Skeletogenesis of Myiopsitta monachus (Psittaciformes) and sequence heterochronies in Aves.

The ossification sequence of Myiopsitta monachus was determined. Myiopsitta has a similar sequence to other altricial birds, with delayed skeletons compared to precocial species. The hindlimbs ossify before the forelimbs, a condition that could be linked to altriciality. To determine the stability of the sequences of ossification across birds, we selected species of different groups of Aves and used event-pairing method and character mapping on a phylogeny. Our results show that the homogeneity in the development of birds was supported by 56.77% of the character states. Event-pair cracking phylogenetic method was applied to identify sequence heterochronies. Results reveal a high number of heterochronies and show that the long bones in limbs may behave as modules. In Myiopsitta, the ossa ectethmoidale and mesethmoidale ossify early. These bones provide the origin site of the Psittaciformes' novel adductor m. ethmomandibularis, associated with strong bite forces, and its acceleration in the sequence may correspond to the functional hypothesis. Also, the early appearance of some hyoid apparatus elements occurs, and could be related to the development of tongue in Psittaciformes and its role in handling food, and is in concordance with the functional and size hypothesis.

Development of the trigeminal motor neurons in parrots: implications for the role of nervous tissue in the evolution of jaw muscle morphology.

Vertebrates have succeeded to inhabit almost every ecological niche due in large part to the anatomical diversification of their jaw complex. As a component of the feeding apparatus, jaw muscles carry a vital role for determining the mode of feeding. Early patterning of the jaw muscles has been attributed to cranial neural crest-derived mesenchyme, however, much remains to be understood about the role of nonneural crest tissues in the evolution and diversification of jaw muscle morphology. In this study, we describe the development of trigeminal motor neurons in a parrot species with the uniquely shaped jaw muscles and compare its developmental pattern to that in the quail with the standard jaw muscles to uncover potential roles of nervous tissue in the evolution of vertebrate jaw muscles. In parrot embryogenesis, the motor axon bundles are detectable within the muscular tissue only after the basic shape of the muscular tissue has been established. This supports the view that nervous tissue does not primarily determine the spatial pattern of jaw muscles. In contrast, the trigeminal motor nucleus, which is composed of somata of neurons that innervate major jaw muscles, of parrot is more developed compared to quail, even in embryonic stage where no remarkable interspecific difference in both jaw muscle morphology and motor nerve branching pattern is recognized. Our data suggest that although nervous tissue may not have a large influence on initial patterning of jaw muscles, it may play an important role in subsequent growth and maintenance of muscular tissue and alterations in cranial nervous tissue development may underlie diversification of jaw muscle morphology.

Molecular and cellular changes associated with the evolution of novel jaw muscles in parrots.

Vertebrates have achieved great evolutionary success due in large part to the anatomical diversification of their jaw complex, which allows them to inhabit almost every ecological niche. While many studies have focused on mechanisms that pattern the jaw skeleton, much remains to be understood about the origins of novelty and diversity in the closely associated musculature. To address this issue, we focused on parrots, which have acquired two anatomically unique jaw muscles: the ethmomandibular and the pseudomasseter. In parrot embryos, we observe distinct and highly derived expression patterns for Scx, Bmp4, Tgfß2 and Six2 in neural crest-derived mesenchyme destined to form jaw muscle connective tissues. Furthermore, immunohistochemical analysis reveals that cell proliferation is more active in the cells within the jaw muscle than in surrounding connective tissue cells. This biased and differentially regulated mode of cell proliferation in cranial musculoskeletal tissues may allow these unusual jaw muscles to extend towards their new attachment sites. We conclude that the alteration of neural crest-derived connective tissue distribution during development may underlie the spatial changes in jaw musculoskeletal architecture found only in parrots. Thus, parrots provide valuable insights into molecular and cellular mechanisms that may generate evolutionary novelties with functionally adaptive significance.

Evolution of craniofacial novelty in parrots through developmental modularity and heterochrony.

Parrots (order Psittaciformes) have developed novel cranial morphology. At the same time, they show considerable morphological diversity in the cranial musculoskeletal system, which includes two novel structures: the suborbital arch and the musculus (M.) pseudomasseter. To understand comprehensively the evolutionary pattern and process of novel cranial morphology in parrots, phylogenetic and developmental studies were conducted. Firstly, we undertook phylogenetic analyses based on mitochondrial ribosomal RNA gene sequences to obtain a robust phylogeny among parrots, and secondly we surveyed the cranial morphology of parrots extensively to add new information on the character states. Character mapping onto molecular phylogenies indicated strongly the repeated evolution of both the suborbital arch and the well-developed M. pseudomasseter within parrots. These results also suggested that the direction of evolutionary change is not always identical in the two characters, implying that these characters are relatively independent or decoupled structures behaving as separate modules. Finally, we compared the developmental pattern of jaw muscles among bird species and found a difference in the timing of M. pseudomasseter differentiation between the cockatiel Nymphicus hollandicus (representative of a well-developed condition) and the peach-faced lovebird Agapornis roseicollis (representative of an underdeveloped condition). On the basis of this study, we suggest that in the development of novel traits, modularity and heterochrony facilitate the diversification of parrot cranial morphology.

Sex allocation theory aids species conservation.

Supplementary feeding is often a key tool in the intensive management of captive and threatened species. Although it can increase such parameters as breeding frequency and individual survival, supplementary feeding may produce undesirable side effects that increase overall extinction risk. Recent attempts to increase breeding frequency and success in the kakapo Strigops habroptilus using supplementary feeding inadvertently resulted in highly male-biased chick sex ratios. Here, we describe how the inclusion of sex allocation theory has remedied this conservation dilemma. Our study is the first to manipulate chick sex ratios in an endangered species by altering maternal condition and highlights the importance of incorporating evolutionary theory into modern conservation practice.

Cranial neural crest cell migration in cockatiel Nymphicus hollandicus (Aves: Psittaciformes).

Parrots have developed unique jaw muscles in their evolutionary history. The M. pseudomasseter, which completely covers the lateral side of the jugal bar, is regarded as a jaw muscle unique to parrots. In a previous study, I presented a hypothesis on the relevance of modifications in the regulation of cranial neural crest cell (NCC) development to the generation of this novel jaw muscle based on histological analyses (Tokita [2004] J Morphol 259:69-81). In the present study, I investigated distribution and migration patterns of cranial neural crest cells (NCCs) through parrot embryogenesis with immunohistochemical techniques to further understand the role of cranial NCCs in the evolution of the M. pseudomasseter, and to provide new information on the relative plasticity in cranial NCC migration at early stages of avian development. The basic nature of cranial NCC development was mostly conserved between chick and parrot. In both, cranial NCCs migrated from the dorsal tip of the neural tube in a ventral direction. Three major populations were identified in their cranial NCCs. Migration pathways of these cells were almost identical between chick and parrot. The principal difference was seen in the relative timing of cranial NCC migration. In the parrot, cranial NCC migration into the first pharyngeal arch was more advanced than in the chick at early stages of development. Such a temporal shift in cranial NCC migration might influence architectural patterning of parrot jaw muscles that generates new muscle like M. pseudomasseter.

Morphogenesis of parrot jaw muscles: understanding the development of an evolutionary novelty.

Parrots have developed novel head structures in their evolutionary history. The appearance of two new muscles for strong jaw adduction is especially fascinating in developmental and evolutionary contexts. However, jaw muscle development of parrots has not been described, despite its uniqueness. This report first presents the normal developmental stages of the cockatiel (Nymphicus hollandicus), comparable to that of the chick. Next, the peculiar skeletal myogenesis in the first visceral arch of parrots is described, mainly focusing on the development of two new jaw muscles. One of the parrot-specific muscles, M. ethmomandibularis, was initially detected at Nymphicus Stage 28 (N28) as the rostral budding of M. pterygoideus. After N32, the muscle significantly elongates rostrodorsally toward the interorbital septum, following a course lateral to the palatine bone. Another parrot-specific muscle, M. pseudomasseter, was first recognized at N36. The muscle branches off from the posteromedial M. adductor mandibulae externus and grows in a dorsolateral direction, almost covering the lateral surface of the jugal bar. The upper tip of the muscle is accompanied by condensed mesenchyme, which seems to be derived from cephalic neural crest cells.

The skull development of parrots with special reference to the emergence of a morphologically unique cranio-facial hinge.

The order Psittaciformes (parrots) has unique morphological features in the head that are evolutionarily novel. To better understand the unique evolution of the head in parrots, the developmental pattern of the skull of the budgerigar (Melopsittacus undulatus) was initially described on the basis of transparent skeletal specimens. Although the fundamental pattern of the skull development of birds is conserved in parrots, some differences were observed between parrots and other groups of birds. In parrots, the vacuity in the interorbital septum did not emerge throughout ontogeny, in contrast to other lineages of birds, for example Galliformes and Coliiformes. This feature seems to be concerned with the attachment of the unique jaw muscle of parrots, M. ethmomandibularis, to the interorbital septum. In spite of a prokinetic skull, the cranio-facial hinge of parrots was brought about by secondary transformation of dermal bones unlike that of birds with a standard prokinetic skull (e.g. Corvus) in which the nasal-frontal suture directly becomes a hinge of bending. To further understand the evolution of "pseudoprokinesis" in parrots, the construction of a robust avian phylogeny is desired. The parrot-specific suborbital arch and cranio-facial hinge are not seen until birds leave the nest and can feed themselves. In conclusion, these structures are considered to be essential for eating hard and/or large meals.

Varied egg gas conductance, air cell gas tensions and development in Agapornis roseicollis.

Different color varieties of the small African parrot, Agapornis roseicollis , lay eggs which differ by as much as a factor of 7 in gas conductance. Oxygen consumption (VO2) and air cell gas tensions (PAO2, PACO2) were measured repeatedly on individual eggs during development. No differences were observed in the ontogeny of VO2, incubation period, or hatchling mass of eggs with different gas conductances, in spite of large differences in PAO2 and PACO2. Low conductance eggs reached PAO2 as low as 46.0 torr (6.13 kPa) and PACO2 as high as 90.5 torr (12.07 kPa). Although pipping occurred earlier in low conductance eggs, pipping did not occur at similar air cell gas tensions in eggs differing in conductance. Chorioallantoic membrane development was about 75% complete on day 12 and not fully complete until day 18 of the 22-23 day incubation period. The capacity of avian embryos to develop and hatch normally in eggs of different conductances may be important in allowing adaptation to varying nesting environments.