Structural tissue organization in the beak of Java and Darwin's finches

Birds are well known for occupying diverse feeding niches, and for having evolved diverse beak morphologies associated with dietary specialization. Birds that feed on hard seeds typically possess beaks that are both deep and wide, presumably because of selection for fracture avoidance, as suggested by prior studies. It follows then that birds that eat seeds of different size and hardness should vary in one or more aspects of beak morphology, including the histological organization of the rhamphotheca, the cellular interface that binds the rhamphotheca to the bone, and the organization of trabeculae in the beak. To explore this expectation we here investigate tissue organization in the rhamphotheca of the Java finch, a large granivorous bird, and describe interspecific differences in the trabecular organization of the beak across 11 species of Darwin's finches. We identify specializations in multiple layers of the horny beak, with the dermis anchored to the bone by Sharpey's fibers in those regions that are subjected to high stresses during biting. Moreover, the rhamphotheca is characterized by a tight dermo‐epidermal junction through interdigitations of these two tissues. Herbst corpuscles are observed in high density in the dermis of the lateral aspect of the beak as observed in other birds. Finally, the trabecular organization of the beak in Darwin's finches appears most variable in regions involved most in food manipulation, with the density of trabeculae in the beak generally mirroring loading regimes imposed by different feeding habits and beak use in this clade.     

Sex-specific ontogenetic patterns of cranial morphology,theoretical bite force,and underlying jaw musculature in fishers and American martens

The carnivoran cranium undergoes tremendous growth in size and development of shape to process prey as adults and, importantly, these ontogenetic processes can also differ between the sexes. How these ontogenetic changes in morphology actually relate to the underlying jaw musculature and overall bite performance has rarely been investigated. In this study, I examined sex-specific ontogenetic changes in cranial morphology, jaw adductor muscles, and theoretical bite force between subadults and adults in the fisher (Pekania pennanti) and American marten (Martes americana). I found evidence that cranial size alone does not completely explain ontogenetic increases in bite forces as found in other mammalian species. Instead, cranial shape development also drives ontogenetic increases in relative bite force by broadening the zygomatic arches and enlargement of the sagittal crest, both of which enable relatively larger jaw adductor muscles to attach. In contrast, examination of sexual dimorphism within each age-class revealed that cranial shape dimorphism did not translate to dimorphism in either size-corrected bite forces or size-corrected physiological cross-sectional area of the jaw adductor muscles. These results reveal that morphological size and shape variation can have different influences on bite performance depending on the level of intraspecific variation that is examined (i.e. ontogenetic versus sexual dimorphism).     

Proximate determinants of bite force in Anolis lizards

Performance measures associated with the vertebrate jaw system may provide important insights into vertebrate ecology and evolution because of their importance in many ecologically relevant tasks. Previous studies have shown that in many taxa, evolution toward higher bite force has gone hand in hand with the evolution of larger body size. However, independent of differences in overall body size, bite force may vary depending on head size and shape as well. Moreover, the underlying musculature may also drive variation in bite force. Here, we investigate the proximate determinants of bite force in lizards of the genus Anolis. We dissected the jaw muscles and quantified muscle mass, fibre length, and cross‐sectional area. Data were analysed for both sexes independently given the sexual dimorphism detected in the dataset. Our results show that the traits that explain bite force are similar in both males and females with overall body size and muscle mass being the principal determinants. Among the different muscles examined, the adductor externus and the pseudotemporalis groups were the best determinants of bite force. However, models run for males predicted the variation in bite force better than models for females, suggesting that selection on morphology improving bite force may be stronger in males.     

The influence of siblings on the development of sexual preferences of male zebra finches

Broods of young zebra finches were either raised by their own species or cross-fostered by Bengalese finches. Both were isolated visually from other birds at the age of 2 months. Sexual preferences of males, were examined at maturity, in a choice between 1 zebra finch female and 1 Bengalese finch female, by measuring the number of song strophes directed at each. Males raised by their own species sang exclusively for the zebra finch female. Cross-fostered males raised without siblings or with only 1 sibling sang exclusively for the Bengalese finch female. A large number of cross-fostered males raised with 2–4 siblings showed at least 5% singing for the zebra finch female, and a small number did so predominantly. It is concluded the under the conditions of these experiments, the development of sexual preferences of zebra finch males is affected by both parental and sibling influences. It is possible that the earlier evidence for a predisposition to respond to conspecifics put forward by Immelmann could be explained by hitherto uncontrolled differences in experience.     

Morphology and Biomechanics of the Pinniped Jaw: Mandibular Evolution Without Mastication

Pinnipeds (seals, sea lions, and walruses) underwent a shift in jaw function away from typical carnivoran mastication to more novel marine behaviors during the terrestrial‐aquatic transition. Here we test the effect of aquatic prey capture and male‐male combat on the morphological evolution of a mammal jaw that does not masticate. Nine three‐dimensional landmarks were taken along the mandible for 25 species (N = 83), and corpus and symphysis external and cortical breadths for a subset of five species (N = 33). Principal components analysis was performed on size‐corrected landmark data to assess variation in overall jaw morphology across pinnipeds. Corpus breadths were input to a beam model to calculate strength properties and estimated bite force of specific species with contrasting behaviors (filter feeding, suction feeding, grip‐and‐tear feeding, and male‐male combat). Results indicate that, although phylogenetic signal in jaw shape is strong, function is also important in determining morphology. Filter feeders display an elongate symphysis and a long toothrow that may play a role in filtering krill. Grip‐and‐tear feeders have a long jaw and large estimated bite force relative to non‐biting species. However, the largest estimated bite forces were observed in males of male‐male combative species, likely due to the high selection pressure associated with male success in highly polygynous species. The suction feeding jaw is weak in biting but has a different morphology in the two suction feeding taxa. In conclusion, familial patterns of pinniped jaw shape due to phylogenetic relatedness have been modified by adaptations to specialized behavior of individual taxa. Anat Rec, 296:1049–1063, 2013. © 2013 Wiley Periodicals, Inc.     

Experimental evidence for transmission of Mycoplasma gallisepticum in house finches by fomites.

Ever since Mycoplasma gallisepticum emerged among house finches in North America, it has been suggested that bird aggregations at feeders are an important cause of the epidemic of mycoplasmal conjunctivitis because diseased birds could deposit droplets of pathogen onto the feeders and thereby promote indirect transmission by fomites. In this paper we bring the first experimental evidence that such transmission (bird-to-feeder-to-bird) does actually take place. House finches infected via this route, however, developed only mild disease and recovered much more rapidly than birds infected from the same source birds but directly into the conjunctiva. While it is certainly probable that house finch aggregations at artificial feeders enhance pathogen transmission, to some degree transmission of M. gallisepticum by fomites may serve to immunize birds against developing more severe infections. Some such birds develop M. gallisepticum antibodies, providing indication of an immune response, although no direct evidence of protection.     

Cranial biomechanics,bite force and function of the endocranial sinuses in Diprotodon optatum,the largest known marsupial

The giant extinct marsupial Diprotodon optatum has unusual skull morphology for an animal of its size, consisting of very thin bone and large cranial sinuses that occupy most of the internal cranial space. The function of these sinuses is unknown as there are no living marsupial analogues. The finite element method was applied to identify areas of high and low stress, and estimate the bite force of Diprotodon to test hypotheses on the function of the extensive cranial sinuses. Detailed three‐dimensional models of the cranium, mandible and jaw adductor muscles were produced. In addition, manipulations to the Diprotodon cranial model were performed to investigate changes in skull and sinus structure, including a model with no sinuses (sinuses ‘filled’ with bone) and a model with a midsagittal crest. Results indicate that the cranial sinuses in Diprotodon significantly lighten the skull while still providing structural support, a high bite force and low stress, indicating the cranium may have been able to withstand higher loads than those generated during feeding. Data from this study support the hypothesis that pneumatisation is driven by biomechanical loads and occurs in areas of low stress. The presence of sinuses is likely to be a byproduct of the separation of the outer surface of the skull from the braincase due to the demands of soft tissue including the brain and the large jaw adductor musculature, especially the temporalis. In very large species, such as Diprotodon, this separation is more pronounced, resulting in extensive cranial sinuses due to a relatively small brain compared with the size of the skull.     

Molecular characterization of a recently identified circovirus in zebra finches (Taeniopygia guttata) associated with immunosuppression and opportunistic infections

A recently identified circovirus (family Circoviridae) was detected in 14 zebra finches (Taeniopygia guttata) from seven aviaries and hobbyist breeders using polymerase chain reaction followed by sequencing. Full genome sequences of virus strains from six zebra finches consistently revealed characteristic circoviral genomic features such as a stem-loop structure and two major open reading frames (ORFs) encoding the replication-associated protein and the putative capsid protein. One further ORF encoding a protein of unknown function was additionally identified in all six genomes. Based on full genome nucleotide comparison, zebra finch circovirus was most similar to Finch circovirus originating from a Gouldian finch (Chloebia gouldiae) sharing 78% nucleotide identity. High genetic diversity was detected in the circoviruses from individual zebra finches. Comparison of the six full genome sequences revealed two genetic subgroups, which shared pairwise nucleotide identities between 91.4% and 92.7%. Analyses including partial sequences of the replication-associated protein gene of the zebra finch circovirus strains from all 14 birds supported the existence of two main clusters. Clinical diseases associated with circovirus infection were found in nestlings, fledglings and adult birds and varied from mild to severe with high mortality caused by secondary infections. Macrorhabdus ornithogaster was the most frequently detected opportunistic pathogen. Feathering disorders were seen in two birds. Lymphocytic depletion of the spleen and leukocytopaenia were detected in individual birds, suggesting immunosuppression and a pathogenesis common to circovirus infections in other birds.     

Molecular identification of novel and genetically diverse adenoviruses in Passeriform birds

Knowledge about adenoviruses in birds of the order Passeriformes is very scarce. Based on molecular characterizations, only two siadenoviruses, great tit adenovirus 1 and Gouldian finch adenovirus, have been described so far occurring in great tits and Gouldian finches, respectively. Assuming a broader occurrence of adenoviruses, various passeriform birds including pet, zoo, and wild birds were examined using a broad-range PCR targeting a fragment of the adenovirus DNA polymerase gene. Adenoviruses were detected in 25 individual birds belonging to 13 species and seven zoological families (Ploceidae, Fringillidae, Estrildidae, Paridae, Sylviidae, Turdidae, Muscicapidae). The putative viruses were further characterized by sequencing the PCR products and phylogenetic analyses. DNA of adenoviruses affiliating to 3 genera including aviadenovirus, siadenovirus, and atadenovirus was found. Viruses with sequences identical or closely related to great tit adenovirus 1 and Gouldian finch adenovirus 1 were detected in a great tit and in two zebra finches, respectively. Based on polymerase amino acid sequence comparisons, the viruses found in the remaining 22 birds revealed phylogenetic distances larger than 15% to adenoviruses known so far suggesting that they may belong to at least 14 different virus species. In some bird species (great tit, zebra finch, vitelline masked weaver) varying adenovirus genera were detected. These results suggest a broad variety of adenoviruses circulating in passeriform birds.

     

Masticatory Apparatus Performance and Functional Morphology in the Extremely Large Mice from Gough Island

Since their arrival approximately 200 years ago, the house mice (Mus musculus) on Gough Island (GI) rapidly increased in size to become the largest wild house mice on record. Along with this extreme increase in body size, GI mice adopted a predatory diet, consuming significant quantities of seabird chicks and eggs. We studied this natural experiment to determine how evolution of extreme size and a novel diet impacted masticatory apparatus performance and functional morphology in these mice. We measured maximum bite force and jaw opening (i.e., gape) along with several musculoskeletal dimensions functionally linked to these performance measurements to test the hypotheses that GI mice evolved larger bite forces and jaw gapes as part of their extreme increase in size and/or novel diet. GI mice can bite more forcefully and open their jaws wider than a representative mainland strain of house mice. Similarly, GI mice have musculoskeletal features of the masticatory apparatus that are absolutely larger than WSB mice. However, when considered relative to body size or jaw length, as a relevant mechanical standard, GI mice show reduced performance, suggesting a size-related decrease in these abilities. Correspondingly, most musculoskeletal features are not relatively larger in GI mice. Incisor biting leverage and condylar dimensions are exceptions, suggesting relative increases in biting efficiency and condylar rotation in GI mice. Based on these results, we hypothesize that evolutionary enhancements in masticatory performance are correlated with the extreme increase in body size and associated musculoskeletal phenotypes in Gough Island mice. Anat Rec, 2019. © 2018 American Association for Anatomy.     

Dimorphism throughout the European eel's life cycle: are ontogenetic changes in head shape related to dietary differences?

A well‐known link exists between an organism's ecology and morphology. In the European eel, a dimorphic head has been linked to differences in feeding ecology, with broad‐headed eels consuming harder prey items than narrow‐headed ones. Consequently, we hypothesized that broad‐heads should exhibit a cranial musculoskeletal system that increases bite force and facilitates the consumption of harder prey. Using 3D‐reconstructions and a bite model, we tested this hypothesis in two life stages: the sub‐adult yellow eel stage and its predecessor, the elver eel stage. This allowed us to test whether broad‐ and narrow‐headed phenotypes show similar trait differences in both life stages and whether the dimorphism becomes more pronounced during ontogeny. We show that broad‐headed eels in both stages have larger jaw muscles and a taller coronoid, which are associated with higher bite forces. This increased bite force together with the elongated upper and lower jaws in broad‐headed eels can also improve grip during spinning behavior, which is used to manipulate hard prey. Head shape variation in European eel is therefore associated with musculoskeletal variation that can be linked to feeding ecology. However, although differences in muscle volume become more pronounced during ontogeny, this was not the case for skeletal features.     

Chromosomal polymorphism and comparative painting analysis in the zebra finch

The zebra finch (Taeniopygia guttata) is often studied because of its interesting behaviour and neurobiology. Genetic information on this species has been lacking, making analysis of informative mutants difficult. Here we report on an improved cytological method for preparation of metaphase chromosomes suitable for fluorescent in situ hybridization of adult birds. We found that individual chicken chromosome paints usually hybridized to single zebra finch chromosomes, indicating only minor chromosomal rearrangements since the evolutionary divergence of these two species, and suggesting that the genomic location of chicken genes will predict the location of zebra finch orthologues. Chicken chromosome 1 appears to have split into two macrochromosomes in zebra finches, and chicken chromosome 4 paint hybridizes to a zebra finch macrochromosome and a microchromosome. This pattern was confirmed by mapping the androgen receptor (AR), which is located on chicken chromosome 4 but on a zebra finch microchromosome. We detected a telocentric/submetacentric polymorphism of chromosome 6 in our colony of zebra finches, and found that the polymorphism was inherited in a Mendelian pattern     

From yellow to silver: Transforming cranial morphology in European eel (Anguilla anguilla)

The European eel (Anguilla anguilla) has been extensively studied, especially because of its highly specialized migratory behaviour associated with substantial phenotypic transformations. During this migration, one of those transformations the eel undergoes is from yellow to silver eel, a process known as silvering. Although the cranial morphology during the earlier glass, elver and yellow eel stages are well studied, little is known about actual morphological changes during the transformation process from the yellow to the silver eel stage. Yet, literature suggests drastic changes in musculoskeletal anatomy. Here, we investigated the cranial musculoskeletal morphology of 11 male European eels at different stages during silvering, resulting both from natural and artificial maturation. Using 3D-reconstructed µCT data of the head, the skull and cranial muscles associated with jaw closing and respiration were studied. Eye size was used as a proxy for the silvering stage. Size-adjusted jaw muscle volumes increased during silvering, although insignificantly. Accordingly, a near-significant increase in bite force was observed. Respiratory muscles size did increase significantly during silvering, however. Considering the eel's long migration, which often includes deep and thus potentially oxygen-poor environments, having a better performing respiratory system may facilitate efficient migration. Both overall skull dimensions and specifically orbit size increased with eye index, suggesting they play a role in accommodating the enlarging eyes during silvering. Finally, artificially matured eels had a wider and taller skull, as well as larger jaw muscles than wild silver eels. This could be caused (a) by different conditions experienced during the yellow eel stage, which are maintained in the silver eel stage, (b) by side effects of hormonal injections or (c) be part of the maturation process as artificially induced silver eels had a higher eye index than the wild silver eels.     

The evolution of bite force in horned lizards: the influence of dietary specialization

Dietary specialization is an important driver of the morphology and performance of the feeding system in many organisms, yet the evolution of phenotypic specialization has only rarely been examined within a species complex. Horned lizards are considered primarily myrmecophagous (ant eating), but variation in diet among the 17 species of horned lizards (Phrynosoma) makes them an ideal group to examine the relationship between dietary specialization and the resultant morphological and functional changes of the feeding system. In this study, we perform a detailed analysis of the jaw adductor musculature and use a biomechanical model validated with in vivo bite force data to examine the evolution of bite force in Phrynosoma. Our model simulations demonstrate that bite force varies predictably with respect to the gape angle and bite position along the tooth row, with maximal bite forces being attained at lower gape angles and at the posterior tooth positions. Maximal bite forces vary considerably among horned lizards, with highly myrmecophagous species exhibiting very low bite forces. In contrast, members of the short‐horned lizard clade are able to bite considerably harder than even closely related dietary generalists. This group appears to be built for performing crushing bites and may represent a divergent morphology adapted for eating hard prey items. The evolutionary loss of processing morphology (teeth, jaw and muscle reduction) and bite force in ant specialists may be a response to the lack of prey processing rather than a functional adaptation per se.     

Cranial joint histology in the mallard duck (Anas platyrhynchos): new insights on avian cranial kinesis

The evolution of avian cranial kinesis is a phenomenon in part responsible for the remarkable diversity of avian feeding adaptations observable today. Although osteological, developmental and behavioral features of the feeding system are frequently studied, comparatively little is known about cranial joint skeletal tissue composition and morphology from a microscopic perspective. These data are key to understanding the developmental, biomechanical and evolutionary underpinnings of kinesis. Therefore, here we investigated joint microstructure in juvenile and adult mallard ducks (Anas platyrhynchos; Anseriformes). Ducks belong to a diverse clade of galloanseriform birds, have derived adaptations for herbivory and kinesis, and are model organisms in developmental biology. Thus, new insights into their cranial functional morphology will refine our understanding of avian cranial evolution. A total of five specimens (two ducklings and three adults) were histologically sampled, and two additional specimens (a duckling and an adult) were subjected to micro‐computed tomographic scanning. Five intracranial joints were sampled: the jaw joint (quadrate‐articular); otic joint (quadrate‐squamosal); palatobasal joint (parasphenoid‐pterygoid); the mandibular symphysis (dentary‐dentary); and the craniofacial hinge (a complex flexion zone involving four different pairs of skeletal elements). In both the ducklings and adults, the jaw, otic and palatobasal joints are all synovial, with a synovial cavity and articular cartilage on each surface (i.e. bichondral joints) ensheathed in a fibrous capsule. The craniofacial hinge begins as an ensemble of patent sutures in the duckling, but in the adult it becomes more complex: laterally it is synovial; whereas medially, it is synostosed by a bridge of chondroid bone. We hypothesize that it is chondroid bone that provides some of the flexible properties of this joint. The heavily innervated mandibular symphysis is already fused in the ducklings and remains as such in the adult. The results of this study will serve as reference for documenting avian cranial kinesis from a microanatomical perspective. The formation of: (i) secondary articular cartilage on the membrane bones of extant birds; and (ii) their unique ability to form movable synovial joints within two or more membrane bones (i.e. within their dermatocranium) might have played a role in the origin and evolution of modern avian cranial kinesis during dinosaur evolution.     

Evolution of birdsong syntax by interjection communication

Animals use diverse forms of communication, from sound signals to body postures. Recent ethological studies have reported a unique syntactic communication of a songbird, the Bengalese finch (Lonchura striata var. domestica). Male Bengalese finches sing complex courtship songs, which can be reconstructed by finite automata, and female Bengalese finches prefer complex songs, as opposed to monotonous or random ones. These facts suggest that the song syntaxes of male birds may have evolved as a result of sexual selection by female birds. Inspired by this hypothesis, we developed a communication model that is a system coupling different types of automaton, one for song production by males and another for song evaluation by females. We applied this model to study the evolution of syntactic animal communication in terms of the self-organization of coevolving automata. Three types of courting strategies as well as a relationship between the song syntax and female preference emerged. We argue that despite the simple communication involved, the complexity and diversity of song syntaxes can evolve via diverse female preferences.     

Comparative infectiousness of three passerine bird species after experimental inoculation with Mycoplasma gallisepticum

Mycoplasma gallisepticum has been isolated from various species of free-living birds, and we therefore tested the hypothesis that bird species other than the main host, the house finch (Carpodacus mexicanus), could play a role in the epidemiology of the infection. We compared the disease course in the house finch, American goldfinch (Carduelis tristis) and house sparrow (Passer domesticus) after inoculation into the conjunctival sac with M. gallisepticum, and also the degree to which the three species were infectious to other naïve house finches. Severity of clinical signs was least in house sparrows, intermediate in American goldfinch and the highest in house finch. House sparrows were only mildly infectious to naïve house finches for a short time, whereas American goldfinches remained infectious for up to 49 days post inoculation, although by then there were no physical signs of disease. We conclude that since American goldfinches can be infectious without showing any conjunctivitis, and since they often make long-distance movements, they might play an as yet unsuspected but important role in M. gallisepticum dynamics in house finches.