The evolution of protamine P1 genes in dasyurid marsupials

We report the complete DNA sequences of the protamine P1 gene and flanking regions for 13 species of the marsupial family Dasyuridae. The structure of the protamine locus is conserved in dasyurids and consists of two exons (of lengths 142–151 and 47 bp) separated by an intron (208–240 bp). A key feature of the dasyund intron is a 38–40 by duplication found in all species examined to date. This duplication apparently predates the radiation of modern dasyurid lineages and may be homologous to a similar feature in the marsupial mole (Notoryctes). Sequences from a species of Planigale demonstrate that this genus is unique among marsupials in possessing cysteine residues in its protamine P1 molecules. Cysteines may provide enhanced chemical stability for condensed sperm nuclei, a physiological feature that would converge on the common eutherian pattern. Phylogenetic analysis of the protamine genes yields a tree that is largely congruent with previous molecular systematic studies in two areas: (1) There are three main dasyurid lineages corresponding to the Sminthopsinae, Dasyurinae, and Phascogalinae; (2) Dasyurinae and Phascogalinae are sister groups. This study is the first estimate of dasyurid relationships based on a nuclear DNA sequence.Correspondence to: J.D. Retief     

Ontogeny, anatomy, and the problem of homology: Carl Gegenbaur and the American tradition of cell lineage studies

Summary In this paper we analyze Carl Gegenbaur’s conception of the relationship between embryology (“Ontogenie”) and comparative anatomy and his related ideas about homology. We argue that Gegenbaur’s conviction of the primacy of comparative anatomy and his careful consideration of caenogenesis led him to a more balanced view about the relationship between ontogeny and phylogeny than his good friend Ernst Haeckel. We also argue that Gegenbaur’s ideas about the centrality of comparative anatomy and his definitions of homology actually laid the conceptual foundations for Hans Spemann’s (1915) later analysis of homology. We also analyze Gegenbaur’s reception in the United States and how the discussions between E.B. Wilson and Edwin Conklin about the role of the “embryological criterion of homology” and the latter’s argument for an even earlier concept of cellular homology reflect the recurring theme of preformism in ontogeny, a theme that finds its modern equivalent in various genetic definitions of homology, only recently challenged by the emerging synthesis of evolutionary developmental biology. Finally, we conclude that Gegenbaur’s own careful methodological principles can serve as an important model for proponents of present day “evo-devo”, especially with respect to the integration of ontogeny with phylogeny embedded in comparative anatomy.     

Development of physiological regulatory systems: altering the timing of crucial events

There is currently tremendous interest in how the physiology of individual animals changes and develops during ontogeny. One of the key areas is the extent to which the timing and/or rate of physiological development is fixed within an individual and to what extent can it be altered. We propose that plasticity in the timing of the onset of a particular physiological regulatory system during an individuals development be referred to as physiological heterokairy (to clearly distinguish this phenomenon from physiological heterochrony, which is an evolutionary pattern), and we marshal evidence for three different patterns of heterokairy: 1. altering relative position in the physiological itinerary; 2. altering overall rate of development per se and; 3. a combination of 1 and 2. Using these patterns as a starting point, we develop a framework for investigating physiological heterokairy which takes cognizance of the facts that multiple components of each regulatory system could appear at different times and multiple regulatory systems could come 'on-line' at different times. We finish by placing physiological heterokairy in the wider context of its ecological and evolutionary implications and its relationship to physiological genomics and heterochrony.     

Heterochrony in Shell Sculpture Development within the Ostracode Genus Hemicythere

The evolutionary issues of taxonomic significance of the shell sculpture in Ostracoda are addressed. This is a comparative ontogenetic study of three types of lateral sculpture (fossa-mural reticulation, punctation, and foveolation), as well as flanges, ridges, and tubercles is made in different age stages and morphological variations of three ostracode species with different strengths of the expression of sculpture: Hemicythere borealis (Brady, 1868), H. villosa (Sars, 1866), and H. nana (Schornikov, 1974). It is shown that the development of each sculpture type proceeds relatively independently and represents a mosaic; developmental stages are accompanied by numerous heterochronies. This results in many parallelisms, and even the trend of the evolution of a structure can change. The pathways of morphological evolution of Hemicythere species are discussed.     

Gene mapping in marsupials and monotremes. II. Assignments to the X chromosome of dasyurid marsupials

Somatic cell hybrids have been obtained between HPRT Chinese hamster cells and cells from several dasyurid marsupial species. These hybrids show the extensive loss of marsupial chromosomes characteristic of the majority of marsupial-eutherian somatic cell hybrids. Although all of the hybrids expressed the selected marsupial marker, HPRT, the only other markers observed were PGK, GLA, and G6PD, consistent with the conservation of X-linked genes extending to this major group of marsupials. Counterselection confirmed the synteny of PGK and GLA with HPRT, whereas G6PD showed decreased concordance.     

Coming of age in fringillid birds: heterochrony in the ontogeny of secondary sexual characters

The great variation in the timing of development of adult plumages in North American male passerine birds has in recent years provoked much theoretical interest. It has commonly been assumed that the heterochronic process involved is invariably a retardation of the development of adult plumages. On the basis of a phylogenetic analysis of the nine-primaried oscines (Fringillidae), I suggest that the heterochronic process that has operated most frequently in North American taxa is not a retardation, but an acceleration. I also suggest that sexual dimorphism in plumage, and late plumage maturation in males, may arise as a secondary result of selection for neoteny in females with a correlated response in males, and not necessarily, as traditionally thought, as a result of selection for bright plumages in males.     

Phylogenetic analysis of cytochromeb sequences in the dasyurid marsupial subfamily phascogalinae: Systematics and the evolution of reproductive strategies

We report DNA sequence variation in 861 bp of the mitochondrial cytochromeb gene from 10 species of the dasyurid marsupial subfamily Phascogalinae (including the New Guinean genusMurexia) and an outgroup planigale (Planigale ingrami). Phylogenetic analyses of these sequences indicate that (1) the subfamily consists of three major clades corresponding to (a)Phascogale, (b) AustralianAntechinus, and (c) New Guinean Antechinus andMurexia; (2) Antechinus habbema constitutes the earliest branch of the New Guinean clade; and (3); Antechinus melanurus and A. naso are sister species within the New Guinean clade. Among Australian antechnuses,A. stuartii andA. swainsonii are more closely related to each other than either is toA. flavipes, a result that is seemingly at odds with all previous systematic studies. Although resolution is limited, it appears thatAntechnius andMurexia species form a clade to the exclusion ofPhascogale. This relationship suggests that male semelparity is not a strong synapomorphy for Australian antechinuses and phascogales, despite its apparent physiological similarity in the two groups.To whom correspondence should be addressed.     

Innervation of the human upper primary dentition: Implications for understanding tooth initiation and rethinking growth and eruption patterns

Recent comparisons of humans with apes and early fossil hominids have prompted renewed interest in the study of sequences of dental growth and development. Such comparisons, however, rely on certain assumptions about tooth development and dental homology and the biological reality of distinguishing “deciduous” from “permanent” teeth. In light of earlier suggestions by Schwartz that there might be a correlation between nerves and the stem progenitors of tooth classes, and thus between nerve branch number and number of tooth classes, we studied a large sample of ～ 3 month fetuses to elucidate the nature of nerve branching patterns and the development of the primary dentition (i.e., the “deciduous” incisors, canine, and molars, and the first “permanent” molar). Contrary to expectation, variation in nerve branch patterning was the rule. If nerve fibers do have a role in tooth development, it can only be at the time of initiation, with definitive innervation occurring late in tooth development. In taking into consideration the entire span of tooth development—from initiation to innervation to eruption—and the process by which successional teeth arise (each from the external dental epithelium of a predecessor tooth), we suggest that dividing tooth growth and eruption into patterns of the “deciduous” teeth vs. those of the “permanent” is artificial and that a more meaningful approach would be the study of the entire dentition.     

Shape, variance and integration during craniogenesis: contrasting marsupial and placental mammals

Studies of morphological integration can provide insight into developmental patterns, even in extinct taxa known only from skeletal remains, thus making them an important tool for studies of evolutionary development. However, interpreting patterns of integration and assessing their significance for organismal evolution requires detailed understanding of the developmental interactions that shape integration and how those interactions change through ontogeny. Thus far, relatively little comparative data have been produced for this important topic, and the data that do exist are overwhelmingly from humans and their close relatives or from laboratory models such as mice. Here, we compare data on shape, variance and integration through postnatal ontogeny for a placental mammal, the least shrew, Cryptotis parva, and a marsupial mammal, the gray short-tailed opossum, Monodelphis domestica. Cranial variance decreased dramatically from early to late ontogeny in Cryptotis, but remained stable through ontogeny in Monodelphis, potentially reflecting functional constraints related to the short gestation and early ossification of oral bones in marsupials. Both Cryptotis and Monodelphis showed significant changes in cranial integration through ontogeny, with a mixture of increased, decreased and stable levels of integration in different cranial regions. Of particular note is that Monodelphis showed an unambiguous decrease in integration of the oral region through ontogeny, potentially relating to their early ossification. Selection at different stages of development may have markedly different effects if patterns of integration change substantially through ontogeny. Our results suggest that high integration of the oral region combined with functional constraints for suckling during early postnatal ontogeny may drive the stagnant variance observed in Monodelphis and potentially other marsupials.     

The morphology and evolution of the ventral gill arch skeleton in batoid fishes (Chondrichthyes: Batoidea)

The ventral gill arch skeleton was examined in some representatives of batoid fishes. The homology of the components was elucidated by comparing similarities and differences among the components of the ventral gill arches in chondrichthyans, and attempts were made to justify the homology by giving causal mechanisms of chondrogenesis associated with the ventral gill arch skeleton. The ceratohyal is present in some batoid fishes, and its functional replacement, the pseudohyal, seems incomplete in most groups of batoid fishes, except in stingrays. The medial fusion of the pseudohyal with successive ceratobranchials occurs to varying degrees among stingray groups. The ankylosis between the last two ceratobranchials occurs uniquely in stingrays, and it serves as part of the insertion of the last pair of coracobranchialis muscles. The basihyal is possibly independently lost in electric rays, the stingray genus Urotrygon (except U. daviesi) and pelagic myiiobatoid stingrays. The first hypobranchial is oriented anteriorly or anteromedially, and it varies in shape and size among batoid fishes. It is represented by rami projecting posterolaterally from the basihyal in sawfishes, guitarfishes and skates. It consists of a small piece of cartilage which extends anteromedially from the medial end of the first ccratobranchial in electric rays. It is a large cartilaginous plate in most of stingrays. It is absent in pelagic myliobatoid stingrays. The remaining hypobranchial cartilages also vary in shape and size among batoid fishes. Torpedo and possibly the Jurassic Belemnobalis and Spathobatis possess the generalized or typical chondrichthyan ventral gill arch structure in which the hypobranchials form a Σ-shaped pattern. In the electric ray Hypnos and narkinidid and narcinidid electric rays, the hypobranchial components are oriented longitudinally along the mid-portion of the ventral gill arches. They form a single cartilaginous plate in the narkinidid electric rays, Narcine and Diplobatis. In guitarfishes and skates, the second hypobranchial is unspecialized, and in skates, it does not have a direct contact with the second ceratobranchial. In both groups, the third and fourth hypobranchials are composed of a small cartilage which forms a passage for the afferent branches of the ventral aorta and serve as part of the insertion of the coracobranchialis muscle. In sawfishes and stingrays, the hypobranchials appear to be included in the medial plate. In sawfishes, the second and third components separately chondrify in adults, but the fourth component appears to be fused with the middle medial plate. In stingrays, a large medial plate appears to include the second through to the last hypobranchial and most of the basibranchial copulae. The medial plate probably develops independently in sawfishes and stingrays. Because the last basibranchial copula appears to be a composite of one to two hypobranchials and at least two basibranchial copulae, the medial plate may be formed by several developmental processes of chondrogenesis. More detailed comparative anatomical and developmental studies are needed to unveil morphogenesis and patternings of the ventral gill arch skeleton in batoid fishes.     

Comparative studies of epididymal morphology and sperm distribution in dasyurid marsupials during the breeding season

The structural features of the epididymis and the number and distribution of spermatozoa along the duct, during the breeding season, were examined in two semelparous and three iteroparous dasyurid marsupials. Total numbers of epididymal spermatozoa were extremely low in all of these species when compared with epididymal sperm numbers in most other marsupials and eutherian mammals. Although semelparous dasyurids had significantly more epididymal spermatozoa than itcroparous species, very few spermatozoa were seen in the distal cauda epididymidis of any of the species examined. This coincided with distinct changes in duct shape and the surface area of the lumen in caudal regions which resulted in a reduced sperm storage capacity in the cauda epididymidis of these species. The data suggest that, like Antechinus stuartii (Taggart & Temple-Smith, 1990a), sperm content of the ejaculates in these species will be extremely low, and that sperm motility and/or transport in the female tract is highly efficient. The functional and evolutionary significance of the reproductive strategies of semelparous and iteroparous dasyurid marsupials is still obscure and further study is needed to determine if the length of sperm storage in the female and sperm competition for storage sites is related to sperm distribution in the male and mating activities. This study does, however, clearly indicate that large numbers of spermatozoa are not required to ensure successful fertilization in either semelparous or iteroparous members of the family Dasyuridae.     

Ontogeny and phylogeny in temnospondyls: a new method of analysis

A new method has been devised to compare the ontogeny and phylogeny of some of the better documented tetrapods from the Stephanian to the Trias. This approach is based on global parsimony analysis of several temnospondyl amphibians, in which some ontogenetic sequences have been highlighted. Forty-one homologous morphoanatomical character states have been separated into larval, juvenile and adult stages of each of six tetrapod species. The taxonomic congruence (TC) approach involves comparing trees based on larval, juvenile and adult character states. These so-called 'ontotrees' are not congruent, either in their topologies or in the distribution of the character states. The total evidence (TE) approach involves a combined analysis of all the character states observed in the various growth stages of the taxa, and is secondarily used in order to test this taxonomic incongruence. In this case, the TE result corroborates the TC analysis: the TE tree is robust and reveals a few homoplasies which cause the taxonomic incongruence. This is interpreted as either the result of heterochronic events in temnospondyl evolution, or as the product of inaccurate identification of larval and metamorphic fossil forms.     

Conservation of chromosomal location of nucleolus organizer in American marsupials (Didelphidae)

The distribution and expression of nucleolus organizer regions (NORs) were analyzed in seven species of marsupials representative of the three karyotypes (2n = 14, 18 and 22) found in the American family Didelphidae. Analyses comprised silver-staining of NORs and fluorescence in situ hybridization with an rDNA probe. In addition to confirming the variability in number and distribution of NORs in Didelphidae, we demonstrated the conserved location of NORs on one autosome pair in the three karyotypes. In Monodelphis domestica (2n = 18), the NOR on the X chromosome was not inactivated in females.     

Patterns of tooth size variability in the dentition of primates

Published data on tooth size in 48 species of non-human primates have been analyzed to determine patterns of variability in the primate dentition. Average coefficients of variation calculated for all species, with males and females combined, are greatest for teeth in the canine region. Incisors tend to be somewhat less variable, and cheek teeth are the least variable. Removing the effect of sexual dimorphism, by pooling coefficients of variation calculated for males and females separately, reduces canine variability but does not alter the basic pattern. Ontogenetic development and position in functional fields have been advanced to explain patterns of variability in the dentition, but neither of these appears to correlate well with patterns documented here. We tentatively suggest another explanation. Variability is inversely proportional to occlusal complexity of the teeth. This suggests that occlusal complexity places an important constraint on relative variability within the dentition. Even when the intensity of natural selection is equal at all tooth positions, teeth with complex occlusal patterns must still be less variable than those with simple occlusion in order to function equally well. Hence variability itself cannot be used to estimate the relative intensity of selection. Low variability of the central cheek teeth ( \documentclass{article}\pagestyle{empty}\begin{document}$ \mathop {\rm M}\frac{1}{1} $\end{document} and \documentclass{article}\pagestyle{empty}\begin{document}$ \mathop {\rm M}\frac{2}{2} $\end{document}) makes them uniquely important for estimating body size in small samples, and for distinguishing closely related species in the fossil record.