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.     

A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems

A major goal of evolutionary science is to understand how biological diversity is generated and altered. Despite considerable advances, we still have limited insight into how phenotypic variation arises and is sorted by natural selection. Here we argue that an integrated view, which merges ecology, evolution and developmental biology (eco evo devo) on an equal footing, is needed to understand the multifaceted role of the environment in simultaneously determining the development of the phenotype and the nature of the selective environment, and how organisms in turn affect the environment through eco evo and eco devo feedbacks. To illustrate the usefulness of an integrated eco evo devo perspective, we connect it with the theory of resource polymorphism (i.e. the phenotypic and genetic diversification that occurs in response to variation in available resources). In so doing, we highlight fishes from recently glaciated freshwater systems as exceptionally well‐suited model systems for testing predictions of an eco evo devo framework in studies of diversification. Studies on these fishes show that intraspecific diversity can evolve rapidly, and that this process is jointly facilitated by (i) the availability of diverse environments promoting divergent natural selection; (ii) dynamic developmental processes sensitive to environmental and genetic signals; and (iii) eco evo and eco devo feedbacks influencing the selective and developmental environments of the phenotype. We highlight empirical examples and present a conceptual model for the generation of resource polymorphism – emphasizing eco evo devo, and identify current gaps in knowledge.     

Roles for modularity and constraint in the evolution of cranial diversity among Anolis lizards

Complex organismal structures are organized into modules, suites of traits that develop, function, and vary in a coordinated fashion. By limiting or directing covariation among component traits, modules are expected to represent evolutionary building blocks and to play an important role in morphological diversification. But how stable are patterns of modularity over macroevolutionary timescales? Comparative analyses are needed to address the macroevolutionary effect of modularity, but to date few have been conducted. We describe patterns of skull diversity and modularity in Caribbean Anolis lizards. We first diagnose the primary axes of variation in skull shape and then examine whether diversification of skull shape is concentrated to changes within modules or whether changes arose across the structure as a whole. We find no support for the hypothesis that cranial modules are conserved as species diversify in overall skull shape. Instead we find that anole skull shape and modularity patterns independently converge. In anoles, skull modularity is evolutionarily labile and may reflect the functional demands of unique skull shapes. Our results suggest that constraints have played little role in limiting or directing the diversification of head shape in Anolis lizards.     

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.     

CONVERGENT EVOLUTION OF SEXUAL DIMORPHISM IN SKULL SHAPE USING DISTINCT DEVELOPMENTAL STRATEGIES

Studies integrating evolutionary and developmental analyses of morphological variation are of growing interest to biologists as they promise to shed fresh light on the mechanisms of morphological diversification. Sexually dimorphic traits tend to be incredibly divergent across taxa. Such diversification must arise through evolutionary modifications to sex differences during development. Nevertheless, few studies of dimorphism have attempted to synthesize evolutionary and developmental perspectives. Using geometric morphometric analysis of head shape for 50 Anolis species, we show that two clades have converged on extreme levels of sexual dimorphism through similar, male‐specific changes in facial morphology. In both clades, males have evolved highly elongate faces whereas females retain faces of more moderate proportion. This convergence is accomplished using distinct developmental mechanisms; one clade evolved extreme dimorphism through the exaggeration of a widely shared, potentially ancestral, developmental strategy whereas the other clade evolved a novel developmental strategy not observed elsewhere in the genus. Together, our analyses indicate that both shared and derived features of development contribute to macroevolutionary patterns of morphological diversity among Anolis lizards.     

Chironomid midges: a forgotten model of developmental biology research

For more than a century, embryologists have been exploring various model systems to gain insights into developmental processes. This article presents an overview of the role of chironomid midges in embryology research since their introduction as model organisms in the 19th century. We present the vestiges of bibliography since the days of Weismann (1834–1914), who raised preliminary queries to unravel many unique features of insect embryogenesis using midges as a crucible. Unfortunately, over the years, chironomid midges got lost into obscurity as a model for developmental biology, which is evident from the paucity of developmental biology–related literature on midges in the past decades. Through this essay, the authors intend to share reminiscences of the heydays of chironomid research with the wider community of zoologists with an aim of reviving chironomid embryology. Midges not only possess the basic qualities essential for an ideal model system, but being one of the ancestral dipteran stocks, they can also prove an excellent test system for evo‐devo, transgenetic, and embryogenomic investigations that utilize methodologies at the interface of developmental biology and high‐throughput molecular genetic and genomics approach. An introspection of re‐introducing chironomid midgesas model system will be rewarding for the contemporary developmental biologists.     

Artificial selection sheds light on developmental mechanisms of limb elongation

Species diversity in limb lengths and proportions is thought to have evolved adaptively in the context of locomotor and habitat specialization, but the heritable cellular processes that drove this evolution within species are poorly understood. In this study, we take a novel “micro‐evo‐devo” approach, using artificial selection on relative limb length to amplify phenotypic variation in a population of mice, known as Longshanks, to examine the cellular mechanisms of postnatal limb development that contribute to intraspecific limb length variation. Cross‐sectional growth data indicate that differences in bone length between Longshanks and random‐bred controls are not due to prolonged growth, but to accelerated growth rates. Histomorphometric and cell proliferation assays on proximal tibial growth plates show that Longshanks’ increased limb bone length is associated with an increased number of proliferative chondrocytes. In contrast, we find no differences in other growth plate cellular features known to underlie interspecific differences in limb bone size and shape, such as the rates of chondrocyte proliferation or the size and number of hypertrophic cells in the growth plate. These data suggest that small differences among individuals in the number of proliferating chondrocytes are a potentially important determinant of selectable intraspecific variation in individual limb bone lengths, independent of body size.     

Functional consequences of phenotypic variation between locally adapted populations: Swimming performance and ventilation in extremophile fish

Natural selection drives the evolution of traits to optimize organismal performance, but optimization of one aspect of performance can influence other aspects of performance. Here, we asked how phenotypic variation between locally adapted fish populations affects locomotion and ventilation, testing for functional trade‐offs and trait–performance correlations. Specifically, we investigated two populations of livebearing fish (Poecilia mexicana) that inhabit distinct habitat types (hydrogen‐sulphide‐rich springs and adjacent nonsulphidic streams). For each individual, we quantified different metrics of burst swimming during simulated predator attacks, steady swimming and gill ventilation. Coinciding with predictions, we documented significant population differences in all aspects of performance, with fish from sulphidic habitats exhibiting higher steady swimming performance and higher ventilation capacity, but slower burst swimming. There was a significant functional trade‐off between steady and burst swimming, but not between different aspects of locomotion and ventilation. Although our findings about population differences in locomotion performance largely parallel the results from previous studies, we provide novel insights about how morphological variation might impact ventilation and ultimately oxygen acquisition. Overall, our analyses provided insights into the functional consequences of previously documented phenotypic variation, which will help to disentangle the effects of different sources of selection that may coincide along complex environmental gradients.     

Early Holocene human remains from the Argentinean Pampas: Additional evidence for distinctive cranial morphology of early South Americans

The cranial morphology of Early Holocene American human samples is characterized by a long and narrow cranial vault, whereas more recent samples exhibit a shorter and wider cranial vault. Two hypotheses have been proposed to account for the morphological differences between early and late‐American samples: (a) the migratory hypothesis that suggests that the morphological variation between early and late American samples was the result of a variable number of migratory waves; and (b) the local diversification hypothesis, that is, the morphological differences between early and late American samples were mainly generated by local, random (genetic drift), and nonrandom factors (selection and phenotypic plasticity). We present the first craniometric study of three early skulls from the Argentinean Pampas, dated ～8,000 cal. years BP (Arroyo Seco 2, Chocorí, and La Tigra), and one associated with mega‐faunal remains (Fontezuelas skull). In addition, we studied several Late Holocene samples. We show that the skulls from the Argentinean Pampas are morphologically similar to other Early Holocene American skulls (i.e., Lagoa Santa from Brazil, Tequendama, Checua, and Aguazuque from Colombia, Lauricocha from Peru, and early Mexicans) that exhibit long and narrow cranial vaults. These samples differ from the Late Holocene American samples that exhibit a shorter and wider cranial vault. Our results underscore the important differences in cranial morphology between early and late‐American samples. However, we emphasize the need for further studies to discuss alternative hypotheses regarding such differences. Am J Phys Anthropol 143:298–305, 2010. © 2010 Wiley‐Liss, Inc.     

Woodstoich III: Integrating tools of nutritional geometry and ecological stoichiometry to advance nutrient budgeting and the prediction of consumer‐driven nutrient recycling

Within the last two decades, ecological stoichiometry (ES) and nutritional geometry (NG, also known as geometric framework for nutrition) have delivered novel insights into core questions of nutritional ecology. These two nutritionally explicit frameworks differ in the ‘nutrient currency’ used and the focus of their past research; behavioural feeding strategies in NG, mainly investigating terrestrial organisms, and trophic ecology in ES, mainly in aquatic settings. However, both NG and ES have developed in explaining patterns across various scales of biological organization. Integrating specific tools of these frameworks could advance the field of nutritional ecology by unifying theoretical and empirical approaches from the organismal to ecosystem level processes. Toward this integration, we identified 1) nutrient/element budgets as a shared concept of both frameworks that encompass nutrient intake, retention, and release, 2) response surface plots of NG as powerful tools to illustrate processes at the organismal level and 3) the concept of consumer‐driven nutrient recycling (CNR) of ES as a useful tool bridging organism and ecosystem scales. We applied response surface plots to element budget data from an ES study to show how this approach can deliver new insights at the organismal level, e.g. by showing the interplay between egestion and excretion depending simultaneously on the consumed amount of carbon and phosphorus based on variation across individuals. By integrating concepts of ES and NG to model microbial uptake and mineralization of nitrogenous wastes reported in a NG study, we also demonstrate that considering biochemically explicit mineralization rates of organic wastes can improve predictions of CNR by reducing over‐ or underestimation of mineralization depending on the quality of the consumer's diet. Our presented tools and approaches can help to bridge the organismal and ecosystem level, advancing the predictive power of studies in nutritional ecology at multiple ecological scales.     

Evolution and molecular mechanisms of adaptive developmental plasticity

Aside from its selective role in filtering inter-individual variation during evolution by natural selection, the environment also plays an instructive role in producing variation during development. External environmental cues can influence developmental rates and/or trajectories and lead to the production of distinct phenotypes from the same genotype. This can result in a better match between adult phenotype and selective environment and thus represents a potential solution to problems posed by environmental fluctuation. The phenomenon is called adaptive developmental plasticity. The study of developmental plasticity integrates different disciplines (notably ecology and developmental biology) and analyses at all levels of biological organization, from the molecular regulation of changes in organismal development to variation in phenotypes and fitness in natural populations. Here, we focus on recent advances and examples from morphological traits in animals to provide a broad overview covering (i) the evolution of developmental plasticity, as well as its relevance to adaptive evolution, (ii) the ecological significance of alternative environmentally induced phenotypes, and the way the external environment can affect development to produce them, (iii) the molecular mechanisms underlying developmental plasticity, with emphasis on the contribution of genetic, physiological and epigenetic factors, and (iv) current challenges and trends, including the relevance of the environmental sensitivity of development to studies in ecological developmental biology, biomedicine and conservation biology.     

Development of a bicistronic expression system in the branchiopod crustacean Daphnia magna

The viral 2A peptides have recently been used for bicistronic expression in various organisms. In this system, a single mRNA that codes for two proteins flanking the 2A peptide can be translated simultaneously into each protein by ribosomal skipping at this peptide sequence. Here, we tested the function of the Thosea asigna insect virus 2A (T2A) peptide in the branchiopod crustacean Daphnia magna—an emerging model of evolutionary developmental biology. First, we used transgenic Daphnia that expresses a potential bicistronic RNA containing mCherry and histone H2B‐ green fluorescent protein (GFP) open reading frames upstream and downstream of the T2A sequence, respectively. Microscopic observation revealed difference of localization of the two proteins in the cell, homogenous distribution of mCherry and nuclear localization of H2B‐GFP. Second, we changed localization of mCherry from cytoplasm to plasma membrane by attachment of a consensus myristoylation motif in the bicistronic reporter. RNA that codes for this new bicistronic reporter was injected into eggs. At gastrulation stage, we found spectrally distinct fluorescence with enough intensity and resolution to detect membrane localized mCherry and nuclear GFP. These results indicate that the T2A peptide functions in D. magna and T2A‐mediated bicistronic expression would be a promising tool for evo‐devo studies of this species.     

What can and can't we say about indirect land‐use change in Brazil using an integrated economic – land‐use change model?

It is commonly recognized that large uncertainties exist in modelled biofuel‐induced indirect land‐use change, but until now, spatially explicit quantification of such uncertainties by means of error propagation modelling has never been performed. In this study, we demonstrate a general methodology to stochastically calculate direct and indirect land‐use change (dLUC and iLUC) caused by an increasing demand for biofuels, with an integrated economic – land‐use change model. We use the global Computable General Equilibrium model MAGNET, connected to the spatially explicit land‐use change model PLUC. We quantify important uncertainties in the modelling chain. Next, dLUC and iLUC projections for Brazil up to 2030 at different spatial scales and the uncertainty herein are assessed. Our results show that cell‐based (5 × 5 km²) probabilities of dLUC range from 0 to 0.77, and of iLUC from 0 to 0.43, indicating that it is difficult to project exactly where dLUC and iLUC will occur, with more difficulties for iLUC than for dLUC. At country level, dLUC area can be projected with high certainty, having a coefficient of variation (cv) of only 0.02, while iLUC area is still uncertain, having a cv of 0.72. The latter means that, considering the 95% confidence interval, the iLUC area in Brazil might be 2.4 times as high or as low as the projected mean. Because this confidence interval is so wide that it is likely to straddle any legislation threshold, our opinion is that threshold evaluation for iLUC indicators should not be implemented in legislation. For future studies, we emphasize the need for provision of quantitative uncertainty estimates together with the calculated LUC indicators, to allow users to evaluate the reliability of these indicators and the effects of their uncertainty on the impacts of land‐use change, such as greenhouse gas emissions.     

Phylogeographic and phenotypic outcomes of brown anole colonization across the Caribbean provide insight into the beginning stages of an adaptive radiation

Some of the most important insights into the ecological and evolutionary processes of diversification and speciation have come from studies of island adaptive radiations, yet relatively little research has examined how these radiations initiate. We suggest that Anolis sagrei is a candidate for understanding the origins of the Caribbean Anolis adaptive radiation and how a colonizing anole species begins to undergo allopatric diversification, phenotypic divergence and, potentially, speciation. We undertook a genomic and morphological analysis of representative populations across the entire native range of A. sagrei, finding that the species originated in the early Pliocene, with the deepest divergence occurring between western and eastern Cuba. Lineages from these two regions subsequently colonized the northern Caribbean. We find that at the broadest scale, populations colonizing areas with fewer closely related competitors tend to evolve larger body size and more lamellae on their toepads. This trend follows expectations for post‐colonization divergence from progenitors and convergence in allopatry, whereby populations freed from competition with close relatives evolve towards common morphological and ecological optima. Taken together, our results show a complex history of ancient and recent Cuban diaspora with populations on competitor‐poor islands evolving away from their ancestral Cuban populations regardless of their phylogenetic relationships, thus providing insight into the original diversification of colonist anoles at the beginning of the radiation. Our research also supplies an evolutionary framework for the many studies of this increasingly important species in ecological and evolutionary research.     

Evolution of insect wings and development – new details from Palaeozoic nymphs

The nymphal stages of Palaeozoic insects differ significantly in morphology from those of their modern counterparts. Morphological details for some previously reported species have recently been called into question. Palaeozoic insect nymphs are important, however – their study could provide key insights into the evolution of wings, and complete metamorphosis. Here we review past work on these topics and juvenile insects in the fossil record, and then present both novel and previously described nymphs, documented using new imaging methods. Our results demonstrate that some Carboniferous nymphs – those of Palaeodictyopteroidea – possessed movable wing pads and appear to have been able to perform simple flapping flight. It remains unclear whether this feature is ancestral for Pterygota or an autapomorphy of Palaeodictyopteroidea. Further characters of nymphal development which were probably in the ground pattern of Pterygota can be reconstructed. Wing development was very gradual (archimetaboly). Wing pads did not protrude from the tergum postero‐laterally as in most modern nymphs, but laterally, and had well‐developed venation. The modern orientation of wing pads and the delay of wing development into later developmental stages (condensation) appears to have evolved several times independently within Pterygota: in Ephemeroptera, Odonatoptera, Eumetabola, and probably several times within Polyneoptera. Selective pressure appears to have favoured a more pronounced metamorphosis between the last nymphal and adult stage, ultimately reducing exploitation competition between the two. We caution, however, that the results presented herein remain preliminary, and the reconstructed evolutionary scenario contains gaps and uncertainties. Additional comparative data need to be collected. The present study is thus seen as a starting point for this enterprise.     

Anatomical diversification of a skeletal novelty in bat feet

Neomorphic, membrane‐associated skeletal rods are found in disparate vertebrate lineages, but their evolution is poorly understood. Here we show that one of these elements—the calcar of bats (Chiroptera)—is a skeletal novelty that has anatomically diversified. Comparisons of evolutionary models of calcar length and corresponding disparity‐through‐time analyses indicate that the calcar diversified early in the evolutionary history of Chiroptera, as bats phylogenetically diversified after evolving the capacity for flight. This interspecific variation in calcar length and its relative proportion to tibia and forearm length is of functional relevance to flight‐related behaviors. We also find that the calcar varies in its tissue composition among bats, which might affect its response to mechanical loading. We confirm the presence of a synovial joint at the articulation between the calcar and the calcaneus in some species, which suggests the calcar has a kinematic functional role. Collectively, this functionally relevant variation suggests that adaptive advantages provided by the calcar led to its anatomical diversification. Our results demonstrate that novel skeletal additions can become integrated into vertebrate body plans and subsequently evolve into a variety of forms, potentially impacting clade diversification by expanding the available morphological space into which organisms can evolve.     

Deconstructing morphology

Scholtz, G. 2010. Deconstructing morphology. —Acta Zoologica (Stockholm) 91 : 44–63 Morphology as the science of form is, in particular, related to the overwhelming diversity of animal forms. Due to its long pre‐Darwinian tradition, organismic morphology is partly burdened by ahistorical typological views. On the other hand, the study of organismic form has always implied concepts of transformation, which helped to pave the way for evolutionary theories. This contradictory history and the fact that we need words to describe organismic form lead in many cases to morphological concepts implying a mixture of structural, functional, developmental, ecological, typological, and evolutionary aspects in current morphological approaches. Because these mixed views lead to contradictory and misleading interpretations of animal form, I stress the need to deconstruct morphological concepts at all levels. I propose a morphology that analyses transformation of animal forms strictly at the structural level in combination with genealogical thinking. Function and other biological aspects of form should be considered in an independent second analytical step. A comparative pattern approach, including developmental patterns, of animal structure in an evolutionary framework allows for the analysis of morphological change, in particular, phylogenetic reconstructions, homology assessment, and the recognition of evolutionary independent morphological units.     

The landscape of human mutually exclusive splicing

Mutually exclusive splicing of exons is a mechanism of functional gene and protein diversification with pivotal roles in organismal development and diseases such as Timothy syndrome, cardiomyopathy and cancer in humans. In order to obtain a first genomewide estimate of the extent and biological role of mutually exclusive splicing in humans, we predicted and subsequently validated mutually exclusive exons (MXEs) using 515 publically available RNA‐Seq datasets. Here, we provide evidence for the expression of over 855 MXEs, 42% of which represent novel exons, increasing the annotated human mutually exclusive exome more than fivefold. The data provide strong evidence for the existence of large and multi‐cluster MXEs in higher vertebrates and offer new insights into MXE evolution. More than 82% of the MXE clusters are conserved in mammals, and five clusters have homologous clusters in Drosophila. Finally, MXEs are significantly enriched in pathogenic mutations and their spatio‐temporal expression might predict human disease pathology.     

Sun skink landscape genomics: assessing the roles of micro‐evolutionary processes in shaping genetic and phenotypic diversity across a heterogeneous and fragmented landscape

Incorporating genomic data sets into landscape genetic analyses allows for powerful insights into population genetics, explicitly geographical correlates of selection, and morphological diversification of organisms across the geographical template. Here, we utilize an integrative approach to examine gene flow and detect selection, and we relate these processes to genetic and phenotypic population differentiation across South‐East Asia in the common sun skink, Eutropis multifasciata. We quantify the relative effects of geographic and ecological isolation in this system and find elevated genetic differentiation between populations from island archipelagos compared to those on the adjacent South‐East Asian continent, which is consistent with expectations concerning landscape fragmentation in island archipelagos. We also identify a pattern of isolation by distance, but find no substantial effect of ecological/environmental variables on genetic differentiation. To assess whether morphological conservatism in skinks may result from stabilizing selection on morphological traits, we perform F_ST–P_ST comparisons, but observe that results are highly dependent on the method of comparison. Taken together, this work provides novel insights into the manner by which micro‐evolutionary processes may impact macro‐evolutionary scale biodiversity patterns across diverse landscapes, and provide genomewide confirmation of classic predictions from biogeographical and landscape ecological theory.