Cranial neural crest-cell migration in the direct-developing frog, Eleutherodactylus coqui: molecular heterogeneity within and among migratory streams

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.     

What is metamorphosis?

Metamorphosis (Gr. meta- "change" + morphe "form") as a biologicalprocess is generally attributed to a subset of animals: mostfamously insects and amphibians, but some fish and many marineinvertebrates as well. We held a symposium at the 2006 Societyfor Integrative and Comparative Biology (SICB) annual meetingin Orlando, FL (USA) to discuss metamorphosis in a comparativecontext. Specifically, we considered the possibility that theterm "metamorphosis" could be rightly applied to non-animalsas well, including fungi, flowering plants, and some marinealgae. Clearly, the answer depends upon how metamorphosis isdefined. As we participants differed (sometimes quite substantially)in how we defined the term, we decided to present each of ourconceptions of metamorphosis in 1 place, rather than attemptingto agree on a single consensus definition. Herein we have gatheredtogether our various definitions of metamorphosis, and offeran analysis that highlights some of the main similarities anddifferences among them. We present this article not only asan introduction to this symposium volume, but also as a referencetool that can be used by others interested in metamorphosis.Ultimately, we hope that this article—and the volume asa whole—will represent a springboard for further investigationsinto the surprisingly deep mechanistic similarities among independentlyevolved life cycle transitions across kingdoms.     

Fine-scale genetic structure in a salamander with two reproductive modes: Does reproductive mode affect dispersal?

Reproduction is intimately linked with dispersal, but the effects of changes in reproductive strategies on dispersal have received little attention. Such changes have occurred in many taxonomic groups, resulting in profound alterations in life-history. In amphibians, many species shifted from oviparous/larviparous aquatic reproduction (deposition of eggs or pre-metamorphic larvae in water) to pueriparous terrestrial reproduction (parturition of terrestrial juveniles). The latter provides greater independence from water by skipping the aquatic larval stage; however, the eco-evolutionary implications of this evolutionary step have been underexplored, largely because reproductive modes rarely vary at the intraspecific level, preventing meaningful comparisons. We studied the effects of a transition to pueriparity on dispersal and fine-scale genetic structure in the fire salamander (Salamandra salamandra), a species exhibiting two co-occurring reproductive modes: larviparity and pueriparity. We performed genetic analyses (parentage and genetic spatial autocorrelation) using 11 microsatellite loci to compare dispersal and fine-scale genetic structure in three larviparous and three pueriparous populations (354 individuals in total). We did not find significant differences between reproductive modes, but in some larviparous populations movement patterns may be influenced by site-specific features (type of water bodies), possibly due to passive water-borne dispersal of larvae along streams. Additionally, females (especially larviparous ones) appeared to be more philopatric, while males showed greater variation in dispersal distances. This study also points to future avenues of research to better understand the eco-evolutionary implications of changes in reproductive modes in amphibians.     

Cellular Aspects of the Control of Physiological Color Changes in Amphibians

SYNOPSIS. The present paper is concerned mainly with the melanin-dispersingeffect of melanocyte-stimulating hormones (MSH's) on the skinmelanophores of amphibians. In addition, some of the more recentevidence for the unihumoral theory of the control of color changeis reviewed. The mechanism of dispersion of melanin is stillunknown, but evidence is accumulating that the action of MSHmay be mediated by an increase in the melanophoric content ofadenosine 3', 5'-monophosphate (cyclic AMP). For example, cyclicAMP has a specific, reversible melanin-dispersing effect onthe melanophores of the isolated skin of R. pipiens and Xenopuslaevis. It also has a reversible "melanophore—expanding"effect on the tissue—cultured embryonic melanophores ofthe spotted salamander, Ambystoma maculatum. The effect of cyclicAMP on melanophores of R. pipiens does not require sodium butis inhibited by hypertonicity. Finally, new evidence is presented that confirms that the melanin-dispersingeffect of catecholamines on melanophores of X. laevis is mediatedby beta adrenergic receptors,because it is blocked by the highlyspecific ß—blocking agent, propranolol. On theother hand, the melanin-aggregating effect of catecholamineson amphibian melanophores appears to be mediated by alpha adrenergicreceptors. There is even a possibility that the effects of catecholaminesare also mediated through a control of cyclic AMP levels inmelanophores, with beta adrenergic stimulation producing anincrease in cyclic AMP levels, followed by dispersion of melanin,and alpha adrenergic stimulation producing a decrease in cyclicAMP levels, followed by aggregation of melanin.     

Endosulfan-enhanced crest induction in Daphnia longicephala: evidence for cholinergic innervation of kairomone receptors

Daphnia iongicephala were reared from early embryogenesis inthe presence or absence of crest-inducing kairomones releasedby Anisops gratus (Notonectidae) and from birth in one of fiveconcentrations of the organochiorine pesticide, endosulfan (0,0.1, 1.0, 10 or 100 g 1^–1 The morphologyof the daphnidswas measured 3 days after birth and on production of the firstbrood of eggs. The reproductive parameters, first brood size,age at first reproduction, mean egg volume and total egg volume,were also measured. Endosulfan significantly induced crest developmentin 3-day-old daphnids at 0.1, 1.0 and 10 g ^1– in thepresence and absence of Anisops kairomone, although crest sizein the absence of kairomone was only marginally greater thancontrols. A concentration of 10 pg 1^–1 endosulfan significantlyenhanced crest growth of kairomone-exposed daphnids at maturity.The Anisops kairomone alone induced a large crest in D.iongicephola,reduced first brood size, mean egg volume and total egg volume,and increased age at maturity. The coefficient of variationof mean egg volume was significantly reduced by Anisops kairomone.It is hypothesized that endosulfan enhances crest developmentbyinhibition of .     

Egg size and reproductive allocation in eusocial thrips

Reproductive allocation, in terms of fecundity and egg size,has been given little consideration in eusocial societies. Tobegin to address this, absolute and body size–adjustedegg volumes were compared, along with fecundity, between thefoundress and her subfertile soldier offspring in the eusocial,gall-inducing thrips, Kladothrips hamiltoni, Kladothrips waterhousei,and Kladothrips habrus, and a congeneric, Kladothrips morrisi,with fully fecund soldiers. Soldiers produced significantlylarger eggs than the foundress in all species except K. morrisi,where egg volumes did not differ. After accounting for bodysize, soldiers produced significantly smaller eggs than thefoundress in K. morrisi and marginally so in K. waterhousei,but egg sizes did not differ in K. hamiltoni and K. habrus.When egg size and fecundity data are combined, K. morrisi soldiersinvest less in reproduction than the foundress, and in conjunctionwith other life-history features the species can be consideredeusocial. Maximum likelihood analyses reveal relatively lowreproductive allocation skew in the ancestral lineages and highskew in the derived lineages, but the trend is not significantwhen fecundity and egg size are considered separately. Gallsize covaried negatively with soldier-to-foundress relativebody size–adjusted egg size and reproductive allocationand marginally so with fecundity, suggesting that gall sizeis a determinant of egg size and fecundity trade-offs in eusocialthrips and providing the strongest support to date that gallsize has featured in the social evolution of this clade. Thisstudy highlights that data on fecundity alone may be insufficientfor assessing reproductive division of labor.     

Profiles of Leaf Senescence During Reproductive Growth of Sunflower and Maize

We investigated the effect of reproductive growth on the profilesof leaf senescence in maize (Zea mays L.) and sunflower (Helianthusannuus L.). Leaf senescence after flowering was assessed usingboth structural (leaf chlorophyll, nitrogen and dry matter)and functional (photosynthesis) variables in undisturbed plants(+G) and in plants in which grain set was prevented (-G). Twoweeks after flowering, lack of grain accelerated senescencein maize and delayed senescence in sunflower as indicated byleaf chlorophyll; leaf nitrogen and dry matter were less sensitiveresponse variables. Lack of interaction between reproductivetreatment and leaf position indicates that the senescence signal,whatever its nature, was equally effective throughout the plantin both species. In both species, feedback inhibition of photosynthesiswas first detected 30–35 d after flowering; excess carbohydratein the leaves was therefore an unlikely trigger of acceleratedsenescence in maize. As reproductive development progressed,differences between +G and -G plants were more marked in sunflower,and tended to disappear or reverse in maize. In sunflower, interactionsbetween leaf position and reproductive treatment—attributableto the local effect of grain—were detected around 20–27d after flowering. Copyright 2000 Annals of Botany Company Helianthus annuus, Zea mays, chlorophyll, light, nitrogen, photosynthesis, reproductive growth, senescence, source-sink, SPAD.     

Relationships Between Invertebrate Phyla Based on Functional-Mechanical Analysis of the Hydrostatic Skeleton

SYNOPSIS. The phylogeny of the major groups of deuterostomecoelomates—the chordates,hemichordates and echinoderms—isdiscussed based on a mechanical-functional analysis of the hydrostaticskeleton and associated structures. The basic approach is tofirst establish transformation series of individual featuresand of functional complexes of features and secondto determinetheir "Lesrichtung" by showing the direction of increased economy(i.e., better adaptation) with respect to environmental factors.It is argued that a metameric coelom is primitive with respectto an oligomeric one and that the ancestral form of the deuterostomecoelomates is a metameric, coelomate worm-like animal with acomplex set of circular, transverse andlongitudinal body muscles.The coelom plus the complex body musculature formed the hydrostaticskeleton.The sequence of structural modifications leading to chordatesis: (a) appearance of the notochord; (b) specialization of thedorsal longitudinal muscles with a reduction and disappearanceof the transverse and circular muscles; (c) simultaneous appearanceof the dorsal hollow nerve cord; (d) development of a postanaltail; and (e) appearance and specialization of the branchialbasket with gill slits as a filter feeding apparatus. The primitivechordate would be most similar to the lancelet (Acrania). Tunicatesare advanced chordates specialized forsessile life and lostmost chordate features in the adult, but retained them in thelarvae as adaptations for active dispersal. Enteropneusts (acornworms) are another advanced group specialized for burrowingin fine sediments and that evolved the anterior proboscis asa peristaltic burrowing organ. The notochord was lost as wasthe dorsal nerve cord and segmented conditionof the coelom.A collar originated as a means to prevent discharged water fromre-entering themouth. Pterobranchs arose from enteropneustlikeforms; their major structural changes are reduction of the branchialbasket and modification of the collar into tentacles which areassociated with life in a closed tube. Finally, echinodermsarose from a pterobranch-like ancestor by specializing for sessilelife and feeding with tentacles and by final loss of the branchialbasket. Groups such as the tunicates, hemichordates and echinodermscould be eliminated as ancestral forms within the deuterostomecoelomates because the evolution of acraniates and vertebratesfrom each of these groups would involve the appearance of gillslits before the notochord and/or the evolution of a metamericcoelom from an oligomeric one, both of which are exceedinglyimprobable. Central to the methods used to establish the transformationseries of features and their direction of evolutionary change(Lesrichtung) are functional (mechanical) analysis and adaptiveinterpretation of features; hence, functional-adaptive analysesare an integral and essential part of the methodology of phylogeneticinvestigation.     

Cranial ontogeny in the direct-developing frog, Eleutherodactylus coqui (Anura: Leptodactylidae), analyzed using whole-mount immunohistochemistry.

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.(ABSTRACT TRUNCATED AT 250 WORDS)     

Physical Analysis of Tissue Mechanics in Amphibian Gastrulation

During morphogenesis, intercellular attachments constrain cellmobility so that embryonic tissues may (i) deform as solid sheetsof tightly bound cells, (ii) disperse to migrate as separatecells or (iii) flow as multicellular liquids (in which cellsremain aggregated yet can still slide past one another). Bymodelling deep germ layers as multicellular liquids in amphibiangastrulation, Davis and I have predicted, and then confirmedexperimentally, (i) the area-invariance of deep-germ-layer surfacetensions in vitro, (ii) spontaneous cell slippage in deformeddeep—germ—layer cell aggregates and (iii) correlationsof tissue surface tensions with tissue positioning in deep-germ-layercell-sorting and aggregate—fusion experiments. Liquid—tissueflow involves intercalations of interior cells into expandingtissue interfaces (or withdrawal of surface cells from shrinkingtissue interfaces). Tissue surface tensions are macroscopicreflections of the microscopic, tissue—specific adhesivedifferentials which direct these cell translocations. Such adhesivedifferentials may act independently of, or together with, activecell—shape changes, chemotaxis, contact guidance and/orhaptotaxis in controlling embryonic tissue rearrangements. Deepcell intercalations in vivo occur throughout amphibian gastrulation:during ectodermal epiboly; during marginal—zone extensionand convergence (and therefore blastopore closure); during mesodermalinvolution; and probably during the anterior spreading and axialextension (and therefore dorsal convergence) of involuted mesoderm.Tissue—surface—tension measurements may help determine(i) which of these cell—intercalation processes are activeand which are passive, (ii) the specific contributions of variousmicroscopic cell properties to the regulation of liquid—likegerm—layer assembly and (iii) similarities and differencesbetween in vitro and in vivo control mechanisms governing amphibiangastrulation.     

Studies on the vegetative life cycle of Chlamydomonas reinhardi Dangeard in synchronous culture II. Effects of chloramphenicol and cycloheximide on the length of cell cycle

Cells of Chlamydomonas reinhardi Dangeard were synchronouslygrown under a 12 hr light— 12 hr dark regime. When thesecells were brought into contact with chloramphenicol for a shortperiod at early stages in the cell cycle, zoospore liberationwas delayed for a period which was nearly the same as that ofthe duration of contact with the antibiotic. When given at laterstages, the antibiotic caused no such effect. Cycloheximide,on the other hand, caused—when provided at some intermediatestage of the cell cycle— two different prolonging effectson the length of the cell cycle: one doubled the normal length(observed when the drug was administered at certain stages)and the other caused a delay similar to that caused by chloramphenicol.Interestingly, no prolonging effect was observed when cycloheximidewas given either at early stages or at later stages, such asduring the last 1/4 period of the cell cycle preceding zoosporeliberation. Based on these results, three phases were distinguishedin the algal cell cycle: "chloramphenicolsensitive", "cycloheximide-sensitive"and "insensitive" phases. Considering the known facts aboutthe modes of action of the two antibiotics inhibiting proteinsynthesis, discussions were made on the significance of proteinsynthesis in chloroplasts and in cytoplasm in determining thelength of the cell cycle. (Received October 12, 1970; )     

Crocodylian Snouts in Space and Time: Phylogenetic Approaches Toward Adaptive Radiation

Recent phylogenetic analyses of fossil and living crocodyliansallow us to compare the taxonomic, geographic, and temporaldistributions of morphological features, such as snout shapes.A few basic snout morphotypes—generalized, blunt, slender,deep, and excessively broad ("duck-faced")—occur multipletimes in distantly-related lineages. Some clades—especiallythose found in the Northern Hemisphere or with minimum originationdates in the Cretaceous or lower Tertiary—are morphologicallyuniform, but geographically widespread; crocodylian faunas ofthe early Tertiary tend to be composite, with sympatric taxabeing distantly related, and similar-looking taxa on differentcontinents being close relatives. In contrast, crocodylian faunasof the later Tertiary tend to be more endemic, with local adaptiveradiations occurring in Africa and Australia containing membersof most basic snout shapes. Endemic radiations in Africa andAustralia have largely been replaced by Crocodylus, which canbe divided into subclades that may individually represent endemicadaptive radiations.     

Limb development in a "nonmodel" vertebrate, the direct-developing frog Eleutherodactylus coqui.

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 (Dlx) 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.     

Plant Growth-promoting Rhizobacteria and Soybean [ Glycine max (L.) Merr.] Growth and Physiology at Suboptimal Root Zone Temperatures

Application of plant growth-promoting rhizobacteria (PGPR) hasbeen shown to increase legume growth and development under optimaltemperature conditions, and specifically to increase nodulationand nitrogen fixation of soybean [Glycine max (L.) Merr.] overa range of root zone temperatures (RZTs). Nine rhizobacteriaapplied into soybean rooting media were tested for their abilityto reduce the negative effects of low RZT on soybean growthand development by improving the physiological status of theplant. Three RZTs were tested: 25, 17.5, and 15 °C. At eachtemperature some PGPR strains increased plant growth and development,but the stimulatory strains varied with temperature. The strainsthat were most stimulatory at each temperatures were as follows:15 °C—Serratia proteamaculans 1–102; 17.5 °C—Aeromonashydrophila P73, and 25 °C—Serratia liquefaciens 2–68.Because enhancement of plant physiological activities were detectedbefore the onset of nitrogen fixation, these stimulatory effectscan be attributed to direct stimulation of the plant by thePGPR rather than stimulation of plant growth via improvementof the nitrogen fixation symbiosis. Legume; nitrogen fixation; nodulation; root zone temperature; PGPR     

Requirements for Floral Induction in Contrasting White Clover (Trifolium repens) Populations

Norm, I. B. 1987. Requirements for floral induction in contrastingwhite clover (Trifolium repens) populations.—J. exp. Bot.38: 900–907. Floral initiation and development of four contrasting whiteclover (Trifolium repens) populations was examined after differentinduction treatments (16 h, 5 ?C and 8 h, 5 ?C. The number of reproductive stolons and of reproductive budsper stolon was increased after cold induction. Varietal differencesin response to daylength were large; some varieties respondingbetter to a long day cold period, others to a short day coldperiod while one variety required no induction at all. Whetherthe daylength effect was due to photoperiod, irradiance or totheir interaction was not known. The induction periods had a subsequent effect upon pedunclelength, floret and ovule number. Short days and chilling reducedpeduncle length but increased ovule number, whereas long daysand chilling tended to increase floret number. Nectar concentrationwas highest after short day induction. Key words: White clover, floral initiation, floral induction     

"I'll see it when I believe it!"*: Investigating Nervous System/Reproductive System Interactions in Animal Organisms

From the time of August Weismann's characterization of fundamentaldifferences between the role of the reproductive system (topreserve the "immortal" germplasm) and the other, somatic tissuesof the organism (to maintain the organism) biologists have inheritedan interesting organismic conundrum. How, indeed, are we tounderstand the relationship between the somatic systems (especiallythe nervous system—that characterize the animal organism)and the reproductive system, within that organism? In this paperit is argued that: (1) neuron-gamete-organism interactions areessential, organismic phenomena that have scarcely begun tobe investigated; (2) with reference to at least three differentkinds of animals it is possible to determine developmental,structural, functional and behavioral relationships betweenthe (species-oriented) reproductive systems, and the (individual,organism-oriented) nervous systems of those animals; and (3)results of such investigations make sense only in terms of thepeculiar evolutionary history and environmental adaptationsof specific kinds of animal organisms.     

Evolutionary history of vertebrate appendicular muscle

The evolutionary history of muscle development in the paired fins of teleost fish and the limbs of tetrapod vertebrates is still, to a large extent, uncertain. There has been a consensus, however, that in the vertebrate clade the ancestral mechanism of fin and limb muscle development involves the extension of epithelial tissues from the somite into the fin/limb bud. This mechanism has been documented in chondrichthyan, dipnoan, chondrostean and teleost fishes. It has also been assumed that in amniotes, in contrast, individual progenitor cells of muscles migrate from the somites into the limb buds. Neyt et al. now present the exciting finding that in zebrafishes this presumably derived mechanism involving individual cell migration, is present. They conclude, based on data on sharks, zebrafishes, chickens, quails and mice that the derived mechanism was present in the sarcopterygians. This conclusion, however, may be premature in the light of further data available in the literature, which show a highly mosaic distribution of this character in the vertebrate clade. Furthermore, a developmental mode exists that is intermediate between the supposed ancestral and derived modes in teleosts, reptiles and possibly amphibians.     

Segmentation of the vertebrate skull: neural-crest derivation of adult cartilages in the clawed frog, Xenopus laevis

We utilize a novel, transgenic cell-labeling system to assess the embryonic derivation of cartilages in the post-metamorphic skull of anuran amphibians. Many of these cartilages form de novo at metamorphosis and have no obvious precursors within the larval skeleton. Most adult cartilages are derived from mandibular- or hyoid-stream neural crest, either individually or in combination; branchial-stream neural crest makes a modest contribution. Each stream also contributes to at least one cartilage in the middle ear or external ear. Four cartilages are composite elements; each is derived from at least two distinct cell populations. Many boundaries between adjacent neural-crest territories are cryptic insofar as they do not coincide with anatomical boundaries. The system of adult cranial segmentation revealed by these fate-mapping results differs in important respects from both the segmentation of the ontogenetically earlier larval skull and the cranial segmentation in amniotes. Most striking is the rostral "inversion" of neural-crest-derived cartilages in Xenopus, such that mandibular stream-derived elements are deployed caudal to those derived from the hyoid stream, which predominate anteriorly. This novel pattern of rostral segmentation may be a consequence of the complex, biphasic life history that is characteristic of most species of living amphibians, and especially anurans, in which cranial architecture is significantly reconfigured at metamorphosis. Neural-crest derivation of the vertebrate skull is not invariant; instead, embryonic derivation of individual components of the cranial skeleton may vary widely among species.     

Kingdom animalia: The zoological malaise from a microbial perspective

Pain and cognitive dissonance abounds amongst biologists: theplant-animal, botany-zoology wound has nearly healed and thenew gash—revealed by department and budget reorganizations—is"molecular" vs. "organismic" biology. Here I contend that resolutionof these tensions within zoology requires that an autopoietic-gaianview replace a mechanical-neodarwinian perspective; in the interestof brevity and since many points have been discussed elsewhere,rather than develop detailed arguments I must make staccatostatements and refer to a burgeoning literature. The first centralconcept is that animals, all organisms developing from blastularembryos, evolved from single protist cells that were unableto reproduce their undulipodia. The second points to the usefulnessof recognizing the analogy between cyclically established symbiosesand meiotic sexuality