scholarly journals A histological survey of avian post-natal skeletal ontogeny

PeerJ ◽  
2021 ◽  
Vol 9 ◽  
pp. e12160
Author(s):  
Jessie Atterholt ◽  
Holly N. Woodward

Bone histology of crown-group birds is a research topic of great interest, permitting insight into the evolution of remarkably high growth rates in this clade and variation across the altricial-precocial spectrum. In this study, we describe microanatomical characteristics of the humerus and femur in partial growth series from 14 crown group birds representing ten major clades (Struthioniformes, Galliformes, Apodiformes, Columbiformes, Charadriiformes, Accipitriformes, Strigiformes, Psittaciformes, Falconiformes, and Passeriformes). Our goals were to: (1) describe the microanatomy of each individual; (2) make inter-and intra-taxonomic comparisons; (3) assess patterns that correspond with developmental mode; and (4) to further parse out phylogenetic, developmental, and functional constraints on avian osteological development. Across taxa, the femoral and humeral tissue of neonates can be broadly characterized as highly-vascularized, disorganized woven bone with great variation in cortical thickness (inter-and intrataxonomically, within an individual specimen, and within a single section). The tissue of precocial chicks is relatively more mature at hatching than in altricial, but other categories along the developmental spectrum were less easy to distinguish, thus we were unable to identify a definitive histological proxy for developmental mode. We did not find evidence to support hypotheses that precocial chicks exclusively have thicker cortices and more mature bone in the femur than the humerus at time of hatching; instead, this is a characteristic of nearly all taxa (regardless of developmental mode), suggesting deep evolutionary origins and the effects of developmental channeling. Bone tissue in adults exhibited unexpected variation, corresponding to differences in body size. Large-bodied birds have cortices of fibrolamellar bone, but organization of tissue increases and vascularity decreases with diminishing body size. The outer circumferential layer (OCL) also appears at earlier growth stages in small-bodied taxa. Thus, while the OCL is indicative of a cessation of appositional growth it is not always indicative of cortical maturity (that is, maximum organization of bony tissue for a given taxon). Small size is achieved by truncating the period of fast growth; manipulation of the timing of offset of bone growth is therefore an important factor in changing growth trajectories to alter adult body size.

PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e9192 ◽  
Author(s):  
Thomas D. Carr

Background During the growth of complex multicellular organisms, chronological age, size and morphology change together in a hierarchical and coordinated pattern. Among extinct species, the growth of Tyrannosaurus rex has received repeated attention through quantitative analyses of relative maturity and chronological age. Its growth series shows an extreme transformation from shallow skulls in juveniles to deep skulls in adults along with a reduction in tooth count, and its growth curve shows that T. rex had a high growth rate in contrast to its closest relatives. However, separately, these sets of data provide an incomplete picture of the congruence between age, size, and relative maturity in this exemplar species. The goal of this work is to analyze these data sets together using cladistic analysis to produce a single hypothesis of growth that includes all of the relevant data. Methods The three axes of growth were analyzed together using cladistic analysis, based on a data set of 1,850 morphological characters and 44 specimens. The analysis was run in TNT v.1.5 under a New Technology search followed by a Traditional search. Correlation tests were run in IBM SPSS Statistics v. 24.0.0.0. Results An initial analysis that included all of the specimens recovered 50 multiple most parsimonious ontograms a series of analyses identified 13 wildcard specimens. An analysis run without the wildcard specimens recovered a single most parsimonious tree (i.e., ontogram) of 3,053 steps. The ontogram is composed of 21 growth stages, and all but the first and third are supported by unambiguously optimized synontomorphies. T. rex ontogeny can be divided into five discrete growth categories that are diagnosed by chronological age, morphology, and, in part, size (uninformative among adults). The topology shows that the transition from shallow to deep skull shape occurred between 13 and 15 years of age, and the size of the immediate relatives of T. rex was exceeded between its 15th and 18th years. Although size and maturity are congruent among juveniles and subadults, congruence is not seen among adults; for example, one of the least mature adults (RSM 2523.8) is also the largest and most massive example of the species. The extreme number of changes at the transition between juveniles and subadults shows that the ontogeny of T. rex exhibits secondary metamorphosis, analogous to the abrupt ontogenetic changes that are seen at sexual maturity among teleosts. These results provide a point of comparison for testing the congruence between maturity and chronological age, size, and mass, as well as integrating previous work on functional morphology into a rigorous ontogenetic framework. Comparison of the growth series of T. rex with those of outgroup taxa clarifies the ontogenetic trends that were inherited from the common ancestor of Archosauriformes.


2013 ◽  
Vol 59 (1) ◽  
pp. 142-150 ◽  
Author(s):  
Lixia Zhang ◽  
Xin Lu

Abstract Why do two sexes of the same species differ in body size holds a long-standing question of evolutionary biology. While many across-species comparisons have focused on ultimate causes behind sexual size dimorphism (SSD), only have a few been directed toward elucidating its ontogenetic basis. Urodeles are an amphibian group in which the direction and degree of SSD vary greatly among species. Using demographic data yielded by skeletochronology for 33 urodele species, the current study reveals a positive across-species correlation between SSD and the sex difference in mean age of adult animals, and the latter increases with the corresponding difference in age at maturity; annual growth rate does not differ between the sexes. We conclude that extended longevities in one sex, which is mediated by delayed maturation, would allow it to grow for longer and get larger, with growth rate making a weak contribution to body size. The sex-specific divergence in ontogenetic trajectory might be explained by potentially high growth costs of reproduction to females in association with stronger fecundity selection, and to males that are expected to experience stronger sexual selection.


2010 ◽  
Vol 60 (1) ◽  
pp. 25-41 ◽  
Author(s):  
Jacques Castanet ◽  
Jorge Cubo ◽  
Laëtitia Montes

AbstractA debate on the determinism (phylogenetic versus functional) of the diversity of bone histological features has centred the interest of bone comparative biologists. While some authors have noticed the presence of a phylogenetic signal in bone tissue variation, many others have argued that these characters may not include much phylogenetic information, but rather reflect functional factors. Here we quantify both components in a sample of amniotes. We hypothesize that: 1/ the observed variation is partly the outcome of shared ancestry (phylogenetic factor) and 2/ for a given quantity of bone produced, tissues formed at a rapid rate may have a higher fraction of vascular cavities than those produced at a slower rate (functional factor). Variation partitioning analyses show that the phylogeny explains a significant portion of the variation of bone vascularity (85.3%), bone growth rate also explains a significant portion of this variation (68.3%), and there is an important overlap (67.9%). Finally, an optimization through least-squares parsimony of bone growth rates onto the phylogeny shows that the most important evolutionary change may have occurred after the split between crocodiles and birds. This change may be linked to the origin of avian endothermic metabolism because high growth rates involve high protein turnover, which is very energy consuming. We conclude that the debate on the dichotomy between phylogenetic versus functional causation of bone histological diversity is misleading, because we have shown that bone vascularity has, at the same time, a functional significance and a phylogenetic signal.


2016 ◽  
Author(s):  
Mark E Samuels ◽  
Sophie Regnault ◽  
John R Hutchinson

The patella is a sesamoid bone located in the major extensor tendon of the knee joint, in the hindlimb of many tetrapods. Although numerous aspects of knee morphology are ancient and conserved among most tetrapods, the evolutionary occurrence of the patella is highly variable. Among extant (crown clade) groups it is found in most birds, most lizards, the monotreme mammals and almost all placental mammals, but it is absent in most marsupial mammals as well as many reptiles. Here we integrate data from the literature and first-hand studies of fossil and recent skeletal remains to reconstruct the evolution of the mammalian patella. We infer that patellae most likely evolved between four to six times in crown group Mammalia: in monotremes, in the extinct multituberculates, in one or more stem-mammal genera outside of therian or eutherian mammals, and up to three times in therian mammals. Furthermore, a patella was lost several times in mammals, not including those with absent hindlimbs: once or more in marsupials (with some re-acquisition), and at least once in bats. Our inferences about patellar evolution in mammals are reciprocally informed by the existence of several human genetic conditions in which the patella is either absent or severely reduced. Clearly, development of the patella is under close genomic control, although its responsiveness to its mechanical environment is also important (and perhaps variable among taxa). Where a patella is present it plays an important role in hindlimb function; especially in resisting gravity by providing an enhanced lever system for the knee joint. Yet the evolutionary origins, persistence and modifications of a patella in diverse groups with widely varying habits and habitats -- from digging to running to aquatic, small or large body sizes, bipeds or quadrupeds -- remain complex and perplexing, impeding a conclusive synthesis of form, function, development and genetics across mammalian evolution. This meta-analysis takes an initial step toward such a synthesis by collating available data and elucidating areas of promising future inquiry.


2021 ◽  
Vol 53 (1) ◽  
Author(s):  
Jing Li ◽  
Song Peng ◽  
Liepeng Zhong ◽  
Lisheng Zhou ◽  
Guorong Yan ◽  
...  

Abstract Background Carcass length is very important for body size and meat production for swine, thus understanding the genetic mechanisms that underly this trait is of great significance in genetic improvement programs for pigs. Although many quantitative trait loci (QTL) have been detected in pigs, very few have been fine-mapped to the level of the causal mutations. The aim of this study was to identify potential causal single nucleotide polymorphisms (SNPs) for carcass length by integrating a genome-wide association study (GWAS) and functional assays. Results Here, we present a GWAS in a commercial Duroc × (Landrace × Yorkshire) (DLY) population that reveals a prominent association signal (P = 4.49E−07) on pig chromosome 17 for carcass length, which was further validated in two other DLY populations. Within the detected 1 Mb region, the BMP2 gene stood out as the most likely causal candidate because of its functions in bone growth and development. Whole-genome gene expression studies showed that the BMP2 gene was differentially expressed in the cartilage tissues of pigs with extreme carcass length. Then, we genotyped an additional 267 SNPs in 500 selected DLY pigs, followed by further whole-genome SNP imputation, combined with deep genome resequencing data on multiple pig breeds. Reassociation analyses using genotyped and imputed SNP data revealed that the rs320706814 SNP, located approximately 123 kb upstream of the BMP2 gene, was the strongest candidate causal mutation, with a large association with carcass length, with a ~ 4.2 cm difference in length across all three DLY populations (N = 1501; P = 3.66E−29). This SNP segregated in all parental lines of the DLY (Duroc, Large White and Landrace) and was also associated with a significant effect on body length in 299 pure Yorkshire pigs (P = 9.2E−4), which indicates that it has a major value for commercial breeding. Functional assays showed that this SNP is likely located within an enhancer and may affect the binding affinity of transcription factors, thereby regulating BMP2 gene expression. Conclusions Taken together, these results suggest that the rs320706814 SNP on pig chromosome 17 is a putative causal mutation for carcass length in the widely used DLY pigs and has great value in breeding for body size in pigs.


2020 ◽  
Author(s):  
Bingxing An ◽  
Lei Xu ◽  
Jiangwei Xia ◽  
Xiaoqiao Wang ◽  
Jian Miao ◽  
...  

Abstract Background: Body size traits as one of the main breeding selection criteria was widely used to monitor cattle growth and to evaluate the selection response. In this study, body size was defined as body height (BH), body length (BL), hip height (HH), heart size (HS), abdominal size (AS), and cannon bone size (CS). We performed genome-wide association studies (GWAS) of these traits over the course of three growth stages (6, 12 and 18 months after birth) using three statistical models, single-trait GWAS, multi-trait GWAS and LONG-GWAS. The Illumina Bovine HD 770K BeadChip was used to identify genomic single nucleotide polymorphisms (SNPs) in 1217 individuals. Results: In total, 19, 29, and 10 significant SNPs were identified by the three models, respectively. Among these, 21 genes were promising candidate genes, including SOX2, SNRPD1, RASGEF1B, EFNA5, PTBP1, SNX9, SV2C, PKDCC, SYNDIG1, AKR1E2, and PRIM2 identified by single-trait analysis; SLC37A1, LAP3, PCDH7, MANEA, and LHCGR identified by multi-trait analysis; and P2RY1, MPZL1, LINGO2, CMIP, and WSCD1 identified by LONG-GWAS. Conclusions: Multiple association analysis was performed for six growth traits at each growth stage. These findings offer valuable insights for the further investigation of potential genetic mechanism of growth traits in Simmental beef cattle.


2020 ◽  
Author(s):  
Bingxing An ◽  
Lei Xu ◽  
Jiangwei Xia ◽  
Xiaoqiao Wang ◽  
Jian Miao ◽  
...  

Abstract Background: Body size traits as one of the main breeding selection criteria was widely used to monitor cattle growth and to evaluate the selection response. In this study, body size was defined as body height (BH), body length (BL), hip height (HH), heart size (HS), abdominal size (AS), and cannon bone size (CS). We performed genome-wide association studies (GWAS) of these traits over the course of three growth stages (6, 12 and 18 months after birth) using three statistical models, single-trait GWAS, multi-trait GWAS and LONG-GWAS. The Illumina Bovine HD 770K BeadChip was used to identify genomic single nucleotide polymorphisms (SNPs) in 1217 individuals. Results: In total, 19, 29, and 10 significant SNPs were identified by the three models, respectively. Among these, 21 genes were promising candidate genes, including SOX2, SNRPD1, RASGEF1B, EFNA5, PTBP1, SNX9, SV2C, PKDCC, SYNDIG1, AKR1E2, and PRIM2 identified by single-trait analysis; SLC37A1, LAP3, PCDH7, MANEA, and LHCGR identified by multi-trait analysis; and P2RY1, MPZL1, LINGO2, CMIP, and WSCD1 identified by LONG-GWAS. Conclusions: Multiple association analysis was performed for six growth traits at each growth stage. These findings offer valuable insights for the further investigation of potential genetic mechanism of growth traits in Simmental beef cattle.


2019 ◽  
Vol 19 (1) ◽  
Author(s):  
Lisa Schnetz ◽  
Cathrin Pfaff ◽  
Eugen Libowitzky ◽  
Zerina Johanson ◽  
Rica Stepanek ◽  
...  

Abstract Background Chondrichthyans represent a monophyletic group of crown group gnathostomes and are central to our understanding of vertebrate evolution. Like all vertebrates, cartilaginous fishes evolved concretions of material within their inner ears to aid with equilibrium and balance detection. Up to now, these materials have been identified as calcium carbonate-bearing otoconia, which are small bio-crystals consisting of an inorganic mineral and a protein, or otoconial masses (aggregations of otoconia bound by an organic matrix), being significantly different in morphology compared to the singular, polycrystalline otolith structures of bony fishes, which are solidified bio-crystals forming stony masses. Reinvestigation of the morphological and chemical properties of these chondrichthyan otoconia revises our understanding of otolith composition and has implications on the evolution of these characters in both the gnathostome crown group, and cartilaginous fishes in particular. Results Dissections of Amblyraja radiata, Potamotrygon leopoldi, and Scyliorhinus canicula revealed three pairs of singular polycrystalline otolith structures with a well-defined morphology within their inner ears, as observed in bony fishes. IR spectroscopy identified the material to be composed of carbonate/collagen-bearing apatite in all taxa. These findings contradict previous hypotheses suggesting these otoconial structures were composed of calcium carbonate in chondrichthyans. A phylogenetic mapping using 37 chondrichthyan taxa further showed that the acquisition of phosphatic otolith structures might be widespread within cartilaginous fishes. Conclusions Differences in the size and shape of otoliths between taxa indicate a taxonomic signal within elasmobranchs. Otoliths made of carbonate/collagen-bearing apatite are reported for the first time in chondrichthyans. The intrinsic pathways to form singular, polycrystalline otoliths may represent the plesiomorphic condition for vertebrates but needs further testing. Likewise, the phosphatic composition of otoliths in early vertebrates such as cyclostomes and elasmobranchs is probably closely related to the lack of bony tissue in these groups, supporting a close relationship between skeletal tissue mineralization patterns and chemical otolith composition, underlined by physiological constraints.


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