The amniote paratympanic organ develops from a previously undiscovered sensory placode

Abstract

The paratympanic organ (PTO), a mechanosensory hair cell-containing pouch in the amniote middle ear, was first described 100 years ago yet its origins remain unresolved. Homology with the anamniote spiracular organ is supported by association with homologous skeletal elements and similar central targets of afferent neurons, suggesting it might be a remnant of the water-dependent lateral line system, otherwise lost during the amniote transition to terrestrial life. However, this is incompatible with studies suggesting it arises from the first epibranchial (geniculate) placode. Here we show that a previously undiscovered Sox2-positive placode, immediately dorsal to the geniculate placode, forms the PTO and its afferent neurons, which are molecularly and morphologically distinct from geniculate neurons. These data remove the only obstacle to accepting the homology of the PTO and spiracular organ. We hypothesise that the PTO/spiracular organ represents an ancient head ectoderm module, developmentally and evolutionarily independent of both lateral line and epibranchial placodes.

Vertebrate Cranial Placodes as Evolutionary Innovations—The Ancestor's Tale

“…Moreover, in lampreys and hagfishes, the adenohypophysis and olfactory epithelium arise from a single unpaired nasohypophyseal placode (Oisi, Ota, Kuraku, Fujimoto, & Kuratani, 2013;Uchida, Murakami, Kuraku, Hirano, & Kuratani, 2003) and only a reduced complement of adenohypophyseal cell types is present (see below). Finally, there are some smaller placodes, which are only found in some vertebrates such as the hypobranchial placodes of frogs which produce viscerosensory neurons of unknown function (Schlosser, 2003;Schlosser & Northcutt, 2000) and the paratympanic placode of birds, which forms the mechanoreceptors of the paratympanic organ and the sensory neurons innervating it (O'Neill, Mak, Fritzsch, Ladher, & Baker, 2012).…”

Evolution and Development of Hair Cell Polarity and Efferent Function in the Inner Ear

“…Many new insights now suggest a stepwise transformation of a general cell type that resembled a single cell ancestor of animals into a sensory hair cell. Four aspects appear to be relevant for the evolution of vertebrate mechanosensory hair cells: (a) the obvious similarity of developing mechanosensory hair cells to nonmechanosensory hair cells, such as vertebrate electroreceptive hair cells [Fritzsch, 1993;Jørgensen, 1989] but also to non-vertebrate sensory cells [Manley and Ladher, 2008;Rigon et al, 2013]; (b) the experimental evidence that all hair cells, including the electroreceptive, nonmechanosensory hair cells, derive from dorsolateral placodes [O'Neill et al, 2012]; (c) the molecular evidence that hair cells require a conserved transcription factor for their development and that this transcription factor can be exchanged between different phyla [Fritzsch et al, 2010], and (d) the existence of extremely conserved microRNAs that are uniquely associated with hair cell development and cause hair cell defects when only a single nucleotide is changed [Pierce et al, 2008].…”

Atoh1 in sensory hair cell development: constraints and cofactors

“…In Drosophila, the generation of external sensory organs (bristles) responsible for touch, requires the activity of bHLH transcription factors of the achaete-scute complex (15) (see Box 1). In vertebrates, Atoh1's function is confined to two different mechanosensory cell types: I) the above-mentioned hair cells, found both in the inner ear and in some animals also found in the lateral line and paratympanic organ (13,16,17); II) the epidermal Merkel cells necessary for encoding light touch responses (18). Thus, Atonal/Atoh1 govern the formation of only a subset of mechanosensory cells, but seem to have a particularly important conserved function in those cells that mediate hearing and balance.…”