The "Standard Event System" (SES) to Study Vertebrate Embryos was developed in 2009 to establish a common language in comparative embryology.[1] Homologous developmental characters are defined therein and should be recognisable in all vertebrate embryos. The SES includes a protocol on how to describe and depict vertebrate embryonic characters. The SES was initially developed for external developmental characters of organogenesis, particularly for turtle embryos. However, it is expandable both taxonomically and in regard to anatomical or molecular characters. This article should act as an overview on the species staged with SES and document the expansions of this system. New entries need to be validated based on the citation of scientific publications. The guideline on how to establish new SES-characters and to describe species can be found in the original paper of Werneburg (2009).[1]
SES-characters are used to reconstruct ancestral developmental sequences in evolution such as that of the last common ancestor of placental mammals.[2] Also the plasticity of developmental characters can be documented and analysed.
SES-staged species
Overview on the vertebrate species staged with SES.
New SES-characters are continuously described in new publications. Currently, characters of organogenesis are described for Vertebrata (V), Gnathostomata (G), Tetrapoda (T), Amniota (A), Sauropsida (S), Squamata (SQ), Mammalia (M), and Monotremata (MO). In total, 166 SES-characters are currently defined.
Character complex
Character
Character description
Reference
Illustration
A. Egg (V01).
A1. Egg lay (V01a).
Most authors begin to create their staging tables shortly after or around egg lay time.
The dorsal borders of the neural folds come in touch and begin to form the neural tube that encloses the neural tube. The anterior and posterior regions of the primitive streak remain open.
Correlated to the internal differentiation and partly due to the carapace forming in turtles somite borders become blurred in specific regions until somites are completely inconspicuous.
The total number of somite pairs is count, filled in a formula for each specimen and afterwards grouped within the somite cluster of five somites each. Seldom the left and the right side show a different number of mesodermal segments. By definition the row with the maximum is to be count. Often a somite pair underlies a forming process. This one should also be counted.
The forming of a mesencephalic (or/and a diencephalic) projection in the posterodorsal region of the head is characterized by a continuing growth and can not be defined as a distinguishable event. But the disappearance of the structure resulting in a flat occipital head region can be well defined and is possibly associated to skull ossification.
An optic vesicle forms lateral of the prosencephalic region. It can be mistaken for the trigeminal ganglion which is proportional enlarged in Tachyglossus or Monodelphis at this early period of development. But the ganglion lies more caudally.
The optic or choroid fissure represents the blood vessel agglomeration, which supplies the developing lens. It forms a clear streak between the lens and the ventral most curvature of the optic cup. When the lens is completely formed the optic fissure disappears, which is a fluent process that can not be defined as a distinct event.
Although in many references a tail is arbitrarily described very early or in association to the development to the hind limb bud here the occurrence of the tail bud is defined as a distinct constriction of the caudal body region.
On the distal part of the forelimb bud an apical ectodermal ridge (AER) is formed in a horizontal longitude. Often it is only visible as a slightly eruption and in a particular angle of view.
In the distal region of the forelimb a round digital plate is formed by flattening of its paddle like end in a horizontal plane. The digital plate is clearly separated from the tube shaped leg by a surrounding step.
Scales on the dorsum of the head occur. The forming of scutes on throat and lower eyelid are encoded separately. Due feathers and scales are assumed to be homologous the scale characters are also applicable to bird development. Mammalian hears are formed differently and are not regarded here.
O. Maxillary process of the mandibular arch (G01).
O1. Maxillary bud (G01a).
The maxillary process of the mandibular arch occurs as a bud posterior to the eye. Often it is clearly seen as the anterodorsal process of the first pharyngeal arch.
O. Maxillary process of the mandibular arch (G01).
O2. Maxillary process posterior to eye (G01b).
The maxillary process lies posterior to the eye for a long period. First, when a clear rostrad development of the maxillary process is recognizable, its position at the level of the posterior margin of the optic cup should be noted. For identifying the level of the maxillary process in respect to the eye the ventral border of the telencephalic/diencephalic head region must be orientated horizontally.
O. Maxillary process of the mandibular arch (G01).
O4. Maxillary process anterior to lens (G01d).
The tip of the maxillary process is located beyond the optic fissure and is situated around the level of the anterior borders of pupil, iris, lens and scleral papillae.
The first pharyngeal (mandibular) arch is generally the first pharyngeal arch to occur as a bud. It forms later on a dorsal maxillary and a ventral mandibular process.
P2. Mandibular process of the mandibular arch posterior eye (G02b).
The mandibular process lays posterior to the eye for a long period. First, when a clear rostrad development of the mandibular process is recognizable, its position around the level of the posterior margin of the optic cup should be noted. For defining the level of the mandibular process in respect to the eye the ventral border of the telencephalic/diencephalic head region must be orientated horizontally.
The tip of the mandibular process is located beyond the optic fissure and is situated around the level of the anterior borders of pupil, iris, lens and scleral papillae.
During development of different species a 90° cervical flexure can occur and reverse several times. Only the first occurrence of a 90° cervical flexure is to be noted.
The caruncle (egg tooth) is first visible as a medial calcification of the skin that covers the symphysis of the maxillaries and lies between the nasal openings. Later on it enlarges and fuses with the maxillaries to get a mechanical support for slashing the egg while hatching.
The everted hemipenes are seen as paired structures sticking out on each side of the cloaca. Depending on the taxa, different forms are possible. The hemipenes are only found in males.
^Werneburg and Spiekman (2016). Mammalian embryology and organogenesis. From gametes to weaning. In: Zachos F., Asher R. (eds.). Mammalia. Series: The Handbook of Zoology / Handbuch der Zoologie. De Gruyter, Berlin
^ abcdefghWerneburg I and Sánchez-Villagra MS (2009). Timing of organogenesis support basal position of turtles in the amniote tree of life. BMC Evolutionary Biology, 9:82 http://www.biomedcentral.com/1471-2148/9/82
^Werneburg I, Hugi J, Müller J, Sánchez-Villagra MS (2009). Embryogenesis and ossification of Emydura subglobosa (Testudines, Pleurodira, Chelidae) and patterns of turtle development. Developmental Dynamics, Volume 238, Issue 11 Pages 2770-2786 http://onlinelibrary.wiley.com/doi/10.1002/dvdy.22104/abstract
^Nunes Silva R and Sobral Sampaio F (2014). Immunoreactivity of Mel1a-like melatonin receptor and NRH: Quinone reductase enzyme (QR2) in testudine whole embryo and in developing whole retinas Trends in Developmental Biology 8:39-46.
^ abcdPolachowski KM and Werneburg I (2013). Late embryos and bony skull development in Bothropoides jararaca (Serpentes, Viperidae). Zoology
^Roscito and Rodriges (2012). Embryonic development of the fossorial gymnophthalmid lizards Nothobachia ablephara and Calyptommatus sinebranchiatus. Zoology 115:302-318
^Werneburg et al. (2015). Bony skull development in the Argus monitor (Squamata, Varanidae, Varanus panoptes) with comments on developmental timing and adult anatomy. Zoology 118(4):255-280
^Ollonen, J., Da Silva, F.O., Mahlow, K. and Di-Poï, N., 2018. Skull development, ossification pattern, and adult shape in the emerging lizard model organism Pogona vitticeps: a comparative analysis with other squamates. Frontiers in physiology, 9, p.278.
^ abcdefghijklmnopqrstuvwxyzaaabacadaeafWerneburg I, Laurin M, Koyabu D, Sánchez-Villagra (2016). Evolution of organogenesis and the origin of altriciality in mammals. Evolution and Development
^González B, Soria-Escobar AM, Rojas-Díaz V, Pustovrh MC, Monsalve LS, Rougier GW (2020). The embryo of the silky shrew opossum, Caenolestes fuliginosus (Tomes, 1863): First description of the embryo of Paucituberculata. Journal of Morphology 2020: 1-12
^ abWerneburg I, Tzika AC, Hautier L, Asher RJ, Milinkovitch MC, Sánchez-Villagra MR (2013). Development and embryonic staging in non-model organisms: the case of an afrotherian mammal. The Journal of Anatomy 222:2-18
^ abcdefghTaro Nojiri, Dai Fukui, Ingmar Werneburg, Takashi Saitoh, Hideki Endo, Daisuke Koyabu (2021). Embryonic staging of bats with special reference to Vespertilio sinensis and its cochlear development. Development Dynamics, DOI10.1002/dvdy.325
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