Cephalopods are part of a long tradition in evolutionary neuroscience and are often highlighted as an ideal example of convergent evolution of nervous systems (Young, 1965; Young, 1985; Abbott et al., 1995). Their large brains, relative to body size, and behavioral repertoires offer opportunities for comparative analysis of the evolution of learning and memory mechanisms. Cephalopods possess a sophisticated nervous system that resembles that of vertebrates in relative size and cognitive abilities (Young, 1991; Hochner et al., 2006). These complex behavioral abilities include various forms of learning, problem-solving, and body color and pattern changes used either as predatory or anti-predatory behaviors or for social communication (Fiorito et al., 1990; Langridge et al., 2007; Staudinger et al., 2013; Darmaillacq et al., 2014; Schnell et al., 2015; Richter et al., 2016; Lin and Chiao, 2017; Marini et al., 2017; Mather and Dickel, 2017; Hanlon and Messenger, 2018). The fossil record suggests that cephalopods were more prominent in marine ecosystems over 300 million years ago with a higher biodiversity than today. It is assumed that the rise of bony fishes and resulting competition for resources in that ecological niche played a major role in the extinction of many clades of cephalopods, including all the shelled cephalopods except few members of the subclass Nautiloidea. Today, the class Cephalopoda has over 800 current living species with extremely diversified lifestyles and body shapes (Kröger et al., 2011). The vast majority of current cephalopod species belong to the soft-bodied subclass Coleoidea (cuttlefishes, octopuses, and squids), and a small handful belong to the subclass Nautiloidea (nautiluses). Coleoid cephalopods, which have internalized or lost their shell over evolutionary time, were able to swim more easily and could compete with other predators in open waters. The continuous competition with other animals to access resources has been proposed to have been the main trigger for the selection of cephalopods that could develop specialized strategies for accessing resources unavailable to competing species. In coleoid cephalopods, this evolutionary process resulted in larger brains, camera-type eyes, as well as abilities to voluntarily change their skin pattern and texture for camouflage and social communication (Young, 1973; Hanlon and Messenger, 2018; Amodio et al., 2019).

The European squid Loligo vulgaris is well known for its economic role in the food and fishing industry but is much less studied for its fascinating biology. This species is known for its striking ability for camouflage typically in open-water environments by the use of its specialized iridescent cells to reflect light in different manners depending on its surroundings. The neuroanatomy and nervous system morphology of L. vulgaris have been described in detail in histological studies (Young, 1976; Wild et al., 2015). Detailed staging of the embryonic development of the related species Loligo pealii was established and can be used as a reference for L. vulgaris (Arnold, 1965). While the gross anatomy of squids is well known from histology and morphological studies, we are currently lacking resolution at the molecular level to identify genes that specify the many cell types that make up the unique cephalopod body-plan and nervous system. Since the publication of the first complete genome sequence of Octopus bimaculoides, there has been increasing interest in cephalopod biology and neuroscience. In addition, the availability of genomic sequences of other cephalopods, such as Euprymna scolopes (Sepiida), Architeuthis dux (Oegopsida), and Nautilus pompilius (Nautilida), opens the possibility for molecular comparisons between these distant clades of cephalopods with drastically different morphologies and lifestyles. These comparisons constitute a major step for understanding the molecular basis of cephalopod evolution (Albertin et al., 2015; Belcaid et al., 2019; da Fonseca et al., 2020; Zhang et al., 2021).

Single-cell transcriptomics experiments in different cephalopods have shed light on the cell type diversity of the O. bimaculoides visual system, the brain of Octopus vulgaris, and the nervous system of the squid Euprymna berryi (Gavriouchkina et al., 2022; Songco-Casey et al., 2022; Styfhals et al., 2022).

To gain further insights into the cellular diversity and cell type-specific gene expression in squids, we performed single-cell transcriptomics on whole L. vulgaris heads (stages 28–30 based on Arnold, 1965, pre-hatchling stage). Additionally, we used hybridization chain reaction in situ hybridization (HCR ISH) to visualize gene expression in situ and correlate single-cell transcriptomes with anatomical features. By combining these methods, we were able to identify and assess common cell types found in most bilaterians, such as different types of neurons, muscles, and connective tissues. Interestingly, even in these canonical tissues, we found certain clusters that highly express cephalopod-specific genes, as exemplified by some subtypes of connective tissues. Thus, while cells can be assigned a certain identity based on well-characterized marker genes, such as collagens, these cell types have likely further diverged in cephalopods. Neural tissues are prominent in the head and include the brain, optic ganglia, eyes, and other sensory organs. We identified and analyzed new markers of different cells in the nervous system, including widely expressed pan-neuronal genes, genes marking distinct stages of neural differentiation, markers for neural subsets, as well as sensory cell types. In addition, we also characterized cephalopod-specific cell types, such as the chromatophores or cells of the suckers. Our study provides new insights into the transcriptomic signatures of cell types in L. vulgaris. By analyzing the expression patterns of many cell type-specific genes, we assessed the conservation of features previously described in other animal clades but also previously unknown features and modalities of cell types that appear specific for cephalopods.

We here provide molecular insights into the cell types present in the head of L. vulgaris by combining two state-of-the-art techniques HCR ISH and scRNAseq. The combination of these two techniques allowed us to provide insights into the different cell types that make up the L. vulgaris head, into the process of nervous system development and the identity of neuronal subtypes. The data produced for this article enabled the identification of 34 cell clusters that we used as a correlate for cell type diversity. Although the data can provide a broad overview of cell diversity, we note that few cell types that would be expected in the head of cephalopods such as components of the vascular and digestive systems could not be confidently identified in this study. The apparent lack of resolution in the clusters and their low number is likely to be in large part caused by the lack of completeness of the reference transcriptome, which resulted in a lower mapping rate of the single-cell reads. It has been shown in other cephalopods that having a high-quality genome largely contributes to improving cluster resolution (Gavriouchkina et al., 2022; Songco-Casey et al., 2022; Styfhals et al., 2022). Because of the lack of a reference genome for L. vulgaris, a non-redundant transcriptome was used as a mapping reference in this study, which has shown to be sufficient for identifying cell types and describing the expression some of their characteristic marker genes but is however not sufficient to affirm full coverage of cell type diversity of this organism. The use of a transcriptome instead of a genome as a reference has been previously shown to enable molecular description of cell types but can lack in resolution (Duruz et al., 2021). Additionally, it is likely that the transcriptome assembly could be improved by obtaining more RNA from L. vulgaris by including different embryonic stages and adult stages. We are convinced that re-running this analysis with a better reference would reinforce our analysis and provide better cell type resolution. In our analysis of the nervous system, we were able to recognize broad neuronal markers that are expressed throughout the nervous system while showing different levels of expression in predicted neuronal cell types. These newly identified neuronal markers will provide a new perspective to study the characteristics of the nervous systems of cephalopods. Particularly, the genes tetraspanin-8 and amyloid beta-binding-like show strikingly elevated expression pan-neuronally. Besides the identified sensory cells, the homogeneity of the neuronal clusters was rather surprising. Different neuronal subpopulations were expected to be identified by the expression of genes neurotransmitter synthesis pathway to distinguish neurons by their chemical modalities. Such fine distinctions between neuronal populations could be found in the nervous systems of E. berryi and O. vulgaris (Gavriouchkina et al., 2022; Songco-Casey et al., 2022; Styfhals et al., 2022). It is likely that this lack of resolution is due to missing genes in our reference transcriptome, which would classically contribute to distinguishing neuronal populations. The analysis of the expression of two highly expressed members of the ELAV family elav-like 1 and elav-like 2 revealed that although they can be found in most lobes of the nervous system, their expression levels differ in different clusters. Previous studies of ELAV proteins in S. officinalis revealed that the gene Sof-Elav1 was expressed in all the lobes of the nervous system but also during early embryogenesis while the other gene Sof-Elav2 was not specific to neurons (Buresi et al., 2013). In O. bimaculoides, a single neuronal ELAV protein was identified and was observed to be also expressed during neurogenesis and could be used as a neuronal marker to study nervous system development during embryogenesis, similarly to Sepia (Shigeno et al., 2015). It is interesting to note that contrarily to what was described in cuttlefish and octopus we show two cell type-specific elav genes, which are both expressed in neurons. This challenges the hypothesis of a duplication of the elav gene during lophotrochozoan evolution proposed after the observation of two elav genes in Capitella sp., one of which is expressed in neurons while the other is expressed mainly in the mesoderm (Meyer and Seaver, 2009). The identification of two neuronal elav genes in L. vulgaris raises the question of whether they are orthologous to the genes studies in Sepia and Octopus but their function is different. Alternatively, these two neuronal elav genes could the result of another duplication of the neuronal elav. Such questions would need to be further investigated by more thoroughly studying the sequence homology of these genes and reconstruct their phylogeny. We identified key transcription factors involved in stem cells and development. The expression of these genes likely reflects different states of neuronal differentiation and suggests a migration of neuronal progenitors towards the nervous system. We could show that proliferating cells that express of the transcription factor e2f3 are located in the lateral lips near the nervous system. We interestingly observed the expression of asc in the same region, together with several proliferation markers. Extensive study of neurogenesis in D. melanogaster has shown that the proneural complex asc can determine the neuronal fate of quiescent multipotent ectodermal cells (Campuzano and Modolell, 1992; Skeath and Doe, 1996). In vertebrates, on the other hand, asc is expressed in cells that have already undergone neuronal specification but are self-renewing (Bertrand et al., 2002; Soares et al., 2022). Studies of neurogenesis in the annelid Capitella teleta have shown that, similarly to vetrebrates, proneural genes such as asc are expressed in self-renewing neuronal progenitors (Sur et al., 2020). Our data suggests that asc is also expressed in proliferating cells, similiarly to vertrebrates and C. teleta but unlike Drosophila. This is consistent with documented co-expression of asc and the mitotic marker phosphor-histone H3 in O. vulgaris (Deryckere et al., 2021). The observation of soxB1 expression together with asc strengthened their characterization as neuronal progenitors due to the documented role of this gene in neuronal differentiation (Miyagi et al., 2009). However, strong soxB1 expression in differentiated neurons has been shown in the gastropod Patella vulgate and in the cephalopods S. officinalis and O. vulgaris (Le Gouar et al., 2004Focareta and Cole, 2016; Deryckere et al., 2021). In L. vulgaris, we observe similar results where soxB1 is expressed in the lateral lips together with asc but is also expressed in differentiated neurons. This was consistently shown by the HCR ISH experiments as well as the single-cell analysis. Therefore, the hypothesis proposed for the action of soxB1 in the early stages as well as the later stages of neuronal differentiation in O. vulgaris is consistent with our data (Deryckere et al., 2021). The unexpected expression of foxD1 in the nervous system of L. vulgaris, together with existing evidence of the role of this gene in neuronal development, motivated the grouping of the foxD1⁺ clusters with other clusters characterized as neuronal progenitors for further analysis (Herrera et al., 2004; Polevoy et al., 2017; Newman et al., 2018; Janssen et al., 2022). Our trajectory inference analysis using monocle3 and slingshot showed that foxD1 is expressed in cells that could represent an intermediate neuronal differentiation stage following the expression of asc but before the expression of amyloid beta-binding-like and the second peak of soxB1 expression. Such a role has been proposed in O. vulgaris in the cells expressing neuroD that are expressed in a gradient between the lateral lip and the central nervous system, which may indicate a pattern of migration of differentiating neurons (Deryckere et al., 2021). We could, however, not correlate these results with our hypothesis of an intermediate foxD1-expressing stage because neuroD expression could not be detected in specific clusters in our single-cell dataset. Although the trajectories we calculated point towards a role of FoxD1 in neuronal differentiation, the relatively poor cluster resolution and the lack of cells along the trajectory axes shown in Figure 3 suggest that this hypothesis would require further investigation that should include a more complete set of genes that have been involved with cephalopod neurogenesis. In our analysis of sensory cells, we provide valuable information regarding the different sensory systems of L. vulgaris and could identify photoreceptors and additionally describe newly identified markers of the olfactory organ and mechanosensory cells. The sensory cells of cephalopods have been extensively studied and are known to be very complex and can have multiple sensory modalities (van Giesen et al., 2020; Buresch et al., 2022). In O. bimaculoides and S. officinalis, several chemosensory receptors could be identified and characterized (van Giesen et al., 2020; Andouche et al., 2021). In our analysis of the L. vulgaris head, we were however not able to identify putative chemosensory genes, likely due to the absence of characteristic receptors in our transcriptome. The chemosensory function of cells analyzed here was only inferred because of their expression in the olfactory organ. A full analysis of chemosensory genes in L. vulgaris would be required to be able to truly describe the diversity of their sensory cell types. Finally, we further characterize the highly specialized epidermis of L. vulgaris and cephalopod-specific cell types such as suckers or iridophores. The expression of a few genes facilitated the characterization of some of these cell types as exemplified by the expression of egf-like in epidermal cells, suckerin-6 in suckers, and reflectin-8 in iridophores. However, many cluster-specific genes could not be assigned to a specific function. The abundance of papilin-expressing cells on the surface of the epidermis is striking and had not been previously documented. The gene madnf is known to play a role in the maturation and maintenance of dopaminergic neurons in D. melanogaster and C. elegans (Palgi et al., 2009; Richman et al., 2018). We found discrepancies between the observation of madnf in non-neuronal clusters and in a small cluster of mechanosensory cells and the expression patterns shown by HCR ISH, where expression is found in different areas of the brain, optic lobes, and olfactory organs. Similarly, the expression of reflectin-8 is not limited to the chromatophores but is also in the nervous system. The expression of these non-neuronal makers inside the nervous system results highlights the importance of considering non-neuronal cell types, even when aiming to answer neurobiological questions. Many cell types remain unidentified, and further characterization of these cells and the function of the genes that they differentially express could advance our understanding of cephalopod biology. The combination of high-resolution imaging rendered possible by HCR in conjunction with the data provided by single-cell transcriptomics enabled us to extend our understanding of the cell types of cephalopods. The experimental approach is efficient to identify and explore conserved sets of genes conferring cell type identity in these animals while comparing cell type markers across different clades. On the other hand, the accurate anatomical description gained with HCR ISH allowed us to find previously undescribed cell type-specific genes by identifying the anatomical features in which they are expressed, enabling the exploration not only of conserved cell types but also novel ones. By applying single-cell RNA sequencing in a member of this fascinating clade of mollusks and by correlating this data with high-resolution mRNA imaging techniques, we can further understand the main molecular features that drive cell type identity in L. vulgaris. The analysis of the expression of selected genes of interest can provide insight into their function, which can be a starting point for future investigations of cephalopod cell types. Further studies of the nervous system of squids and the different cell types that compose them could help fill important gaps in our understanding of the evolution of the nervous system and could provide insights into how brains complexified independently in very distant clades of animals. By comparing the molecular features of neuronal cell types of cephalopods with other species, we could better understand the evolutionary history of the unique brains of cephalopods and identify what confers them such unique capabilities. This is a significant step in the study of convergent evolution of brains and provides a valuable resource for future research on cephalopods.

Sequencing data have been deposited in GEO under accession code GSE200108.

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Author details

1. Jules Duruz

   Department of Biology, Institute of Zoology, University of Fribourg, Fribourg, Switzerland

   Contribution

   Formal analysis, Validation, Investigation, Visualization, Methodology, Writing - original draft

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-1860-9546

2. Marta Sprecher

   Department of Biology, Institute of Zoology, University of Fribourg, Fribourg, Switzerland

   Contribution

   Formal analysis, Methodology

   Competing interests

   No competing interests declared

3. Jenifer C Kaldun

   Department of Biology, Institute of Zoology, University of Fribourg, Fribourg, Switzerland

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

4. Al-Sayed Al-Soudy

   Department of Biology, Institute of Zoology, University of Fribourg, Fribourg, Switzerland

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7830-9660

5. Heidi EL Lischer

   Interfaculty Bioinformatics Unit and Swiss Institute of Bioinformatics, University of Bern, Bern, Switzerland

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9616-2092

6. Geert van Geest

   Interfaculty Bioinformatics Unit and Swiss Institute of Bioinformatics, University of Bern, Bern, Switzerland

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1561-078X

7. Pamela Nicholson

   Institute of Genetics, University of Bern, Bern, Switzerland

   Contribution

   Investigation, Methodology, Project administration

   Competing interests

   No competing interests declared

8. Rémy Bruggmann

   Interfaculty Bioinformatics Unit and Swiss Institute of Bioinformatics, University of Bern, Bern, Switzerland

   Contribution

   Investigation, Methodology, Project administration

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-4733-7922

9. Simon G Sprecher

   Department of Biology, Institute of Zoology, University of Fribourg, Fribourg, Switzerland

   Contribution

   Conceptualization, Supervision, Funding acquisition, Writing - original draft, Project administration

   For correspondence

   simon.sprecher@unifr.ch

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-9060-3750

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