Talk:Platypus Development

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Cite this page: Hill, M.A. (2024, April 16) Embryology Platypus Development. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Talk:Platypus_Development

Smith GE. Further observations on the anatomy of the brain in the monotremata. (1899) J Anat Physiol. 33(2): 309–342.

2018

Martin HC, Batty EM, Hussin J, Westall P, Daish T, Kolomyjec S, Piazza P, Bowden R, Hawkins M, Grant T, Moritz C, Grutzner F, Gongora J & Donnelly P. (2018). Insights into Platypus Population Structure and History from Whole-Genome Sequencing. Mol. Biol. Evol. , 35, 1238-1252. PMID: 29688544 DOI.

Insights into Platypus Population Structure and History from Whole-Genome Sequencing The platypus is an egg-laying mammal which, alongside the echidna, occupies a unique place in the mammalian phylogenetic tree. Despite widespread interest in its unusual biology, little is known about its population structure or recent evolutionary history. To provide new insights into the dispersal and demographic history of this iconic species, we sequenced the genomes of 57 platypuses from across the whole species range in eastern mainland Australia and Tasmania. Using a highly improved reference genome, we called over 6.7 M SNPs, providing an informative genetic data set for population analyses. Our results show very strong population structure in the platypus, with our sampling locations corresponding to discrete groupings between which there is no evidence for recent gene flow. Genome-wide data allowed us to establish that 28 of the 57 sampled individuals had at least a third-degree relative among other samples from the same river, often taken at different times. Taking advantage of a sampled family quartet, we estimated the de novo mutation rate in the platypus at 7.0 × 10-9/bp/generation (95% CI 4.1 × 10-9-1.2 × 10-8/bp/generation). We estimated effective population sizes of ancestral populations and haplotype sharing between current groupings, and found evidence for bottlenecks and long-term population decline in multiple regions, and early divergence between populations in different regions. This study demonstrates the power of whole-genome sequencing for studying natural populations of an evolutionarily important species. PMID: 29688544 PMCID: PMC5913675 DOI: 10.1093/molbev/msy041

2013

Identification and functional characterization of a novel monotreme- specific antibacterial protein expressed during lactation

PLoS One. 2013;8(1):e53686. doi: 10.1371/journal.pone.0053686. Epub 2013 Jan 9.

Bisana S, Kumar S, Rismiller P, Nicol SC, Lefèvre C, Nicholas KR, Sharp JA.

Source Centre for Chemistry and Biotechnology, Deakin University, Geelong, Victoria, Australia. swathib@ccmb.res.in

Abstract

Monotremes are the only oviparous mammals and exhibit a fascinating combination of reptilian and mammalian characters. They represent a component of synapsidal reproduction by laying shelled eggs which are incubated outside the mother's body. This is accompanied by a prototherian lactation process, marking them as representatives of early mammals. The only extant monotremes are the platypus, and the short- and long- beaked echidnas, and their distributions are limited to Australia and New Guinea. Apart for a short weaning period, milk is the sole source of nutrition and protection for the hatchlings which are altricial and immunologically naive. The duration of lactation in these mammals is prolonged relative to the gestational length and period of incubation of eggs. Much of the development of monotreme young occurs in the non-sterile ex-utero environment. Therefore the role of milk in the growth, development and disease protection of the young is of significant interest. By sequencing the cDNA of cells harvested from monotreme milk, we have identified a novel monotreme- specific transcript, and the corresponding gene was designated as the EchAMP. The expression profile of this gene in various tissues revealed that it is highly expressed in milk cells. The peptides corresponding to the EchAMP protein have been identified in a sample of echidna milk In silico analysis indicated putative antimicrobial potential for the cognate protein of EchAMP. This was further confirmed by in vitro assays using a host of bacteria. Interestingly, EchAMP did not display any activity against a commensal gut floral species. These results support the hypothesis of enhancement of survival of the young by antimicrobial bioactives of mammary gland origin and thus emphasize the protective, non- nutritional role of milk in mammals.

PMID 23326486

2012

Development of the cerebellum in the platypus (Ornithorhynchus anatinus) and short-beaked echidna (Tachyglossus aculeatus)

Brain Behav Evol. 2012;79(4):237-51. Epub 2012 May 3.

Ashwell KW. Source Department of Anatomy, School of Medical Sciences, The University of New South Wales, Sydney, Australia.

Abstract

The monotremes are a unique group of mammals whose young are incubated in a leathery-shelled egg and fed with milk from teatless areolae after hatching. As soon as they hatch, monotreme young must be able to maneuver around the nest or maternal pouch to locate the areolae and stimulate milk ejection. In the present study, the embryological collections at the Museum für Naturkunde, Berlin, have been used to follow the development of the monotreme cerebellum through incubation and lactational phases, to determine whether cerebellar circuitry is able to contribute to the coordination of locomotion in the monotreme hatchling, and to correlate cerebellar development with behavioral maturation. The structure of the developing monotreme cerebellum and the arrangement of transitory neuronal populations are similar to those reported for fetal and neonatal eutherians, but the time course of the key events of later cerebellar development is spread over a much longer period. Expansion of the rostral rhombic lip and formation of the nuclear and cortical transitory zones occurs by the time of hatching, but it is not until after the end of the first post-hatching week that deep cerebellar neurons begin to settle in their definitive positions and the Purkinje cell layer can be distinguished. Granule cell formation is also prolonged over many post-hatching months and the external granular layer persists for more than 20 weeks after hatching. The findings indicate that cerebellar circuitry is unlikely to contribute to the coordination of movements in the monotreme peri-hatching period. Those activities are most likely controlled by the spinal cord and medullary reticular formation circuitry. Copyright © 2012 S. Karger AG, Basel.

PMID 22572119

Distinct development of the cerebral cortex in platypus and echidna

Brain Behav Evol. 2012;79(1):57-72. Epub 2011 Dec 6.

Ashwell KW, Hardman CD. Source Department of Anatomy, School of Medical Sciences, The University of New South Wales, Sydney, NSW, Australia. k.ashwell@unsw.edu.au

Abstract

Both lineages of the modern monotremes have distinctive features in the cerebral cortex, but the developmental mechanisms that produce such different adult cortical architecture remain unknown. Similarly, nothing is known about the differences and/or similarities between monotreme and therian cortical development. We have used material from the Hill embryological collection to try to answer key questions concerning cortical development in monotremes. Our findings indicate that gyrencephaly begins to emerge in the echidna brain shortly before birth (crown-rump length 12.5 mm), whereas the cortex of the platypus remains lissencephalic throughout development. The cortices of both monotremes are very immature at the time of hatching, much like that seen in marsupials, and both have a subventricular zone (SubV) within both the striatum and pallium during post-hatching development. It is particularly striking that in the platypus, this region has an extension from the palliostriatal angle beneath the developing trigeminoreceptive part of the somatosensory cortex of the lateral cortex. The putative SubV beneath the trigeminal part of S1 appears to accommodate at least two distinct types of cell and many mitotic figures and (particularly in the platypus) appears to be traversed by large numbers of thalamocortical axons as these grow in. The association with putative thalamocortical fibres suggests that this region may also serve functions similar to the subplate zone of Eutheria. These findings suggest that cortical development in each monotreme follows distinct paths from at least the time of birth, consistent with a long period of independent and divergent cortical evolution. Copyright © 2011 S. Karger AG, Basel.

PMID 22143038

2011

Monotreme ossification sequences and the riddle of Mammalian skeletal development

Evolution. 2011 May;65(5):1323-35. doi: 10.1111/j.1558-5646.2011.01234.x. Epub 2011 Feb 18.

Weisbecker V. Source Earth Sciences, University of Cambridge, Downing St. CB2 3EQ, Cambridge, United Kingdom Institut für Spezielle Zoologie und Evolutionsbiologie, Friedrich-Schiller Universität Jena, Erbertstr.1, 07743 Jena, Germany E-mail: vw248@cam.ac.uk.

Abstract

The developmental differences between marsupials, placentals, and monotremes are thought to be reflected in differing patterns of postcranial development and diversity. However, developmental polarities remain obscured by the rarity of monotreme data. Here, I present the first postcranial ossification sequences of the monotreme echidna and platypus, and compare these with published data from other mammals and amniotes. Strikingly, monotreme stylopodia (humerus, femur) ossify after the more distal zeugopodia (radius/ulna, tibia/fibula), resembling only the European mole among all amniotes assessed. European moles also share extreme humeral adaptations to rotation digging and/or swimming with monotremes, suggesting a causal relationship between adaptation and ossification heterochrony. Late femoral ossification with respect to tibia/fibula in monotremes and moles points toward developmental integration of the serially homologous fore- and hindlimb bones. Monotreme cervical ribs and coracoids ossify later than in most amniotes but are similarly timed as homologous ossifications in therians, where they are lost as independent bones. This loss may have been facilitated by a developmental delay of coracoids and cervical ribs at the base of mammals. The monotreme sequence, although highly derived, resembles placentals more than marsupials. Thus, marsupial postcranial development, and potentially related diversity constraints, may not represent the ancestral mammalian condition.

© 2011 The Author(s). Evolution© 2011 The Society for the Study of Evolution.

PMID: 21521190

2010

Early development and embryology of the platypus

Hughes RL, Hall LS. Philos Trans R Soc Lond B Biol Sci. 1998 Jul 29;353(1372):1101-14. Review. PMID: 9720108


Cereb Cortex. 2010 May;20(5):1071-81. Epub 2009 Sep 2. The subventricular zone is the developmental milestone of a 6-layered neocortex: comparisons in metatherian and eutherian mammals. Cheung AF, Kondo S, Abdel-Mannan O, Chodroff RA, Sirey TM, Bluy LE, Webber N, DeProto J, Karlen SJ, Krubitzer L, Stolp HB, Saunders NR, Molnár Z.

Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3QX, UK. Abstract The major lineages of mammals (Eutheria, Metatheria, and Monotremata) diverged more than 100 million years ago and have undergone independent changes in the neocortex. We found that adult South American gray short-tailed opossum (Monodelphis domestica) and tammar wallaby (Macropus eugenii) possess a significantly lower number of cerebral cortical neurons compared with the mouse (Mus musculus). To determine whether the difference is reflected in the development of the cortical germinal zones, the location of progenitor cell divisions was examined in opossum, tammar wallaby, and rat. The basic pattern of the cell divisions was conserved, but the emergence of a distinctive band of dividing cells in the subventricular zone (SVZ) occurred relatively later in the opossum (postnatal day [P14]) and the tammar wallaby (P40) than in rodents. The planes of cell divisions in the ventricular zone (VZ) were similar in all species, with comparable mRNA expression patterns of Brn2, Cux2, NeuroD6, Tbr2, and Pax6 in opossum (P12 and P20) and mouse (embryonic day 15 and P0). In conclusion, the marsupial neurodevelopmental program utilizes an organized SVZ, as indicated by the presence of intermediate (or basal) progenitor cell divisions and gene expression patterns, suggesting that the SVZ emerged prior to the Eutherian-Metatherian split.

PMID: 19726493


Evolution of lactation: ancient origin and extreme adaptations of the lactation system

Annu Rev Genomics Hum Genet. 2010 Sep 22;11:219-38.

Lefèvre CM, Sharp JA, Nicholas KR. Source Institute for Technology Research and Innovation, Deakin University, Waurn Ponds, VIC 3217, Australia. clefevre@deakin.edu.au

Abstract

Lactation, an important characteristic of mammalian reproduction, has evolved by exploiting a diversity of strategies across mammals. Comparative genomics and transcriptomics experiments have now allowed a more in-depth analysis of the molecular evolution of lactation. Milk cell and mammary gland genomic studies have started to reveal conserved milk proteins and other components of the lactation system of monotreme, marsupial, and eutherian lineages. These analyses confirm the ancient origin of the lactation system and provide useful insight into the function of specific milk proteins in the control of lactation. These studies also illuminate the role of milk in the regulation of growth and development of the young beyond simple nutritive aspects.

PMID: 20565255 http://www.ncbi.nlm.nih.gov/pubmed/20565255

http://www.annualreviews.org/doi/abs/10.1146/annurev-genom-082509-141806

Phylogenetic origins of early alterations in brain region proportions

Brain Behav Evol. 2010;75(2):104-10. Epub 2010 Mar 23.

Charvet CJ, Sandoval AL, Striedter GF. Source Department of Neurobiology and Behavior and Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, Calif. 92687-4550, USA. ccharvet@uci.edu

Abstract

Adult galliform birds (e.g. chickens) exhibit a relatively small telencephalon and a proportionately large optic tectum compared with parrots and songbirds. We previously examined the embryonic origins of these adult species differences and found that the optic tectum is larger in quail than in parakeets and songbirds at early stages of development, prior to tectal neurogenesis onset. The aim of this study was to determine whether a proportionately large presumptive tectum is a primitive condition within birds or a derived feature of quail and other galliform birds. To this end, we examined embryonic brains of several avian species (emus, parrots, songbirds, waterfowl, galliform birds), reptiles (3 lizard species, alligators, turtles) and a monotreme (platypuses). Brain region volumes were estimated from serial Nissl-stained sections. We found that the embryos of galliform birds and lizards exhibit a proportionally larger presumptive tectum than all the other examined species. The presumptive tectum of the platypus is unusually small. The most parsimonious interpretation of these data is that the expanded embryonic tectum of lizards and galliform birds is a derived feature in both of these taxonomic groups.

Copyright 2010 S. Karger AG, Basel.

PMID: 20332607 http://www.ncbi.nlm.nih.gov/pubmed/20332607

http://content.karger.com/produktedb/produkte.asp?DOI=000300573&typ=pdf

Those other mammals: the immunoglobulins and T cell receptors of marsupials and monotremes

Semin Immunol. 2010 Feb;22(1):3-9. Epub 2009 Dec 8. Miller RD. Source Center for Evolutionary and Theoretical Immunology, Department of Biology, University of New Mexico, Albuquerque, NM 87110, USA. rdmiller@unm.edu

Abstract

This review summarizes analyses of marsupial and monotreme immunoglobulin and T cell receptor genetics and expression published over the past decade. Analyses of recently completed whole genome sequences from the opossum and the platypus have yielded insight into the evolution of the common antigen receptor systems, as well as discovery of novel receptors that appear to have been lost in eutherian mammals. These species are also useful for investigation of the development of the immune system in organisms notable for giving birth to highly altricial young, as well as the evolution of maternal immunity through comparison of oviparous and viviparous mammals.

(c) 2009 Elsevier Ltd. All rights reserved.

PMID: 20004116 http://www.ncbi.nlm.nih.gov/pubmed/20004116

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2880534

2008

Genome analysis of the platypus reveals unique signatures of evolution

Nature. 2008 May 8;453(7192):175-83.

Warren WC, Hillier LW, Marshall Graves JA, Birney E, Ponting CP, Grützner F, Belov K, Miller W, Clarke L, Chinwalla AT, Yang SP, Heger A, Locke DP, Miethke P, Waters PD, Veyrunes F, Fulton L, Fulton B, Graves T, Wallis J, Puente XS, López-Otín C, Ordóñez GR, Eichler EE, Chen L, Cheng Z, Deakin JE, Alsop A, Thompson K, Kirby P, Papenfuss AT, Wakefield MJ, Olender T, Lancet D, Huttley GA, Smit AF, Pask A, Temple-Smith P, Batzer MA, Walker JA, Konkel MK, Harris RS, Whittington CM, Wong ES, Gemmell NJ, Buschiazzo E, Vargas Jentzsch IM, Merkel A, Schmitz J, Zemann A, Churakov G, Kriegs JO, Brosius J, Murchison EP, Sachidanandam R, Smith C, Hannon GJ, Tsend-Ayush E, McMillan D, Attenborough R, Rens W, Ferguson-Smith M, Lefèvre CM, Sharp JA, Nicholas KR, Ray DA, Kube M, Reinhardt R, Pringle TH, Taylor J, Jones RC, Nixon B, Dacheux JL, Niwa H, Sekita Y, Huang X, Stark A, Kheradpour P, Kellis M, Flicek P, Chen Y, Webber C, Hardison R, Nelson J, Hallsworth-Pepin K, Delehaunty K, Markovic C, Minx P, Feng Y, Kremitzki C, Mitreva M, Glasscock J, Wylie T, Wohldmann P, Thiru P, Nhan MN, Pohl CS, Smith SM, Hou S, Nefedov M, de Jong PJ, Renfree MB, Mardis ER, Wilson RK. Source Genome Sequencing Center, Washington University School of Medicine, Campus Box 8501, 4444 Forest Park Avenue, St Louis, Missouri 63108, USA. wwarren@wustl.edu Erratum in Nature. 2008 Sep 11;455(7210):256. Nefedov, Mikhail [added]; de Jong, Pieter J [added]. Abstract We present a draft genome sequence of the platypus, Ornithorhynchus anatinus. This monotreme exhibits a fascinating combination of reptilian and mammalian characters. For example, platypuses have a coat of fur adapted to an aquatic lifestyle; platypus females lactate, yet lay eggs; and males are equipped with venom similar to that of reptiles. Analysis of the first monotreme genome aligned these features with genetic innovations. We find that reptile and platypus venom proteins have been co-opted independently from the same gene families; milk protein genes are conserved despite platypuses laying eggs; and immune gene family expansions are directly related to platypus biology. Expansions of protein, non-protein-coding RNA and microRNA families, as well as repeat elements, are identified. Sequencing of this genome now provides a valuable resource for deep mammalian comparative analyses, as well as for monotreme biology and conservation.

PMID: 18464734 [PubMed - indexed for MEDLINE] PMCID: PMC2803040

http://www.ncbi.nlm.nih.gov/pubmed/18464734

2007

Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences

Nature. 2007 May 10;447(7141):167-77.

Mikkelsen TS, Wakefield MJ, Aken B, Amemiya CT, Chang JL, Duke S, Garber M, Gentles AJ, Goodstadt L, Heger A, Jurka J, Kamal M, Mauceli E, Searle SM, Sharpe T, Baker ML, Batzer MA, Benos PV, Belov K, Clamp M, Cook A, Cuff J, Das R, Davidow L, Deakin JE, Fazzari MJ, Glass JL, Grabherr M, Greally JM, Gu W, Hore TA, Huttley GA, Kleber M, Jirtle RL, Koina E, Lee JT, Mahony S, Marra MA, Miller RD, Nicholls RD, Oda M, Papenfuss AT, Parra ZE, Pollock DD, Ray DA, Schein JE, Speed TP, Thompson K, VandeBerg JL, Wade CM, Walker JA, Waters PD, Webber C, Weidman JR, Xie X, Zody MC; Broad Institute Genome Sequencing Platform; Broad Institute Whole Genome Assembly Team, Graves JA, Ponting CP, Breen M, Samollow PB, Lander ES, Lindblad-Toh K. Source Broad Institute of MIT and Harvard, 7 Cambridge Center, Cambridge, Massachusetts 02142, USA. kersli@broad.mit.edu

Abstract

We report a high-quality draft of the genome sequence of the grey, short-tailed opossum (Monodelphis domestica). As the first metatherian ('marsupial') species to be sequenced, the opossum provides a unique perspective on the organization and evolution of mammalian genomes. Distinctive features of the opossum chromosomes provide support for recent theories about genome evolution and function, including a strong influence of biased gene conversion on nucleotide sequence composition, and a relationship between chromosomal characteristics and X chromosome inactivation. Comparison of opossum and eutherian genomes also reveals a sharp difference in evolutionary innovation between protein-coding and non-coding functional elements. True innovation in protein-coding genes seems to be relatively rare, with lineage-specific differences being largely due to diversification and rapid turnover in gene families involved in environmental interactions. In contrast, about 20% of eutherian conserved non-coding elements (CNEs) are recent inventions that postdate the divergence of Eutheria and Metatheria. A substantial proportion of these eutherian-specific CNEs arose from sequence inserted by transposable elements, pointing to transposons as a major creative force in the evolution of mammalian gene regulation.

PMID: 17495919 http://www.ncbi.nlm.nih.gov/pubmed/17495919

2003

Immunoglobulin genetics of Ornithorhynchus anatinus (platypus) and Tachyglossus aculeatus (short-beaked echidna)

Comp Biochem Physiol A Mol Integr Physiol. 2003 Dec;136(4):811-9. Belov K, Hellman L. Source Evolutionary Biology Unit, Australian Museum, 6 College Street, Sydney 2010, Australia. kathyb@austmus.gov.au Abstract In this paper, we review data on the monotreme immune system focusing on the characterisation of lymphoid tissue and of antibody responses, as well the recent cloning of immunoglobulin genes. It is now known that monotremes utilise immunoglobulin isotypes that are structurally identical to those found in marsupials and eutherians, but which differ to those found in birds and reptiles. Monotremes utilise IgM, IgG, IgA and IgE. They do not use IgY. Their IgG and IgA constant regions contain three domains plus a hinge region. Preliminary analysis of monotreme heavy chain variable region diversity suggests that the platypus primarily uses a single VH clan, while the short-beaked echidna utilises at least 4 distinct VH families which segregate into all three mammalian VH clans. Phylogenetic analysis of the immunoglobulin heavy chain constant region gene sequences provides strong support for the Theria hypothesis. The constant region of IgM has proven to be a useful marker for estimating the time of divergence of mammalian lineages.

PMID: 14667846 http://www.ncbi.nlm.nih.gov/pubmed/14667846

1991

Cartilaginous bone extremities of growing monotremes appear unique

Anat Rec. 1991 Apr;229(4):447-52.

Thorp BH, Dixon JM. Source Department of Veterinary Preclinical Science, University of Melbourne, Parkville, Victoria, Australia.

Abstract

Cartilage canals are present in the epiphyseal cartilage of most mammals and birds. They are considered necessary for the maintenance of chondrocytes and for the formation of epiphyseal ossification centers. The epiphyseal cartilage of marsupials was recently shown not to contain cartilage canals, and placental rats appear not to have cartilage canals, although some confusion exists in the literature. The present study examines the cartilaginous epiphyses and physes from the knee and hip of the rat and the two Australian monotremes (platypus, Ornithorhynchus anatinus and echidna, Tachyglossus aculeatus). In all three species, cartilage canals were absent. Vessels to epiphyseal ossification centers were present, however. In the center of the cartilaginous femoral head of the echidna, but not in the platypus or rat, there was a large cavity, which contained connective tissue and was lined by an endochondrium of chondroproginator cells. These appeared to be contributing to growth of the cartilaginous epiphysis. No similar structure has previously been described in the cartilaginous epiphysis of other species. There was no ligament of the femoral head in the hip joints of the monotremes, and it is suggested the absence of a ligament may be significant in the development of the cavity. It was noted in all specimens that despite being avascular the epiphyseal and physeal cartilage appeared viable and functionally normal. The small size of the cartilaginous epiphyses of the rat may account for their avascularity; but the epiphyses of the monotremes were much larger, especially the echidna, yet still avascular. These features provide strong evidence for fundamental differences between the avascular cartilage of monotremes and the vascular cartilage of most mammals.

PMID 2048749

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