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Formation and Subdivision of the Head Field in the Centipede Strigamia

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Formation and Subdivision of the Head Field in the Centipede Strigamia Hunnekuhl and Akam EvoDevo (2017) 8:18 DOI 10.1186/s13227-017-0082-x EvoDevo RESEARCH Open Access Formation and subdivision of the head feld in the centipede Strigamia maritima, as revealed by the expression of head gap gene orthologues and hedgehog dynamics Vera S. Hunnekuhl1,2* and Michael Akam1 Abstract Background: There have been few studies of head patterning in non-insect arthropods, and even in the insects, much is not yet understood. In the fy Drosophila three head gap genes, orthodenticle (otd), buttonhead (btd) and empty spiracles (ems) are essential for patterning the head. However, they do not act through the same pair-rule genes that pattern the trunk from the mandibular segment backwards. Instead they act through the downstream factors collier (col) and cap‘n’collar (cnc), and presumably other unknown factors. In the beetle Tribolium, these same gap and downstream genes are also expressed during early head development, but in more restricted domains, and some of them have been shown to be of minor functional importance. In the spider Parasteatoda tepidariorum, hedgehog (hh) and otd have been shown to play an important role in head segmentation. Results: We have investigated the expression dynamics of otx (otd), SP5/btd, ems, and the downstream factors col, cnc and hh during early head development of the centipede Strigamia maritima. Our results reveal the process of head condensation and show that the anteroposterior sequence of specifc gene expression is conserved with that in insects. SP5/btd and otx genes are expressed prior to and during head feld formation, whereas ems is not expressed until after the initial formation of the head feld, in an emerging gap between SP5/btd and otx expression. Further- more, we observe an early domain of Strigamia hh expression in the head feld that splits to produce segmental stripes in the ocular, antennal and intercalary segments. Conclusions: The dynamics of early gene expression in the centipede show considerable similarity with that in the beetle, both showing more localised expression of head gap genes than occurs in the fy. This suggests that the broad overlapping domains of head gap genes observed in Drosophila are derived in this lineage. We also suggest that the splitting of the early hh segmental stripes may refect an ancestral and conserved process in arthropod head pattern- ing. A remarkably similar stripe splitting process has been described in a spider, and in the Drosophila head hh expres- sion starts from a broad domain that transforms into three stripes. Background segment boundaries in the trunk are also used in the head Te mechanisms that specify the head segments of (engrailed, wingless, hedgehog), but how the expression of arthropods are fundamentally diferent from those that these segment polarity genes is linked to upstream axial operate in the trunk [1–4]. Some of the genes that defne patterning remains unclear. Currently, most insights into arthropod head pattern- ing are based on studies from the fy Drosophila mela- *Correspondence: vera.terblanche@uni‑goettingen.de nogaster. A gradient of the maternally provided anterior 2 Department of Evolutionary Developmental Genetics, Georg-August-Universität Göttingen, Caspari Haus, morphogen bicoid (bcd) in the blastoderm stage embryo Justus‑von‑Liebig‑Weg 11, 37077 Göttingen, Germany [5] leads to the activation of the so-called head gap genes Full list of author information is available at the end of the article © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Hunnekuhl and Akam EvoDevo (2017) 8:18 Page 2 of 17 orthodenticle (otd), empty spiracles (ems) and buttonhead Another transcription factor of interest for insect head (btd) in broad overlapping domains. Tey were termed patterning is collier (col), which acts downstream of the gap genes because mutations in these genes delete a head gap genes btd and ems in the fy. Col was the frst coherent block of specifc head segments [6–10]. Sloppy intermediately acting factor to be identifed in Drosophila paired has also been proposed as a head gap gene [11], head segmentation [22]. It directly controls the expres- but its role in head development remains unclear. It is not sion of segment polarity genes in the intercalary seg- known whether these genes are direct targets of bcd, but ment [22, 23]. It is also required for correct expression cis-acting elements that contain bcd binding sites have of cap‘n’collar, a factor that specifes mandibular iden- been identifed upstream of ems and btd [8, 9]. tity [22, 24]. Furthermore, col is repressed at its poste- In Drosophila, the domains of expression of these head rior limit by the trunk pair rule gene even-skipped, hence gap genes are out of phase by one segment [1, 2, 6]. Each taking input from both the head and the trunk pattern- factor is required for the correct establishment of a sub- ing system [22]. Expression of col in the pre-mandibular set of segmental stripes of wingless (wg) and/or hedge- region is conserved in other insects and in the millipede hog (hh) expression in the head [12]. It has not yet been Glomeris marginata and has been discussed as being fully elucidated whether there is direct control of seg- responsible for the appendage-less phenotype of the ment polarity gene expression by the head gap genes or intercalary segment in insects and myriapods [25, 26]. whether their efects are transduced through second level However, the lack of a homeotic phenotype after removal mediators that would replace the pair rule patterning sys- of col, and its function in head segmentation in Dros- tem that acts in the Drosophila trunk but not in the head ophila [22, 26, 27], rather speak in favour of a crucial role (see [1]). in head segmentation and integration of head and trunk Te whole head segmentation mechanism in Drosoph- patterning that might be conserved in myriapods. Tere- ila is likely to be in at least some respects specifc to the fore, we included col in our analysis of head patterning higher Diptera: bcd as a major anterior determinant is genes in the centipede. only present in the higher fies [13–15]. Diferent mater- Further insights into arthropod head patterning come nal signals are used in other insects [16, 17]. In many from work on the spider Parasteatoda tepidariorum (for- arthropods, the embryo is patterned after cellularisation, merly called Achaearanea tepidariorum). Here, the sig- and any link between maternal coordinates and embry- nalling factor hedgehog (hh) is dynamically expressed in onic patterning remains unknown. Since the earliest pat- a cephalic domain that splits into three segmental stripes terning mechanism is so specialised in Drosophila, it is [3, 4]. Subdivision of a cephalic hh domain into ocular, also questionable whether the downstream mechanism antennal and intercalary segmental stripes also happens of gap gene patterning is present in the same way in other in Drosophila head segmentation [28], though this pro- arthropods. cess has been little studied. A study in the millipede G. More recently, the beetle Tribolium castaneum has marginata has shown that the anterior-most hh stripes, been established as a second model for insect head belonging to the ocular and the antennal segment, are patterning. Work in Tribolium has shown that ortho- also generated by a stripe splitting event [29]. Tese simi- logues of the Drosophila gap genes otd, ems and btd are lar patterns suggest that a domain-splitting mechanism, expressed during early head development [18–20], but rather than a sequential addition of segments [4], might their expression domains are not as broadly overlap- generally characterise arthropod head segmentation. We ping as they are in Drosophila. RNAi mediated knock- ask whether subdivision of an early cephalic hh domain down of ems and btd had no (for btd) or only rather also occurs in this centipede, and how this domain and subtle (for ems) efects when compared to the gap gene resulting subdomains relate to the expression of other mutant phenotypes in Drosophila. Only the knock- early expressed head patterning genes. down of otd produced a severe head phenotype [20]. We chose to study the centipede Strigamia maritima RNAi knockdown of ems and otd orthologues in the to provide information on head patterning from another milkweed bug Oncopeltus fasciatus also gave mild phe- distant outgroup to the insects and to facilitate an evolu- notypes. No btd orthologue could be isolated from this tionary comparison of head patterning across the arthro- species [21]. In both Tribolium and Oncopeltus, these pods. Our work complements the recent work on head mild phenotypes may be due to limitations of the RNAi patterning in another myriapod, the millipede G. margin- method and need to be confrmed by gene knockout. ata, where otd and a putative btd orthologue were found Regardless of this, the results suggest that orthologues to be anteriorly expressed [30], and the work on head of Drosophila head gap genes are expressed during patterning in the spider P. tepidariorum discussed above. early head development in other insects, but their role Only little data are available on gene expression during may be rather diferent. head patterning in crustaceans [31, 32]. Hunnekuhl and Akam EvoDevo (2017) 8:18 Page 3 of 17 Te S.
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