An Integrated Perspective of Evolution and Development: From Genes to Function to Ear, Lateral Line and Electroreception

Abstract

Four sensory systems (vestibular, lateral line, electroreception, auditory) are unique and project exclusively to the brainstem of vertebrates. All sensory neurons depend on a common set of genes (Eya1, Sox2, Neurog1, Neurod1) that project to a dorsal nucleus and an intermediate nucleus, which differentiate into the vestibular ear, lateral line and electroreception in vertebrates. In tetrapods, a loss of two sensory systems (lateral line, electroreception) leads to the development of a unique ear and auditory system in amniotes. Lmx1a/b, Gdf7, Wnt1/3a, BMP4/7 and Atoh1 define the lateral line, electroreception and auditory nuclei. In contrast, vestibular nuclei depend on Neurog1/2, Ascl1, Ptf1a and Olig3, among others, to develop an independent origin of the vestibular nuclei. A common origin of hair cells depends on Eya1, Sox2 and Atoh1, which generate the mechanosensory cells. Several proteins define the polarity of hair cells in the ear and lateral line. A unique connection of stereocilia requires CDH23 and PCDH15 for connections and TMC1/2 proteins to perceive mechanosensory input. Electroreception has no polarity, and a different system is used to drive electroreceptors. All hair cells function by excitation via ribbons to activate neurons that innervate the distinct target areas. An integrated perspective is presented to understand the gain and loss of different sensory systems.

Vision and retina evolution: How to develop a retina

“…We propose two different sized clusters in Thalia and Ciona evolved into pineal/parapineal and the third, largest, cluster evolved into the lateral eyes of vertebrates. By analogy with a split into distinct cell types (sensory cells and ganglion cells) from a single cell type (neurosensory cells) in lancelet and ascidians ( Fritzsch, 2021 , Fritzsch and Elliott, 2017 , Holland and Daza, 2018 ), we suggest a split into distinct retina-like structures that is shown by the presence in lampreys of the pineal, parapineal, and bilateral retinas proper. An intermediate stage of this process may be represented by the direct neuropil projections of sensory cells in certain lampreys and hagfish.…”

“…Emergence of the genes Atoh in sensory cells and Neurog in spinal cord has been demonstrated for ascidians ( Cao et al, 2019 , Stolfi et al, 2015 , Tang et al, 2013 ). Furthermore, a duplication of Neurog1/2 and formation of a bHLH gene, Neurod1 , is associated with the emergence of distinct sensory cells (under control of Atoh1 ) and neurons (under control of Neurog1/2; Neurod1 ) in vertebrates ( Fritzsch, 2021 ). In addition, we highlight the numbers of Neurod1 (4 in vertebrates), Neurog1 (3 in vertebrates), Atoh/atonal/lin-32 (2 in vertebrates,3 in flies) and Olig’s (3 in vertebrates, 2 in the lancelet; Fig.…”

“…CP, choroid plexus; DRG, dorsal root ganglia; WGD, whole genome duplication. Modified after ( Elliott et al, 2021 , 2022 ; Fritzsch, 2021 ; Holland, 2020 ; Holland and Daza, 2018 ; Stolfi, et al, 2015 ; Tang, et al, 2013 ; Zhao, et al, 2020 ).

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“…Among the two Atoh -like genes in ascidians, one is clearly related to Atoh1 and develops with Neurog to innervate the sensory cells and reach out to the anterior motor ganglion ( Cao et al, 2019 , Fritzsch, 2021 , Stolfi et al, 2015 , Tang et al, 2013 ). Another gene, Foxg1 , that is expressed in the olfactory system in vertebrates ( Dvorakova, et al, 2020 ) is also expressed in the brain, which is housed in the anterior neural plate ( C. intestinalis; Fig.…”

Neurosensory development of the four brainstem-projecting sensory systems and their integration in the telencephalon

“…Second-order neuronal projections from the trigeminal, solitary tract, vestibular, and cochlear nuclei project in a relay to several additional nuclei before reaching the thalamus, whereas other second-order predictions are direct. Compared to the trigeminal projection that is common across vertebrates, information from taste, vestibular, and auditory nuclei is limited, and in addition, there is a unique loss of lateral line and electroreception in some species that are instead developing the auditory nuclei from frogs and amniotes (Grothe et al, 2004;Wullimann and Grothe, 2013;Fritzsch, 2021).…”