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Evolution of maternal control of axial patterning in insects
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Evolution of maternal control of axial patterning in insects Jeremy A Lynch Positional and cell fate cues provided maternally to eggs are important factors in the development of many animals. The insects are a model clade where maternal establishment of embryonic axes is widespread and has been a topic of intense classical and molecular embryological analysis. Recently, significant progress has been made in revealing the molecular basis of some classical embryological experiments. In addition, observations of novel forms of maternal positional cues have been made. Finally, it has become increasingly clear that no maternal source of positional information acts alone without input and feedback from zygotic target genes to ensure precise and repeatable pattern formation in the early embryo. These advances will be discussed in the context of historical experiments, our current understanding of how positional cues can be generated, stored, and transmitted in insect ovaries and eggs, and how the nature of the cues can change in evolution. Address University of Illinois at Chicago, Chicago, IL, USA Corresponding author: Lynch, Jeremy A ([email protected])
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This review comes from a themed issue on Development and regulation
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Edited by Elisabeth Marchal and Dolors Piulachs
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https://doi.org/10.1016/j.cois.2018.07.011
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2214-5745/ã 2018 Published by Elsevier Inc.
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Unique features of insect ovaries
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Insect ovaries have an anterior–posterior (AP) polarity that typically follows that of the female. Typically, a germline stem-cell resides at the anterior end (Figure 1a). When this stem cell divides to produce a gametic progenitor (Figure 1b), the latter moves posteriorly and begins differentiation. Repetition of this process leads to the production of a string of differentiating germ cells of increasing age from anterior to posterior. Thus, each developing oocyte is flanked by a younger oocyte progenitor at its anterior, and an older one to its posterior (Figure 1c,d). If this asymmetric information could be transmitted and stored, it would be a potent source of positional cues. That such transmission occurs was clear
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well before the molecular era, as it was observed that the anterior–posterior polarity of insect eggs almost always is tightly correlated to the AP polarity of the ovariole [1,2].
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Another intrinsic property of the insect oocyte is the asymmetric movement of the germinal vesicle (oocyte nucleus) from a symmetric position in the central column of cytoplasm (Figure 1d) to a highly asymmetric location at the plasma membrane (Figure 1e). This movement is necessary to prepare the oocyte nucleus for the resumption and completion of meiosis when the egg is laid and activated [3]. The importance of this movement was also strongly implied by early investigators, where it was observed that position of the oocyte nucleus very often marks the dorsal pole of the egg and embryo [4,5].
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Crucially, there is a strong interaction between germline cells and somatic cells in the insect ovary. A single layer of somatic cells surrounds a single germline cell (Figure 1c–e), or a clone of sister germline cells, forming the functional unit of the insect ovary, the egg chamber. The somatic cells surrounding the germline cells are called follicle cells, and these cells can receive, store, and transmit positional information through communication among themselves and with the germ cells [2]. Since the follicle cells secrete the eggshell, information can be stored in structure of the eggshell layers, or in the fluid that separates the egg from the innermost eggshell layer. Thus, information can be passed to the developing embryos (Figure 1f), even after follicle cells are gone.
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Finally, communication among the germline and somatic cells can lead to the polarization of the oocyte itself, allowing for the differential localization of macromolecules at different poles of the egg (Figure 1d,e), which are also maintained in the embryo (Figure 1f).
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Maternal patterning information in Drosophila melanogaster
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The molecular basis of maternal positional information has been intensively studied in insects, primarily in D. melanogaster. A relay system involving Jak/STAT and Notch signaling operates in the ovary to position the oocyte correctly within the egg chamber, and pass positional information from the older egg chambers to the newly specified oocyte [6]. This relay system leads to the establishment of AP polarity within the oocyte, and the proper localization of mRNA for the anterior determinant bicoid and posterior/germ cell determinant oskar at their respective poles. Localized bcd mRNA gives rise to a
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Generation and storage positional information in the insect ovary. Ovariole highly schematic to represent common features of all types of oogenesis. (a) Anteriorly localized germline stem cell. (b) Differentiating oocyte. (c) Oocyte surrounded by follicle cell layer (solid black circles). Blue arrows indicate oocyte receiving signals from specialized follicle cells (solid red circles), leading to polarization of the embryo. In this case, it is a hypothetical situation, drawn from knowledge gained from D. melanogaster. (d) Maturing egg chamber with polarized oocyte (indicated by posteriorly localized blue), sending signals (orange arrows) to anterior follicle cells (green), which in turn signal to the next younger oocyte to induce polarity (again a hypothetical mechanism). (e) Late stage egg chamber. The oocyte nucleus (black and white checkered circle) has migrated to the cortex, where it induces signaling to and differentiation of, the overlying follicle cells (yellow circles). (f) Schematic representation of a typical insect embryo, with regions of potential eggshell modification and embryonic RNA localization marked with colors corresponding to their origin the ovary (c–f).
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gradient of protein that acts as a morphogen to establish cell fates in the anterior half of the embryo. Oskar protein is crucial for assembling the germplasm (which specifies the primordial germ cells) and stabilizing nanos mRNA. Posterior Nanos protein plays a permissive role in preventing the early translation of maternal hunchback (hb) mRNA [7]. The molecular basis of maternal establishment DV polarity is also well described in D. melanogaster. mRNA for the EGF ligand gurken (grk) is localized around the oocyte nucleus which becomes localized at an asymmetric location at the anterior. Grk protein is secreted and activates Current Opinion in Insect Science 2018, 1:1–6 Please cite this article in press as:
EGF receptor expressed in the follicle cells. This leads to a ventrally localized modification of the eggshell. This information stored in the eggshell is then transmitted back to the embryo through localized processing of the Toll ligand Spaetzle to the ventral half of the egg. Again, this leads to a graded source of patterning information, this time in the form of nuclear uptake of the Toll target transcription factor Dorsal. The Dorsal gradient also regulates its targets in a concentration dependent fashion, and has been described as a morphogen [8].
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Maternal contribution to AP patterning in other insects
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Establishing oocyte polarity
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Whether the developmental and molecular bases of inducing AP polarity in the oocyte are conserved outside of D. melanogaster is an interesting topic, especially in light of the variability in the structure of ovaries across insects. D. melanogaster has polytrophic meroistic ovaries, which means that the oocyte is one of a clone of sister germline cells. The other germline cells become ‘nurse cells’ which are specialized to produce macromolecules provided to the oocyte. These germ cells are surrounded as a unit by follicle cells to form egg chambers. Many insects have telotrophic meroistic ovaries, where a common pool of nurse cells located toward the anterior end of the ovary feed oocytes that become encapsulated by follicle cells as they mature and move posteriorly. Finally, panoistic ovaries lack nurse cells, and each oocyte is encapsulated singly by follicle cells [2,8].
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Since the polarization of the D. melanogaster oocyte occurs in the context of the selection and migration of the oocyte in the context of its sister cells in the specialized polytrophic ovaries of the fly [6], it might stand to reason that the D. melanogaster system may not be broadly conserved, especially in systems with different ovary types. Indeed, it appears that JAK/STAT signaling does not have a role in establishing AP polarity of the ooctye in the telotrophic ovaries of the beetle Tribolium castaneum, despite a partially conserved role in specifying the stalk cells that separate egg chambers from each other [9]. On the other hand, Notch signaling between the germline and soma appears to have a conserved role in establishing AP polarity with in the T. castaneum oocyte [10]. Examination of Notch signaling in the cockroach Blatella germanica indicates that signaling between germline and soma is conserved, but any effect on oocyte polarity is yet to be shown [11].
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Diverse roles of localized mRNAs
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Although bcd is the absolutely crucial anterior determinant in D. melanogaster and its relatives in the Brachycera, it has long been known that this molecule is a novelty within this group, and that other molecules must be used in other species [12,13]. A wide variety of such anterior determinants have been found, and evidence indicates
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that the identity of molecules used as anterior determinants varies widely. For example, in the wasp Nasonia vitripennis, the transcription factors orthodenticle-1 (Nvotd1) and giant (Nv-gt) are required for proper anterior patterning, with Nv-otd1 playing an instructive role, and Nv-gt playing a permissive role [14,15]. By contrast, in the honeybee Apis, orthodenticle is not localized [16], and several pair-rule genes show localization and appear to act as anterior determinants [17]. A spectacular case of unexpected novelty in anterior determinants was found in the midge Chironomus riparius, where the novel gene panish [18] plays a role in specifying the anterior pole. The existence of such a factor was predicted by classical embryological manipulations [19]. Recently, a surprising factor was discovered to have the ability to define the anterior pole in the beetle T. castaneum germ-cell-less (gcl) is a component of the posteriorly localized germ plasm in D. melanogaster, and is important for proper formation of the pole cells [20]. T. castaneum gcl (Tc-gcl) mRNA is maternally localized to the anterior pole and RNA interference (RNAi) knockdown of Tc-gcl leads to the replacement of anterior structures with posterior ones, producing a mirror image symmetrical doubleabdomen embryo and larva. The mechanism behind this appears to be partially related to proper localization of the wingless signaling inhibitor Tc-axin to the anterior pole. However, since knockdown of Tc-axin has previously been shown to be important for anterior patterning, but did not produce double-abdomen embryos [21], the authors propose that another factor must also be regulated by maternal Tc-gcl. However, another analysis of Tc-axin showed that double abdomens do appear at low frequency when Tc-axin is knocked-down [22]. This would indicate that Tc-axin could be the sole crucial target of Tc-gcl at the anterior. A role for localized mRNA acting as an anterior determinant has been shown in another beetle, the bean beetle Callosobruchus maculatus [23]. Classical constriction experiments had implied that a strong anterior patterning center operated in this beetle [24]. These results were extended in recent experiments involved exposing different regions of the embryo to RNAse. Only embryos where the anterior pole was exposed to RNAse produced mirror image double-abdomen embryos, which showed that the anterior patterning center is a localized RNA in the C. maculatus. The identity of the causative molecule has yet to be determined. By contrast to the above insects, a search for localized mRNAs encoding AP patterning determinants did not produce any clear candidates in the milkweed bug Oncopeltus fasciatus [25]. This may indicate that other ways of storing and sensing positional information may exist in this species. Such mechanisms could include localized www.sciencedirect.com Please cite this article in press as:
protein in the oocyte, subtly enriched mRNA at one or both poles, or the storage of AP patterning information in the eggshell.
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Finally, an extraordinary system for maternal influence of early embryonic patterning is found in the Lepidoptera. In both the silkmoth Bombyx mori [26] and the speckled wood butterfly Pararge aegeria [27], an extraordinary amount of mRNA based pre-patterning is found in the oocytes. This pre-patterning is such that the patterns of maternal mRNA localization are almost identical to expected patterns of zygotic expression for some gap genes such as orthodenticle and caudal. It is difficult to reconcile this pre-patterning with the relatively simple cytoskeletal polarity known in D. melanogaster, so uncovering the mechanism underlying the Lepidopteran system will be a very interesting and important endeavor.
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Maternal input into DV patterning
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Unlike the staggering diversity of anterior patterning components described above, the maternal components of DV patterning seem to be much more evolutionarily stable. Asymmetric EGF signaling from the region surrounding the oocyte nucleus to the overlying follicle cells is broadly conserved across insect phylogeny [28]. It turns out the grk is a highly derived duplication of an EGF ligand similar to spitz in the fly. Other insects generally have a single ortholog [28]. Further, knockdown of EGF signaling components leads to major disruptions of DV patterning in T. castaneum and N. vitripennis, and DV asymmetry in oocyte shape is lost in the cricket Gryllus bimaculatus (RNAi against EGF components led to sterility in the cricket) [28]. In addition, it appears that asymmetric maternal EGF signaling acts to restrict maternal Toll signaling to the ventral side of the egg across insect species [29,30]. This indicates that this association of EGF and Toll signaling in setting up the DV axis is an ancestral feature of insect patterning systems.
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Although the identity of the maternal components of the DV system are broadly conserved, the way they are deployed varies greatly. In D. melanogaster, Toll signaling, shaped by maternal EGF signaling, plays a direct role in activating and repressing at least 70 target genes along the axis [31]. Among those targets are several components of the BMP signaling pathway, which patterns the dorsal half of the embryo. In the wasp N. vitripennis, where DV patterning outputs look almost identical to D. melanogaster (despite 300 million years of evolutionary separation) EGF signaling is crucial for regulating Toll signaling, and keeping activation of this pathway in a consistent stripe parallel to the long axis of the embryo [28]. However, in contrast to D. melanogaster, the EGF-Toll system has little to no effect on the BMP signaling pathway, or on patterning the dorsal half of the wasp embryo [30]. This indicates that there is an independent, maternal system
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that controls the formation of the BMP patterning gradient in N. vitripennis.
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On the other end of the spectrum, the DV patterning system of O. fasciatus, perhaps like the AP system of this insect, seems to have a minimal amount of maternally generated patterning information. In this insect, Toll signaling (presumably controlled by maternal EGF) appears to have a very limited direct patterning role, in stark contrast to D. melanogaster. Instead, it appears to serve primarily a symmetry breaking role, with the vast majority of DV patterning being carried out by BMP signaling [29].
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Future directions
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Determining origin of anterior determinant diversity
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One of the most striking features of maternal input into early embryonic patterning is the very surprising diversity in the molecules that play the role of anterior determinants. The reasons for this pattern, and the mechanisms that allow anterior determinants to radically change, are unclear, and should be a focus for future research.
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One pair of crucial questions is: how important are high levels of maternal positional information for development in different species?, and under what ecological conditions is there pressure to change the amount or nature of maternal patterning information? The Bicoid gradient of D. melanogaster pointed to a reliance on maternally provided patterning information controlling zygotic gene expression along most of the long axis of the insect embryo. However, D. melanogaster is likely to be an exceptional case, as it represents an extreme form of ‘long germ’ embryogenesis, and rapidly patterns both axes more or less simultaneously before gastrulation mostly under the influence of maternal inputs [32]. However, most insects rely significantly on interactions among zygotic genes in a dynamic developmental environment, especially in embryos of the ‘short germ’ type, where only anterior segments are patterned under the influence of maternal factors [32]. For example, in T. castaneum it appears that the small input of maternally localized genes is sufficient to polarize the embryo by restricting the expression of a relative handful of zygotic genes near the poles [20]. The detailed patterning is then left to dynamic interactions among zygotic genes in a rapidly changing embryo. One can extrapolate this to a case like O. fasciatus, where a potentially very subtle source of AP asymmetry may be sufficient to polarize the embryo [25], with zygotic interactions performing the remaining work of generating and interpreting additional positional information. Furthermore, the strictly hierarchical patterning mode proposed for long germ embryos based on knowledge from D. melanogaster may not be universal. In another long Current Opinion in Insect Science 2018, 1:1–6 Please cite this article in press as:
germ model system, the wasp N. vitripennis, there is significant dynamic gene expression before the final pattern of gap and pair-rule genes is set, indicating a less strictly instructive role for maternal patterning information in the wasp compared to D. melanogaster [14,33].
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Even more to the point, recent results have shown that the D. melanogaster AP system shows remnants of a temporally regulated patterning system shared at least with the short-germ T. castaneum embryo [34,35]. Although we cannot yet extrapolate that this system was ancestral to insects (sampling of other insect lineages such as the Hymenoptera, Paraneoptera, and other hemimetabolous lineages will be required), these results give a starting point to understand how strong maternal determinants can arise and become increasingly powerful in establishing polarity and pattern in early embryos.
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Understanding the different evolutionary patterns of DV and AP maternal determinants
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By contrast to the variability in AP maternal determinants, the DV system appears to be much more conserved. In all cases so far examined Toll signaling (provided and regulated by EGF maternally) establishes the ventral pole, and works in opposition to BMP signaling with a peak at the dorsal pole. The reasons for the stability of the DV system are obscure. Perhaps the patterning problem that DV patterning presents in typical insect embryos is a source of constraint. Most insect eggs are sausage shaped cylinders with elongated AP axes. Creating a strong source of patterning information is relatively simple for the AP axis, as a point-like source of a diffusible molecule can be placed at one or both poles of the embryo, allowing for efficient and straightforward gradient formation. For the DV axis, a polar source of positional information would have to be more line-like to provide consistent input along the whole axis. Known properties of oocyte cytoskeletal polarity are quite compatible with generating point-like localization of mRNAs at the anterior and posterior poles, but the formation of a line on the DV axis would require novel, presently unknown mechanisms. Such mechanisms can arise, as DV stripes of localized mRNA have been observed in honeybee and wasp oocytes [28,36], but no new transcription factor or signaling system is yet known to have replaced the EGF-Toll-BMP patterning system.
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Conclusions
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The evolution of maternal contribution of patterning information to insect eggs is an important model for understanding the evolution of development. This is because the egg represents a crucial transition point in the life history of insects. The egg is generated by the mother, whose provision determines the amount of energy and patterning information the egg has to work with, for example. Once laid, the egg has to be able to survive in the environment in which it was laid long
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enough to allow the larva or nymph to develop and hatch, and many innovations in eggshell architecture and specialized embryonic tissues have been made to adapt to the wide variety of environments insect eggs find themselves in (e.g., [37–39]). Finally, embryonic development must produce a larva or imago that is best equipped to survive and exploit the niche into which it hatches. Each of the above considerations can present trade-offs that can affect the type, amount, and nature of maternally produced patterning information provided to the embryo. Further sampling of insect developmental diversity will provide important insights into innovations and tradeoffs that have been made in the processes of adaptation.
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Funding
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JAL was supported by NIH grant 1R03HD078578 and startup fund from University of Illinois at Chicago.
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34. Clark E., Peel AD: Evidence for the temporal regulation of insect segmentation by a conserved sequence of transcription factors. Development 2018 http://dx.doi.org/10.1242/ dev.155580. PubMed PMID: 29724758; PMCID: PMC6001374. This paper shows that there was likely a conserved temporal basis of segment patterning in the most recent common ancestor of Tribolium and Drosophila, making understanding transitions between the long and short germ modes of development more easy to understand.
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35. Clark E: Dynamic patterning by the Drosophila pair-rule network reconciles long-germ and short-germ segmentation. PLoS Biol 2017, 15:e2002439 http://dx.doi.org/10.1371/journal. pbio.2002439 PubMed PMID: 28953896; PMCID: PMC5633203.
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36. Wilson M.J., Kenny NJ, Dearden PK: Components of the dorsal– ventral pathway also contribute to anterior–posterior patterning in honeybee embryos (Apis mellifera). Evodevo. 2014, 5 doi: Artn 11/2041-9139-5-11. PubMed PMID: WOS:000334642500001.
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37. Jacobs C.G.C., Rezende GL, Lamers GEM, van der Zee M: The extraembryonic serosa protects the insect egg against desiccation. Proc R Soc B-Biol Sci 2013, 280 doi: ARTN 20131082/rspb.2013.1082. PubMed PMID: WOS:000320649400018.
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38. Jacobs C.G.C., Spaink HP, van der Zee M: The extraembryonic serosa is a frontier epithelium providing the insect egg with a full-range innate immune response. Elife 2014, 3 doi: ARTN e04111/eLife.04111. PubMed PMID: WOS:000346170300011.
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39. Hinton H.E.: The structure and function of the egg-shell in the Nepidae (Hemiptera). J Insect Physiol 1961, 7:224-257 http://dx. doi.org/10.1016/0022-1910(61)90075-0.
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Evolution of maternal control of axial patterning in insects Jeremy A Lynch Positional and cell fate cues provided maternally to eggs are important factors in the development of many animals. The insects are a model clade where maternal establishment of embryonic axes is widespread and has been a topic of intense classical and molecular embryological analysis. Recently, significant progress has been made in revealing the molecular basis of some classical embryological experiments. In addition, observations of novel forms of maternal positional cues have been made. Finally, it has become increasingly clear that no maternal source of positional information acts alone without input and feedback from zygotic target genes to ensure precise and repeatable pattern formation in the early embryo. These advances will be discussed in the context of historical experiments, our current understanding of how positional cues can be generated, stored, and transmitted in insect ovaries and eggs, and how the nature of the cues can change in evolution. Address University of Illinois at Chicago, Chicago, IL, USA Corresponding author: Lynch, Jeremy A ([email protected])
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Unique features of insect ovaries
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Insect ovaries have an anterior–posterior (AP) polarity that typically follows that of the female. Typically, a germline stem-cell resides at the anterior end (Figure 1a). When this stem cell divides to produce a gametic progenitor (Figure 1b), the latter moves posteriorly and begins differentiation. Repetition of this process leads to the production of a string of differentiating germ cells of increasing age from anterior to posterior. Thus, each developing oocyte is flanked by a younger oocyte progenitor at its anterior, and an older one to its posterior (Figure 1c,d). If this asymmetric information could be transmitted and stored, it would be a potent source of positional cues. That such transmission occurs was clear
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well before the molecular era, as it was observed that the anterior–posterior polarity of insect eggs almost always is tightly correlated to the AP polarity of the ovariole [1,2].
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Another intrinsic property of the insect oocyte is the asymmetric movement of the germinal vesicle (oocyte nucleus) from a symmetric position in the central column of cytoplasm (Figure 1d) to a highly asymmetric location at the plasma membrane (Figure 1e). This movement is necessary to prepare the oocyte nucleus for the resumption and completion of meiosis when the egg is laid and activated [3]. The importance of this movement was also strongly implied by early investigators, where it was observed that position of the oocyte nucleus very often marks the dorsal pole of the egg and embryo [4,5].
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Crucially, there is a strong interaction between germline cells and somatic cells in the insect ovary. A single layer of somatic cells surrounds a single germline cell (Figure 1c–e), or a clone of sister germline cells, forming the functional unit of the insect ovary, the egg chamber. The somatic cells surrounding the germline cells are called follicle cells, and these cells can receive, store, and transmit positional information through communication among themselves and with the germ cells [2]. Since the follicle cells secrete the eggshell, information can be stored in structure of the eggshell layers, or in the fluid that separates the egg from the innermost eggshell layer. Thus, information can be passed to the developing embryos (Figure 1f), even after follicle cells are gone.
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Finally, communication among the germline and somatic cells can lead to the polarization of the oocyte itself, allowing for the differential localization of macromolecules at different poles of the egg (Figure 1d,e), which are also maintained in the embryo (Figure 1f).
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Maternal patterning information in Drosophila melanogaster
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The molecular basis of maternal positional information has been intensively studied in insects, primarily in D. melanogaster. A relay system involving Jak/STAT and Notch signaling operates in the ovary to position the oocyte correctly within the egg chamber, and pass positional information from the older egg chambers to the newly specified oocyte [6]. This relay system leads to the establishment of AP polarity within the oocyte, and the proper localization of mRNA for the anterior determinant bicoid and posterior/germ cell determinant oskar at their respective poles. Localized bcd mRNA gives rise to a
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Generation and storage positional information in the insect ovary. Ovariole highly schematic to represent common features of all types of oogenesis. (a) Anteriorly localized germline stem cell. (b) Differentiating oocyte. (c) Oocyte surrounded by follicle cell layer (solid black circles). Blue arrows indicate oocyte receiving signals from specialized follicle cells (solid red circles), leading to polarization of the embryo. In this case, it is a hypothetical situation, drawn from knowledge gained from D. melanogaster. (d) Maturing egg chamber with polarized oocyte (indicated by posteriorly localized blue), sending signals (orange arrows) to anterior follicle cells (green), which in turn signal to the next younger oocyte to induce polarity (again a hypothetical mechanism). (e) Late stage egg chamber. The oocyte nucleus (black and white checkered circle) has migrated to the cortex, where it induces signaling to and differentiation of, the overlying follicle cells (yellow circles). (f) Schematic representation of a typical insect embryo, with regions of potential eggshell modification and embryonic RNA localization marked with colors corresponding to their origin the ovary (c–f).
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gradient of protein that acts as a morphogen to establish cell fates in the anterior half of the embryo. Oskar protein is crucial for assembling the germplasm (which specifies the primordial germ cells) and stabilizing nanos mRNA. Posterior Nanos protein plays a permissive role in preventing the early translation of maternal hunchback (hb) mRNA [7]. The molecular basis of maternal establishment DV polarity is also well described in D. melanogaster. mRNA for the EGF ligand gurken (grk) is localized around the oocyte nucleus which becomes localized at an asymmetric location at the anterior. Grk protein is secreted and activates Current Opinion in Insect Science 2018, 1:1–6 Please cite this article in press as:
EGF receptor expressed in the follicle cells. This leads to a ventrally localized modification of the eggshell. This information stored in the eggshell is then transmitted back to the embryo through localized processing of the Toll ligand Spaetzle to the ventral half of the egg. Again, this leads to a graded source of patterning information, this time in the form of nuclear uptake of the Toll target transcription factor Dorsal. The Dorsal gradient also regulates its targets in a concentration dependent fashion, and has been described as a morphogen [8].
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Establishing oocyte polarity
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Whether the developmental and molecular bases of inducing AP polarity in the oocyte are conserved outside of D. melanogaster is an interesting topic, especially in light of the variability in the structure of ovaries across insects. D. melanogaster has polytrophic meroistic ovaries, which means that the oocyte is one of a clone of sister germline cells. The other germline cells become ‘nurse cells’ which are specialized to produce macromolecules provided to the oocyte. These germ cells are surrounded as a unit by follicle cells to form egg chambers. Many insects have telotrophic meroistic ovaries, where a common pool of nurse cells located toward the anterior end of the ovary feed oocytes that become encapsulated by follicle cells as they mature and move posteriorly. Finally, panoistic ovaries lack nurse cells, and each oocyte is encapsulated singly by follicle cells [2,8].
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Since the polarization of the D. melanogaster oocyte occurs in the context of the selection and migration of the oocyte in the context of its sister cells in the specialized polytrophic ovaries of the fly [6], it might stand to reason that the D. melanogaster system may not be broadly conserved, especially in systems with different ovary types. Indeed, it appears that JAK/STAT signaling does not have a role in establishing AP polarity of the ooctye in the telotrophic ovaries of the beetle Tribolium castaneum, despite a partially conserved role in specifying the stalk cells that separate egg chambers from each other [9]. On the other hand, Notch signaling between the germline and soma appears to have a conserved role in establishing AP polarity with in the T. castaneum oocyte [10]. Examination of Notch signaling in the cockroach Blatella germanica indicates that signaling between germline and soma is conserved, but any effect on oocyte polarity is yet to be shown [11].
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Diverse roles of localized mRNAs
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Although bcd is the absolutely crucial anterior determinant in D. melanogaster and its relatives in the Brachycera, it has long been known that this molecule is a novelty within this group, and that other molecules must be used in other species [12,13]. A wide variety of such anterior determinants have been found, and evidence indicates
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that the identity of molecules used as anterior determinants varies widely. For example, in the wasp Nasonia vitripennis, the transcription factors orthodenticle-1 (Nvotd1) and giant (Nv-gt) are required for proper anterior patterning, with Nv-otd1 playing an instructive role, and Nv-gt playing a permissive role [14,15]. By contrast, in the honeybee Apis, orthodenticle is not localized [16], and several pair-rule genes show localization and appear to act as anterior determinants [17]. A spectacular case of unexpected novelty in anterior determinants was found in the midge Chironomus riparius, where the novel gene panish [18] plays a role in specifying the anterior pole. The existence of such a factor was predicted by classical embryological manipulations [19]. Recently, a surprising factor was discovered to have the ability to define the anterior pole in the beetle T. castaneum germ-cell-less (gcl) is a component of the posteriorly localized germ plasm in D. melanogaster, and is important for proper formation of the pole cells [20]. T. castaneum gcl (Tc-gcl) mRNA is maternally localized to the anterior pole and RNA interference (RNAi) knockdown of Tc-gcl leads to the replacement of anterior structures with posterior ones, producing a mirror image symmetrical doubleabdomen embryo and larva. The mechanism behind this appears to be partially related to proper localization of the wingless signaling inhibitor Tc-axin to the anterior pole. However, since knockdown of Tc-axin has previously been shown to be important for anterior patterning, but did not produce double-abdomen embryos [21], the authors propose that another factor must also be regulated by maternal Tc-gcl. However, another analysis of Tc-axin showed that double abdomens do appear at low frequency when Tc-axin is knocked-down [22]. This would indicate that Tc-axin could be the sole crucial target of Tc-gcl at the anterior. A role for localized mRNA acting as an anterior determinant has been shown in another beetle, the bean beetle Callosobruchus maculatus [23]. Classical constriction experiments had implied that a strong anterior patterning center operated in this beetle [24]. These results were extended in recent experiments involved exposing different regions of the embryo to RNAse. Only embryos where the anterior pole was exposed to RNAse produced mirror image double-abdomen embryos, which showed that the anterior patterning center is a localized RNA in the C. maculatus. The identity of the causative molecule has yet to be determined. By contrast to the above insects, a search for localized mRNAs encoding AP patterning determinants did not produce any clear candidates in the milkweed bug Oncopeltus fasciatus [25]. This may indicate that other ways of storing and sensing positional information may exist in this species. Such mechanisms could include localized www.sciencedirect.com Please cite this article in press as:
protein in the oocyte, subtly enriched mRNA at one or both poles, or the storage of AP patterning information in the eggshell.
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Finally, an extraordinary system for maternal influence of early embryonic patterning is found in the Lepidoptera. In both the silkmoth Bombyx mori [26] and the speckled wood butterfly Pararge aegeria [27], an extraordinary amount of mRNA based pre-patterning is found in the oocytes. This pre-patterning is such that the patterns of maternal mRNA localization are almost identical to expected patterns of zygotic expression for some gap genes such as orthodenticle and caudal. It is difficult to reconcile this pre-patterning with the relatively simple cytoskeletal polarity known in D. melanogaster, so uncovering the mechanism underlying the Lepidopteran system will be a very interesting and important endeavor.
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Unlike the staggering diversity of anterior patterning components described above, the maternal components of DV patterning seem to be much more evolutionarily stable. Asymmetric EGF signaling from the region surrounding the oocyte nucleus to the overlying follicle cells is broadly conserved across insect phylogeny [28]. It turns out the grk is a highly derived duplication of an EGF ligand similar to spitz in the fly. Other insects generally have a single ortholog [28]. Further, knockdown of EGF signaling components leads to major disruptions of DV patterning in T. castaneum and N. vitripennis, and DV asymmetry in oocyte shape is lost in the cricket Gryllus bimaculatus (RNAi against EGF components led to sterility in the cricket) [28]. In addition, it appears that asymmetric maternal EGF signaling acts to restrict maternal Toll signaling to the ventral side of the egg across insect species [29,30]. This indicates that this association of EGF and Toll signaling in setting up the DV axis is an ancestral feature of insect patterning systems.
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Although the identity of the maternal components of the DV system are broadly conserved, the way they are deployed varies greatly. In D. melanogaster, Toll signaling, shaped by maternal EGF signaling, plays a direct role in activating and repressing at least 70 target genes along the axis [31]. Among those targets are several components of the BMP signaling pathway, which patterns the dorsal half of the embryo. In the wasp N. vitripennis, where DV patterning outputs look almost identical to D. melanogaster (despite 300 million years of evolutionary separation) EGF signaling is crucial for regulating Toll signaling, and keeping activation of this pathway in a consistent stripe parallel to the long axis of the embryo [28]. However, in contrast to D. melanogaster, the EGF-Toll system has little to no effect on the BMP signaling pathway, or on patterning the dorsal half of the wasp embryo [30]. This indicates that there is an independent, maternal system
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that controls the formation of the BMP patterning gradient in N. vitripennis.
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On the other end of the spectrum, the DV patterning system of O. fasciatus, perhaps like the AP system of this insect, seems to have a minimal amount of maternally generated patterning information. In this insect, Toll signaling (presumably controlled by maternal EGF) appears to have a very limited direct patterning role, in stark contrast to D. melanogaster. Instead, it appears to serve primarily a symmetry breaking role, with the vast majority of DV patterning being carried out by BMP signaling [29].
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Future directions
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Determining origin of anterior determinant diversity
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One of the most striking features of maternal input into early embryonic patterning is the very surprising diversity in the molecules that play the role of anterior determinants. The reasons for this pattern, and the mechanisms that allow anterior determinants to radically change, are unclear, and should be a focus for future research.
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One pair of crucial questions is: how important are high levels of maternal positional information for development in different species?, and under what ecological conditions is there pressure to change the amount or nature of maternal patterning information? The Bicoid gradient of D. melanogaster pointed to a reliance on maternally provided patterning information controlling zygotic gene expression along most of the long axis of the insect embryo. However, D. melanogaster is likely to be an exceptional case, as it represents an extreme form of ‘long germ’ embryogenesis, and rapidly patterns both axes more or less simultaneously before gastrulation mostly under the influence of maternal inputs [32]. However, most insects rely significantly on interactions among zygotic genes in a dynamic developmental environment, especially in embryos of the ‘short germ’ type, where only anterior segments are patterned under the influence of maternal factors [32]. For example, in T. castaneum it appears that the small input of maternally localized genes is sufficient to polarize the embryo by restricting the expression of a relative handful of zygotic genes near the poles [20]. The detailed patterning is then left to dynamic interactions among zygotic genes in a rapidly changing embryo. One can extrapolate this to a case like O. fasciatus, where a potentially very subtle source of AP asymmetry may be sufficient to polarize the embryo [25], with zygotic interactions performing the remaining work of generating and interpreting additional positional information. Furthermore, the strictly hierarchical patterning mode proposed for long germ embryos based on knowledge from D. melanogaster may not be universal. In another long Current Opinion in Insect Science 2018, 1:1–6 Please cite this article in press as:
germ model system, the wasp N. vitripennis, there is significant dynamic gene expression before the final pattern of gap and pair-rule genes is set, indicating a less strictly instructive role for maternal patterning information in the wasp compared to D. melanogaster [14,33].
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Even more to the point, recent results have shown that the D. melanogaster AP system shows remnants of a temporally regulated patterning system shared at least with the short-germ T. castaneum embryo [34,35]. Although we cannot yet extrapolate that this system was ancestral to insects (sampling of other insect lineages such as the Hymenoptera, Paraneoptera, and other hemimetabolous lineages will be required), these results give a starting point to understand how strong maternal determinants can arise and become increasingly powerful in establishing polarity and pattern in early embryos.
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Understanding the different evolutionary patterns of DV and AP maternal determinants
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By contrast to the variability in AP maternal determinants, the DV system appears to be much more conserved. In all cases so far examined Toll signaling (provided and regulated by EGF maternally) establishes the ventral pole, and works in opposition to BMP signaling with a peak at the dorsal pole. The reasons for the stability of the DV system are obscure. Perhaps the patterning problem that DV patterning presents in typical insect embryos is a source of constraint. Most insect eggs are sausage shaped cylinders with elongated AP axes. Creating a strong source of patterning information is relatively simple for the AP axis, as a point-like source of a diffusible molecule can be placed at one or both poles of the embryo, allowing for efficient and straightforward gradient formation. For the DV axis, a polar source of positional information would have to be more line-like to provide consistent input along the whole axis. Known properties of oocyte cytoskeletal polarity are quite compatible with generating point-like localization of mRNAs at the anterior and posterior poles, but the formation of a line on the DV axis would require novel, presently unknown mechanisms. Such mechanisms can arise, as DV stripes of localized mRNA have been observed in honeybee and wasp oocytes [28,36], but no new transcription factor or signaling system is yet known to have replaced the EGF-Toll-BMP patterning system.
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Conclusions
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The evolution of maternal contribution of patterning information to insect eggs is an important model for understanding the evolution of development. This is because the egg represents a crucial transition point in the life history of insects. The egg is generated by the mother, whose provision determines the amount of energy and patterning information the egg has to work with, for example. Once laid, the egg has to be able to survive in the environment in which it was laid long
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enough to allow the larva or nymph to develop and hatch, and many innovations in eggshell architecture and specialized embryonic tissues have been made to adapt to the wide variety of environments insect eggs find themselves in (e.g., [37–39]). Finally, embryonic development must produce a larva or imago that is best equipped to survive and exploit the niche into which it hatches. Each of the above considerations can present trade-offs that can affect the type, amount, and nature of maternally produced patterning information provided to the embryo. Further sampling of insect developmental diversity will provide important insights into innovations and tradeoffs that have been made in the processes of adaptation.
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JAL was supported by NIH grant 1R03HD078578 and startup fund from University of Illinois at Chicago.
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