species richness and phylogenies on islands of different ages. We find that peak richness lags behind peak island area, and that endemic species age increases with island age on volcanic islands. When diversity negatively affects rates of immigration and cladogenesis, our model predicts speciation slowdowns on old islands. Importantly, we find that branching times of in situ radiations can be informative of an island''s ontogenetic stage. This novel framework provides a quantitative means of uncovering processes responsible for island biogeography patterns using phylogenies.     

Asymmetric expression of a poplar ACC oxidase controls ethylene production during gravitational induction of tension wood

Ethylene is produced in wood-forming tissues, and when applied exogenously, it has been shown to cause profound effects on the pattern and rate of wood development. However, the molecular regulation of ethylene biosynthesis during wood formation is poorly understood. We have characterised an abundant 1-aminocyclopropane-1-carboxylic acid (ACC) oxidase gene (PttACO1) in the wood-forming tissues of Populus tremula (L.) x P. tremuloides (Michx). PttACO1 is primarily expressed in developing secondary xylem, and is specifically upregulated during secondary wall formation. Nevertheless, according to GC-MS analysis combined with tangential cryosectioning, the distribution of ACC was found to be fairly uniform across the cambial-region tissues. Gravitational stimulation, which causes tension wood to form on the upper side of the stem, resulted in a strong induction of PttACO1 expression and ACC oxidase activity in the tension wood-forming tissues. The ACC levels increased in parallel to the PttACO1 expression. However, the increase on the upper (tension wood) side was only minor, whereas large amounts of both ACC and its hydrolysable conjugates accumulated on the lower (opposite) side of the stem. This suggests that the relatively low level of ACC on the tension wood side is a result of its conversion to ethylene by the highly upregulated PttACO1, and the concurrent accumulation of ACC on the opposite side of the wood is because of the low PttACO1 levels. We conclude that PttACO1 and ACC oxidase activity, but not ACC availability, are important in the control of the asymmetric ethylene production within the poplar stem when tension wood is induced by gravitational stimulation.     

The role of post-natal ontogeny in the evolution of phenotypic diversity in Podarcis lizards

Understanding the role of the developmental pathways in shaping phenotypic diversity allows appreciating in full the processes influencing and constraining morphological change. Podarcis lizards demonstrate extraordinary morphological variability that likely originated in short evolutionary time. Using geometric morphometrics and a broad suite of statistical tests, we explored the role of developmental mechanisms such as growth rate change, ontogenetic divergence/convergence/parallelism as well as morphological expression of heterochronic processes in mediating the formation of their phenotypic diversity during the post-natal ontogeny. We identified hypermorphosis - the prolongation of growth along the same trajectory - as the process responsible for both intersexual and interspecific morphological differentiation. Albeit the common allometric pattern observed in both sexes of any species constrains and canalizes their cephalic scales variation in a fixed portion of the phenotypic space, the extended growth experienced by males and some species allows them to achieve peramorphic morphologies. Conversely, the intrasexual phenotypic diversity is accounted for by non-allometric processes that drive the extensive morphological dispersion throughout their ontogenetic trajectories. This study suggests a model of how simple heterochronic perturbations can produce phenotypic variation, and thus potential for further evolutionary change, even within a strictly constrained developmental pathway.     

Advancement in studies of tree growth and ecophysiology incorporating micro-sampling approach

The recently developed micro-sampling approach has been widely used to extract micro-tree-cores at weekly intervals to monitor the process of stem cambial activity and xylem formation. Compared with the traditional dendrochronology, the micro-sampling approach enables us to better understand the inherent physiological processes in tree growth and their relationships with the environment at a more precise level. This review article aims to: 1) summarize the progresses in the micro-sampling approach-based studies published over recent years and its potential applications, and 2) elucidate the relationships between primary growth and secondary growth and the response mechanisms of radial growth of trees to global change (global warming, drought, and carbon and nitrogen fertilization effects) based on information from literature. It is anticipated that this review will assist with predicting productivity and carbon sink potential of forests, and help policy-makers with sustainable forest management decisions.     

Ontogeny, anatomy, and the problem of homology: Carl Gegenbaur and the American tradition of cell lineage studies

Summary In this paper we analyze Carl Gegenbaur’s conception of the relationship between embryology (“Ontogenie”) and comparative anatomy and his related ideas about homology. We argue that Gegenbaur’s conviction of the primacy of comparative anatomy and his careful consideration of caenogenesis led him to a more balanced view about the relationship between ontogeny and phylogeny than his good friend Ernst Haeckel. We also argue that Gegenbaur’s ideas about the centrality of comparative anatomy and his definitions of homology actually laid the conceptual foundations for Hans Spemann’s (1915) later analysis of homology. We also analyze Gegenbaur’s reception in the United States and how the discussions between E.B. Wilson and Edwin Conklin about the role of the “embryological criterion of homology” and the latter’s argument for an even earlier concept of cellular homology reflect the recurring theme of preformism in ontogeny, a theme that finds its modern equivalent in various genetic definitions of homology, only recently challenged by the emerging synthesis of evolutionary developmental biology. Finally, we conclude that Gegenbaur’s own careful methodological principles can serve as an important model for proponents of present day “evo-devo”, especially with respect to the integration of ontogeny with phylogeny embedded in comparative anatomy.     

A mathematical framework for modelling cambial surface evolution using a level set method

Background and Aims

During their lifetime, tree stems take a series of successive nested shapes. Individual tree growth models traditionally focus on apical growth and architecture. However, cambial growth, which is distributed over a surface layer wrapping the whole organism, equally contributes to plant form and function. This study aims at providing a framework to simulate how organism shape evolves as a result of a secondary growth process that occurs at the cellular scale.

Methods

The development of the vascular cambium is modelled as an expanding surface using the level set method. The surface consists of multiple compartments following distinct expansion rules. Growth behaviour can be formulated as a mathematical function of surface state variables and independent variables to describe biological processes.

Key Results

The model was coupled to an architectural model and to a forest stand model to simulate cambium dynamics and wood formation at the scale of the organism. The model is able to simulate competition between cambia, surface irregularities and local features. Predicting the shapes associated with arbitrarily complex growth functions does not add complexity to the numerical method itself.

Conclusions

Despite their slenderness, it is sometimes useful to conceive of trees as expanding surfaces. The proposed mathematical framework provides a way to integrate through time and space the biological and physical mechanisms underlying cambium activity. It can be used either to test growth hypotheses or to generate detailed maps of wood internal structure.