Hanken, J., Jennings, D.H. & Olsson, L., 1997. Mechanistic basis of life-history evolution in anuran amphibians: Direct development. American Zoologist , 37 , pp. 160-171.Abstract

The primitive, or ancestral reproductive mode for Recent amphibians involves a complex, biphasic life history, Yet evolutionarily derived, alternate modes are seen in all three living orders and predominate in some clades, Analysis of the consequences and mechanistic bases of one such mode-direct development-can provide insights into the evolutionary opportunities and constraints conferred by the ancestral metamorphic ontogeny, Direct development in the anuran genus Eleutherodactylus involves fundamental alterations to many features of embryonic and posthatching development, At hatching, young emerge as fully formed, albeit tiny versions of the adult; most larval features are absent, Pervasive changes in ontogenetic timing, in particular the precocious (embryonic) formation of many adult structures, appear to be correlated with early development of the thyroid axis, although responsiveness to exogenous thyroid hormone is diminished or even lacking in at least some peripheral tissues, Changes in cranial patterning are likely mediated by the embryonic neural crest, although many gross features of crest biology are highly conserved, Laboratory-based analyses of direct development and other derived reproductive modes in amphibians, using contemporary methods developed for more standard, ''model'' organisms, may contribute important insights into life-history evolution that complement those derived from analyses of morphology, ecology and phylogeny.

Richardson, M.K., et al., 1997. There is no highly conserved embryonic stage in the vertebrates: Implications for current theories of evolution and development. Anatomy and Embryology , 196 , pp. 91-106.Abstract

Embryos of different species of vertebrate share a common organisation and often look similar. Adult differences among species become more apparent through divergence at later stages. Some authors have suggested that members of most or all vertebrate clades pass through a virtually identical, conserved stage. This idea was promoted by Haeckel, and has recently been revived in the context of claims regarding the universality of developmental mechanisms. Thus embryonic resemblance at the tailbud stage has been linked with a conserved pattern of developmental gene expression - the zootype. Haeckel's drawings of the external morphology of various vertebrates remain the most comprehensive comparative data purporting to show a conserved stage. However, their accuracy has been questioned and only a narrow range of species was illustrated. In view of the current widespread interest in evolutionary developmental tal biology, and especially in the conservation of developmental mechanisms, re-examination of the extent of variation in vertebrate embryos is long overdue, We present here the first review of the external morphology of tailbud embryos, illustrated with original specimens from a wide range of vertebrate groups, We find that embryos at the tailbud stage - thought to correspond to a conserved stage - show variations in form due to allometry, heterochrony, and differences in body plan and somite number. These variations foreshadow important differences in adult body form. Contrary to recent claims that all vertebrate embryos pass through a stage when they are the same size, we find a greater than 10-fold variation in greatest length at the tailbud stage. Our survey seriously undermines the credibility of Haeckel's drawings, which depict not a conserved stage for vertebrates, but a stylised amniote embryo. In fact, the taxonomic level of greatest resemblance among vertebrate embryos is below the subphylum. The wide variation in morphology among vertebrate embryos is difficult to reconcile with the idea of a phyogenetically-conserved tailbud stage, and suggests that at least some developmental mechanisms are not highly constrained by the zootype, Our study also highlights the dangers of drawing general conclusions about vertebrate development from studies of gene expression in a small number of laboratory species.

Hanken, J. & Carl, T.F., 1996. The shape of evolutionary developmental biology [review of R.A. Taff, The Shape of Life: Genes, Development, and the Evolution of the Animal Form]. Trends Ecol. Evol. , 11 , pp. 441-442. PDF
Hanken, J., 1996. The art of the skull. Natural History , 105 , pp. 34-39. PDF
Olsson, L. & Hanken, J., 1996. Cranial neural crest migration and chondrogenic fate in the oriental fire-bellied toad Bombina orientalis: Defining the ancestral pattern of head development in anuran amphibians. Journal of Morphology , 229 , pp. 105-120.Abstract

We assess cranial neural-crest cell migration and contributions to the larval chondrocranium in the phylogenetically basal and morphologically generalized anuran Bombina orientalis (Bombinatoridae). Methods used include microdissection, scanning electron microscopy, and vital dye labeling, in conjunction with confocal and fluorescence microscopy. Cranial neural-crest cells begin migrating before neural-fold closure and soon form three primary streams. These streams contribute to all cranial cartilages except two medial components of the hyobranchial skeleton (basihyal and basibranchial cartilages), the posterior portion of the trabecular plate, and the otic capsule, the embryonic origin of which is unknown. Chondrogenic fate is regionalized within the cranial neural folds, with the anterior regions contributing to anterior cartilages and the posterior regions to posterior cartilages. A neural-crest contribution also was consistently observed in several cranial nerves and the connective tissue component of many cranial muscles. Notwithstanding minor differences among species in the initial configuration of migratory streams, cranial neural-crest migration and chondrogenic potential in metamorphosing anurans seem to be highly stereotyped and evolutionarily conservative. This includes a primary role for the neural crest in the evolutionary origin of the paired suprarostral and infrarostral cartilages, two prominent caenogenetic features of the rostral skull unique to anuran larvae. Our results provide a model of the ancestral pattern of embryonic head development in anuran amphibians. This model can serve as a basis for examining the ontogenetic mechanisms that underlie the diversity of cranial morphology and development displayed by living frogs, as well as the evolutionary consequences of this diversity. (C) 1996 Wiley-Liss, Inc.

Wake, D.B. & Hanken, J., 1996. Direct development in the lungless salamanders: What are the consequences for developmental biology, evolution and phylogenesis?. International Journal of Developmental Biology , 40 , pp. 859-869.Abstract

Direct development is a widespread alternate reproductive mode in living amphibians that is characterized by evolutionary loss of the free-living, aquatic larval stage. Courtship, mating, and oviposition occur on land, and the terrestrial egg hatches as a fully formed, miniature adult. While it is the most common reproductive mode in urodeles, development outside the reproductive tract of the female that proceeds directly to a terrestrial hatchling occurs in only a single lineage, the lungless salamanders of the family Plethodontidae. Evolution of direct development in plethodontids has contributed importantly to the extraordinary evolutionary success of this speciose, geographically widespread, and morphologically and ecologically diverse taxon. Developmental consequences and correlates include increased egg size and embryonic development time, loss of larval structures and ontogenetic repatterning, and altered pattern formation in organogenesis. Evolutionary and phylogenetic consequences and correlates include the loss of larval constraints and origin of morphological novelty, and frequent homoplasy. Analysis of direct development in an evolutionary context illustrates the complex interplay between processes of phylogenetic divergence and developmental biology, and substantiates the prominent role of developmental processes in both constraining phenotypic variation and promoting phenotypic diversity. Despite the proven suitability of direct-developing plethodontid salamanders for laboratory and field study, knowledge of basic features of their developmental biology remains far below that available for many other urodeles. Examination of such features of these ''non-model'' organisms is an appropriate and deserving goal of future research.

Packard, M.J., Jennings, D.H. & Hanken, J., 1996. Growth and uptake of mineral by embryos of the direct-developing frog Eleutherodactylus coqui. Comp. Physiol. Biochem. , 113A , pp. 343-349.Abstract

Embryos of the direct-developing frog Elutherodactylus coqui cake up small quantities of yolk and yolk mineral early in incubation but increase their uptake of yolk reserves at later stages of development. Growth and accumulation of calcium and magnesium by embryos also occur slowly at first and at a higher rate later. Accumulation of calcium and magnesium by embryos is largely a function of variation in size of embryos, but uptake of phosphorus is unrelated to size. Although patterns of growth and uptake of mineral by embryonic coquis resemble those for embryos of oviparous amniotes, embryonic coquis do not deplete the yolk of its nutrients to the same degree. Thus, residual yolk of coqui hatchlings contains a high percentage of the nutrient reserves originally present in the egg. This difference between embryonic coquis and embryos of oviparous amniotes may indicate that transfer of nutrients from yolk to embryo becomes limiting during the growth phase. Alternatively, some aspects of the neurologic system are so poorly developed at hatching that coqui may not be able to find prey effectively. A large nutrient reserve could sustain hatchlings while the neurologic system continues to mature.

Hanken, J., 1995. Development and evolution in amphibians. In M. Slatkin, ed. Exploring Evolutionary Biology: Readings from American Scientist. Sunderland. Sunderland: Sinauer Assoc., Inc. pp. 224-231.
Moury, J.D. & Hanken, J., 1995. Early cranial neural crest migration in the direct-developing frog, Eleutherodactylus coqui. Acta Anatomica , 153 , pp. 243-253.Abstract

Direct development is a common reproductive mode in Living amphibians characterized by absence of the free-living, aquatic larval stage. In Eleutherodactylus, a species-rich genus of New World frogs, evolution of direct development from the ancestral biphasic ontogeny is correlated with a comprehensive modification in embryonic cranial patterning, including the loss of many larval-specific components and the precocious formation of many adult (postmetamorphic) structures, We use scanning electron microscopy (SEM) to examine the emergence and early migration of cranial neural crest cells in Eleutherodactylus coqui to begin to assess the possible role of the neural crest in mediating these evolutionary changes. As in metamorphosing frogs, cranial crest cells emerge prior to neural fold closure and assemble into three streams: rostral, rostral otic, and caudal otic. These streams contribute to the face and first visceral (mandibular) arch, to the second (hyoid) arch, and to posterior (branchial) arches, respectively. Rostrocaudal position, morphology, and/or migration patterns distinguish subpopulations of cells within the rostral stream and caudal otic stream. With the possible exception of the small size of the rostral otic and caudal otic streams, evolution of direct development in E. coqui has not altered basic patterns of neural crest emergence or early migration as assessed by SEM. Lf observed evolutionary changes in embryonic cranial patterning are mediated by the neural crest, then they likely involve later aspects of crest migration or more subtle features related to pattern formation such as cell behavior and commitment, or gene expression.

Hanken, J. & Wake, D.B., 1994. Five New Species of Minute Salamanders, Genus Thorius (Caudata, Plethodonitdaee, from Northern Oaxaca, Mexico. Copeia , pp. 573-590.Abstract

Five new species of diminutive salamanders of the endemic Mexican genus Thorius (Plethodontidae) are described from the Sierra de Juarez in northern Oaxaca. The species are diagnosed by adult body size, external proportions, dentition, osteology and coloration. The three species that have been studied using protein electrophoresis are genetically unique; all differ from T. macdougalli, the only species of the genus previously known from these mountains. Each of the six species studied has distinct geographic and elevational ranges, and there is a complex pattern of geographic overlap and replacement. As many as three species co-occur locally at elevations up to 2955 m on Cerro Pelon, and each species is sympatric with at least one other. One species descends to approximately 800 m, which is the lowest known elevational record for the genus. The new taxa include the full size range of the genus, with two large and three small species.

Seufert, D.W., Hanken, J. & Klymkowsky, M.W., 1994. Type II Collagen Distribution during Cranial Development in Xenopus Laevis. Anatomy and Embryology , 189 , pp. 81-89.Abstract

Epithelially expressed type II collagen is thought to play a prominent role in the embryonic patterning and differentiation of the vertebrate skull, primarily on the basis of data derived from amniotes. We describe the spatiotemporal distribution of type II collagen in the embryonic head of the African clawed frog, Xenopus laevis, using whole-mount and serial-section immunohistochemical analysis. We studied embryos spanning Nieuwkoop and Faber (1967) stages 21-39, a period including cranial neural crest cell migration and ending immediately before the onset of neurocranial chondrogenesis. Xenopus displays a transient expression of type II collagen beginning at least as early as stage 21; staining is most intense and widespread at stages 33/34 and 35/36 and subsequently diminishes. Collagen-positive areas include the ventrolateral surface of the brain, sensory vesicles, notochord, oropharynx, and integument. This expression pattern is similar, but not identical, to that reported for the mouse and two bird species (Japanese quail, domestic fowl); thus epithelially expressed type II collagen appears to be a phylogenetically widespread feature of vertebrate cranial development. Consistent with the proposed role of type II collagen in mediating neurocranial differentiation, most collagen-positive areas lie adjacent to subsequent sites gf chondrogenesis in the neurocranium but not the visceral skeleton. However, much of the collagen is expressed after the migration of cranial neural crest, including presumptive chondrogenic crest, seemingly too late to pattern the neurocranium by entrapment of these migrating cells.

Hanken, J., 1993. Adaptation of bone growth to miniaturization of body size. In B. K. Hall, ed. Bone, Volume 7: Bone Growth - B. Boca Raton. Boca Raton: CRC Press, pp. 79-104. PDF
Hall, B.K. & Hanken, J., 1993. Bibliography of skull development: 1937-1989. In J. Hanken & B. K. Hall, ed. The Skull: Vol. 1, Development. Chicago. Chicago: University of Chicago Press, pp. 378-577.
Hanken, J. & Hall, B.K., 1993. Mechanisms of skull diversity and evolution. In J. Hanken & B. K. Hall, ed. The Skull: Vol. 3, Functional and Evolutionary Mechanisms. Chicago. Chicago: University of Chicago Press, pp. 1-36. PDF
Hanken, J. & Hall, B.K. ed., 1993. The Skull: Vol. 1, Development; Vol. 2, Patterns of Structural and Systematic Diversity; Vol. 3, Functional and Evolutionary Mechanisms, Chicago: University of Chicago Press.
Hanken, J. & Thorogood, P., 1993. Evolution and Development of the Vertebrate Skull - the Role of Pattern Formation. Trends in Ecology & Evolution , 8 , pp. 9-15.Abstract

The vertebrate skull is anatomically complex and phylogenetically diverse; it presents unique opportunities to examine the role of developmental processes in evolutionary change. Previous studies have largely examined phylogenetic trends in tissue composition or change in the timing of developmental events (heterochrony). Additional important insights may be gained if skull evolution and development are viewed from the standpoint of pattern formation. Contemporary models of pattern formation offer the possibility of linking developmental mechanisms of cranial morphogenesis from the level of genes, through cell biology, to adult form.

Hanken, J. & Wake, D.B., 1993. Miniaturization of Body Size: Organismal Consequences and Evolutionary Significance. Annual Review of Ecology and Systematics , 24 , pp. 501-519.Abstract

Miniaturization, or the evolution of extremely small adult body size, is a widespread phenomenon in animals. It has important consequences for both organismal biology and phyletic diversification above the species level. The miniaturized phenotype is a complex combination of ancestral and derived traits, including reduction and structural simplification, increased variability, and morphological novelty. Many features likely represent secondary consequences of size decrease, which may be the result of selection primarily for small body size or some related attribute such as life history characteristics. In some cases, miniaturization has resulted in novel bauplans associated with the origin of higher taxa. Evaluation of causes and consequences of miniaturization should consider obvious features of physical size as well as less obvious, but biologically important, features such as genome and cell size.

Hanken, J., 1993. Model Systems Versus Outgroups: Alternative Approaches to the Study of Head Development and Evolution. American Zoologist , 33 , pp. 448-456.Abstract

There is widespread recognition of a recent coming together of developmental and evolutionary biology in the study of problems of mutual interest. Contemporary studies into the development and evolution of the head largely comprise two parallel approaches, or research strategies: the model systems approach and the comparative approach. The two strategies share the same general goal-greater understanding of cranial development and evolution-but typically emphasize different problems, ask different questions, and employ different methods, reflecting the contrasting backgrounds and biases of each group of investigators; there has been relatively little true synthesis. Each strategy is making important and valid contributions, but both have limitations. Resolution. of many fundamental and long-standing problems in cranial development and evolution will require a combined approach that incorporates the technical and conceptual strengths of each discipline.

Thorogood, P. & Hanken, J., 1992. Body building exercises. Curr. Biol. , 2 , pp. 83-85. PDF
Hanken, J., et al., 1992. Cranial Ontogeny in the Direct-Developing Frog, Eleutherodactylus coqui (Anura, Leptodactylidae), Analyzed Using Whole-Mount Immunohistochemistry. Journal of Morphology , 211 , pp. 95-118.Abstract

Direct development in amphibians is an evolutionarily derived life-history mode that involves the loss of the free-living, aquatic larval stage. We examined embryos of the direct-developing anuran Eleutherodactylus coqui (Leptodactylidae) to evaluate how the biphasic pattern of cranial ontogeny of metamorphosing species has been modified in the evolution of direct development in this lineage. We employed whole-mount immunohistochemistry using a monoclonal antibody against the extracellular matrix component Type II collagen, which allows visualization of the morphology of cartilages earlier and more effectively than traditional histological procedures; these latter procedures were also used where appropriate. This represents the first time that initial chondrogenic stages of cranial development of any vertebrate have been depicted in whole-mounts.Many cranial cartilages typical of larval anurans, e.g., suprarostrals, cornua trabeculae, never form in Eleutherodactylus coqui. Consequently, many regions of the skull assume an adult, or postmetamorphic, morphology from the inception of their development. Other components, e.g., the lower jaw, jaw suspensorium, and the hyobranchial skeleton, initially assume a mid-metamorphic configuration, which is subsequently remodeled before hatching. Thirteen of the adult complement of 17 bones form in the embryo, beginning with two bones of the jaw and jaw suspensorium, the angulosplenial and squamosal. Precocious ossification of these and other jaw elements is an evolutionarily derived feature not found in metamorphosing anurans, but shared with some direct-developing caecilians. Thus, in Eleutherodactylus cranial development involves both recapitulation and repatterning of the ancestral metamorphic ontogeny. These modifications, however, are not associated with any fundamental change in adult morphology and cannot at this time be causally linked to the evolutionary success of this extraordinarily speciose genus.