The early development of the echidna, Tachyglossus aculeatus (Mammalia: Monotremata), and patterns of mammalian development

Werneburg, Ingmar; Sánchez‐Villagra, Marcelo R.

doi:10.1111/j.1463-6395.2009.00447.x

Cited by 40 publications

(60 citation statements)

References 67 publications

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“…A mosaic of derived and plesiomorphic characters in monotremes, as exemplified by our analysis of the echidna rhodopsin sequence, has also been reported from anatomic, genomic, physiological, and developmental studies (Bolk et al, 1934;Gresser & Noback, 1935;Griffiths, 1989;Young & Pettigrew, 1991;Warren et al, 2008;Werneburg & Sánchez-Villagra, 2010). This aspect of the echidna rhodopsin sequence would support the yet controversial Theria hypothesis that monotremes are sister to marsupials and placentals (Janke et al, 2002;Rowe et al, 2008).…”

Section: Echidna Rhodopsin Sequence Analysissupporting

confidence: 85%

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Functional characterization of the rod visual pigment of the echidna (Tachyglossus aculeatus), a basal mammal

et al. 2012

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Monotremes are the most basal egg-laying mammals comprised of two extant genera, which are largely nocturnal. Visual pigments, the first step in the sensory transduction cascade in photoreceptors of the eye, have been examined in a variety of vertebrates, but little work has been done to study the rhodopsin of monotremes. We isolated the rhodopsin gene of the nocturnal short-beaked echidna (Tachyglossus aculeatus) and expressed and functionally characterized the protein in vitro. Three mutants were also expressed and characterized: N83D, an important site for spectral tuning and metarhodopsin kinetics, and two sites with amino acids unique to the echidna (T158A and F169A). The k max of echidna rhodopsin (497.9 6 1.1 nm) did not vary significantly in either T158A (498.0 6 1.3 nm) or F169A (499.4 6 0.1 nm) but was redshifted in N83D (503.8 6 1.5 nm). Unlike other mammalian rhodopsins, echidna rhodopsin did react when exposed to hydroxylamine, although not as fast as cone opsins. The retinal release rate of light-activated echidna rhodopsin, as measured by fluorescence spectroscopy, had a half-life of 9.5 6 2.6 min À1 , which is significantly shorter than that of bovine rhodopsin. The half-life of the N83D mutant was 5.1 6 0.1 min À1 , even shorter than wild type. Our results show that with respect to hydroxylamine sensitivity and retinal release, the wild-type echidna rhodopsin displays major differences to all previously characterized mammalian rhodopsins and appears more similar to other nonmammalian vertebrate rhodopsins such as chicken and anole. However, our N83D mutagenesis results suggest that this site may mediate adaptation in the echidna to dim light environments, possibly via increased stability of light-activated intermediates. This study is the first characterization of a rhodopsin from a most basal mammal and indicates that there might be more functional variation in mammalian rhodopsins than previously assumed.

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Section: Echidna Rhodopsin Sequence Analysissupporting

confidence: 85%

“…All living monotremes are nocturnal, homeothermic, and possess a low rate of reproduction (Dawson et al, 1979;Rismiller, 1999;Werneburg & Sánchez-Villagra, 2010). However, some diurnal activity has also been occasionally observed for echidnas (T. aculeatus multiaculeatus) (Rismiller & McKelvey, 2009).…”

Section: Introductionmentioning

confidence: 99%

Functional characterization of the rod visual pigment of the echidna (Tachyglossus aculeatus), a basal mammal

et al. 2012

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“…Many works have emphasized the necessity to use comparative and quantitative approaches to document the evolution of the phenotype in parallel to experimental and genomic studies, and for that the expansion of the set of model species for developmental studies is fundamental (Jenner and Wills 2007;Milinkovitch and Tzika 2007). Among the recent descriptions of staging systems or developmental series in mammals are those of some bats (Cretekos et al 2005;Tokita 2006;Wang et al 2010), tenrecs (Werneburg et al 2013a), and the echidna (Werneburg and Sánchez-Villagra 2011). These studies have been stimulated not only by the experimental approaches to understand evolutionary novelties arising in development and involving molecular biology (e.g., Sears 2011;Tokita et al 2012;Montandon et al 2014).…”

Section: Integrating Traditional Embryology With Modern Analytical Tementioning

confidence: 99%

“…Many features can be used to characterize developing mammals externally, and each can evolve. Among them are aspects of the integument such as hair, the limbs, and structures of the head such as the external ear or the eyelids (Schoenwolf 2008;Werneburg and Sánchez-Villagra 2011;Werneburg et al 2016).…”

Section: Introductionmentioning

confidence: 99%

Mammalian organogenesis in deep time: tools for teaching and outreach

Sánchez‐Villagra

Werneburg

2016

Evo Edu Outreach

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Mammals constitute a rich subject of study on evolution and development and provide model organisms for experimental investigations. They can serve to illustrate how ontogeny and phylogeny can be studied together and how the reconstruction of ancestors of our own evolutionary lineage can be approached. Likewise, mammals can be used to promote 'tree thinking' and can provide an organismal appreciation of evolutionary changes. This subject is suitable for the classroom and to the public at large given the interest and familiarity of people with mammals and their closest relatives. We present a simple exercise in which embryonic development is presented as a transformative process that can be observed, compared, and analyzed. In addition, we provide and discuss a freely available animation on organogenesis and life history evolution in mammals. An evolutionary tree can be the best tool to order and understand those transformations for different species. A simple exercise introduces the subject of changes in developmental timing or heterochrony and its importance in evolution. The developmental perspective is relevant in teaching and outreach efforts for the understanding of evolutionary theory today.

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“…development within the leathery-shelled egg) is of 10-11 days duration [Renfree et al, 2009]. Neural development during incubation begins with neural tube closure, but the forebrain is still very immature at hatching [Werneburg and Sánchez-Villagra, 2011]. It is convenient to divide incubation into three subphases of about 3-4 days duration each.…”

Section: Development Of the Trigeminal Sensory Nuclei In Pre-and Perimentioning

confidence: 99%

Distinct Development of the Trigeminal Sensory Nuclei in Platypus and Echidna

Ashwell¹,

Hardman²

2012

Brain Behav Evol

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Both lineages of the modern monotremes have been reported to be capable of electroreception using the trigeminal pathways and it has been argued that electroreception arose in an aquatic platypus-like ancestor of both modern monotreme groups. On the other hand, the trigeminal sensory nuclear complex of the platypus is highly modified for processing tactile and electrosensory information from the bill, whereas the trigeminal sensory nuclear complex of the short-beaked echidna (Tachyglossus aculeatus) is not particularly specialized. If the common ancestor for both platypus and echidna were an electroreceptively and trigeminally specialized aquatic feeder, one would expect the early stages of development of the trigeminal sensory nuclei in both species to show evidence of structural specialization from the outset. To determine whether this is the case, we examined the development of the trigeminal sensory nuclei in the platypus and short-beaked echidna using the Hill and Hubrecht embryological collections. We found that the highly specialized features of the platypus trigeminal sensory nuclei (i.e. the large size of the principal nucleus and oral part of the spinal trigeminal nuclear complex, and the presence of a dorsolateral parvicellular segment in the principal nucleus) appear around the time of hatching in the platypus, but are never seen at any stage in the echidna. Our findings support the proposition that the modern echidna and platypus are derived from a common ancestor with only minimal trigeminal specialization and that the peculiar anatomy of the trigeminal sensory nuclei in the modern platypus emerged in the ornithorhynchids after divergence from the tachyglossids.

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The early development of the echidna, Tachyglossus aculeatus (Mammalia: Monotremata), and patterns of mammalian development

Cited by 40 publications

References 67 publications

Functional characterization of the rod visual pigment of the echidna (Tachyglossus aculeatus), a basal mammal

Functional characterization of the rod visual pigment of the echidna (Tachyglossus aculeatus), a basal mammal

Mammalian organogenesis in deep time: tools for teaching and outreach

Distinct Development of the Trigeminal Sensory Nuclei in Platypus and Echidna

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