Development of the cypriniform protrusible jaw complex in Danio rerio: Constructional insights for evolution

Studies on the evolution of complex biological systems are difficult because the construction of these traits cannot be observed during the course of evolution. Complex traits are defined as consisting of multiple elements, often of differing embryological origins, with multiple linkages integrated to form a single functional unit. An example of a complex system is the cypriniform oral jaw apparatus. Cypriniform fishes possess an upper jaw characterized by premaxillary protrusion during feeding. Cypriniforms effect protrusion via the kinethmoid, a synapomorphy for the order. The kinethmoid is a sesamoid ossification suspended by ligaments attaching to the premaxillae, maxillae, palatines, and neurocranium. Upon mouth opening, the kinethmoid rotates as the premaxillae move anteriorly. Along with bony and ligamentous elements, there are three divisions of the adductor mandibulae that render this system functional. It is unclear how cypriniform jaws evolved because although the evolution of sesamoid elements is common, the incorporation of the kinethmoid into the protrusible jaw results in a function that is atypical for sesamoids. Developmental studies can show how biological systems are assembled within individuals and offer clues about how traits might have been constructed during evolution. We investigated the development of the protrusible upper jaw in zebrafish to generate hypotheses regarding the evolution of this character. Early in development, the adductor mandibulae arises as a single unit. The muscle divides after ossification of the maxillae, on which the A1 division will ultimately insert. A cartilaginous kinethmoid first develops within the intermaxillary ligament; it later ossifies at points of ligamentous attachment. We combine our structural developmental data with published kinematic data at key developmental stages and discuss potential functional advantages in possessing even the earliest stages of a system for protrusion. J. Morphol. 2010. © 2010 Wiley‐Liss, Inc.     

Development and evolution of melanophore patterns in fishes of the genus Danio (Teleostei: Cyprinidae)

Pigmentation patterns in vertebrates have become an important model for those interested in mechanisms of pattern determination. I present detailed information on the development of melanophore patterns in the zebrafish, Danio rerio, five close relatives of that species, and an outgroup. The comparison of the ontogeny of melanophore patterns in this group is an important first step towards understanding the developmental basis of the interspecific variation. Pigment patterns in this group range from no distinct patterning at all to stripes of differing numbers and widths to reticulated stripes. Species examined form identical larval patterns and follow a common sequence of events from which different elements are eliminated or altered to produce the variety of patterns seen in the group. As flexion is completed, melanophores move from larval positions onto the flanks of the fish. In D. rerio, D. rerio ‘leo,’ D. kerri, and D. malabaricus, xanthophores become established on the body of the fish as the melanophores move; erythrophores become established on the flanks of D. albolineatus and D. sp. cf. aequipinnatus. An increase in melanophore number, begun at this time, continues at a higher rate in D. rerio, D. kerri, D. sp. cf. aequipinnatus and Tanichthys albonubes than in the other three species. This results in a greater number of melanophores on adults in those species with a higher rate of melanophore increase. No distinct pattern forms, except on the caudal peduncle, in D. albolineatus. In all other Danio species, melanophore stripes form first below then above the horizontal myoseptum. Additional stripes are added first below then above these initial two stripes. D. kerri develops fewer, wider melanophore stripes than D. rerio. After initial stripe formation, D. malabaricus and D. sp. cf. aequipinnatus both developed vertical pattern elements and reticulations in the melanophore pattern. Differences in patterns between species are similar in several cases to described mutants of the zebrafish, suggesting that some aspects of interspecific pigmentation pattern variation may be under relatively simple genetic control. J. Morphol. 241:83–105, 1999. © 1999 Wiley‐Liss, Inc.     

Heterochrony of the ostracod hingement and its significance for taxonomy

The hingement of cytheracean ostracods is a very significant character for taxonomy. In some taxa, adult hinge characters develop abruptly at the last moult, whilst in others no significant change of hingement is observed throughout ontogeny. These two types of hinge development are regarded to as 'leap type' and 'gradual type', respectively. In the five major cytheracean families examined, heterochronic relationships were detected in 11 pairs, i.e. in each family, the adult hinge character of the gradual-type taxon corresponds to the A-1 hingement of the leap-type taxon. Furthermore, these 11 heterochronic pairs can be classified into two categories. The first are 'complete pairs', in which the adult hinge character of gradual-type taxa can be almost completely identified in the A-1 of the counterpart leap-type taxa. The second group are 'incomplete pairs', in which the relationship is not so complete. Palaeontological evidence indicates that in most cases the heterochronic evolution is characterized by paedomorphosis, because the leap type always has the older fossil record than the gradual type in each pair. Most of the gradual-type species of complete pairs originated in the Miocene, while all the gradual-type species of incomplete pairs appeared in and after the Pleistocene. Heterochronic changes must occur universally in the cytheracean ostracods, but the degree of completeness of the heterochronic pair seems to be related to the age of speciation.     

School Formation and Concurrent Developmental Changes in Carangid Fish with Reference to Dietary Conditions

The ontogeny of schooling behaviour was studied in comparison to the development of sensory and swimming organs and taxis in carangid fish. Striped jack, Pseudocaranx dentex, larvae showed strong phototaxis at 3 days after hatching (3.5 mm in TL) when they developed pigmentation in the retina. Rheotaxis and optokinetic responses were apparent at 4.0-6.0 mm TL as larvae completed development of the basic structure of their eyes. A major inflection of allometric growth occurred at 9 mm, and fin ray formation was completed at these stages. Schooling behaviour, represented by one TL of inter-individual distance and parallel orientation, only appeared at 16 mm TL, and just prior to this behaviour, fish showed mutual attraction through vision at 12 mm TL. Canalization of buccal lateral lines was complete at 18 mm TL, whereas that of trunk lateral lines started at 23 mm TL and was complete at 30 mm TL. With these results, we assumed that critical factors of the ontogeny of schooling behaviour in carangid fish include not only the development of sensory or swimming organs, but also other factors such as development of the central nervous system. To show this, we reared another carangid species, the yellowtail Seriola quinqueradiata, with dietary depletion of DHA (docosahexaenoic acid), which is indispensable for the development of the central nervous system. Although DHA-free fish showed optokinetic response, they did not show schooling behaviour when they attained their schooling size. Tracer experiments using radioisotope labelled DHA showed that DHA is incorporated into the brain, spinal cord, and retina of juvenile fish. Under natural conditions, carangid fish larvae should intake enough DHA through diet to develop schooling behaviour, the fluctuation of dietary quality in zooplankton might therefore influence the development of indispensable antipredatory behaviour. Morphological changes of striped jack occurred in two steps; first at 9-12 mm (fin formation and inflection of allometric growth) and then second at 20-30 mm (scale and lateral line formation), and these changes corresponded with the development of schooling and recruitment to coastal waters, respectively. Since the onset of schooling is the first step of active antipredatory behaviour, we considered that 12 mm TL is the size at which they attain the juvenile period.     

Speciation within blidingia minima (chlorophyta) in japan: evidence from morphology, ontogeny, and analyses of nuclear rdna its sequence

The genus Blidingia is a common, sometimes abundant, component of northern hemisphere temperate and subarctic shores. Species determination relies on characteristic differences in morphology and early ontogenic development. Within the species Blidingia minima (Naegeli ex Kuetzing) Kylin in Japan, however, there appear to be three distinct types, the F-, D-, and M-types, which are differentiated in early ontogeny. The M-type can be further categorized into three subtypes. Results of intensive field and culture studies supported the view that morphological characteristics do not reliably separate the F-, D-, and M-types and that all three may potentially cross breed. The F-type has characteristics in early ontogeny of the species B. chadefaudii (  J. Feldmann) Bliding in European waters and this, combined with the morphological and cross breeding studies, suggest that B. chadefaudii should be merged with B. minima. In this study, molecular analyses of nuclear rDNA from samples of the F- and D-types indicated that both have a distinctive and characteristic identity. Sequence data also examined from two of the M-type subtypes indicated that each of these also has a characteristic molecular identity clearly distinguished from that of the F- and D-types. Analyses indicated that there is a close relationship between the D-type and one of the M-type subtypes, and that these are more closely related to the F-type than to the other M-type examined. Comparison with studies of this gene region in other ulvophytic algae indicated a wide range of variation within B. minima. Such variation may be useful in assessing distribution patterns in Japanese waters of the developmental types within this species.     

Polymorphic segregation in Arctic charr Salvelinus alpinus (L.) from Vatnshlidarvatn, a shallow Icelandic lake

We studied the salmonid fish Arctic charr, Salvelinus alpinus , in a small and shallow landlocked lake in NW Iceland. The lake is productive but die only fish present is Arctic charr. Despite the apparent absence of discrete benthic and limnetic habitats for fish, two forms of Arctic charr are found in the lake. They show subde differences in morphology related to swimming performance and manoeuvrability, but differences in life history such as growth, and age and size at sexual maturation are more pronounced. Both forms have benthic feeding habits with one form consuming greater number of species than the other. We suggest that the segregation of these forms is based on the evolution of a specialist from a local generalist and that this has been made possible by the absence of a common fish competitor in similar lakes, the threespined stickleback Gasterosteous aculeatus.     

Ontogenetic patterns of leaf CO2 exchange, morphology and chemistry in Betula pendula trees

In order to explore ontogenetic variation in leaf-level physiological traits of Betula pendula trees, we measured changes in mass- (A _mass) and area-based (A _area) net photosynthesis under light-saturated conditions, mass- (RS_mass) and area-based (RS_area) leaf respiration, relative growth rate, leaf mass per area (LMA), total nonstructural carbohydrates (TNC), and macro- and micronutrient concentrations. Expanding leaves maintained high rates of A _area, but due to high growth respiration rates, net CO₂ fixation occurred only at irradiances >200 μmol photons m^–2 s^–1. We found that full structural leaf development is not a necessary prerequisite for maintaining positive CO₂ balance in young birch leaves. Maximum rates of A _area were realized in late June and early July, whereas the highest values of A _mass occurred in May and steadily declined thereafter. The maintenance respiration rate averaged ≈8 nmol CO₂ g^–1 s^–1, whereas growth respiration varied between 0 and 65 nmol CO₂ g^–1 s^–1. After reaching its lowest point in mid-June, leaf respiration increased gradually until the end of the growing season. Mass and area-based dark respiration were significantly positively correlated with LMA at stages of leaf maturity, and senescence. Concentrations of P and K decreased during leaf development and stabilized or increased during maturity, and concentrations of immobile elements such as Ca, Mn and B increased throughout the growing season. Identification of interrelations between leaf development, CO₂ exchange, TNC and leaf nutrients allowed us to define factors related to ontogenetic variation in leaf-level physiological traits and can be helpful in establishing periods appropriate for sampling birch leaves for diagnostic purposes such as assessment of plant and site productivity or effects of biotic or abiotic factors. Received: 29 December 1998 / Accepted: 26 July 1999     

Ontogenetic Evidence for Dental Homologies and Premolar Replacement in Fossil and Extant Caenolestids (Marsupialia)

It is generally accepted that the South American marsupial family Caenolestidae is characterized in part by the absence or noneruption of the third deciduous premolar (dP3) in both jaws, although juvenile stages have rarely been identified in extant or fossil representatives of the family. Published illustrations of the dentary of the Miocene caenolestid Stilotherium suggested to us, however, that P3 erupted relatively late during ontogeny, after the eruption of M4. In extant marsupials, this eruption sequence appears to represent the plesiomorphic state and this pattern is generally associated with the eruption of dP3 earlier in ontogeny, and its subsequent replacement by the erupting P3. Therefore, we suspected that a dP3 erupted in earlier ontogenetic stages of caenolestids; to test this hypothesis we searched the mammalogy collections of three museums for evidence of dP3 in juvenile specimens of caenolestids. Examination of more than 180 specimens of the three extant genera of caenolestid marsupials resulted in the identification of only nine juvenile or subadult stages of dental eruption. Seven specimens of Caenolestes and Rhyncholestes corroborated our hypotheses of late eruption of P3 in Caenolestidae. In addition, the two youngest specimens of Caenolestes possessed a tiny, rudimentary dP3, measuring about 0.4 to 0.5 mm in greatest length, associated with a mesiolingual eruption pit containing the apex of the larger P3 in very early phases of eruption above the alveolar margins. The tiny dP3 is clearly nonfunctional in occlusion, and it is questionable whether it erupted above the gun margins in life. Comparison of the dentaries of subadult caenolestids with four dentaries of the Miocene genus Stilotherium corroborated our initial impression that the fossil genus exhibited evidence of a late-erupting P3, comparable to the condition in extant caenolestids. We suggest that examination of other specimens of juvenile dentitions, skulls, and skeletons in museum collections can provide additional insight into the developmental and evolutionary biology of mammals.     

Comparison of diaphyseal growth between the Libben population and the Hamann-Todd chimpanzee sample

The differences in limb lengths and proportions between humans and chimpanzees are widely known. Humans have relatively shorter forelimbs and longer hind limbs than chimpanzees. Humans have a longer period of long bone formation than chimpanzees. Recent advances in estimating age-at-death in chimpanzees from their dentition have allowed us to reexamine long bone growth in chimpanzees using their skeletal remains and compare it with similar data for humans. A chronological normalization procedure allowing direct interspecific comparison of long bone growth is presented. The preadult chimpanzee sample (n = 43) is from the Hamann-Todd Osteological Collection from the Cleveland Museum of Natural History. All human specimens (n = 202) are from the late Woodland Libben Population currently housed at Kent State University. Relying on these cross-sectional data, we conclude that both species elongate their femora at similar absolute (length per unit time) but different relative (length relative to normalized dental age) rates. The species differ in the absolute growth rate of the humerus but share a common normalized rate of growth. Forelimb segment proportion differences between species are due to differential elongation rates of the segments. Hind limb diaphyseal proportions are the same in both species, which suggests that changes in segment length are proportional. Therefore, alternative developmental mechanisms exist in these closely related species which can produce changes in limb length. © 1996 Wiley-Liss, Inc.