Journal Articles and Book Chapters: Present - 2010

2015
Meegaskumbura, M., et al., 2015. Patterns of reproductive-mode evolution in Old World tree frogs (Anura, Rhacophoridae). Zoologica Scripta , doi:10.1111/zsc.12121. PDF
McPhillips, T., et al., 2015. YesWorkflow: A User-Oriented, Language-Independent Tool for Recovering Workflow Information from Scripts. International Journal for Digital Curation , 10 , pp. 298-313. PDF
Sefton, E.M., Piekarski, N. & Hanken, J., 2015. Dual embryonic origin and patterning of the pharyngeal skeleton in the axolotl (Ambystoma mexicanum). Evolution & Development , 17 , pp. 175-184. PDF
Jennings, D.H., Evans, B. & Hanken, J., 2015. Development of neuroendocrine components of the thyroid axis in the direct-devoloping frog Eleutherodactylus coqui: formation of the median eminence and the onset of pituitary TSH production. Gen. Comp. Endocrinol. , 214 , pp. 62-67. PDF
Hanken, J., 2015. Is heterochrony still an effective paradigm for contemporary studies of evo-devo?. In A. C. Love, ed. Conceptual Change in Biology: Scientific and Philosophical Perspectives on Evolution and Development. Boston Studies in the Philosophy and History of Science. Berlin. Berlin: Springer-Verlag, pp. 97-110. PDF
2014
Song, T., et al., 2014. Toward automated design, analysis, and optimization of declarative curation workflows. Internat. J. Dig. Curat. , 9 , pp. 111-122. PDF
Piekarski, N., Gross, J.B. & Hanken, J., 2014. Evolutionary innovation and conservation in the embryonic derivation of the vertebrate skull. Nature Communications , 5 , pp. 5661.Abstract

Development of the vertebrate skull has been studied intensively for more than 150 years, yet many essential features remain unresolved. One such feature is the extent to which embryonic derivation of individual bones is evolutionarily conserved or labile. We perform long-term fate mapping using GFP-transgenic axolotl and Xenopus laevis to document the contribution of individual cranial neural crest streams to the osteocranium in these amphibians. Here we show that the axolotl pattern is strikingly similar to that in amniotes; it likely represents the ancestral condition for tetrapods. Unexpectedly, the pattern in Xenopus is much different; it may constitute a unique condition that evolved after anurans diverged from other amphibians. Such changes reveal an unappreciated relation between life history evolution and cranial development and exemplify 'developmental system drift', in which interspecific divergence in developmental processes that underlie homologous characters occurs with little or no concomitant change in the adult phenotype.

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Cook, J.A., et al., 2014. Natural History Collections as Emerging Resources for InnovativeEducation. Bioscience , 64 , pp. 725-734.Abstract

There is an emerging consensus that undergraduate biology education in the United States is at a crucial juncture, especially as we acknowledge the need to train a new generation of scientists to meet looming environmental and health crises. Digital resources for biology now available online provide an opportunity to transform biology curricula to include more authentic and inquiry-driven educational experiences. Digitized natural history collections have become tremendous assets for research in environmental and health sciences, but, to date, these data remain largely untapped by educators. Natural history collections have the potential to help transform undergraduate science education from passive learning into an active exploration of the natural world, including the exploration of the complex relationships among environmental conditions, biodiversity, and human well-being. By incorporating natural history specimens and their associated data into undergraduate curricula, educators can promote participatory learning and foster an understanding of essential interactions between organisms and their environments.

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2013
Rovito, S.M., et al., 2013. Adaptive radiation in miniature: the minute salamanders of the Mexican highlands (Amphibia: Plethodontidae: Thorius). Biological Journal of the Linnean Society , 109 , pp. 622-643.Abstract

The small size and apparent external morphological similarity of the minute salamanders of the genus Thorius have long hindered evolutionary studies of the group. We estimate gene and species trees within the genus using mitochondrial and nuclear DNA from nearly all named and many candidate species and find three main clades. We use this phylogenetic hypothesis to examine patterns of morphological evolution and species coexistence across central and southern Mexico and to test alternative hypotheses of lineage divergence with and without ecomorphological divergence. Sympatric species differ in body size more than expected after accounting for phylogenetic relationship, and morphological traits show no significant phylogenetic signal. Sympatric species tend to differ in a combination of body size, presence or absence of maxillary teeth, and relative limb or tail length, even when they are close relatives. Sister species of Thorius tend to occupy climatically similar environments, which suggests that divergence across climatic gradients does not drive species formation in the genus. Rather than being an example of cryptic species formation, Thorius more closely resembles an adaptive radiation, with ecomorphological divergence that is bounded by organism-level constraints.(c) 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 622-643.

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Bloom, S., et al., 2013. Developmental origins of a novel gut morphology in frogs. Evolution & Development , 15 , pp. 213-223.Abstract

Phenotypic variation is a prerequisite for evolution by natural selection, yet the processes that give rise to the novel morphologies upon which selection acts are poorly understood. We employed a chemical genetic screen to identify developmental changes capable of generating ecologically relevant morphological variation as observed among extant species. Specifically, we assayed for exogenously applied small molecules capable of transforming the ancestral larval foregut of the herbivorous Xenopus laevis to resemble the derived larval foregut of the carnivorous Lepidobatrachus laevis. Appropriately, the small molecules that demonstrate this capacity modulate conserved morphogenetic pathways involved in gut development, including downregulation of retinoic acid (RA) signaling. Identical manipulation of RA signaling in a species that is more closely related to Lepidobatrachus, Ceratophrys cranwelli, yielded even more similar transformations, corroborating the relevance of RA signaling variation in interspecific morphological change. Finally, we were able to recover the ancestral gut phenotype in Lepidobatrachus by performing a reverse chemical manipulation to upregulate RA signaling, providing strong evidence that modifications to this specific pathway promoted the emergence of a lineage-specific phenotypic novelty. Interestingly, our screen also revealed pathways that have not yet been implicated in early gut morphogenesis, such as thyroid hormone signaling. In general, the chemical genetic screen may be a valuable tool for identifying developmental mechanisms that underlie ecologically and evolutionarily relevant phenotypic variation.

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Ziermann, J.M., et al., 2013. Morphology of the cranial skeleton and musculature in the obligate carnivorous tadpole of Lepidobatrachus laevis (Anura: Ceratophryidae). Acta Zoologica , 94 , pp. 101-112.Abstract

Ziermann, J.M., Infante, C., Hanken, J. and Olsson, L. 2011. Morphology of the cranial skeleton and musculature in the obligate carnivorous tadpole of Lepidobatrachus laevis (Anura: Ceratophryidae). Acta Zoologica (Stockholm) 00:112. Lepidobatrachus laevis (Ceratophryidae: Ceratophryinae) is a bizarre frog endemic to the Chacoan desert of central South America. Its tadpole is an obligate carnivore that can catch and consume live prey nearly its own size. Morphological adaptations associated with this unique feeding mode, including the larval skull anatomy and associated cranial musculature, have only been partly described. We studied the head of Stages 2627 larvae using gross dissection, immunohistochemistry, and standard histology. Derived features of this tadpole compared to the microphagous, herbivorous larvae of most other anurans include simplified chondrocranial cartilages and very robust jaw muscles. The mm. suspensorio- et quadratoangularis do not take their origin from the processus muscularis of the palatoquadrate, as in most other tadpoles, but instead originate from the corpus of the palatoquadrate caudal to this process. The jaw levators are unusually large. The tadpole of Ceratophrys, another member of the ceratophryine clade, also consumes large animal prey, but its morphology is very different. It probably has evolved independently from a generalized, mainly herbivorous tadpole similar to the larva of Chacophrys, the third ceratophryine genus. Most specialized features of the larval head of Lepidobatrachus laevis are adaptations for megalophagyingestion of whole, very large animal prey.

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Whited, J.L., et al., 2013. Pseudotyped retroviruses for infecting axolotl in vivo and in vitro. Development , 140 , pp. 1137-1146.Abstract

Axolotls are poised to become the premiere model system for studying vertebrate appendage regeneration. However, very few molecular tools exist for studying crucial cell lineage relationships over regeneration or for robust and sustained misexpression of genetic elements to test their function. Furthermore, targeting specific cell types will be necessary to understand how regeneration of the diverse tissues within the limb is accomplished. We report that pseudotyped, replication-incompetent retroviruses can be used in axolotls to permanently express markers or genetic elements for functional study. These viruses, when modified by changing their coat protein, can infect axolotl cells only when they have been experimentally manipulated to express the receptor for that coat protein, thus allowing for the possibility of targeting specific cell types. Using viral vectors, we have found that progenitor populations for many different cell types within the blastema are present at all stages of limb regeneration, although their relative proportions change with time.

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Morris, R.A., et al., 2013. Semantic Annotation of Mutable Data. Plos One , 8.Abstract

Electronic annotation of scientific data is very similar to annotation of documents. Both types of annotation amplify the original object, add related knowledge to it, and dispute or support assertions in it. In each case, annotation is a framework for discourse about the original object, and, in each case, an annotation needs to clearly identify its scope and its own terminology. However, electronic annotation of data differs from annotation of documents: the content of the annotations, including expectations and supporting evidence, is more often shared among members of networks. Any consequent actions taken by the holders of the annotated data could be shared as well. But even those current annotation systems that admit data as their subject often make it difficult or impossible to annotate at fine-enough granularity to use the results in this way for data quality control. We address these kinds of issues by offering simple extensions to an existing annotation ontology and describe how the results support an interest-based distribution of annotations. We are using the result to design and deploy a platform that supports annotation services overlaid on networks of distributed data, with particular application to data quality control. Our initial instance supports a set of natural science collection metadata services. An important application is the support for data quality control and provision of missing data. A previous proof of concept demonstrated such use based on data annotations modeled with XML-Schema.

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Wu, Y.K., et al., 2013. Significance of pre-Quaternary climate change for montane species diversity: Insights from Asian salamanders (Salamandridae: Pachytriton). Molecular Phylogenetics and Evolution , 66 , pp. 380-390.Abstract

Despite extensive focus on the genetic legacy of Pleistocene glaciation, impacts of earlier climatic change on biodiversity are poorly understood. Because amphibians are highly sensitive to variations in precipitation and temperature, we use a genus of Chinese montane salamanders (Salamandridae: Pachytriton) to study paleoclimatic change in East Asia, which experienced intensification of its monsoon circulation in the late Miocene associated with subsequent Pliocene warming. Using both nuclear and mitochondrial DNA sequences, we reconstruct the species tree under a coalescent model and demonstrate that all major lineages originated before the Quaternary. Initial speciation within the genus occurred after the summer monsoon entered a stage of substantial intensification. Heavy summer precipitation established temporary water connectivity through overflows between adjacent stream systems, which may facilitate geographic range expansion by aquatic species such as Pachytriton. Species were formed in allopatry likely through vicariant isolation during or after range expansion. To evaluate the influence of Pliocene warming on these cold-adapted salamanders, we construct a novel temperature buffer-zone model, which suggests widespread physiological stress or even extinction during the warming period. A significant deceleration of species accumulation rate is consistent with Pliocene range contraction, which affected P. granulosus and P. archospotus the most because they lack large temperature buffer zones. In contrast, demographic growth occurred in species for which refugia persist. The buffer-zone model reveals the Huangshan Mountain as a potential climatic refugium, which is similar to that found for other East Asian organisms. Our approach can incorporate future climatic data to evaluate the potential impact of ongoing global warming on montane species (particularly amphibians) and to predict possible population declines. (C) 2012 Elsevier Inc. All rights reserved.

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2012
Wu, Y.K., Wang, Y.Z. & Hanken, J., 2012. Comparative Osteology of the Genus Pachytriton (Caudata: Salamandridae) from Southeastern China. Asian Herpetological Research , 3 , pp. 83-102.Abstract

Osteological evidence provides invaluable insights into patterns of amphibian biodiversity. In small montane streams of southeastern China, an endemic genus of salamanders (Pachytriton) displays remarkable aquatic specializations, many of which are reflected in skeletal morphology, but these specializations remain to be studied in an integrated perspective. Attempts to fully resolve the taxonomy within the genus also can benefit from knowledge of internal morphology. We present a detailed description of the adult skeleton of P. brevipes, P. inexpectatus and P. archospotus by analyzing both cleared-and-stained and radiographed specimens in a comparative framework. Compared to terrestrial and amphibious salamanders, the most distinctive osteological features of Pachytriton include a modified hyobranchial apparatus, a reduced frontosquamosal arch, and deep neural and haemal arches of the caudal vertebrae. The hyobranchial apparatus of P. archospotus is distinctly different from that of congeners and likely secondarily derived. Patterns of interspecific variation suggest that northeastern P. inexpectatus is more closely related to P. brevipes than it is to southwestern P. inexpectatus, thereby reinforcing results from earlier molecular phylogenetic analyses. We advocate assigning northeastern P. inexpectatus to P. brevipes.

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Dou, L., et al., 2012. Kurator: A Kepler Package for Data Curation Workflows. Proceedings of the International Conference on Computational Science, Iccs 2012 , 9 , pp. 1614-1619.Abstract

Data curation is critical for scientific data digitization, sharing, integration, and use. This paper presents Kurator, a software package for automating data curation pipelines in the Kepler scientific workflow system. Several curation tools and services are integrated into this package as actors to enable construction of workflows to perform and document various data curation tasks. The integration of Google cloud services (e. g., Google spreadsheets), allows workflow steps to invoke human experts outside the workflow in a manner that greatly simplifies the complex data handling in distributed, multi-user curation workflows. The Kepler platform provides the modeling, execution and management ability, including a collection-oriented model of computation (COMAD), and provenance tracking and browsing for the curation package. These features not only allow workflows to be easily modeled, maintained, and evolved, but also QA/QC of curation results is facilitated through examination of provenance information recorded during workflow execution. Effectiveness of the Kurator package is demonstrated through a workflow for data curation of natural science collections.

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Wheeler, Q.D., et al., 2012. Mapping the biosphere: exploring species to understand the origin, organization and sustainability of biodiversity. Systematics and Biodiversity , 10 , pp. 1-20.Abstract

The time is ripe for a comprehensive mission to explore and document Earth's species. This calls for a campaign to educate and inspire the next generation of professional and citizen species explorers, investments in cyber-infrastructure and collections to meet the unique needs of the producers and consumers of taxonomic information, and the formation and coordination of a multi-institutional, international, transdisciplinary community of researchers, scholars and engineers with the shared objective of creating a comprehensive inventory of species and detailed map of the biosphere. We conclude that an ambitious goal to describe 10 million species in less than 50 years is attainable based on the strength of 250 years of progress, worldwide collections, existing experts, technological innovation and collaborative teamwork. Existing digitization projects are overcoming obstacles of the past, facilitating collaboration and mobilizing literature, data, images and specimens through cyber technologies. Charting the biosphere is enormously complex, yet necessary expertise can be found through partnerships with engineers, information scientists, sociologists, ecologists, climate scientists, conservation biologists, industrial project managers and taxon specialists, from agrostologists to zoophytologists. Benefits to society of the proposed mission would be profound, immediate and enduring, from detection of early responses of flora and fauna to climate change to opening access to evolutionary designs for solutions to countless practical problems. The impacts on the biodiversity, environmental and evolutionary sciences would be transformative, from ecosystem models calibrated in detail to comprehensive understanding of the origin and evolution of life over its 3.8 billion year history. The resultant cyber-enabled taxonomy, or cybertaxonomy, would open access to biodiversity data to developing nations, assure access to reliable data about species, and change how scientists and citizens alike access, use and think about biological diversity information.

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Wu, Y.K., Wang, Y.Z. & Hanken, J., 2012. New species of Pachytriton (Caudata: Salamandridae) from the Nanling Mountain Range, southeastern China. Zootaxa , pp. 1-16.Abstract

New species of amphibians are being reported at an astonishingly fast rate. These include some that have been known to the commercial pet trade for years but have not been formally described due to uncertain origin. The distinctive phenotype of "Pachytriton B" among the Chinese stout newts (also known as paddle-tailed newts) is one such example. Through examination of museum specimens, we locate a population from Mt. Mang within the Nanling Mountain Range with morphology and coloration similar to Pachytriton B. Molecular phylogenetic analyses strongly suggest that this population and Pachytriton B belong to the same species, which differs from congeners morphologically and chromatically and is described here as a new species. This species is characterized by a large and stout body, uniformly light brown dorsum, and orange spots or blotches that extend ribbon-like along the dorsolateral sides of the body. A mitochondrial genealogy suggests that the new species is the sister taxon to the group (P. brevipes + P. feii). Morphologically, this species is significantly stouter than P. feii and has significantly longer limbs than P. brevipes.

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Wake, D.B., et al., 2012. Taxonomic status of the enigmatic salamander Cryptotriton adelos (Amphibia: Plethodontidae) from northern Oaxaca, Mexico, with observations on its skull and postcranial skeleton. Zootaxa , pp. 67-70. PDF
Zimkus, B.M., et al., 2012. Terrestrialization, Miniaturization and Rates of Diversification in sub-Saharan Frogs (Anura: Phrynobatrachidae). Plos One , 7 , pp. 1-11 e35118.Abstract

Terrestrialization, the evolution of non-aquatic oviposition, and miniaturization, the evolution of tiny adult body size, are recurring trends in amphibian evolution, but the relationships among the traits that characterize these phenomena are not well understood. Furthermore, these traits have been identified as possible "key innovations'' that are predicted to increase rates of speciation in those lineages in which they evolve. We examine terrestrialization and miniaturization in sub-Saharan puddle frogs (Phrynobatrachidae) in a phylogenetic context to investigate the relationship between adaptation and diversification through time. We use relative dating techniques to ascertain if character trait shifts are associated with increased diversification rates, and we evaluate the likelihood that a single temporal event can explain the evolution of those traits. Results indicate alternate reproductive modes evolved independently in Phrynobatrachus at least seven times, including terrestrial deposition of eggs and terrestrial, non-feeding larvae. These shifts towards alternate reproductive modes are not linked to a common temporal event. Contrary to the "key innovations'' hypothesis, clades that exhibit alternate reproductive modes have lower diversification rates than those that deposit eggs aquatically. Adult habitat, pedal webbing and body size have no effect on diversification rates. Though these traits putatively identified as key innovations for Phrynobatrachus do not seem to be associated with increased speciation rates, they may still provide opportunities to extend into new niches, thus increasing overall diversity.

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