The evolution of cranial design and performance in squamates: Consequences of skull-bone reduction on feeding behavior

The evolution of cranial design in lepidosaurians is characterizedby a general trend toward the loss of cranial elements. Theevolution of relatively lighter skulls in squamates appearstightly coupled to a reduction in relative mass of the jaw adductor,implying functional consequences for bite force and feedingbehavior. Interestingly, among squamates the postorbital barwas reduced or lost at least twice independently and taxa characterizedby the loss of these cranial elements (e.g., geckos and varanids)are generally reported as having a mobile skull. In Gekkotans,the loss of the postorbital bar was accompanied by a reductionof the supratemporal bar, resulting in a pronounced cranialkinesis. Our data show that having a kinetic skull has functionalconsequences and results in a reduction in bite force. The lowerbite force may in turn be responsible for the decreased feedingefficiency as reflected in the longer duration of intra-oraltransport cycles. Gekkotans, however, appear to exploit theirintracranial mobility in ways that increases the velocity ofjaw movement during opening and closing, which may allow themto capture more elusive prey. The morphological changes observedin the evolution of the cranial system in squamates appear tightlylinked to functional and constructional demands on the skull,making squamate skull evolution a model system to investigatethe consequences of morphological changes in a complex integratedsystem of performance, behavior, and ecology.     

The evolution of cranial design, diet, and feeding mechanisms in batoid fishes

The batoid fishes (electric rays, sawfishes, skates, guitarfishes,and stingrays) are a trophically and morphologically diverseclade in which the observed range of diets is a product of afeeding mechanism with few parts and therefore a limited numberof functional interactions. This system allows an intriguingcomparison to the complex network of associations in the feedingapparatus of bony fishes and an anatomically simple frameworkfor investigations of the mechanisms underlying the evolutionof functional and phenotypic diversity. We quantified morphologyfrom reconstructed CT scans of 40 batoid species, representingmore than half of the extant genera. We used pairwise comparisonsto evaluate the extent of coevolution among components of thefeeding apparatus and among morphologies and diets. These relationshipswere then used to predict diets in poorly studied taxa and ina reconstruction of the batoid ancestor. Although functionallythere are fewer examples of convergence in the batoid feedingmechanism than in bony fishes, our data show multiple evolutionsof similar dietary compositions underlain by a broad morphologicaldiversity. Elements of the feeding apparatus evolved independentlyof one another, suggesting that decoupling components of thehead skeleton created separate but interacting evolutionarymodules that allowed trophic diversification. Our data implythat food habits exhibit strong independent and convergent evolutionand that suites of morphologies are associated with certaindiets; however, lack of behavioral data for this clade, andone example of divergent diets underlain by convergent morphology,caution against the assumption of simplistic relationships betweenform and function. We therefore urge future work to ground truthour study by testing the functional, dietary and evolutionaryhypotheses suggested by our data.     

EGF receptor signaling: putting a new spin on eye development

The coordinated polarization of cells within an epithelium is required for the development and function of some tissues. Recent work has shown that the EGF receptor signaling pathway plays a key role in establishing epithelial polarity in the compound eye of Drosophila.     

The comparative morphology and evolution of the eyes of caecilians (Amphibia,Gymnophiona)

Summary Caecilians (Amphibia, Gymnophiona) have been reported to have vestigial eyes, to lack some or all of the extrinsic eye muscles and their nerves, and to utilize eye muscles and glands, or derivatives of them, to effect movement of the tentacle, a chemosensory structure unique among vertebrates. Morphological evidence indicates that the eye is a functional photoreceptor in virtually all species examined, with an intact retina and optic nerve. The pattern of retention of extrinsic muscles varies. The ontogeny of the eye of Dermophis mexicanus is typical of that of most vertebrates, though components of accommodation never develop. Several taxa are reported in the literature to lack various eye structures; the present study reveals them to be variously present. Evolutionary trends in caecilian eye morphology include the following: (1) the eye is overlain by thicker, often glandular skin, to overlain by bone as well as skin; (2) extrinsic muscles become attenuate, and some to all may be lost; (3) the retina has the typical vertebrate layered organization, to having a reduced cell number, to becoming net-like rather than stratal; (4) the optic nerve is present, becoming attenuate, perhaps represented only by glial cells; (5) the lens is round (aquatic forms, larval and adult) to spheroid; lens crystalline to cellular (retention of the embryonic condition) to amorphous to absent; (6) the vitreous body is reduced or lost; (7) the cornea adheres to the overlying dermis or periosteum; the lens is free to adherent to cornea to adherent to both cornea and retina. Scolecomorphids have the eye pulled out of the socket and embedded in the tentacle under the skin of the upper jaw. This pattern of trends in eye reduction is similar to that observed in other vertebrate lineages that are fossorial or troglobitic.     

Deja vu: the evolution of feeding morphologies in the Carnivora

The fossil record of the order Carnivora extends back at least60 million years and documents a remarkable history of adaptiveradiation characterized by the repeated, independent evolutionof similar feeding morphologies in distinct clades. Within theorder, convergence is apparent in the iterative appearance ofa variety of ecomorphs, including cat-like, hyena-like, andwolf-like hypercarnivores, as well as a variety of less carnivorousforms, such as foxes, raccoons, and ursids. The iteration ofsimilar forms has multiple causes. First, there are a limitednumber of ways to ecologically partition the carnivore niche,and second, the material properties of animal tissues (muscle,skin, bone) have not changed over the Cenozoic. Consequently,similar craniodental adaptations for feeding on different proportionsof animal versus plant tissues evolve repeatedly. The extentof convergence in craniodental form can be striking, affectingskull proportions and overall shape, as well as dental morphology.The tendency to evolve highly convergent ecomorphs is most apparentamong feeding extremes, such as sabertooths and bone-crackerswhere performance requirements tend to be more acute. A surveyof the fossil record indicates that large hypercarnivores evolvefrequently, often in response to ecological opportunity affordedby the decline or extinction of previously dominant hypercarnivoroustaxa. While the evolution of large size and carnivory may befavored at the individual level, it can lead to a macroevolutionaryratchet, wherein dietary specialization and reduced populationdensities result in a greater vulnerability to extinction. Asa result of these opposing forces, the fossil record of Carnivorais dominated by successive clades of hypercarnivores that diversifyand decline, only to be replaced by new hypercarnivorous clades.This has produced a marvelous set of natural experiments inthe evolution of similar ecomorphs, each of which start fromphylogenetically and morphologically unique positions.     

Begging signals in a mobile feeding system: the evolution of different call types

In some species, dependent offspring join foraging providers and beg for food. Mobile offspring might benefit from evolving begging signals adapted to the different situations they are exposed to, but this possibility has been ignored. In cooperatively breeding meerkats (Suricata suricatta), dependent offspring use a repertoire of several begging calls when joining foraging adults. We found that these calls can be differentiated on the basis of their acoustic structure and that pups adjusted the use of specific call types according to the social context. Pups continuously gave "repeat" calls when they accompanied foraging adults, and playback of these calls increased provisioning by the adults. When pups saw adults with food, they switched from repeat calls to vigorous "high-pitched" calls; adults also preferred to "feed" loudspeakers broadcasting high-pitched calls rather then loudspeakers broadcasting repeat calls. The elaboration of different begging calls might reflect an adaptation to a situation where dependent young must solicit food from potential feeders while at the same time directing feeders to bring the prey item to themselves and not to another begging pup. Here we show that mobile but dependent offspring adapt to different contexts in a mobile feeding system by using a repertoire of begging calls.     

Rotational correlation times and partition coefficients of a spin label solute in lecithin vesicles

Di-tert-butylnitroxide dissolved in an aqueous suspension of egg yolk lecithin vesicles is distributed between the two phases. Partition coefficients of the nitroxide between the lipid and the water, calculated from the nitroxide electron paramagnetic resonance (EPR) spectra, decrease with decreasing temperature until approximately the freezing point of the solvent. Below this temperature the nitroxide is detected only in the lecithin. The rotational correlation times of the spin label present in the lecithin were calculated for the temperature range from +45 to ?60 °C. At low temperatures, the EPR spectra are characteristic of a superposition of two spectra resulting from the nitroxide dissolved in the lipid in two environments with different rotational correlation times.     

Rotational diffusion and intermolecular collisions of a spin labeled alpha-helical peptide determined by electron spin echo spectroscopy.

Short peptides that are composed mainly of alanine have recently been shown to form alpha-helices in aqueous solution at low temperature (Marqusee, S., and R. L. Baldwin. 1987. Proc. Natl. Acad. Sci. 84:8898-8902; Marqusee, S., V. H. Robbins, and R. L. Baldwin. 1989. Proc. Natl. Acad. Sci. USA. 86:5286-5290). These peptides are excellent models for probing structure and dynamics in isolated helical domains. In previous work we have designed and synthesized spin labeled analogs of these helix-forming peptides and we have shown that these analogs retain the folding characteristics of the parent peptide (Todd, A. P., and G. L. Millhauser. 1991. Biochemistry. 30:5515-5523). Using conventional continuous wave electron spin resonance (CW ESR) we have further shown that local motion is more pronounced near the helix amino terminus than in the central region as the peptide is thermally unfolded (Miick, S. M., A. P. Todd, and G. L. Millhauser. 1991. Biochemistry. 30:9498-9503). In this present work we use electron spin echo (ESE) spectroscopy to further refine our understanding of the solution dynamics of the 3K-8 peptide, which is a 16-mer with a nitroxide spin label attached at position 8. We find that the spin echo decays are well described by a single exponential function and that the determined correlation times are close to those previously derived from CW experiments. Variable concentration ESE experiments have directly revealed Heisenberg spin exchange (HSE) interactions and we find that the interpeptide collision rate is near to that expected for a free species in solution.(ABSTRACT TRUNCATED AT 250 WORDS)     

Rotational correlation times and partition coefficients of a spin label solute in lecithin vesicles.

Di-tert-butylnitroxide dissolved in an aqueous suspension of egg yolk lecithin vesicles is distributed between the two phases. Partition coefficients of the nitroxide between the lipid and the water, calculated from the nitroxide electron paramagnetic resonance (EPR) spectra, decrease with decreasing temperature until approximately the freezing point of the solvent. Below this temperature the nitroxide is detected only in the lecithin. The rotational correlation times of the spin label present in the lecithin were calculated for the temperature range from +45 to -60 degrees C. At low temperatures, the EPR spectra are characteristic of a superposition of two spectra resulting from the nitroxide dissolved in the lipid in two environments with different rotational correlation times.     

Functional evolution of the feeding system in rodents

The masticatory musculature of rodents has evolved to enable both gnawing at the incisors and chewing at the molars. In particular, the masseter muscle is highly specialised, having extended anteriorly to originate from the rostrum. All living rodents have achieved this masseteric expansion in one of three ways, known as the sciuromorph, hystricomorph and myomorph conditions. Here, we used finite element analysis (FEA) to investigate the biomechanical implications of these three morphologies, in a squirrel, guinea pig and rat. In particular, we wished to determine whether each of the three morphologies is better adapted for either gnawing or chewing. Results show that squirrels are more efficient at muscle-bite force transmission during incisor gnawing than guinea pigs, and that guinea pigs are more efficient at molar chewing than squirrels. This matches the known diet of nuts and seeds that squirrels gnaw, and of grasses that guinea pigs grind down with their molars. Surprisingly, results also indicate that rats are more efficient as well as more versatile feeders than both the squirrel and guinea pig. There seems to be no compromise in biting efficiency to accommodate the wider range of foodstuffs and the more general feeding behaviour adopted by rats. Our results show that the morphology of the skull and masticatory muscles have allowed squirrels to specialise as gnawers and guinea pigs as chewers, but that rats are high-performance generalists, which helps explain their overwhelming success as a group.     

Mitochondrial evidence on the phylogenetic position of caecilians (Amphibia: Gymnophiona)

The complete nucleotide sequence (17,005 bp) of the mitochondrial genome of the caecilian Typhlonectes natans (Gymnophiona, Amphibia) was determined. This molecule is characterized by two distinctive genomic features: there are seven large 109-bp tandem repeats in the control region, and the sequence for the putative origin of replication of the L strand can potentially fold into two alternative secondary structures (one including part of the tRNA(Cys)). The new sequence data were used to assess the phylogenetic position of caecilians and to gain insights into the origin of living amphibians (frogs, salamanders, and caecilians). Phylogenetic analyses of two data sets-one combining protein-coding genes and the other combining tRNA genes-strongly supported a caecilian + frog clade and, hence, monophyly of modern amphibians. These two data sets could not further resolve relationships among the coelacanth, lungfishes, and tetrapods, but strongly supported diapsid affinities of turtles. Phylogenetic relationships among a larger set of species of frogs, salamanders, and caecilians were estimated with a mitochondrial rRNA data set. Maximum parsimony analysis of this latter data set also recovered monophyly of living amphibians and favored a frog + salamander (Batrachia) relationship. However, bootstrap support was only moderate at these nodes. This is likely due to an extensive among-site rate heterogeneity in the rRNA data set and the narrow window of time in which the three main groups of living amphibians were originated.     

Actin cytoskeleton: putting a CAP on actin polymerization

Two recent studies have identified a Drosophila homolog of cyclase-associated protein (CAP) as a developmentally important negative regulator of actin polymerization that may also directly mediate signal transduction.     

Variation in the trunk musculature of caecilians (Amphibia: Gymnophiona)

Variation in the trunk musculature of 28 species of caecilians. representing 24 of the 33 genera and all five families. is summarized. All forms examined have the same muscles in similar positions. Existing variation largely conforms to the current classification of the group. and some variation may be attributable to different modes of locomotion. such as burrowing versus swimming. Caecilian trunk musculature is more similar to that of salamanders than to that of frogs. but the similarity is probably syrnplesiomorphous. Trunk musculature so far has provided no clues to lissamphibian relationships.     

The evolution of the dicynodont feeding system

The skull structure of dicynodonts may be regarded as a complex adaptation towards herbivorous feeding. The present work examines how and why this adaptation may have evolved. A cladogram of the dicynodonts is presented and from it a sequence of hypothetical ancestral forms is inferred. The jaw musculature of dicynodonts and other therapsids is described and in particular the early dicynodont Eodicynodon oosthuizeni is described in detail. This information is used to draw up a sequence of ancestral stages whose basic skull anatomy, jaw muscle organization and masticatory properties are described. Differences in masticatory properties between these stages are pinpointed and an explanation to account for the development of these differences is advanced. It is concluded that the changes in skull organization seen during the evolution of dicynodonts are consistent with the hypothesis that a propalinal jaw action was being improved by selection, and that this was required to permit dicynodonts to be efficient herbivores.     

Microbial biogeography: putting microorganisms on the map

We review the biogeography of microorganisms in light of the biogeography of macroorganisms. A large body of research supports the idea that free-living microbial taxa exhibit biogeographic patterns. Current evidence confirms that, as proposed by the Baas-Becking hypothesis, 'the environment selects' and is, in part, responsible for spatial variation in microbial diversity. However, recent studies also dispute the idea that 'everything is everywhere'. We also consider how the processes that generate and maintain biogeographic patterns in macroorganisms could operate in the microbial world.