John O. Reiss

Ultrastructure of the Olfactory Organ in the Clawed Frog, Xenopus laevis, During Larval Development and Metamorphosis

Development of the olfactory epithelia of the African clawed frog, Xenopus laevis, was studied by scanning and transmission electron microscopy. Stages examined ranged from hatching through the end of metamorphosis. The larval olfactory organ consists of two chambers, the principal cavity and the vomeronasal organ (VNO). A third sensory chamber, the middle cavity, arises during metamorphosis. In larvae, the principal cavity is exposed to water‐borne odorants, but after metamorphosis it is exposed to airborne odorants. The middle cavity and the VNO are always exposed to waterborne odorants.

The Meaning of Developmental Time: A Metric for Comparative Embryology

The lack of a suitable metric for developmental time has prevented a comparison of developmental rates and tempos between species, thus precluding analyses of heterochronic processes in evolution that do not depend on the use of morphology or size as an index of age. At least two problems exist in using clock time itself as the measure of developmental time: temperature effects within a species, and size effects across species. Consideration of two important distinctions that can be made in the notion of time-that between time as sequence and time as duration and that between extrinsic and intrinsic time-suggests that a metric, to be useful, must satisfy seven criteria: (1) it should be independent of morphology; (2) it should be independent of size; (3) it should depend on only one a priori homologous event; (4) it should be unaffected by changes in temperature for any given species; (5) closely related organisms should undergo homologous events at similar developmental ages as measured by the metric; (6) it should increase monotonically with clock time; and (7) it should be defined in a physically measurable way. I propose that physiological time, here defined as the integral of mass-specific metabolic rate over clock time, may be such a metric; this definition is based on an extension of previous concepts of physiological time to reflect ontogenetic changes in mass and metabolic rate. The proposed metric inherently satisfies criteria 1, 3, 6, and 7; satisfaction of the others must be assessed empirically. In spite of problems with strict comparability, literature data from 22 vertebrate species strongly suggest that criterion 2 is also satisfied, although they cast doubt on the satisfaction of criterion 5. No available data bear directly on criterion 4, although circumstantial evidence suggests that it may also be satisfied. A more rigorous assessment of the hypothesis awaits additional data, especially those allowing a correlation between physiological time and morphological development. However, even if this particular proposal for a metric proves unworkable-which is likely, given its simple formulation and broad scope-the criteria suggested will serve to judge any future proposal of a metric for developmental time. For the present, one must at least be aware of the hidden assumptions that have entered into much previous work on heterochrony, particularly that of an equivalence between size and age. Without a metric for developmental time, the extent and meaning of evolutionary changes in developmental timing simply cannot be assessed.

Metamorphic remodeling of the primary olfactory projection in Xenopus: Developmental independence of projections from olfactory neuron subclasses

In adult Xenopus, the nasal cavity is divided into separate middle (MC) and principal (PC) cavities; the former is used to smell water-borne odorants, the latter air-borne odorants. Recent work has shown that olfactory neurons of each cavity express a distinct subclass of odorant receptors. Moreover, MC and PC axons project to distinct regions of the olfactory bulb. To examine the developmental basis for this specificity in the olfactory projection, we extirpated the developing MC from early metamorphic (stage 54-57) tadpoles and raised the animals through metamorphosis. In most lesioned animals, the MC partly regenerated. Compared with the unlesioned side, reduction of the region of the glomerular layer of the olfactory bulb receiving MC afferents ranged from 70% to 95%. PC afferents did not occupy regions of the olfactory bulb deprived of MC afferents. These results support a model in which intrinsic cues in the olfactory bulb control the projection pattern attained by ingrowing olfactory axons.

Early Development of Chondrocranium in the Tailed Frog Ascaphus truei (Amphibia: Anura): Implications for Anuran Palatoquadrate Homologies

Chondrocranial development in Ascaphus truei was studied by serial sectioning and graphical reconstruction. Nine stages (21–29; 9–18 mm TL) were examined. Mesodermal cells were distinguished from ectomesenchymal (neural crest derived) cells by retained yolk granules. Ectomesenchymal parts of the chondrocranium include the suprarostrals, pila preoptica, anterior trabecula, and palatoquadrate. Mesodermal parts of the chondrocranium include the orbital cartilage, posterior trabecula, parachordal, basiotic lamina, and otic capsule. Development of the palatoquadrate is as follows. The pterygoid process first connects with the trabecula far rostrally; their fusion progresses caudally. The ascending process connects with a mesodermal bar that extends from the orbital cartilage to the otic capsule, and forms the ventral border of the dorsal trigeminal outlet. This bar is the “ascending process” of Ascaphus adults; it is a neurocranial, not palatoquadrate structure. The basal process chondrifies in an ectomesenchymal strand running from the quadrate keel to the postpalatine commissure. Later, the postpalatine commissure and basal process extend anteromedially to contact the floor of the anterior cupula of the otic capsule, creating separate foramina for the palatine and hyomandibular branches of the facial nerve. Based on these data, and on comparison with other frogs and salamanders, the anuran anterior quadratocranial commissure is homologized with the pterygoid process of salamanders, the anuran basal process (=“pseudobasal” or “hyobasal” process) with the basal process of salamanders, and the anuran otic ledge with the basitrabecular process of salamanders. The extensive similarities in palatoquadrate structure and development between frogs and salamanders, and lacking in caecilians, are not phylogenetically informative. Available information on fossil outgroups suggests that some of these similarities are primitive for Lissamphibia, whereas for others the polarity is uncertain. J. Morphol. 231:63‐100, 1997.

Palatal Metamorphosis in Basal Caecilians (Amphibia: Gymnophiona) as Evidence for Lissamphibian Monophyly

The morphology of the bony palate in larval and metamorphosed Epicrionops bicolor Boulenger and E. petersi Taylor (Rhinatrematidae) was studied to assess the extent of palatal change at metamorphosis. In larvae the maxilla is short; it abuts the dorsolateral process of the palatine at mid-choanal level. The pterygoid is long and straight; it runs anteromedially, close to the lateral edge of the parasphenoid. At metamorphosis the maxilla fuses with the palatine. The maxillary part of the maxillopalatine expands dorsally and caudally, surrounding the orbit and lacrimal ducts and completing the lateral border of the subtemporal fenestra. The anterior part of the pterygoid shifts laterally, broadening the interpterygoid vacuity, and separates from the posterior part of the pterygoid. The quadrate develops a rostrally directed quadratojugal process, overlapped by the maxilla and squamosal. A review of the literature shows that a similar pattern of palatal metamorphosis (except for the division of the pterygoid) is seen in other caecilian genera with free-living larvae: Ichthyophis (Ichthyophiidae), Grandisonia (Caeciliaidae), and probably Uraeotyphlus (Uraeotyphlidae) and Sylvacaecilia (Caeciliaidae). This implies that the shared pattern is plesiomorphic for caecilians. Features of palatal metamorphosis shared among caecilians, salamanders, and frogs support the hypothesis of lissamphibian monophyly. rnal of Herpetol gy, Vol. 30, No. 1, pp. 27-39, 1996 yright 19 6 Society for the Study of Amphibians and Reptiles latal Metamorphosis n Basal Caecilians phibia: Gymnophiona) as Evidence for sa phibian Monophyl Extant amphibians comprise three distinct, monophyletic groups: frogs (Anura), salamanders (Caudata), and caecilians (Gymnophiona) (Duellman and Trueb, 1986; Milner, 1988; Cannatella and Hillis, 1993). The relationship of each group to the others, and of these to fossil taxa, has been much debated. However, an emerging consensus-based on both morphological and molecular evidence-supports the hypothesis first explicitly proposed by Parsons and Williams (1962, 1963; see also Gadow, 1901; 1 Present Address: Department of Molecular and Cellular Biology, University of Arizona, Tucson, Arizona 85721, USA. tant amphibians compris three distinct, onophyletic groups: frogs (Anura), salamaners (Caud ta), and caecilians (Gym ophiona) uellman and Trueb, 1986; Milner, 1988; Canatella and Hillis, 1993). The relationship of ch group to the others, and of the e to fossil Parker, 1956; Szarski, 1962): that the extant groups are a monophyletic unit, the Lissamphibia (e.g., Milner, 1988, 1993; Bolt, 1991; Trueb and Cloutier, 1991; Cannatella and Hillis, 1993; Hedges and Maxson, 1993). Since basal members of all three modern groups have a biphasic life cycle with a discrete metamorphosis from the larval to the juvenile form (Duellman and Trueb, 1986), we might expect to find common character transformations retained in the metamorphosis of each group. Such shared character transformations could serve as additional lissamphibian synapomorphies (cf. de Queiroz, 1985). Both frogs and salamanders undergo profound changes in skull structure at metamorphosis, especially in the palate and the hyoer, 1956; Szarski, 1962): hat the extant ps are a monophyletic unit, the Lissami ia (e.g., Milner, 1988, 1993; Bolt, 1991; Trueb 27 This content downloaded from 157.55.39.32 on Mon, 10 Oct 2016 04:24:55 UTC All use subject to http://about.jstor.org/terms

Olfactory metamorphosis in the coastal tailed frog Ascaphus truei (Amphibia, Anura, Leiopelmatidae)

The structure of the olfactory organ in larvae and adults of the basal anuran Ascaphus truei was examined using light micrography, electron micrography, and resin casts of the nasal cavity. The larval olfactory organ consists of nonsensory anterior and posterior nasal tubes connected to a large, main olfactory cavity containing olfactory epithelium; the vomeronasal organ is a ventrolateral diverticulum of this cavity. A small patch of olfactory epithelium (the “epithelial band”) also is present in the preoral buccal cavity, anterolateral to the choana. The main olfactory epithelium and epithelial band have both microvillar and ciliated receptor cells, and both microvillar and ciliated supporting cells. The epithelial band also contains secretory ciliated supporting cells. The vomeronasal epithelium contains only microvillar receptor cells. After metamorphosis, the adult olfactory organ is divided into the three typical anuran olfactory chambers: the principal, middle, and inferior cavities. The anterior part of the principal cavity contains a “larval type” epithelium that has both microvillar and ciliated receptor cells and both microvillar and ciliated supporting cells, whereas the posterior part is lined with an “adult‐type” epithelium that has only ciliated receptor cells and microvillar supporting cells. The middle cavity is nonsensory. The vomeronasal epithelium of the inferior cavity resembles that of larvae but is distinguished by a novel type of microvillar cell. The presence of two distinct types of olfactory epithelium in the principal cavity of adult A. truei is unique among previously described anuran olfactory organs. A comparative review suggests that the anterior olfactory epithelium is homologous with the “recessus olfactorius” of other anurans and with the accessory nasal cavity of pipids and functions to detect water‐borne odorants. J. Morphol. 2011.

Anuran Postnasal Wall Homology: An Experimental Extirpation Study

The nasal placode was extirpated unilaterally in Gosner stage 18–20 embryos of Rana sylvatica, R. palustris and R. pipiens, in order to test alternative proposed schemes of homology for the ethmoidal attachment of the palatoquadrate in anurans and urodeles. Absence of the nasal sac has no pronounced effect on the formation of larval chondrocranial structures. In contrast, in metamorphosed animals the lamina orbitonasalis and inferior prenasal process are the only nasal capsule structures present on the operated side. The medial nasal branch of the deep ophthalmic nerve passes forward over the dorsal surface of the lamina orbitonasalis, rather than through an orbitonasal foramen. Comparison with previous experimental work on urodeles supports the traditional homology of the anuran lamina orbitonasalis with the antorbital process of urodeles and other vertebrates. J. Morphol. 238:343–353, 1998.

Does selection intensity increase when populations decrease? Absolute fitness, relative fitness, and the opportunity for selection

The variance in relative fitness, commonly called the “opportunity for selection,” is a measure of the maximum amount of selection that can occur in a population. I review the relation between fitness variance and population growth, showing that fitness variance is higher during periods of population decline. This is true both for survival and for commonly used models for variable descendant number (Poisson, negative binomial, generalized Poisson). Empirical evidence suggests that not just the opportunity for selection but also the actual selection occurring is commonly greater during such periods of population reduction.

Relative Fitness, Teleology, and the Adaptive Landscape

The metaphor of the adaptive landscape, introduced by Sewall Wright in 1932, has played, and continues to play, a central role in much evolutionary thought. I argue that the use of this metaphor is tied to a teleological view of the evolutionary process, in which natural selection directs evolution toward an improved future state. I argue further that the use of “relative fitnesses” standardized to an arbitrary value, which is closely connected with the metaphor of an adaptive landscape, produces a disconnect between the mean fitness of a population and any real property of that population. This allows for a vague and ill-defined improvement to occur under the influence of selection. Instead, I suggest that relative fitnesses should be standardized by the mean absolute fitness (expected population growth rate), so that they express the expected rate of increase in frequency, rather than number. Under this definition, the mean relative fitness of all populations is always 1.0, and never changes as long as the population continues to exist.

The ontogeny of the olfactory system in ceratophryid frogs (Anura, Ceratophryidae)

The aquatic‐to‐terrestrial shift in the life cycle of most anurans suggests that the differences between the larval and adult morphology of the nose are required for sensory function in two media with different physical characteristics. However, a better controlled test of specialization to medium is to compare adult stages of terrestrial frogs with those that remain fully aquatic as adults. The Ceratophryidae is a monophyletic group of neotropical frogs whose diversification from a common terrestrial ancestor gave rise to both terrestrial (Ceratophrys, Chacophrys) and aquatic (Lepidobatrachus) adults. So, ceratophryids represent an excellent model to analyze the morphology and possible changes related to a secondary aquatic life. We describe the histomorphology of the nose during the ontogeny of the Ceratophryidae, paying particular attention to the condition in adult stages of the recessus olfactorius (a small area of olfactory epithelium that appears to be used for aquatic olfaction) and the eminentia olfactoria (a raised ridge on the floor of the principal cavity correlated with terrestrial olfaction). The species examined (Ceratophrys cranwelli, Chacophrys pierottii, Lepidobatrachus laevis, and L. llanensis) share a common larval olfactory organ composed by the principal cavity, the vomeronasal organ and the lateral appendix. At postmetamorphic stages, ceratophryids present a common morphology of the nose with the principal, middle, and inferior cavities with characteristics similar to other neobatrachians at the end of metamorphosis. However, in advanced adult stages, Lepidobatrachus laevis presents a recessus olfactorius with a heightened (peramorphic) development and a rudimentary (paedomorphic) eminentia olfactoria. Thus, the adult nose in Lepidobatrachus laevis arises from a common developmental ‘terrestrial’ pathway up to postmetamorphic stages, when its ontogeny leads to a distinctive morphology related to the evolutionarily derived, secondarily aquatic life of adults of this lineage.