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![Spatiotemporal development of lamprey cranial sensory ganglia. Anterior is to the left for all whole-mount images. (A) and (B) Low-power (A) and higher-power view (B) of an embryo at embryonic day 8 (E8) immunostained for the pan-neuronal Elav-family members HuC/D (Hu). HuC/D expression is strong in neurons within the neural tube, with fainter expression in neurons lateral to the rostral neural tube (arrowhead). (C) By E10, discrete lateral patches of HuC/D expression reveal the primordia of all cranial sensory ganglia except the nodose: the ophthalmic trigeminal ganglion (opV), the maxillomandibular trigeminal ganglion (mmV), the geniculate/anterior lateral line ganglionic complex (g/all), the petrosal ganglion (p) and the posterior lateral line ganglion (pll). (D)-(G) HuC/D immunostaining of embryos at E12 (D), E14 (E), E16 (F) and E18 (G) shows the development of the six nodose ganglia in a rostrocaudal sequence dorsal to the branchial arches and the progressive condensation of all the cranial ganglia. Dorsal root ganglia are also visible from E16, adjacent to the dorsal neural tube. (H)-(J) By E20, all the cranial sensory ganglia have formed. (H) Low-power and (I) schematic view of an E20 embryo, showing the location of cranial sensory ganglia [blue in (I)] and dorsal root ganglia [brown in (I)]. (J) A higher-power view of the boxed area in (H), showing distinct opV and mmV ganglia, the geniculate/anterior lateral line ganglionic complex, the vestibuloacoustic ganglion (medial to the otic vesicle, hence hardly stained in whole-mount), the petrosal ganglion, the posterior lateral line ganglion and the most rostral nodose ganglion (n1). (K) Transverse serial sections immunostained for HuC/D (green), starting near the rostral edge of the otic vesicle [see panel (J) for orientation of otic vesicle, which is indicated by a dotted oval] and progressing caudally through the geniculate/aLL ganglionic complex ventral to the otic vesicle (arrow, left-hand three images) and then the vestibuloacoustic ganglion medial to the otic vesicle (arrow, right-hand three images). In the fourth and fifth images, the developing intracapsular ganglion (second ganglion of the anterior lateral line nerve) may also be visible, medial to the vestibuloacoustic ganglion and slightly separated from it by a thin HuC/D-negative space (inset). Abbreviations: all, anterior lateral line ganglion; drgs, dorsal root ganglia; e, eye; g, geniculate ganglion; mmV, maxillomandibular trigeminal ganglion; n, nodose ganglion; opV, ophthalmic trigeminal (profundal) ganglion; ov, otic vesicle; p, petrosal ganglion; pll, posterior lateral line ganglion; va, vestibuloacoustic ganglion. Scale bars: (A)-(J) 0.2 mm; (K) 50 μm.](profile/David-Buckley-14/publication/259570288/figure/fig1/AS:613948067946525@1523388034676/Spatiotemporal-development-of-lamprey-cranial-sensory-ganglia-Anterior-is-to-the-left.png)
Spatiotemporal development of lamprey cranial sensory ganglia. Anterior is to the left for all whole-mount images. (A) and (B) Low-power (A) and higher-power view (B) of an embryo at embryonic day 8 (E8) immunostained for the pan-neuronal Elav-family members HuC/D (Hu). HuC/D expression is strong in neurons within the neural tube, with fainter expression in neurons lateral to the rostral neural tube (arrowhead). (C) By E10, discrete lateral patches of HuC/D expression reveal the primordia of all cranial sensory ganglia except the nodose: the ophthalmic trigeminal ganglion (opV), the maxillomandibular trigeminal ganglion (mmV), the geniculate/anterior lateral line ganglionic complex (g/all), the petrosal ganglion (p) and the posterior lateral line ganglion (pll). (D)-(G) HuC/D immunostaining of embryos at E12 (D), E14 (E), E16 (F) and E18 (G) shows the development of the six nodose ganglia in a rostrocaudal sequence dorsal to the branchial arches and the progressive condensation of all the cranial ganglia. Dorsal root ganglia are also visible from E16, adjacent to the dorsal neural tube. (H)-(J) By E20, all the cranial sensory ganglia have formed. (H) Low-power and (I) schematic view of an E20 embryo, showing the location of cranial sensory ganglia [blue in (I)] and dorsal root ganglia [brown in (I)]. (J) A higher-power view of the boxed area in (H), showing distinct opV and mmV ganglia, the geniculate/anterior lateral line ganglionic complex, the vestibuloacoustic ganglion (medial to the otic vesicle, hence hardly stained in whole-mount), the petrosal ganglion, the posterior lateral line ganglion and the most rostral nodose ganglion (n1). (K) Transverse serial sections immunostained for HuC/D (green), starting near the rostral edge of the otic vesicle [see panel (J) for orientation of otic vesicle, which is indicated by a dotted oval] and progressing caudally through the geniculate/aLL ganglionic complex ventral to the otic vesicle (arrow, left-hand three images) and then the vestibuloacoustic ganglion medial to the otic vesicle (arrow, right-hand three images). In the fourth and fifth images, the developing intracapsular ganglion (second ganglion of the anterior lateral line nerve) may also be visible, medial to the vestibuloacoustic ganglion and slightly separated from it by a thin HuC/D-negative space (inset). Abbreviations: all, anterior lateral line ganglion; drgs, dorsal root ganglia; e, eye; g, geniculate ganglion; mmV, maxillomandibular trigeminal ganglion; n, nodose ganglion; opV, ophthalmic trigeminal (profundal) ganglion; ov, otic vesicle; p, petrosal ganglion; pll, posterior lateral line ganglion; va, vestibuloacoustic ganglion. Scale bars: (A)-(J) 0.2 mm; (K) 50 μm.
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a b s t r a c t Cranial neurogenic placodes and the neural crest make essential contributions to key adult character-istics of all vertebrates, including the paired peripheral sense organs and craniofacial skeleton. Neurogenic placode development has been extensively characterized in representative jawed vertebrates (gnathostomes) but not in jawles...
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... developing cranial sensory ganglia in P. marinus embryos were visualized by whole-mount immunostaining for the neuro- nal Elav RNA-binding protein family members HuC/D (Hinman and Lou, 2008) (Fig. 1) and identified according to established descrip- tions of neurogenic placode and cranial ganglion development in the European brook lamprey Lampetra planeri (also referred to as P. planeri, Ammocoetes planeri) (von Kupffer, 1891(von Kupffer, , 1895Fisk, 1954), the river lamprey Lampetra fluviatilis (Damas, 1944) and the Arctic lamprey ...
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... of Lampetra; junior synonyms include Lethenteron japo- nicum and Lampetra japonica) ( Kuratani et al., 1997;Murakami and Watanabe, 2009). Starting at embryonic day (E) 8 (Piavis stage 12/ 13; Piavis, 1961;Richardson and Wright, 2003), HuC/D was observed in the neural tube, and more weakly, in presumptive opV and/or mmV placode-derived neurons (Fig. 1A and B). By E10 (Piavis stage 14), HuC/D expression revealed the separate opV and mmV ganglia; the small presumptive anterior lateral line (aLL) ganglion lying immediately dorsocaudal to the geniculate ganglion (i.e., the first epibranchial placode-derived ganglion, dorsal to the first pharyngeal pouch); and the very large posterior lateral ...
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... dorsocaudal to the geniculate ganglion (i.e., the first epibranchial placode-derived ganglion, dorsal to the first pharyngeal pouch); and the very large posterior lateral line (pLL) ganglion lying immediately dorsocaudal to the petrosal ganglion (i.e., the second epibranchial placode-derived ganglion, dorsal to the second pharyngeal pouch) (Fig. 1C). Fig. 1D-H show the further development of the cranial sensory ganglia between E12 and E20 (Piavis stages 14-17), now including the developing chain of nodose ganglia (i.e., the third and more caudal epibran- chial placode-derived ganglia, which form dorsal to the third and more caudal pharyngeal pouches), as well as dorsal root ...
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... to the geniculate ganglion (i.e., the first epibranchial placode-derived ganglion, dorsal to the first pharyngeal pouch); and the very large posterior lateral line (pLL) ganglion lying immediately dorsocaudal to the petrosal ganglion (i.e., the second epibranchial placode-derived ganglion, dorsal to the second pharyngeal pouch) (Fig. 1C). Fig. 1D-H show the further development of the cranial sensory ganglia between E12 and E20 (Piavis stages 14-17), now including the developing chain of nodose ganglia (i.e., the third and more caudal epibran- chial placode-derived ganglia, which form dorsal to the third and more caudal pharyngeal pouches), as well as dorsal root ganglia ( Fig. ...
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... 1C). Fig. 1D-H show the further development of the cranial sensory ganglia between E12 and E20 (Piavis stages 14-17), now including the developing chain of nodose ganglia (i.e., the third and more caudal epibran- chial placode-derived ganglia, which form dorsal to the third and more caudal pharyngeal pouches), as well as dorsal root ganglia ( Fig. 1F-H; compare with Figs. 7a and 8a in Kuratani et al., ...
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... E20 (Fig. 1H-J), almost all cranial sensory ganglia could be distinguished except the vestibuloacoustic ganglion (also uniden- tified in Kuratani et al., 1997), which lies medial to the otic vesicle. The whole-mount HuC/D immunostaining data at E20 are sum- marized in schematic form in Fig. 1I. HuC/D immunostaining on transverse serial sections (Fig. ...
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... E20 (Fig. 1H-J), almost all cranial sensory ganglia could be distinguished except the vestibuloacoustic ganglion (also uniden- tified in Kuratani et al., 1997), which lies medial to the otic vesicle. The whole-mount HuC/D immunostaining data at E20 are sum- marized in schematic form in Fig. 1I. HuC/D immunostaining on transverse serial sections (Fig. 1K) confirmed the presence of a large, seemingly contiguous ganglionic complex extending rostral and medial to the otic vesicle. This complex most likely comprises the fused geniculate and aLL ganglia, followed by the vestibulo- acoustic ganglion medial to the otic vesicle and ...
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... E20 (Fig. 1H-J), almost all cranial sensory ganglia could be distinguished except the vestibuloacoustic ganglion (also uniden- tified in Kuratani et al., 1997), which lies medial to the otic vesicle. The whole-mount HuC/D immunostaining data at E20 are sum- marized in schematic form in Fig. 1I. HuC/D immunostaining on transverse serial sections (Fig. 1K) confirmed the presence of a large, seemingly contiguous ganglionic complex extending rostral and medial to the otic vesicle. This complex most likely comprises the fused geniculate and aLL ganglia, followed by the vestibulo- acoustic ganglion medial to the otic vesicle and perhaps also the even more medial intracapsular ganglion ...
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... subsequent develop- ment for 12-14 days, to approximately E18-21 (Piavis stage 17). In embryos in which DiI was injected into a broad patch of anterodorsal head ectoderm, represented by the red dotted line in Fig. 4A, DiI was observed in the condensing opV and mmV ganglia by 12 days post-injection (dpi) (E18-19) (n ¼26; Fig. 4B; compare with Fig. 1G and H). Furthermore, ophthalmic (V1) and upper lip-innervating (V2/3A) nerve branches, originating respectively from the opV and mmV ganglia, were also labeled with DiI ( Fig. 4B arrows and inset). After sectioning in an oblique plane to include both ganglia, HuC/D immunostaining confirmed that the DiI-positive cells were located in the opV ...
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Citations
... In the Arctic lamprey L. camtschaticum, we confirmed that the trigeminal nerve has three main branches, as has been reported in gnathostomes generally. Although the homology of the anteriormost branch or ramus (i.e., the ophthalmic nerve, rV 1 ) is widely accepted, the homology of the other two branches is in doubt [11,20,21]. Therefore, we used the term "rV 2/3A " for the second branch and "rV 2/3B " for the third branch in the lamprey, according to Oisi et al. (2013) [20]; rV 2/3A mainly innervated the upper lip region, whereas rV 2/3B innervated the velar region ( Fig. 1a, b). ...
... Nevertheless, analysis of frozen sections showed that the expression was localized only on the distal side of the ganglion (Fig. 3e, f ). We also confirmed that HmxB was expressed in some sensory ganglia (i.e., gV 2/3 and gVII) by observing colocalization of the immunofluorescence signals of the HuC/HuD antibody (Fig. 2d), which labels developing neuronal somata [21]. ...
The evolutionary origin of the jaw remains one of the most enigmatic events in vertebrate evolution. The trigeminal nerve is a key component for understanding jaw evolution, as it plays a crucial role as a sensorimotor interface for the effective manipulation of the jaw. This nerve is also found in the lamprey, an extant jawless vertebrate. The trigeminal nerve has three major branches in both the lamprey and jawed vertebrates. Although each of these branches was classically thought to be homologous between these two taxa, this homology is now in doubt. In the present study, we compared expression patterns of Hmx, a candidate genetic marker of the mandibular nerve (rV3, the third branch of the trigeminal nerve in jawed vertebrates), and the distribution of neuronal somata of trigeminal nerve branches in the trigeminal ganglion in lamprey and shark. We first confirmed the conserved expression pattern of Hmx1 in the shark rV3 neuronal somata, which are distributed in the caudal part of the trigeminal ganglion. By contrast, lamprey Hmx genes showed peculiar expression patterns, with expression in the ventrocaudal part of the trigeminal ganglion similar to Hmx1 expression in jawed vertebrates, which labeled the neuronal somata of the second branch. Based on these results, we propose two alternative hypotheses regarding the homology of the trigeminal nerve branches, providing new insights into the evolutionary origin of the vertebrate jaw.
Supplementary Information
The online version contains supplementary material available at 10.1186/s40851-023-00222-9.
... We confirmed that also in river lamprey the dermomyotome, like in other vertebrates, contains cells expressing Pax3/7. The Pax3/7 protein belongs to a conservative cyclostome clade of orthologous sequences, including river lamprey LfPax37 [41][42][43][44]. The conservative nature of Pax3/7 in lampreys was also observed in Lampetra japonicum, where LjPax3/7-A was found to be closely related to the jawed Pax3 and Pax7 genes, early regulators of muscle specification [45]. ...
... The analysis of available data shows the conservative nature of amino acid sequences of the LfPax3/7 protein (Figure 6). The Pax3/7 protein belongs to a conservative cyclostome clade of orthologous sequences, including L. fluviatilis LfPax37, Eptatretus burger paired-box protein 3/7, and Lethenteron camtschaticum paired-domain transcription factor Pax3/7-A [41,43,44] (Figure 6A). The known, partial sequence fragment of LfPax37 shows a high degree of homology with both orthologues ( Figure 6A, black frame). ...
The river lamprey (L. fluviatilis) is a representative of the ancestral jawless vertebrate group. We performed a histological analysis of trunk muscle fiber differentiation during embryonal, larval, and adult musculature development in this previously unstudied species. Investigation using light, transmission electron (TEM), and confocal microscopy revealed that embryonal and larval musculature differs from adult muscle mass. Here, we present the morphological analysis of L. fluviatilis myogenesis, from unsegmented mesoderm through somite formation, and their differentiation into multinucleated muscle lamellae. Our analysis also revealed the presence of myogenic factors LfPax3/7 and Myf5 in the dermomyotome. In the next stages of development, two types of muscle lamellae can be distinguished: central surrounded by parietal. This pattern is maintained until adulthood, when parietal muscle fibers surround the central muscles on both sides. The two types show different morphological characteristics. Although lampreys are phylogenetically distant from jawed vertebrates, somite morphology, especially dermomyotome function, shows similarity. Here we demonstrate that somitogenesis is a conservative process among all vertebrates. We conclude that river lamprey myogenesis shares features with both ancestral and higher vertebrates.
... Bona fide neural crest and placode cells are first evident in jawless vertebrates (hagfishes and lampreys), which form a monophyletic group, Cyclostomata (Kuraku, Hoshiyama, Katoh, Suga, & Miyata, 1999;McCauley & Bronner-Fraser, 2003;Modrell et al., 2014;Ota et al., 2007;Stock & Whitt, 1992). Many fossils suggest that the body plan of the early vertebrate ancestor was similar to the body-plan of extant jawless fish ( Janvier, 1996;Janvier & Janvier, 2008). ...
During the course of evolution, animals have become increasingly complex by the addition of novel cell types and regulatory mechanisms. A prime example is represented by the lateral neural border, known as the neural plate border in vertebrates, a region of the developing ectoderm where presumptive neural and non-neural tissue meet. This region has been intensively studied as the source of two important embryonic cell types unique to vertebrates—the neural crest and the ectodermal placodes—which contribute to diverse differentiated cell types including the peripheral nervous system, pigment cells, bone, and cartilage. How did these multipotent progenitors originate in animal evolution? What triggered the elaboration of the border during the course of chordate evolution? How is the lateral neural border patterned in various bilaterians and what is its fate? Here, we review and compare the development and fate of the lateral neural border in vertebrates and invertebrates and we speculate about its evolutionary origin. Taken together, the data suggest that the lateral neural border existed in bilaterian ancestors prior to the origin of vertebrates and became a developmental source of exquisite evolutionary change that frequently enabled the acquisition of new cell types.
... There are many similarities in head development between jawed and jawless vertebrates, including sensory systems and the central nervous system. For example, most jawed vertebrate placodes are clearly identifiable in lampreys [51,52]; cranial nerve organization is similar [51] and gross brain organization well-conserved [53,54]. There is, however, an important difference in the olfactory system. ...
Vertebrates develop an olfactory system that detects odorants and pheromones through their interaction with specialized cell surface receptors on olfactory sensory neurons. During development, the olfactory system forms from the olfactory placodes, specialized areas of the anterior ectoderm that share cellular and molecular properties with placodes involved in the development of other cranial senses. The early-diverging chordate lineages amphioxus, tunicates, lampreys and hagfishes give insight into how this system evolved. Here, we review olfactory system development and cell types in these lineages alongside chemosensory receptor gene evolution, integrating these data into a description of how the vertebrate olfactory system evolved. Some olfactory system cell types predate the vertebrates, as do some of the mechanisms specifying placodes, and it is likely these two were already connected in the common ancestor of vertebrates and tunicates. In stem vertebrates, this evolved into an organ system integrating additional tissues and morphogenetic processes defining distinct olfactory and adenohypophyseal components, followed by splitting of the ancestral placode to produce the characteristic paired olfactory organs of most modern vertebrates.
... Samples were then washed at least three times for 10 min in PBS-Triton X-100 and imaged. HuC/D IHC was performed essentially as described previously 62,67 , diluting the primary antibody (Fisher A-21271) 1:200, and the Alexa Fluor 488-conjugated secondary antibody 1:150 (Fisher A-11001), both in block (5% goat serum). ...
Neural crest cells (NCCs) are migratory, multipotent embryonic cells that are unique to vertebrates and form an array of clade-defining adult features. The evolution of NCCs has been linked to various genomic events, including the evolution of new gene-regulatory networks1,2, the de novo evolution of genes³ and the proliferation of paralogous genes during genome-wide duplication events⁴. However, conclusive functional evidence linking new and/or duplicated genes to NCC evolution is lacking. Endothelin ligands (Edns) and endothelin receptors (Ednrs) are unique to vertebrates3,5,6, and regulate multiple aspects of NCC development in jawed vertebrates7–10. Here, to test whether the evolution of Edn signalling was a driver of NCC evolution, we used CRISPR–Cas9 mutagenesis¹¹ to disrupt edn, ednr and dlx genes in the sea lamprey, Petromyzon marinus. Lampreys are jawless fishes that last shared a common ancestor with modern jawed vertebrates around 500 million years ago¹². Thus, comparisons between lampreys and gnathostomes can identify deeply conserved and evolutionarily flexible features of vertebrate development. Using the frog Xenopus laevis to expand gnathostome phylogenetic representation and facilitate side-by-side analyses, we identify ancient and lineage-specific roles for Edn signalling. These findings suggest that Edn signalling was activated in NCCs before duplication of the vertebrate genome. Then, after one or more genome-wide duplications in the vertebrate stem, paralogous Edn pathways functionally diverged, resulting in NCC subpopulations with different Edn signalling requirements. We posit that this new developmental modularity facilitated the independent evolution of NCC derivatives in stem vertebrates. Consistent with this, differences in Edn pathway targets are associated with differences in the oropharyngeal skeleton and autonomic nervous system of lampreys and modern gnathostomes. In summary, our work provides functional genetic evidence linking the origin and duplication of new vertebrate genes with the stepwise evolution of a defining vertebrate novelty.
... Additionally, a handful of transcription factors that are important in development of the ectoderm generally, and neural crest specifically, also have overlapping functions in early placode development (e.g., Dlx, Msx, Pax, Zic families, Tfap2a, Gata, and Foxi). Of these, there is evidence that a "Pax code" involving Pax6, Pax3/7, and Pax2/5/8 may pattern placodes along the anterior-posterior axis (Mansouri et al., 1996;Dahl et al., 1997;Baker and Bronner-Fraser, 2000;Modrell et al., 2014). Finally, cell type differentiation of placodes requires the activity of transcription factors known to regulate neural and sensory cell differentiation in deuterostomes and bilaterians, including homologs of atonal (Ath1 or Math1 in mouse) and achaete-scute (Ash1 or Mash1 in mouse), as well as NeuroD, Islet1, Phox2a, Phox2b, Brn3a, and Brn3c (Schlosser, 2006). ...
... In general, lampreys have homologs of many of the same placodes and placode-derived structures as present in jawed vertebrates, including, olfactory, adenohypophyseal, lens, trigeminal, otic, epibranchial, and lateral line Bronner-Fraser, 2002, 2003;Modrell et al., 2014). There are a few differences between lampreys and jawed vertebrates as well. ...
... The fused adenohypophyseal placode in lampreys produces the monorhine state of jawless vertebrates compared to that of diplorhiny in jawed vertebrates, and its separation into separate primordia may have precipitated the evolution of articulated jaws in gnathostomes (Murakami et al., 2001;Oisi et al., 2013b). Another difference, revealed by fate-mapping experiments, was that the separate upper lip and lower lip (velum) innervation patterns by neurons of trigeminal maxillomandibular (mmV) origin in the lamprey mouth may result from these placodes arising as distinct primordia early in development (Modrell et al., 2014). The developmental mechanisms underlying formation of the PPE in lampreys are almost entirely unknown, with the exception of DlxB expression uniquely defining this region, along with overlapping expression of MsxA and Tfap2a, among others (Sauka-Spengler et al., 2007). ...
Neural crest and placodes are key innovations of the vertebrate clade. These cells arise within the dorsal ectoderm of all vertebrate embryos and have the developmental potential to form many of the morphological novelties within the vertebrate head. Each cell population has its own distinct developmental features and generates unique cell types. However, it is essential that neural crest and placodes associate together throughout embryonic development to coordinate the emergence of several features in the head, including almost all of the cranial peripheral sensory nervous system and organs of special sense. Despite the significance of this developmental feat, its evolutionary origins have remained unclear, owing largely to the fact that there has been little comparative (evolutionary) work done on this topic between the jawed vertebrates and cyclostomes—the jawless lampreys and hagfishes. In this review, we briefly summarize the developmental mechanisms and genetics of neural crest and placodes in both jawed and jawless vertebrates. We then discuss recent studies on the role of neural crest and placodes—and their developmental association—in the head of lamprey embryos, and how comparisons with jawed vertebrates can provide insights into the causes and consequences of this event in early vertebrate evolution.
... Because of this phylogenetic relationship, developmental-genetic comparisons between cyclostomes and gnathostomes can provide insights into the evolution of developmental programs in early vertebrates (Green & Bronner, 2014;McCauley, Docker, Whyard, & Li, 2015;Oisi, Ota, Kuraku, Fujimoto, & Kuratani, 2013). Similar to jawed vertebrates, cyclostomes have neural crest cells and placodes, and possess differentiated cranial sensory ganglia (Horigome et al., 1999;Kuratani, Ueki, Aizawa, & Hirano, 1997;McCauley & Bronner-Fraser, 2003;Modrell et al., 2014;Newth, 1951;von Kupffer, 1900;Wicht & Northcutt, 1995;Wicht & Tusch, 1998). Using a combination of gene expression analysis, CRISPR/ Cas9-mediated genome editing, and cell lineage tracing of both placodes and neural crest, we probed developmental-genetic mechanisms responsible for patterning cranial ganglia in lamprey, given that lampreys are a more tractable study system than hagfish for experimental embryology (York, Lee, & McCauley, 2019). ...
... Using a combination of gene expression analysis, CRISPR/ Cas9-mediated genome editing, and cell lineage tracing of both placodes and neural crest, we probed developmental-genetic mechanisms responsible for patterning cranial ganglia in lamprey, given that lampreys are a more tractable study system than hagfish for experimental embryology (York, Lee, & McCauley, 2019). We show that a minor population of lamprey cranial neural crest cells migrate into ganglia as has been reported (Modrell et al., 2014), while most other neural crest cells that we labeled surrounded placode-derived sensory neurons. Genetic knockout experiments show that neural crest cell association with sensory neurons is required for the precise morphological organization of those neurons. ...
... Sectioning revealed that DiO-labeled neural crest cells (pseudocolored green) surrounded but were largely absent from within the DiI-labeled (placode-derived) ganglia (pseudocolored red) residing at the core of the posterior lateral line (pll; Figure 1e in the core of ganglia. However, fate-mapping of cranial ganglia in lamprey that were labeled at both earlier and later stages than shown here similarly found that cranial neural crest that colonized ganglia did not appear to overlap with HuC/D-positive neurons within the ganglion core, suggesting a glial fate for these cells (Modrell et al., 2014). ...
Vertebrates possess paired cranial sensory ganglia derived from two embryonic cell populations, neural crest and placodes. Cranial sensory ganglia arose prior to the divergence of jawed and jawless vertebrates, but the developmental mechanisms that facilitated their evolution are unknown. Using gene expression and cell lineage tracing experiments in embryos of the sea lamprey, Petromyzon marinus, we find that in the cranial ganglia we targeted, development consists of placode-derived neuron clusters in the core of ganglia, with neural crest cells mostly surrounding these neuro-nal clusters. To dissect functional roles of neural crest and placode cell associations in these developing cranial ganglia, we used CRISPR/Cas9 gene editing experiments to target genes critical for the development of each population. Genetic ablation of SoxE2 and FoxD-A in neural crest cells resulted in differentiated cranial sensory neu-rons with abnormal morphologies, whereas deletion of DlxB in cranial placodes resulted in near-total loss of cranial sensory neurons. Taken together, our cell-lineage, gene expression, and gene editing results suggest that cranial neural crest cells may not be required for cranial ganglia specification but are essential for shaping the morphology of these sensory structures. We propose that the association of neural crest and placodes in the head of early vertebrates was a key step in the organization of neurons and glia into paired sensory ganglia.
... Most likely hair cells are innervated by individual nerve terminals on round bars or ribbons around 0.4 mm in diameter (Whitear and Lane, 1981). Early investigations on the placodal development of lampreys requires follow up to define the time and process of nerve fibers peripheral innervations (Modrell et al., 2014). ...
... Lateral line and electroreceptors have been described in larval lampreys (Fritzsch, 1998;Fritzsch and Elliott, 2017b;Piotrowski and Baker, 2014;Baker, 2019;Pombal and Megías, 2019) and their placodal development has been detailed (Modrell et al., 2014). Evidence suggests early development of both lateral line and electroreceptors based on an early presentation of both types (Whitear and Lane, 1981;Yamada, 1973). ...
... Description of various early lateral line and electroreceptors (if present) is incomplete in afferent neuron development as well as hair cell differentiation (Piotrowski and Baker, 2014;Hausen, 1983a, 1983b;Northcutt, 1992;Northcutt et al., 1994;Fritzsch and Wahnschaffe, 1983;Bolz and Fritzsch, 1986;Modrell et al., 2014) with limited additional information of afferent innervation and is biased to the analysis of the lateral line (Vetschera et al., 2019;Alexandre and Ghysen, 1999). Mechanosensory lateral line hair cells have expanded with a set of placodal origins (Northcutt and Gans, 1983;Piotrowski and Baker, 2014;Fritzsch et al., 1998a) to have gained slightly different ways to reach the different lateral line neuromasts (Baker and Modrell, 2018;Northcutt et al., 1994). ...
Synopsis
We review the lateral line and electroreceptor systems among craniates and highlight unique gains and losses. Distinctive features permit grouping of derived animals with respect to similarities (stereocilia and kinocilia length) and share with a single afferent versus two afferents among electroreceptors and lateral line, respectively. Transformations of the dorsal and intermediate nuclei exceeds both in loss and gain among vertebrates, in particular derived bony fishes. We are providing an integrated perspective of various craniates, taking both evolution and development into a unique perspective of neurons, hair cells, as well as dorsal and intermediate nuclei into consideration.
... Similar to gnathostomes, the lamprey lateral line contains both mechanosensory neuromasts and electroreceptive epidermal "end bud" organs, suggesting that the vertebrate acquisition of the lateral line predates the gnathostome-agnathan divergence (Akoev and Muraveiko 1984;Gelman et al. 2007;Baker et al. 2013;Modrell et al. 2014). The lateral line and ears together form the acoustico-lateralis system that originates from a common placode; a system that possesses mechanoreceptive hair cells (Schlosser 2002;Gelman et al. 2007;Baker et al. 2013;Piotrowski and Baker 2014). ...
... In gene expression studies, it was shown that placodes present in the developing lamprey embryo express Dlx and Pax transcription factors, likely reflecting an ancient role of Dlx and Pax genes in fate specification of placodes that extends to the base of vertebrates (Neidert et al. 2001;McCauley and Bronner-Fraser 2002). The authors of a recent fate map and gene expression analysis of cranial ganglia development in lamprey support this notion by positing a combinatorial "Pax code" that governs formation and patterning of placode-derived elements of cranial sensory ganglia (Modrell et al. 2014). Nonetheless, our current understanding of pan-vertebrate mechanisms of placode development remains poor, and comparative analyses focusing on the evolution of vertebrate placode development is therefore ripe for investigation using the lamprey as a model. ...
... Several studies have used fluorescent dyes to examine the contributions of cranial neural crest to development of the lamprey head (Horigome et al. 1999;McCauley and Bronner-Fraser 2003;Martin et al. 2009;Häming et al. 2011;Modrell et al. 2014;Green et al. 2017). McCauley and Bronner-Fraser (2003) used DiI to demonstrate that while lamprey cranial neural crest cells migrate along three pathways, as in other vertebrates, the migration of neural crest into the presumptive branchial arches to form the pharyngeal skeleton, or branchial basket, occurs prior to formation of pharyngeal pouches such that presumptive skeletogenic neural crest cells are able to migrate along the rostrocaudal axis. ...
The development of lampreys has fascinated evolutionary developmental (evo-devo) biologists for a long time. Lampreys, as one of the two surviving members of an ancient group of jawless vertebrates, have long been recognized as key for understanding vertebrate evolution due to their basal position in vertebrate phylogeny. While classical descriptions of lamprey development have uncovered many similarities in development among the few lamprey species that have been studied, these studies, together with modern techniques, have provided key insights for understanding how developmental changes have been important for vertebrate evolution. In recent years, the sea lamprey Petromyzon marinus has moved to the forefront of studies on lamprey development due to its invasion into the Great Lakes, and the critical need to understand its biology for management purposes. The sea lamprey genome has also been published and these two developments, taken together, facilitate the use of lampreys in evo-devo investigations. Here we provide a current overview of contributions of lamprey developmental studies for understanding vertebrate evolution, a summary of modern molecular and genetic tools and methods that have been applied in lamprey evo-devo research. Finally, we provide information to facilitate setting up the lamprey as a model organism in a modern research laboratory setting.
... Similar to that in the early neuroectoderm, we also found that Snail does not seem to be required for the onset of SoxB1a-mediated neurogenic expression in the lamprey CNS, during either early (0/22 loss of expression, 0%, T24, Fig. 3A and B) or relatively later (0/16 loss of expression, 0%, T25, Fig. 3C and D) stages of development. We then tested if Snail is required for neurogenesis in the cranial PNS by analyzing expression of Six1/2, Pax3/7, and Phox2 in neurons of different cranial sensory ganglia at T25 (McCauley and Bronner-Fraser, 2002;Modrell et al., 2014;York et al., 2018). Our functional results suggested that Snail activity is essential for the onset of gene expression patterns that promote PNS neurogenesis, as demonstrated by complete or nearly complete loss of expression of Six1/2 in epibranchial and posterior lateral line ganglia (9/13, 69%), Pax3/7 in the ophthalmic division of the trigeminal nerve (7/10, 70%), and in Phox2-positive epibranchial ganglia (12/17, 71%) ( Fig. 3E-J). ...
A major challenge in vertebrate evolution is to identify the gene regulatory mechanisms that facilitated the origin of neural crest cells and placodes from ancestral precursors in invertebrates. Here, we show in lamprey, a primitively jawless vertebrate, that the transcription factor Snail is expressed simultaneously throughout the neural plate, neural plate border, and pre-placodal ectoderm in the early embryo and is then upregulated in the CNS throughout neurogenesis. Using CRISPR/Cas9-mediated genome editing, we demonstrate that Snail plays functional roles in all of these embryonic domains or their derivatives. We first show that Snail patterns the neural plate border by repressing lateral expansion of Pax3/7 and activating nMyc and ZicA. We also present evidence that Snail is essential for DlxB-mediated establishment of the pre-placodal ectoderm but is not required for SoxB1a expression during formation of the neural plate proper. At later stages, Snail regulates formation of neural crest-derived and placode-derived PNS neurons and controls CNS neural differentiation in part by promoting cell survival. Taken together with established functions of invertebrate Snail genes, we identify a pan-bilaterian mechanism that extends to jawless vertebrates for regulating neurogenesis that is dependent on Snail transcription factors. We propose that ancestral vertebrates deployed an evolutionarily conserved Snail expression domain in the CNS and PNS for neurogenesis and then acquired derived functions in neural crest and placode development by recruitment of regulatory genes downstream of neuroectodermal Snail activity. Our results suggest that Snail regulatory mechanisms in vertebrate novelties such as the neural crest and placodes may have emerged from neurogenic roles that originated early in bilaterian evolution.
