Publications

2005
Hanken, J., Wake, D.B. & Savage, J.M., 2005. A solution to the large black salamander problem (genus Bolitoglossa) in Costa Rica and Panama. Copeia , pp. 227-245.Abstract

Several populations of large (adult standard length, 43-134 mm) black salamanders of the widespread neotropical genus Bolitoglossa (Plethodontidae) are known from the cordilleras of western Panama and Costa Rica. These populations constitute at least seven species, including two recently described (B. anthracina, B. copia), one described long ago that remains poorly known (B. nigrescens), and three described herein as new. The long recognized, Aide-ranging B. robusta, which is distinguished by a pale, pigmented ring around the tail base and a unique combination of maxillary and vomerine tooth counts, may occur sympatrically with four of the other taxa. Differences in head and body form, adult size, cranial osteology, and maxillary and vomerine tooth counts separate all recognized taxa from one another. These results confirm and indeed increase the exceedingly high diversity of salamander species known from the Cordillera Talamanca-Baru of Costa Rica and Panama, diversity that now rivals that found anywhere else in the tropics.

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Parra-Olea, G., et al., 2005. Two new species of Pseudoeurycea (Caudata : Plethodontidae) from the mountains of northern Oaxaca, Mexico. Copeia , pp. 461-469.Abstract

We describe two new species of salamanders of the genus Pseudoeurycea from mountains in the northern part of the state of Oaxaca, Mexico. Pseudoeurycea papenfussi, a large, muscular member of the P gadovii group, occurs near the peaks (just below 3000 m) of the highest mountains of the Sierra de Juarez. It is related to P smithi, a more southerly species, and possibly to P aquatica, another species from Oaxaca. Pseudoeurycea obesa, a rotund member of the P leprosa group, is known only from the type locality in the Sierra Mazateca at the northernmost extremity of Oaxaca. It is related to P. werleri and P mystax, which are known from more southern parts of Oaxaca. These descriptions bring to 27 the number of species of salamanders known from Oaxaca. Most of these species are endemic to the state and are known only from regions that are undergoing rapid habitat modification and destruction.

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2004
Parra-Olea, G., et al., 2004. A new species of arboreal salamander (Caudata : Plethodontidae : Pseudoeurycea) from the mountains of Oaxaca, Mexico. Journal of Natural History , 38 , pp. 2119-2131.Abstract

Recent surveys of the plethodontid salamander fauna of Oaxaca, Mexico, disclosed the existence of a new, morphologically distinct arboreal species of the genus Pseudoeurycea. The new species, described here, is from the Sierra Mazateca in northern Oaxaca. Sequences of 1833 base pairs of the 16S, cytochrome b and ND4 mitochondrial DNA ( mtDNA) genes from the new taxon were used to assess its phylogenetic position. Previous phylogenetic analyses based on mtDNA supported recognition of four clades within Pseudoeurycea: P. bellii, P. gadovii, P. juarezi and P. leprosa-Lineatriton species groups. One additional species, P. unguidentis, was not closely allied to any of the four groups. Re-analysis including the additional sequences reported here establishes a sister-group relationship between the new species and P. unguidentis. Moreover, it supports this clade as part of the P. juarezi species group.

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Gross, J.B. & Hanken, J., 2004. Use of fluorescent dextran conjugates as a long-term marker of osteogenic neural crest in frogs. Developmental Dynamics , 230 , pp. 100-106.Abstract

The neural crest is a population of multipotent stem cells unique to vertebrates. In the head, cranial neural crest (CNC) cells make an assortment of differentiated cell types and tissues, including neurons, melanocytes, cartilage, and bone. The earliest understanding of the developmental potentiality of CNC cells came from classic studies using amphibian embryos. Fate maps generated from these studies have been largely validated in recent years. However, a fate map for the most late-developing structures in amphibians, and especially anurans (frogs), has never been produced. One such tissue type, skull bone, has been among the most difficult tissues to study due to the long time required for its development during anuran metamorphosis, which in some species may not occur until several months, or even years, after hatching. We report a relatively simple technique for studying this elusive population of neural crest-derived osteogenic (bone-forming) cells in Xenopus laevis by using fluorescently labeled dextran conjugates. (C) 2004 Wiley-Liss, Inc.

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2003
Hanken, J., 2003. Direct development. In B. K. Hall & W. M. Olson, ed. Keywords & Concepts in Evolutionary Developmental Biology. Cambridge. Cambridge: Harvard University Press, pp. 97-102.
Shapiro, M.D., Hanken, J. & Rosenthal, N., 2003. Developmental basis of evolutionary digit loss in the Australian lizard Hemiergis. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution , 297B , pp. 48-56.Abstract

Loss of limb skeletal elements is a recurring theme in tetrapod evolution, but the developmental mechanisms underlying this phenomenon remain largely unknown. The Australian lizard genus Hemiergis offers an excellent model system to study limb reduction among closely related, naturally occurring populations with different numbers of digits. Evolutionary digit loss in Hemiergis does not result from simple truncation of a pentadactyl skeletal developmental program. Rather, the duration of embryonic expression of the patterning molecule Sonic hedgehog (SHH) is shortened in limbs with reduced numbers of digits, and is correlated with decreased cell proliferation in the posterior aspect of the limb. Moreover, this comparative analysis suggests an early role for SHH in specification of digit identity and later importance in maintaining cell proliferation and survival. Subtle changes in spatial or temporal regulation of SHH may alter proliferation and patterning of the developing limb, thereby effecting divergence in adult limb morphology among closely related species. In contrast, expression of MSX and Distal-less proteins were similar among embryos from different populations. (C) 2003 Wiley Liss, Inc.

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2002
Sierwald, P., et al., 2002. NEON-V: CRIPTON Workshop (Collections, Research, Inventories, and People for Taxonomic Opportunities) - Final Report. National Science Foundation, Washington, DC.
Hanken, J., 2002. Eric Thomas Brazil Francis and the evolutionary morphology of salamanders. Introduction to the reprint of E.T.B. Francis. In The Anatomy of the salamander. Ithaca. Ithaca: Society for the Study of Amphibians and Reptiles, pp. v-xiv. PDF
Falck, P., Hanken, J. & Olsson, L., 2002. Cranial neural crest emergence and migration in the Mexican axolotl (Ambystoma mexicanum). Zoology (Jena) , 105 , pp. 195-202.Abstract

The timing and pattern of cranial neural crest cell emergence and migration in the Mexican axolotl, Ambystoma mexicanum, are assessed using scanning electron microscopy (SEM). Cranial neural crest cells emerge and begin to migrate at the time of neural fold closure and soon form three distinct streams. The most anterior (mandibular) stream emerges first, at the level of the mesencephalon. Cells in this stream migrate rostroventrally around the optic vesicle. The second (hyoid) and third (branchial) streams emerge in close succession at the level of the rhombencephalon and extend ventrolaterally. Cells forming the hyoid stream migrate rostral to the otic vesicle, whereas the branchial stream divides into two parallel streams, which migrate caudal to the otic vesicle. At later stages (stage 26 onwards) the cranial neural crest cells disperse into the adjacent mesoderm and can no longer be followed by dissection and SEM. The pattern of cranial neural crest emergence and migration, and division into migratory streams is similar to that in other amphibians and in the Australian lungfish (Neoceratodus forsteri). Emergence of crest cells from the neural tube, relative to the time of neural tube closure, occurs relatively late in comparison to anurans, but much earlier than in the Australian lungfish. These results establish a morphological foundation for studies in progress on the further development and fate of cranial neural crest cells in the Mexican axolotl, as well as for studies of the role of cranial neural crest in cranial patterning.

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Olsson, L., et al., 2002. Cranial neural crest-cell migration in the direct-developing frog, Eleutherodactylus coqui: molecular heterogeneity within and among migratory streams. Zoology (Jena) , 105 , pp. 3-13.Abstract

Direct development is a specialized reproductive mode that has evolved repeatedly in many different lineages of amphibians, especially anurans. A fully formed, albeit miniature adult hatches directly from the egg; there is no free-living larva. In many groups, the evolution of direct development has had profound consequences for cranial development and morphology, including many components that are derived from the embryonic neural crest. Yet, the developmental bases of these effects remain poorly known. In order to more fully characterize these changes, we used three molecular markers to analyze cranial neural crest-cell emergence and migration in the direct-developing frog, Eleutherodactylus coqui: HNK-1 immunoreactivity, Dlx protein expression, and cholinesterase activity. Our study validates and extends earlier results showing that the comprehensive changes in embryonic cranial patterning, differentiation, and developmental timing that are associated with direct development in Eleutherodactylus have not affected gross features of cranial neural crest biology: the relative timing of crest emergence and the number, configuration and identity of the principal migratory streams closely resemble those seen in metamorphic anurans. The three markers are variably expressed within and among neural crest-cell populations. This variation suggests that determination of cranial neural crest-cells may already have begun at or soon after the onset of migration, when the cells emerge from the neural tube. It is not known how or even if this variation correlates with differential cell lineage or fate. Finally, although HNK-1 expression is widely used to study neural crest migration in teleost fishes and amniotes, E. coqui is the only amphibian known in which it effectively labels migrating neural crest-cells. There are not enough comparative data to determine whether this feature is functionally associated with direct development or is instead unrelated to reproductive mode.

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2001
Olsson, L., et al., 2001. Cranial neural crest cells contribute to connective tissue in cranial muscles in the anuran amphibian, Bombina orientalis. Developmental Biology , 237 , pp. 354-367.Abstract

The contribution of cranial neural crest cells to the development and patterning of cranial muscles in amphibians was investigated in the phylogenetically basal and morphologically generalized frog, Bombina orientalis. Experimental methods included fluorescent marking of premigratory cranial neural crest and extirpation of individual migratory streams. Neural crest cells contributed to the connective tissue component, but not the myofibers, of many larval muscles within the first two branchial arches (mandibular and hyoid), and complex changes in muscle patterning followed neural crest extirpation. Connective tissue components of individual muscles of either arch originate from the particular crest migratory stream that is associated with that arch, and this relationship is maintained regardless of the segmental identity-or embryonic derivation-of associated skeletal components. These developmental relations define a pattern of segmentation in the head of larval anurans that is similar to that previously described in the domestic chicken, the only vertebrate that has been thoroughly investigated in this respect. The fundamental role of the neural crest in patterning skeleton and musculature may represent a primitive feature of cranial development in vertebrates. Moreover, the corresponding developmental processes and cell fates appear to be conserved even when major evolutionary innovations-such as the novel cartilages and muscles of anuran larvae-result in major differences in cranial form. (C) 2001 Academic Press.

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Hanken, J., et al., 2001. Limb development in a "non-model" vertebrate, the direct-developing frog Eleutherodactylus coqui. Journal of Experimental Zoology (Mol. Dev. Vol.) , 291 , pp. 375-388.Abstract

Mechanisms that mediate limb development are regarded as highly conserved among vertebrates, especially tetrapods. Yet, this assumption is based on the study of relatively few species, and virtually none of those that display any of a large number of specialized life-history or reproductive modes, which might be expected to affect developmental pattern or process. Direct development is an alternative life history found in many anuran amphibians. Many adult features that form after hatching in metamorphic frogs, such as limbs, appear during embryogenesis in direct-developing species. Limb development in the direct-developing frog Eleutherodactylus coqui presents a mosaic of apparently conserved and novel features. The former include the basic sequence and pattern of limb chondrogenesis, which are typical of anurans generally and appear largely unaffected by the gross shift in developmental timing; expression of Distal-less protein (D1x) in the distal ectoderm; expression of the gene Sonic hedgehog (Shh) in the zone of polarizing activity (ZPA); and the ability of the ZPA to induce supernumerary digits when transplanted to the anterior region of an early host limb bud. Novel features include the absence of a morphologically distinct apical ectodermal ridge, the ability of the limb to continue distal outgrowth and differentiation following removal of the distal ectoderm, and earlier cessation of the inductive ability of the ZPA. Attempts to represent tetrapod limb development as a developmental "module" must allow for this kind of evolutionary variation among species. (C) 2001 Wiley-Liss, Inc.

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Brame, A.H., et al., 2001. New species of large black salamander, genus Bolitoglossa (Plethodontidae) from western Panama. Copeia , pp. 700-704.Abstract

A new species of plethodontid salamander is one of several large black species found in the Cordillera Talamanca-Baru of Panama and Costa Rica. Bolitoglossa anthracina sp. nov. differs from others in this group in having a very large number of maxillary teeth and a moderate number of vomerine teeth.

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Hanken, J. & Wake, D.B., 2001. A seventh species of minute salamander (Thorius : Plethodontidae) from the Sierra de Juarez, Oaxaca, Mexico. Herpetologica , 57 , pp. 515-523.Abstract

We describe a new terrestrial species of minute lungless salamander of the Mexican genus Thorius (Plethodontidae) from montane pine-oak forests in the Sierra de Juarez of north central Oaxaca, Mexico. The new species is distinguished from congeners by a combination of body size, external morphology, osteology, and dental traits, and it is well differentiated genetically from other named species for which data are available. This is the seventh endemic species of Thorius reported from the Sierra de Juarez, and known localities are geographically isolated from those of all other species. Discovery of another new species of plethodontid salamander from Oaxaca enhances the state's standing as a preeminent center of herpetological diversity within both Mexico and Mesoamerica.

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2000
Hanken, J., 2000. A review of Tadpoles: the Biology of Anuran Larvae. Evol. Devel. , 2 , pp. 174-175. PDF
Carl, T.F., et al., 2000. Green fluorescent protein used to assess cranial neural crest derivatives in the frog, Xenopus laevis. In C. O. Jacobson & L. Olsson, ed. Regulatory Processes in Development: The Legacy of Sven Hörstadius (1898-1996). London. London: Wenner-Gren International Series, Portland Press, pp. 167-172.Abstract

We used RNA encoding green fluorescent protein (GFP) to study the migration and larval derivatives of cranial neural crest cells in the metamorphosing frog, Xenopus laevis. GFP provides an intrinsic cell-lineage marker that is retained after cell division. Moreover, because GFP label introduced at the one-cell stage continues to be expressed well after hatching, it offers a reliable and effective method for assessing the embryonic derivation of many larval, and possibly even adult, tissues in amphibians as well as other vertebrates. Basic patterns of cranial neural crest migration and derivation in X. laevis defined using GFP (including contributions to many larval cranial cartilages) arc similar to those documented in previous studies that used conventional vital stains, lineage markers, and ablation techniques. However, preliminary results also suggest the neural crest derivation of additional components of the larval anuran head, e.g., cranial bone, whose embryonic origins have proven much more difficult to resolve with other methods.

1999
Hanken, J., 1999. An alternative evolutionary synthesis [review of C.D. Schlichting and M. Pigliucci, Phenotypic Evolution: A Reaction Norm Perspective]. Trends Ecol. Evol. , 14 , pp. 162-163. PDF
Hanken, J., 1999. Larvae in amphibian development and evolution. In The Origin and Evolution of Larval Forms. San Diego. San Diego: Academic Press, pp. 61-108. PDF
Hanken, J., 1999. 4,780 and counting. Natural History , 108 , pp. 82-82. PDF
Carl, T.F., et al., 1999. Inhibition of neural crest migration in Xenopus using anti-sense-slug RNA. Developmental Biology , 213 , pp. 101-115.Abstract

Based primarily on studies in the chick, it has been assumed that the zinc finger transcription factor Slug is required for neural crest migration. In the mouse, however, Slug is not expressed in the premigratory neural crest, which forms normally in Slug -/- animals. To study the role of Slug in Xenopus laevis, we used the injection of XSlug antisense RNA and tissue transplantation. Injection of Slug antisense RNA did not suppress the early expression of the related gene XSnail, but led to reduced expression of both XSlug and XSnail in later stage embryos, whereas the expression of another neural crest marker, XTwist, was not affected. Down-regulation of XSlug and XSnail was associated with the inhibition of neural crest cell migration and the reduction or loss of many neural crest derivatives. In particular, the formation of rostral cartilages was often highly aberrant, whereas the posterior cartilages were less frequently affected. The effects of Slug antisense RNA on neural crest migration and cartilage formation were rescued by the injection of either XSlug or XSnail mRNA. These studies indicate that XSlug is required for neural crest migration, that XSlug and XSnail may be functionally redundant, and that both genes are required to maintain each other's expression in the neural crest development of xenopus laevis. (C) 1999 Academic Press.

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