A quantitative atlas of Even-skipped and Hunchback expression in Clogmia albipunctata (Diptera: Psychodidae) blastoderm embryos

Abstract

BackgroundComparative studies of developmental processes are one of the main approaches to evolutionary developmental biology (evo-devo). Over recent years, there has been a shift of focus from the comparative study of particular regulatory genes to the level of whole gene networks. Reverse-engineering methods can be used to computationally reconstitute and analyze the function and dynamics of such networks. These methods require quantitative spatio-temporal expression data for model fitting. Obtaining such data in non-model organisms remains a major technical challenge, impeding the wider application of data-driven mathematical modeling to evo-devo.ResultsWe have raised antibodies against four segmentation gene products in the moth midge Clogmia albipunctata, a non-drosophilid dipteran species. We have used these antibodies to create a quantitative atlas of protein expression patterns for the gap gene hunchback (hb), and the pair-rule gene even-skipped (eve). Our data reveal differences in the dynamics of Hb boundary positioning and Eve stripe formation between C. albipunctata and Drosophila melanogaster. Despite these differences, the overall relative spatial arrangement of Hb and Eve domains is remarkably conserved between these two distantly related dipteran species.ConclusionsWe provide a proof of principle that it is possible to acquire quantitative gene expression data at high accuracy and spatio-temporal resolution in non-model organisms. Our quantitative data extend earlier qualitative studies of segmentation gene expression in C. albipunctata, and provide a starting point for comparative reverse-engineering studies of the evolutionary and developmental dynamics of the segmentation gene system.

Development of the Nervous System of Carinina ochracea (Palaeonemer-tea, Nemertea)

“…Thus, the architecture of the definite CNS in Nemertea is congruent with the hypothetical ancestral spiralian pattern that consists of an anterior brain and paired, unsegmented, possibly lateral nerve cords [7,51]. The occurrence of a transitory caudal neuron in Nemertea supports the recently proposed hypothesis that posterior, possibly transitory neurons is an ancestral trait in the development of nervous systems in Spiralia (see discussion in [48]). A trochophore type larva has been postulated in the last common ancestor of Spiralia (in the sense of [1,52]) [2,4,53,54].…”

“…As outlined above, however, these subapical neurons are not part of the developing definite nervous system [15,18]. In various mollusk species, similar invaginations have been shown to give rise to the cerebral ganglia [43–45], also without displaying immuoreactivity against the respective antibodies [46–48]. While the hypothesis that the fronto-lateral epidermal invaginations represent the primordia of the brain-ring seems to be supported by published information, it is challenged by the fact that at least RFa-lir neurons of the brain likely originate from more dorsally located parts of the frontal epidermis.…”

Expression study of the hunchback ortholog in embryos of the onychophoran Euperipatoides rowelli

“…This contrasts with the situation in the chelicerate, myriapod and insect embryos, in which hunchback mRNA is typically localised anteriorly or in an anterior-to-posterior gradient along the early embryo (Tautz and Pfeifle 1989;Schwager et al 2009;Janssen et al 2011;Chang et al 2013;Duncan et al 2013;Crombach et al 2014;Janssens et al 2014). Moreover, our results provide no evidence for hunchback expression in a group of mesenchymal cells, which would correspond to the cumulus of the chelicerate embryo (Schwager et al 2009).…”

“…It has been shown that hunchback has multiple roles during development of protostome species including maternally mediated anterior patterning, body segmentation as well as patterning of neural and mesodermal tissues (Lehmann and Nüsslein-Volhard 1987;Isshiki et al 2001;Pinnell et al 2006). While the maternal expression of hunchback is shared by a number of arthropod and annelid species, including insects (Drosophila and other dipterans), spiders, myriapods, leeches and polychaetes (Tautz and Pfeifle 1989;Savage and Shankland 1996;Werbrock et al 2001;Schwager et al 2009;Janssen et al 2011;Janssens et al …”

Emerging developmental genetic model systems in holometabolous insects

“…C. alpipunctata has been used as a model in descriptive molecular embryology since the mid 1990's [56,[64][65][66][67][68][69][70][71]. Embryonic transcriptome data and a staging scheme for embryos are also available [59,61]…”