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Developmental Biology 313 (2008) 471–491 www.elsevier.com/developmentalbiology

Review Extraembryonic development in and the acrobatics of blastokinesis ⁎ Kristen A. Panfilio

University Museum of Zoology, Department of Zoology, Downing Street, Cambridge CB2 3EJ, UK Received for publication 10 July 2007; revised 11 October 2007; accepted 2 November 2007 Available online 17 November 2007

Abstract

Extraembryonic development is familiar to mouse researchers, but the term is largely unknown among developmental geneticists. This is not surprising, as the model system Drosophila melanogaster has an extremely reduced extraembryonic component, the amnioserosa. In contrast, most insects retain the ancestral complement of two distinct extraembryonic membranes, amnion and serosa. These membranes are involved in several key morphogenetic events at specific developmental stages. The events of anatrepsis and katatrepsis–collectively referred to as blastokinesis–are specific to hemimetabolous insects. Corresponding events in holometabolous insects are simplified and lack formal names. All insects retain dorsal closure, which has been well studied in Drosophila. This review aims to resurrect both the terminology and awareness of insect extraembryonic development–which were last common currency in the late nineteenth and early twentieth centuries–as a number of recent studies have identified essential components of these events, through RNA interference of developmental genes and ectopic hormonal treatments. As much remains unknown, this topic offers opportunities for research on tissue specification, the regulation of cell shape changes and tissue interactions during morphogenesis, tracing the origins and final fates of cell and tissue lineages, and ascertaining the membranes' functions between morphogenetic events. © 2007 Elsevier Inc. All rights reserved.

Keywords: Insect; Extraembryonic membranes; Morphogenesis; Tissue interactions; Epithelial reorganization; Amnion; Serosa; Blastokinesis; Anatrepsis; Katatrepsis

Introduction “additional complication” (p. 130) to embryogenesis in some insect orders. Yet extraembryonic development is relevant to Insect extraembryonic development encompasses all aspects the development of all insects. Researchers who are currently of embryogenesis involving the amniotic and serosal mem- familiar with this fact include embryological endocrinologists branes. In this review I will focus primarily on the role of the (e.g., Truman and Riddiford, 1999) and classical morpholo- membranes in morphogenetic events, specifically the move- gists (extraembryonic membranes even feature in the logo of ments associated with membrane formation–anatrepsis–and the Arthropodan Embryological Society of Japan). Meanwhile, their last acts–katatrepsis and dorsal closure–prior to their Anderson's view is still prevalent among developmental demise. These movements are particularly well developed in geneticists. Blastokinesis does not occur in the model hemimetabolous insects (those with incomplete metamorpho- organism Drosophila melanogaster, the embryos of which sis) and are collectively known as blastokinesis. Extraembryo- have very reduced extraembryonic tissue (although this tissue is nic membrane ontogeny in the holometabolous insects (those still essential for development). As a consequence, many with complete metamorphosis: embryonic, larval, pupal, and researchers are either unaware of the phenomena of extraem- adult stages) includes a subset of these events. bryonic development or have glossed over them in their own The occurrence of blastokinesis was last reviewed in detail research . This is reflected in searching the PubMed 35 years ago by Anderson (1972a), who regarded it as an database of biomedical and life science articles (http://www. ncbi.nlm.nih.gov), where there are thousands of articles on “insect embryo” generally but only a handful specifically for ⁎ Fax: +44 1223 336 679. “blastokinesis” or “insect extraembryonic development.” As I E-mail address: [email protected]. hope to show here, extraembryonic development is fascinating

0012-1606/$ - see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.ydbio.2007.11.004 472 K.A. Panfilio / Developmental Biology 313 (2008) 471–491 and worthy of researchers' attention in its own right for study of progressively. Among non-insect hexapods (see phylogeny in a multitude of developmental processes. Fig. 2), Collembola and Protura (springtails and allies) possess a This review is two-pronged: it surveys manifestations of serosa and a structure known as the primary dorsal organ (see blastokinesis, and it summarizes relevant functional data on Box 1), but they lack two distinct membranes (Anderson, 1973, these movements. To provide adequate context, I begin with a p. 205; Jura, 1972; Machida, 2006; Uemiya and Ando, 1991). background account of the evolution and possible functional Similarly the Diplura (two-pronged bristletails) have a single, roles of the membranes. To introduce the nature and complexity serosal covering over the yolk, though there is also later of the morphogenetic events, blastokinesis is first described in production of additional extraembryonic tissue, which has been detail in a representative species. This is followed by the termed “amnion” (Ikeda and Machida, 2001). Within the true comparative survey of extraembryonic morphogenesis across insects, the amnion is prefigured by the pro-amniotic/pro- the insects. I then assess the relationship of the membranes to serosal distinction in archaeognathan (bristletail) embryos the execution of these movements in different species. Lastly, I (Heymons and Heymons, 1905; Machida et al., 1994; see present recent data from perturbation studies that elucidate some Box 1). An amnion proper is first seen in the Thysanura of the molecular components underlying extraembryonic (firebrats; Anderson, 1972a, pp. 204–205; Jura, 1972, pp. 80– morphogenesis, and identify possible avenues for further 82). However the thysanuran amnion does not form a complete research. membrane but leaves a persistently open amniotic cavity (Heymons and Heymons, 1905; Woodland, 1957). Complete Phylogeny of extraembryonic membrane elaboration and amnions seem restricted to the pterygote (winged) insects, reduction although the apterygote species survey supporting this claim is limited. Extraembryonic cells or tissues are common features of As Dorn (1976) also indicates, there are deviations from embryogenesis in . This material has become elaborated possession of two extraembryonic membranes in some in the insects to comprise two distinct membranes, with each holometabolous insect species (see phylogeny in Fig. 2). possessing a distinct topography and role. The inner membrane, Here, the lack of a full membrane complement is a derived, the amnion, envelops the ventral side of the developing embryo, secondary condition. Wholesale changes in embryogenesis– creating the fluid-filled amniotic cavity. The outer membrane, such as rapid development from a large embryonic rudiment the serosa, lies just under the chorion (eggshell), and surrounds (relative to egg size)–correlate with a reduction in extraem- embryo, amnion, and yolk (Fig. 1). Presence of these two bryonic tissue (Anderson, 1972a; Roth, 2004). In some lower membranes is regarded as a synapomorphy (shared, derived Hymenoptera (sawflies), the amnion forms but degenerates very character) of the insect egg (Larink, 1997): early in development and may be fragmentary (Ivanova-Kasas, 1959; Shafiq, 1954). Apocritan (higher) Hymenoptera (bees, Serosa and amnion can be considered standard inventory of ants, and wasps) usually lack an amnion, or have only a the insect embryo. The absence of one or the other in temporary amniotic vestige that covers the yolk rather than the apterygote insects is probably indicative of their phyloge- embryo (Anderson, 1972b; Bull, 1982; Fleig and Sander, 1988). netic development, whereas deviations, as they occur in Cyclorrhaphous (higher) Diptera (true flies), including the fruit holometabolous insects, represent presumably environmen- fly Drosophila melanogaster, lack distinct amniotic and serosal tal adjustments. (Dorn, 1976) membranes, retaining a single membrane, the amnioserosa, As implied by the quotation, the membranes arose within the which also covers only the yolk (Anderson, 1972b; Schmidt- lineage of apterygote (primitively wingless) insects, perhaps Ott, 2000).

Proposed functions of the extraembryonic membranes

Given the conserved presence of the extraembryonic mem- branes in most insects, why do they exist? Their designation as extraembryonic signifies that the amnion and the serosa do not directly contribute to the final form of the body. What function do they fulfill to necessitate their temporary existence? Such questions have produced several suggestions. Because Fig. 1. Schematic cartoons of a germband stage embryo, illustrating the the membranes surround the embryo, a general protective positions of the serosa (blue) and amnion (orange) with respect to the embryo (grey) and yolk (yellow). The amniotic cavity (white) is the region between the function has been ascribed (Dorn, 1976; Oseto and Helms, amnion and the ventral surface of the embryo. (a) Mid-sagittal section view. (b) 1972; Zeh et al., 1989). Specifically, the fluid-filled amniotic Transverse section view at the position indicated by the flanking black bars in cavity may cushion the embryo (Anderson, 1972a). The outer schematic a. Orientation: egg-dorsal is up in both images and egg-anterior is left serosa can effect innate immune system responses to wounding in the sagittal view. Abbreviations: a, antenna; am, amnion; ab, abdominal or infection (Chen et al., 2000) or process environmental toxins region; gn, gnathal (mouthpart) region; h, head; ser, serosa; t1–3, thoracic segments/legs 1–3. The position of the embryo is modeled on the immersed (Berger-Twelbeck et al., 2003). In some species, the amnion or germband type, as seen in the milkweed bug Oncopeltus fasciatus (see also Fig. the serosa or both are involved in cuticle production (Cobben, 3, including the labeling of axes). 1968; Dorn, 1976; Heming, 2003; Mellanby, 1936). Cuticle K.A. Panfilio / Developmental Biology 313 (2008) 471–491 473

Fig. 2. Hexapod phylogeny indicating types of blastokinesis and modes of membrane formation in different taxa: see Table 1 for details and symbol key. Names of various levels of taxonomic classification are given, where these are common in the literature. Groupings indicated by solid colored boxes or circled nodes are monophyletic, while those with dashed-line boxes are paraphyletic. Phylogeny based on Gullan and Cranston (2000), Wheeler, et al. (2001), NCBI Browser (Benson et al., 2000; Wheeler et al., 2000), and The Tree of Life Web Project (2003); the latter two were accessed June 2006. Some relationships are still disputed, including those of the basal hexapods (see, e.g., Mallatt and Giribet, 2006), the Paraneoptera (see, e.g., Yoshizawa and Saigusa, 2001), and some Holometabola (see, e.g., Savard et al., 2006). For references on types of blastokinesis and membrane formation, see text. secreted by the amnion can contribute to the embryonic cuticle, 2003; Lamer and Dorn, 2001). Lastly, in some insect species implicating the amnion in effecting embryonic development per with specialized oviposition sites, inflation of the serosa plays se (Dorn, 1976). Serosal cuticle can augment or supplant an active role in hatching from the egg at the end of protection provided by the chorion (Chen et al., 2000; Church embryogenesis (described in Sander, 1976). and Rempel, 1971; Kobayashi, 1998; Miura et al., 2003; However, current role does not equate with original cause of Rakshpal, 1962; Slifer, 1932), but this role is not universally construction (i.e., insect embryos did not develop elaborate applicable (Lamer and Dorn, 2001). The serosa may also have a membrane covers because they would fulfill useful functions role in water regulation (Cobben, 1968; Mori, 1972; Slifer, once established). An extraembryonic epithelium occurs in the 1932; references cited in Dorn, 1976 and Zeh et al., 1989). Both eggs of many taxa outside the insects (Anderson, 1972a; amnion and serosa have also been implicated in yolk catabolism Chipman et al., 2004; Wheeler, 1893; Wolff and Scholtz, 2002). and active transport to sequester resulting metabolic waste, Thus cellularization over the yolk surface may be a general containing it within the amniotic cavity or in the space external phenomenon that simply produces more tissue than that which to the serosa (Dorn, 1976, and references therein; Heming, becomes the embryo proper. Similarly, early speculation on the 474 K.A. Panfilio / Developmental Biology 313 (2008) 471–491 origins of the amnion–being the more specialized and unique of ments are referred to as blastokinesis. Blastokinesis varies the two membranes–explains its creation as a byproduct of between insects in extent and type of movements, and in the physical forces during development. Wheeler (1893) suggested roles of different tissues in effecting the movements. Yet despite that “local induplication of the blastoderm due to rapid the permutations, the extraembryonic membranes are necessary proliferation of a single layer of cells” could produce a fold of for some and are inextricably involved in all of these tissue over the rest of the blastoderm, which could then develop movements. Following an introductory example of blastokin- into a complete membrane. Alternatively, he suggested that the esis in one species, this comparative account reviews some of fluid-filled amniotic cavity might result from “peripheral and the older literature–as the opening quote by Slifer (1932) is no external resistance” to growth of the embryo, making the amnion longer true–and thereby presents the widespread diversity of analogous to a blister, cushioning the embryo from the inner acrobatics performed within different insect eggs. surface of the eggshell! However, as described below, not all amnions form from folds or abut the eggshell, and thus different An introductory example: Blastokinesis in the milkweed bug mechanical reasons would need to account for different methods of amnion formation and different topographies. Here I present an overview of the movements in the Despite over 100 years of entomological research since milkweed bug Oncopeltus fasciatus (order Hemiptera, suborder Wheeler's suggestions, the origins and current roles of these Heteroptera: the “true bugs”). Oncopeltus is a suitable starting membranes remain uncertain, particularly for the amnion point as its blastokinetic movements are both complex and (Anderson, 1972a; Sander, 1976). Ultimately, the ancestral representative of several insect orders. Secondly, because On- impetus for formation of the amnion and the serosa simply may copeltus is sensitive to targeted gene knockdown by RNA have been the consequence of physical forces (whatever their interference (RNAi; Hughes and Kaufman, 2000; Liu and nature) that occur during embryogenesis. Once formed, there Kaufman, 2004), it is used increasingly as a hemimetabolous are clearly a number of useful functions that they may perform model species in comparative functional studies. Consequently, in extant insects. Indeed, it has been observed that in each of the several recent experimental findings on the molecular basis of great bilaterian groups of the deuterostomes and blastokinesis are from this species (see ‘How does it occur? protostomes, it is the group that has developed an amniotic Insights from experimental data’, below). The account of cavity–the amniote vertebrates (mammals and reptiles) and the blastokinesis presented here (from Panfilio et al., 2006, and insects, respectively–that has been the most successful on land unpublished observations) corroborates the classic description with respect to species number and range of colonized habitats of Butt (1949). (Grimaldi and Engel, 2005; Laurin and Gauthier, 1996; Zeh et Broadly, blastokinesis encompasses early entry and later exit al., 1989). Although analogous rather than deriving from a of embryo from yolk, termed anatrepsis and katatrepsis, common ancestral structure, the amnions of vertebrates and respectively. Compared to other developmental stages, both of insects seem to fulfill similar protective and metabolic these events occur quickly. In Oncopeltus each event may take functions. Thus convergence on the possession of an amnion as little as 1% of development (2 h at 25 °C). The embryo, in the egg correlates with an evolutionarily successful life amnion, and serosa are all involved (Fig. 3). history strategy–providing additional motivation for further The early, cellularized blastoderm consists of a continuous research on this extraembryonic structure. cell layer over the egg surface. Around 22% development, This introduction to insect extraembryonic membranes has anatrepsis proceeds by invagination of tissue into the yolk at the dealt with their presence or absence in various taxonomic posterior of the egg (Fig. 3a). This is immersion anatrepsis groups, and roles they may play given the arrangement of inner (further description in the following subsections on anatrepsis), amnion and outer serosa. However, this topography only applies and the invaginating tissue can be likened to a sock being pulled for a fraction of total developmental time of the insect egg. The through its own opening. The tissue that remains on the surface, amnion and the serosa are far from static structures, with the and spreads to fully envelop the yolk and internalized tissue, is developing and mature membranes involved in extensive the serosa. The invaginating tissue is the germ rudiment. movements during embryogenesis in most species. Further, in Although the serosa and germ rudiment arise from a continuous some insects the membranes have become necessary for the sheet of tissue, after invagination the latter becomes isolated in execution of these movements. Details of membrane formation the yolk and separated from the serosa. The germ rudiment and movements, and the possible functions ascribed to these, differentiates into the amnion and embryo, such that one wall of will be discussed in the following sections. the ‘sock’ is the embryo while the amnion comprises the other wall over the ventral side of the embryo. The embryo remains in A comparative survey of blastokinesis this position during the next quarter of development—as it extends in length and then retracts, and during segmentation and appendage formation (Figs. 1, 3b). “Blastokinesis, or the turning of the partially formed Halfway through (50%) development, katatrepsis reverses embryo in the egg, is a phenomenon familiar to all students this topography. The sock-like germ rudiment tissue (elaborated of insect development.” (Slifer, 1932) into amnion and embryo with appendages, but still a continuous The position of the embryo relative to the yolk changes as bag of tissue) everts. Here “eversion” is used in the sense of tissues move during embryogenesis. Collectively these move- turning outward (embryo and amnion), and of turning inside out K.A. Panfilio / Developmental Biology 313 (2008) 471–491 475

Fig. 3. Blastokinesis during Oncopeltus development illustrated by schematic cartoons with accompanying nuclear stainings: (a) immersion anatrepsis, (b) extended germband stage, (c) early katatrepsis, (d) mid katatrepsis, (e) late katatrepsis. The serosa has mostly been removed in the light micrograph in panel a, such that the yolk nuclei and germ rudiment are visible. The embryo is partially visible in panels b, c where it is not deep within the yolk. Images are in lateral aspect. Orientation: egg- anterior is left and dorsal is up. Micrographs are a single focal depth (a) and confocal projections (b–e) of fluorescent nuclear staining. Schematic color coding: blue, serosa; orange, amnion; grey, embryo. Black arrows in cartoons indicate the direction of motion; white arrowheads in micrographs demarcate the amnion–serosa boundary. Abbreviations: A, P, D, and V, anterior, posterior, dorsal, and ventral axes of egg, respectively; A′,P′, and V′, sides of the germband stage embryo; a, antenna; pr. ser, presumptive serosa; ser, serosa; t1, thoracic segment/leg 1. Micrographs in panels a, c, e are adapted from Panfilio et al. (2006), Fig. 3. 476 K.A. Panfilio / Developmental Biology 313 (2008) 471–491

(in the case of the amnion). The previously separate amnion and 1903; Seeger, 1979; Slifer, 1932). “Anatrepsis” is sometimes serosa (re-)fuse over the embryo's head, at the former site of equated with, or considered part of, “gastrulation” in a broad invagination. With the two membranes firmly attached to each sense (Kelly and Huebner, 1989; Roth, 2004), although it is other, they rupture within the area of contact, freeing the head distinct from the formation of the inner layer, or mesoderm, and antennae (Fig. 3c). As the serosa contracts toward the which may occur simultaneously with, after, or before anterior pole of the egg, the internal amnion and embryo emerge anatrepsis (e.g., Goss, 1952; Heming, 1979; Krysan, 1976, and replace the serosa. The embryo occupies the ventral surface respectively). The interval between anatrepsis and katatrepsis while the amnion provides a provisional dorsal and lateral was originally referred to as “diapause” (Wheeler, 1893), but the covering over the yolk. Emergence of embryo from yolk and terms “intertrepsis” (Heming, 2003; Heming and Huebner, membranes entails a 180° revolution, a backflip. As the embryo 1994; Masumoto and Machida, 2006) or simply “germband progressively emerges–first head and antennae, then the legs, stage” (e.g., Liu and Kaufman, 2004) are now more commonly and lastly the abdomen–it also bends backwards over the used. “Blastokinesis” is also used to describe changes in embryo posterior pole to reach the ventral surface. Thus at mid position or shape in the entognathans, the Archaeognatha, and katatrepsis, it forms a U-shape—half in, and half out of the the , but these are recognized as distinct processes yolk (Fig. 3d). By the completion of katatrepsis, all tissue has from blastokinesis in hemimetabolous insects (Fig. 2: denoted emerged from the yolk, and the embryo has advanced until the “Bx,” see Boxes 1 and 2; Anderson, 1972a; Jura, 1972; Wheeler, head is near the anterior pole of the egg (Fig. 3e). The serosa, 1893). Here I use “blastokinesis” to mean the specific formerly covering the entire egg surface, compacts into a small movements of anatrepsis and katatrepsis. cap at the anterior pole. Morphogenetic events involving the extraembryonic mem- Once katatrepsis is complete, the serosa is no longer branes have been described by an array of terminology. In required. It sinks behind the head, forming a structure called particular, there is a problem with the term “revolution,” which the (secondary) dorsal organ, and degenerates. Meanwhile, the usually means katatrepsis but also has been applied to long- flanks of the embryonic body grow dorsal-laterally and replace itudinal rotations of the germband (described below in ‘Variations the amnion, creating a complete body cavity that occupies the on katatrepsis, including rotations’; e.g., Rosay, 1959), or even full volume of the egg. Remaining yolk is now internal, and the changes inthe curvature of the germband (Box 1; e.g., Kobayashi, embryonic gut forms around it. The amnion, made redundant by 1998; Patten, 1884). Historically, insect embryo researchers embryonic dorsal closure, probably degenerates as well (but see tended to interpret data so that they fit contemporary terminology the ‘Future directions and questions’ section). and paradigms, and now “blastokinesis” and “revolution” have The axes of the egg are defined as corresponding to those of come to mean any movement of the embryo within the egg. Here the embryo at hatching (and possibly also to the mother during I apply these terms more strictly: “revolution” refers to the oogenesis: Cobben, 1968; Wheeler, 1893), and are constant. backflip movement at katatrepsis; “rotation” applies to move- Implicit in the above description, blastokinesis causes the ments about the longitudinal axis of the egg. embryo's orientation to change with respect to the axes of the For the following comparative survey, types of blastokinesis egg. Invagination at anatrepsis proceeds by a caudad-first entry and of extraembryonic membrane formation are indicated in of tissue into the yolk. The embryonic tissue remaining near the Fig. 2 and summarized in Table 1. site of invagination, at the posterior pole, develops into the embryonic head. Further, the ventral side of the embryo faces Types of anatrepsis upward: into the yolky interior and toward the dorsal side of the egg. Thus the germband stage embryo is both upside down and “Anatrepsis” describes movements whereby the ventral- backward (note axis key in Fig. 3). This situation is corrected by posteriorly positioned germ rudiment (=presumptive embryo+ the movements of katatrepsis, after which axes of egg and amnion) “moves through an arc till its body is completely embryo correspond. inverted” in an “ascending movement” (Wheeler, 1893). In superficial anatrepsis, the mode that defined the term, the arc Notes on terminology of movement is dictated by the posterior pole, which the embryo slides over in reaching the dorsal surface of the egg. “Blastokinesis,”“anatrepsis,” and “katatrepsis” were coined Alternatively, in immersion anatrepsis, the ascending move- by Wheeler (1893). The latter two derive from the Greek roots ment is synonymous with invagination of the germ rudiment ana (“up”) and kata (“down”), referring to the direction of into the yolk, as in Oncopeltus, preempting movement fully motion of the embryo as it passes in an arc over the posterior onto the dorsal surface. Superficial and immersion modes pole. “Blastokinesis” (Gr.: blastos, “bud, embryo”; kinesis, reflect fundamental differences in the relationship of anatrepsis “movement”) encompasses both events, though usually with to membrane formation (discussed in the following subsection). emphasis on the latter. Indeed, some authors have referred to Furthermore, the limited available evidence suggests that “katatrepsis” as “blastokinesis” (Butt, 1949; Cobben, 1968; these modes occur by distinct processes (discussed below in Dorn, 1976; Enslee and Riddiford, 1981; Johannsen and Butt, ‘Why does blastokinesis occur?’). Although superficial and 1941; Miller, 1939; Slifer, 1932; Truckenbrodt, 1979; Wood- immersed anatrepsis represent discrete categories, the actual land, 1957). In the older literature, katatrepsis is referred to as manifestation of anatrepsis in different species is impressively “revolution” (e.g., Kershaw, 1914; Knower, 1900; Melander, complicated. K.A. Panfilio / Developmental Biology 313 (2008) 471–491 477

Table 1 not attachment to the serosa is maintained. Often a thin film of Morphogenetic variations in insect extraembryonic development yolk may intervene between the serosa and internal tissue, or the Degree of blastokinesis tissues may be separate but apposed (Cobben, 1968; Johannsen • A Full blastokinesis: anatrepsis+katatrepsis ( /K) and Butt, 1941). Persistent attachment to the serosa has been • − Katatrepsis without anatrepsis ( /K) described within the Odonata, for some Orthoptera, and some • Non-blastokinetic (N) Hemiptera (Cobben, 1968, p.96, 308). Method of extraembryonic membrane formation A curious hybrid of immersed and superficial anatrepsis is • by extension/overgrowth from folds at the periphery of the embryonic seen in both suborders of the Orthoptera (Caelifera: Bentley et rudiment (black triangle, ▴) al., 1979; Ensifera: Heymons, 1895; Sarashina et al., 2005; • by extension/overgrowth of membrane tissue from free leading edges (white Vollmar, 1972; Wheeler, 1893). The germband is essentially triangle, △) • by production of a sac-like pocket via invagination (black circle, ●) superficial, but during later anatrepsis, the cephalic region of the developing germband does not follow the caudal region over the Germband positional type surface of the posterior pole in reaching the dorsal surface. • Immersed (“I” in katatreptic orders, “i” in non-katatreptic orders) Rather, this portion of the embryo “takes a short cut through the • “ ” “ ” Superficial ( S in katatreptic orders, s in non-katatreptic orders) yolk system” (Vollmar, 1972), such that it is temporarily Other movements known as “blastokinesis” immersed.

• Embryonic postural change from ventrally convex to concave (B1: see Box 1) There is variation in the extent to which full blastokinesis •‘ ’ Proto-blastokinesis involving a pro-amnion and a pro-serosa (B2: see Box 1) occurs. In nearly all hemimetabolous species, the germband • Lepidopteran blastokinesis (B3: see Box 2) stage embryo is positioned with its head remote from the Symbols refer to the notation used in Fig. 2. anterior pole of the egg, upside down and backward with respect to the egg's axes. However, in species where the germ rudiment Superficial anatrepsis and persistent superficial growth (Fig. is small and originates at or near the posterior pole, an inverted 2: “A/” and “S”) occurs in some Phasmida (stick insects; position is attained without any posterior–dorsalward move- Bedford, 1970). Superficial anatrepsis followed by sinking to an ment in an ascending arc, and therefore these species lack A − immersed position in the yolk (Fig. 2: “ /”, “I,” and black anatrepsis but have later katatrepsis (Fig. 2: “ /K”). This triangles—symbols described below and in Table 1) is seen in: condition is seen in species regardless of whether they are some Blattaria (cockroaches: Heymons and Heymons, 1905; superficial or immersed, and include: the Thysanura (firebrats: Lenoir-Rousseaux and Lender, 1970), the Grylloblattodea (rock Heymons and Heymons, 1905; Masumoto and Machida, 2004; crawlers: Uchifune and Machida, 2005), other Phasmida (cited Masumoto and Machida, 2006; Woodland, 1957), Ephemer- in Bedford, 1970), and some Orthoptera (crickets and grass- optera (mayflies: Tojo and Machida, 1997), Isoptera (termites: hoppers: Rakshpal, 1962). The orthopteran Gryllus assimilis Hu and Xu, 2005; Knower, 1900), Embiidina (web-spinners: has a particularly elaborate manifestation of superficial move- Kershaw, 1914; Melander, 1903), Plecoptera (stoneflies: ment: the germ rudiment is superficial and first posterior, then Kishimoto and Ando, 1985; Miller, 1939, 1940), and dorsal, then ventral before finally sinking into the yolk from the Dermaptera (earwigs: Bhatnagar and Singh, 1965; Heymons, ventral surface and ending up immersed near the dorsal side of 1895). Similar to development involving true anatrepsis, early the egg (Rakshpal, 1962). development in some of these taxa exhibits variation in Immersion anatrepsis (Fig. 2: “A/,”“I,” and black circles) is topographical details such as: a ventral site of invagination exhibited by species of the basal pterygote order Odonata (some Plecoptera), partial immersion in the yolk (some (dragonflies and damselflies: Ando, 1955; Seidel, 1929), and Thysanura, the Isoptera), persistent attachment to the serosa by nearly all of the Paraneoptera (bugs, thrips, lice: Butt, 1949; (some Plecoptera), and even persistently open amniotic cavities Cobben, 1968; Goss, 1952; Heming, 1979; Mellanby, 1935; (the Thysanura: references as above and Hughes et al., 2004). Miura et al., 2003; Oseto and Helms, 1972; Sander, 1959; Lastly, in the recently described–and still controversial–new Seeger, 1979; Seidel, 1924). The site of invagination into the order Mantophasmatodea (heel-walkers or gladiators: Cameron yolk is generally at or near the posterior pole (Fig. 4a), et al., 2006; Klass et al., 2002), the sole account of embryology although a few species exceptionally invaginate from the to date covers only later stages of embryogenesis (Machida et ventral surface (e.g., some Hemiptera: Cobben, 1968; al., 2004). In species of this order, embryos attain an immersed Psocodea [lice]: Seeger, 1979). The degree of immersion position and likely undergo katatrepsis, but it is an outstanding within the yolk following invagination varies, even within a question as to whether there is anatrepsis and what type it may ? single suborder (e.g., the heteropteran Hemiptera: Cobben, be (Fig. 2: “ /K”). 1968), with some species positioned deep within the yolk, Some insects lack anatrepsis and katatrepsis, or are non- while others are only covered by a thin film of yolk on either blastokinetic (Fig. 2: “N”). A few notable exceptions within the the ventral or presumptive dorsal (e.g., Oncopeltus: Fig. 3b) hemimetabolous insects that follow this pattern are: ovovivi- side of the embryo. Partial immersion in the yolk occurs in parous Blattaria (Bullière, 1969; Wheeler, 1889), Mantodea some Odonata, where the embryo is immersed “for only half (praying mantids, known only from: Hagan, 1917), and Cora- its length” (cited in Cobben, 1968, p. 310; and Jura, 1972, nus species of Hemiptera (Cobben, 1968, pp. 299–300). In p. 91). Aside from relative position within the yolk, degree of contrast, within the Holometabola, non-blastokinetic growth is immersion–after both types of anatrepsis–includes whether or predominant in all described orders (Anderson, 1972b): 478 K.A. Panfilio / Developmental Biology 313 (2008) 471–491

Helms, 1972; Seeger, 1979; Seidel, 1924). (However, invagina- tion does not predicate anatrepsis if there is no inversion of embryonic orientation, which is the case in: Ephemeroptera (Tojo and Machida, 1997), Plecoptera (Kishimoto and Ando, 1985; Miller, 1939, 1940), exceptional species of Coleoptera (Krysan, 1976) and Trichoptera (Miyakawa, 1974), and basal Lepidoptera (Ando and Tanaka, 1980; Kobayashi and Ando, 1981). In other species the amnion differentiates earlier: prior to or during movement in anatreptic species, and usually prior to germband elongation in non-blastokinetic species. In the differentiated blastoderm, the periphery of the germ rudiment is the presumptive amniotic tissue (Figs. 5a–a1). This peripheral tissue then roofs over the embryo proper in a characteristic fashion in many taxa (Fig. 5a2, Fig. 2: denoted by black Fig. 4. Blastokinesis involving immersion anatrepsis followed by katatrepsis, triangles; described in: Anderson, 1972a; Roth, 2004). illustrated by schematic cartoons of topographical changes of the embryo (grey), Amniotic tissue posterior to the embryo, and then also lateral amnion (orange), and serosa (blue), with mid-sagittal views at eight successive and anterior to each of the head lobes, arises as folds that stages: (a) invagination (=immersion anatrepsis), (b) extended germband stage, (c) retracted germband stage, (d) amnion–serosa fusion, (e) membrane rupture migrate medially until the tissue meets and fuses, creating an (=initiation of katatrepsis), (f) early katatrepsis, (g) mid katatrepsis, (h) late intact amniotic cavity overlying the embryo. As the amniotic katatrepsis (including final serosal contraction to form the dorsal organ). tissue migrates, it remains attached to the rest of the Orientation: egg-anterior is up and egg-dorsal is right. The positions of the head extraembryonic blastoderm, which gets dragged with it. This (h), thorax (t), and abdomen (ab) are labeled in image (b). In all images the outer tissue then fuses with itself medially and disengages from enlarged head region denotes the anterior end of the embryo. the amnion, thus creating the intact serosa. Variations on the folding pattern just described include the order of formation of Coleoptera (beetles: Beeman and Norris, 1977; Kobayashi et the folds and the number of folds that develop (e.g., Beeman al., 2002; Rempel and Church, 1969, 1971; Stanley and and Norris, 1977; Patten, 1884; Roonwal, 1936). The driving Grundmann, 1970; Storch and Krysan, 1980), Neuropterida force for fold outgrowth is unclear, and may differ between (dobsonflies, lacewings, ant lions: Bock, 1941; Du Bois, 1938; species, such as by serosal proliferation and extension over the Miyakawa, 1979; Strindberg, 1915), Hymenoptera (sawflies, germ rudiment (Thomas, 1936), or by the germ rudiment ants, bees, wasps: Bull, 1982; Fleig and Sander, 1988; Pultz et pushing below the presumptive extraembryonic tissue (Wood- al., 2005), basal Lepidoptera (some : Kobayashi, 1998; land, 1957). Outgrowth of folds is the predominant method of Kobayashi and Ando, 1981), Trichoptera (: Ander- membrane formation across the Insecta, including the Holome- son and Lawson-Kerr, 1977; Kobayashi and Ando, 1990; tabola, and occurs in: Thysanura (Hughes et al., 2004; Patten, 1884), and Diptera (true flies: Ajidagba et al., 1983; Masumoto and Machida, 2006; Woodland, 1957), Isoptera Idris, 1960; Raminani and Cupp, 1975, 1978; Schmidt-Ott, (Knower, 1900; Truckenbrodt, 1979), Blattaria (Bullière, 1969; 2000). The higher Lepidoptera (moths and butterflies: Anderson Lenoir-Rousseaux and Lender, 1970; Wheeler, 1889), Manto- and Wood, 1968; Okada, 1960; Reed and Day, 1966) are a dea (Hagan, 1917), Embiidina (Kershaw, 1914; Melander, notable exception with their own, aforementioned type of 1903), Dermaptera (Heymons, 1895), Grylloblattodea (Uchi- blastokinesis (Fig. 2: “B3”). In some Holometabola, limited fune and Machida, 2005), Phasmida (Bedford, 1970; Thomas, immersion in the yolk occurs, though without blastokinetic 1936), Orthoptera (Bentley et al., 1979; Dearden et al., 2000; movements (Fig. 2: “i” Anderson, 1972b, p. 202; Kobayashi et Rakshpal, 1962; Roonwal, 1936; Wheeler, 1893), Coleoptera al., 2002; Krysan, 1972, 1976; Miyakawa, 1974; Stanley and (Handel et al., 2000; Kobayashi et al., 2002; Rempel and Grundmann, 1970). Church, 1969; Stanley and Grundmann, 1970), Neuropterida (Bock, 1941; Du Bois, 1938; Miyakawa, 1979; Strindberg, Extraembryonic membrane formation and anatrepsis 1915), some lower Hymenoptera (Ivanova-Kasas, 1959), Trichoptera (Kobayashi and Ando, 1990; Patten, 1884), Species differ in the nature of extraembryonic membrane Siphonaptera (fleas: cited in Anderson, 1972a, p. 202; and formation and the extent to which it is related to anatrepsis. Miyakawa, 1975), Mecoptera (scorpionflies, cited from two If the germ rudiment invaginates into the yolk as a sac (Fig. unpublished sources in Miyakawa, 1975), and some lower 2: black circle, Figs. 3a, 4a), the act of invagination defines Diptera (Idris, 1960; Raminani and Cupp, 1975, 1978). extraembryonic membrane formation: sac formation separates Within the Holometabola, a third mechanism of membrane the germ rudiment from the serosa and delimits the amniotic formation is seen in some Lepidoptera (Anderson and Wood, cavity. Thus in species with immersion anatrepsis, anatrepsis 1968; Gross and Howland, 1940; Kobayashi, 1998; Nagy et al., causes membrane formation, as in the Odonata (Seidel, 1929) 1994; Okada, 1960) and some Hymenoptera (e.g., the honeybee; and Paraneoptera (Goss, 1952; Heming, 1979; Johannsen and Bull, 1982; Fleig and Sander, 1988; Lamer and Dorn, 2001; Butt, 1941; Mellanby, 1935; Miura et al., 2003; Oseto and Pultz et al., 2005; Shafiq, 1954). Here the intact serosa is formed K.A. Panfilio / Developmental Biology 313 (2008) 471–491 479

Fig. 5. Development of a non-blastokinetic species illustrated by schematic cartoons of topographical changes of the embryo (grey), amnion (orange), and serosa (blue), with mid-sagittal views at four successive stages: (a) membrane formation (=enveloping of the embryo), (b) extended germband stage, (c) retracted germband, amnion–serosa fusion and rupture, (d) late membrane contraction/dorsal closure (including final serosal contraction to form the dorsal organ). (a1) Ventral surface view of an embryo at the same stage as in panel a, (a2) transverse section, through the region denoted by flanking black bars in panel a1, illustrating membrane formation from lateral folds. (c1–3) Transverse sections through the thoracic region of an embryo at a comparable stage to panel c, at the position of flanking black bars, illustrating successive events: (c1) amnion–serosa fusion, (c2) initiation of membrane rupture at the ventral midline, (c3) mid stage of membrane contraction. Orientation: egg-anterior is up in ventral (a1) and mid-sagittal (a–d) representations and egg-dorsal is right in the latter; in transverse representations (a2, c1–3) egg- dorsal is up. The positions of the head (h), thorax (t), and abdomen (ab) are labeled in image (b), as is the first thoracic leg pair, t1, in panel c1. In images (a–d, a1) the enlarged head region denotes the anterior end of the embryo. before the germ rudiment differentiates into amnion and embryo. Cobben, 1968, p. 121). Within the confines of the egg such This uncoupling of membrane formation is achieved because of extension involves bending of the embryo. Thus many a break in continuity of the blastoderm tissue. The serosa and embryos–immersed or superficial–have characteristic flexures germ rudiment both acquire free leading edges (instead of being along their length. Often the caudal region is flexed such that the joined at folds or at the boundary of an invagination) that migrate posterior abdomen curls back toward the head of the embryo on over underlying tissue independently (Fig. 2: denoted by white its ventral side (Fig. 4b). Depending on the position of the head triangles). In the honeybee this even leads to serosal and region, embryos will form variously a J-shape (Seidel, 1929), a (vestigial) amnion formation by tissue migration in opposite C-shape (Cobben, 1968), or an S-shape (Seeger, 1979). Many directions—ventrally and dorsally, respectively. In the higher variations on these shapes occur, including ‘reverse’ shapes due Lepidoptera, a typical amnion forms from a single fold, but after to dorsal abdominal flexure (Fig. 5b). The degree of immersion the detached germ rudiment has sunk into the yolk (Kobayashi, in the yolk also differs between species at this stage. 1998). Some hymenopteran species show even greater diver- gence in membrane development, with very late serosal Variations on katatrepsis, including rotations membrane formation and no amnion (e.g., Bull, 1982; Shafiq, 1954). Holometabolous species with a reduced extraembryonic Katatrepsis generally occurs halfway through development membrane complement (‘Phylogeny’ section, above) accord- and is rapid, often comprising less than 1% of total develop- ingly lack (complete) amnion formation. mental time (Anderson, 1972a; Cobben, 1968). This phase of In summary, there are temporal and topographic differences blastokinesis reverses the inverted position of the embryo between extraembryonic membrane morphogenesis via invagi- resulting from anatrepsis (or from embryonic development from − nation, from marginal folds, or from free edges. However, the the posterior pole of the egg, Fig. 2: “ /K”). Immersed embryos invaginating and folding modes of amnion formation are similar exit through the original site of invagination, superficial in that the posterior region of the amniotic membrane is typi- embryos slide back down over the posterior pole, and some cally formed first. Indeed, the final covering of the head lobes orthopterans repeat their short cut through the yolk. Exception- by anterior amniotic folds can occur very late in development in ally, species that became immersed from a longitudinal position invaginated embryos (Butt, 1949; Seidel, 1929). take a new route and also exit the yolk at the posterior pole (Cobben, 1968; Rakshpal, 1962; Wheeler, 1893). Once Germband stage (intertrepsis) positional types repositioning of the embryo is sufficiently complete, growth of the embryonic flanks over the yolk closes the embryonic It is during the germband stage that the embryonic events body dorsally, and subsequent development (organogenesis) often studied by developmental geneticists occur, including proceeds. If the embryo is still small relative to the egg at this overt segmentation, early appendage formation, and early stage, such as in the Orthoptera, the correctly oriented embryo neurogenesis. As part of segment formation or patterning, the may still be remote from the anterior egg pole, in which case germband elongates. Some embryos even temporarily become dorsal closure also involves anteriorward growth of the body longer than twice the egg length (e.g., plataspid hemipterans: (e.g., Bentley et al., 1979). 480 K.A. Panfilio / Developmental Biology 313 (2008) 471–491

Various changes to the extraembryonic membranes are • In some Coleoptera and Lepidoptera, dorsal closure occurs associated with katatrepsis. Events in Oncopeltus are typical of within an intact serosa and amnion, with dramatic changes in many species: at the posterior pole the amnion and the serosa the latter. As in other species, at the germband stage the fuse over the embryo's head (Fig. 4d), and then the membranes amnion covers the ventral surface of the embryo, and is rupture (Fig. 4e); the serosa contracts, leaving the embryo and joined to the embryo at its lateral flanks. A second part of the everting amnion in its stead on the egg surface (Fig. 4f, g); the amnion then grows dorsally from the embryonic flank region serosa condenses into a small cap (dorsal organ) and degene- to create the provisional dorsal covering of the yolk below rates (Fig. 4h); the amnion serves as a temporary covering for the serosa. Definitive, embryonic dorsal closure ensues. The the yolk and is then replaced by the embryo during dorsal two parts to the amnion persist until hatching in this closure. In non-blastokinetic species, the amnion and the serosa configuration (cited in Anderson, 1972b; Beeman and still generally fuse with one another, rupture, and then contract Norris, 1977; Kobayashi, 1998). anteriorly/dorsally, though the site of initial membrane rupture is at the ventral midline of the egg and below the anterior/ The ultimate fate of the extraembryonic membranes differs thoracic region of the embryo (Fig. 5c, d; e.g., Bullière, 1969; between species. Usually the amnion and the serosa degenerate. Hagan, 1917; van der Zee et al., 2005; Wheeler, 1889). However, in some species either one or both of the membranes Subsequent dorsal closure is the one event in these proceedings persist and are merely shed at the time of hatching (Anderson, that occurs in Drosophila, and here the dynamics of molecular 1972b; Ivanova-Kasas, 1959; Shafiq, 1954; Wheeler, 1893). and mechanical interactions between the amnioserosa and the Exceptionally, irrespective of blastokinetic type (Box 2), some leading edge epidermal cells are largely understood (Edwards et lepidopteran prolarvae ingest amnion, serosa, and yolk prior to al., 1997; Harden, 2002; Hutson et al., 2003; Jacinto et al., 2000, hatching (Anderson and Wood, 1968; Kobayashi, 1998; Okada, 2002; Kiehart et al., 2000; Köppen et al., 2006; Laplante and 1960; Reed and Day, 1966), though species in the most basal Nilson, 2006; Reed et al., 2001; Stronach and Perrimon, 2001; lineage exhibit typical dorsal organ formation and subsequent Wada et al., 2007; Young et al., 1993). In contrast, which tissue membrane degradation (Kobayashi and Ando, 1981). drives katatrepsis has not been experimentally investigated and A final variation on katatrepsis concerns the orientation may differ between species (cf. Enslee and Riddiford, 1981; attained by the embryo at the completion of movements. In Slifer, 1932), offering a ready subject for biomechanical, Oncopeltus katatrepsis restores the orientation of the embryo to morphodynamic research across the insects. that of its original position at the germ rudiment stage and to that The roles of the amnion and the serosa can be uncoupled from of the egg. However only the anterior–posterior, but not the one another to varying extents during late extraembryonic dorsal–ventral, axis is restored in some taxa, due to longitudinal movements, particularly within the Holometabola. These rotation of the embryo. Rotations may occur at any stage during variations concern the occurrence of membrane rupture, the embryogenesis, and also in non-blastokinetic species: during degree of coordination of amnion and serosa, and how pro- anatrepsis (uniquely within the phasmids: Bedford, 1970, 1978; visional dorsal closure over the yolk is attained. For example: Moscona, 1950), throughout germband stages (Abbassy et al., 1995; Hagan, 1917; Rakshpal, 1962; Rosay, 1959), at • In the planthopper Siphanta acuta (Hemiptera), besides the katatrepsis, at later developmental stages (Bentley et al., amnion and serosa, there are two indusial envelopes 1979), or in some combination of these time points (for an (additional membrane covers peculiar to some species). extended review of rotation, see: Cobben, 1968, pp. 298–300 The inner of these participates with the amnion in membrane and 307–308). Rotation specifically around the time of rupture and contraction at katatrepsis, leaving the surround- katatrepsis may be the most common, and occurs in Odonata, ing serosa and outer indusial membrane intact until hatching Isoptera, some Orthoptera, Thysanoptera (thrips), and some (described in Johannsen and Butt, 1941). On the other hand, Hemiptera (Anderson, 1972a; Cobben, 1968; Heming, 1979; Hu a single indusial envelope may aid the serosa during and Xu, 2005; Sander, 1959; Truckenbrodt, 1979). A single 180° membrane contraction in the mantid Paratenodera sinensis, rotation of the embryo just prior to katatrepsis is typical. When and it subsequently forms a second dorsal organ (Hagan, rotation is not through a full 180°, there are sometimes two 1917). instances of rotation at different developmental stages such that • In apocritan Hymenoptera with an amniotic vestige, the sum total is still a 180° about-face. However, departures from amniotic tissue develops so as to cover the yolk rather than 180° rotation range from only 90° through “irregular prolarval the embryo from the beginning. Dorsal closure occurs within [late developmental stage] rotations … through several circles” the intact serosa, and the amnion is merely replaced without (Cobben, 1968, p. 300). When rotation is simultaneous with any attendant membrane rupture (Fleig and Sander, 1988). katatrepsis, it occurs as a “half-turn corkscrew roll,” and may be • Similarly, in the cyclorrhaphous Diptera (e.g., Drosophila), due to asymmetric fusion of the amnion to the contracting serosa the vestigial amnioserosa serves as a provisional dorsal cover (Cobben, 1968, p. 308), or to periodic, asymmetric contractions throughout its existence, and is also merely replaced during of the embryonic flanks (Truckenbrodt, 1979). dorsal closure (Campos-Ortega and Hartenstein, 1997). Overall, there are many variations on blastokinesis in the • In the (nearly) amnionless Hymenoptera, dorsal closure is hemimetabolous insects, and indeed on extraembryonic mem- effected without the amnion and within an intact serosa brane morphogenesis across the Insecta. However, modes of (Ivanova-Kasas, 1959; Shafiq, 1954). movement are generally conserved among related species. As K.A. Panfilio / Developmental Biology 313 (2008) 471–491 481 noted by Cobben (1968, pp. 310, 380), “within the Order or Anderson, 1972b). Even in the derived condition in Drosophila, Suborder the embryonic shape is almost constant … Family the reduced amnioserosa is required for proper germband groups are distinguished by different types of embryogenesis.” retraction, as evidenced from mutants affecting this tissue and Mapping blastokinetic and membrane formation traits onto a from mechanical studies (Frank and Rushlow, 1996; Hama- phylogeny of the Insecta reveals a great deal of variation within guchi et al., 2004; Irish and Gelbart, 1987; Lamka and Lipshitz, the lineage (Fig. 2), implying evolutionary plasticity. The 1999; Reim et al., 2003; Schöck and Perrimon, 2002; Wakimoto diversity of the details contrasts with the conservation of et al., 1984). Heming (2003) sees the membranes' role in proper blastokinesis as a general phenomenon that arose–probably only germband retraction as a manifestation of blastokinesis. once–in the insects and was subsequently lost multiple times (in However, this is not katatrepsis. Hemimetabolous embryos some Blattaria and some Hemiptera, in the Mantodea, and in the also undergo germband extension and retraction (Figs. 3b, c, lineage leading to the Holometabola). Any phylogenetic signal 4b, c, 5b, c), but retraction is unrelated to katatrepsis, as the that may be detected in these trends is certainly limited or noisy. two events are temporally distinct. Often germband retraction Nevertheless, the ‘proto’ events in the Archaeognatha (Box 1), occurs prior to katatrepsis (Butt, 1949; Hu and Xu, 2005; transitional features in the Thysanura (‘Phylogeny’ section, Mellanby, 1936; Uchifune and Machida, 2005), but it can also above), and then the appearance of full blastokinesis in the occur afterward (Miura et al., 2003). Perhaps even more Pterygota, are suggestive of a conserved evolutionary trajectory convincingly, within the holometabolous Coleoptera, some of elaboration and (predominantly) conserved retention of the species also exhibit germband retraction before non-blastoki- phenomenon. netic membrane rupture (Beeman and Norris, 1977; Rempel and Church, 1971). Thus, in most species germband retraction Relationship of the extraembryonic membranes to is not physically dependent on membrane topography. The blastokinesis, and growth of the embryo dependence of some holometabolous embryos on the extra- embryonic tissue for proper retraction represents a conse- The connection between extraembryonic membrane onto- quence of a novel topographical relationship, rather than a geny and blastokinesis has long been recognized: “The subtle version of katatrepsis. elimination of the envelopes is preceded by katatrepsis just as In sum, the Holometabola are, with the derived exception of their formation was preceded or accompanied by anatrepsis” some Lepidoptera (Box 2), non-blastokinetic, although they (Wheeler, 1893). This coordination may represent an evolutio- derive from insects that have blastokinesis. Confusion is narily conserved feature, given that it is manifest throughout the understandable given the frequent co-occurrence of membrane hemimetabolous Pterygota (excepting only the Mantodea, and embryo ontogenetic events and the lack of suitable terms to based on a sole account: Hagan, 1917). It is also such that the distinguish them. In particular, extraembryonic membrane two phenomena can be confused as defining one another. In rupture/contraction is the morphogenetic event that occurs accounts of holometabolan development, researchers have either at the initiation of katatrepsis or prior to non-blastokinetic discussed manifestations of “blastokinesis” in their non- dorsal closure (except in taxa with reduced extraembryonic blastokinetic species, when in fact they are variously referring membranes). However, as an event that flows seamlessly either to membrane formation or degeneration, germband longitudinal into katatrepsis or dorsal closure, it has been linguistically rotation, or germband extension and retraction (Abbassy et al., subsumed under either “katatrepsis” or “dorsal closure,” even 1995; Ivanova-Kasas, 1959; Rempel and Church, 1971; Stanley by researchers working within the same taxa (Rempel and and Grundmann, 1970). Church, 1971; van der Zee et al., 2005). Which term is used Germband extension has sometimes been analogized to, or reflects whether the researcher's background is in the mistaken for, anatrepsis. However, changes due to increased classical, comparative tradition or in the realm of Drosophila length are distinct from the anatreptic movement (cf. Heming, developmental genetics. Similarly, it is probable that some 2003; Ivanova-Kasas, 1959; Stanley and Grundmann, 1970). In insect endocrinologists refer to hemimetabolous katatrepsis full anatrepsis, the head moves posteriorly and dorsally until it (Kidokoro et al., 2006) or holometabolous late membrane resides at the posterior pole or even on the posterior dorsal development (Palma et al., 1993)as“blastokinesis” because surface. This is not the case in species that lengthen over the early work in the field was conducted on lepidopterans posterior pole of the egg without an associated shift of the (Riddiford and Williams, 1967). Although not catchy, head (like Drosophila and the Isoptera: Campos-Ortega and “membrane rupture/contraction” is certainly more precise if Hartenstein, 1997; Hagan, 1917; Knower, 1900), or even with katatrepsis or lepidopteran blastokinesis is not intended. an anterior shift over the anterior pole of the egg (Fig. 5b; So how do membranes and movements relate? Anatrepsis can such as the wasp Nasonia: Bull, 1982; and Tribolium beetles: contribute to differentiation of amnion, serosa, and embryo, but Stanley and Grundmann, 1970; van der Zee et al., 2005). membrane formation and anatrepsis can also be independent. A more complicated relationship of membranes and move- Immersion in the yolk may result directly from anatrepsis or by ments pertains to germband retraction in some holometabolous simple sinking. In later development, the occurrence and timing species. Here rupture of the extraembryonic membranes is of membrane rupture/contraction and dorsal closure can also coordinated with embryo retraction, and retraction also returns vary extensively between taxa, though the lack of blastokinesis the posterior region of the embryo to the ventral side (many in the Holometabola may contribute permissively to the extent of Coleoptera, also Neuropteroidea, Trichoptera, and Mecoptera: this variation. The only causal relationships are (i) if anatrepsis 482 K.A. Panfilio / Developmental Biology 313 (2008) 471–491

Box 1 Movements in basal Hexapoda and beyond

Non-insect hexapods and species of the earliest-branching insect lineage (see phylogeny in Fig. 2) undergo movements that reposition the embryo and involve extraembryonic tissue. These events are known as blastokinesis, though the entognathan event (“B1”) is analogous to insect blastokinesis while the archaeognathan event (“B2”) may represent an evolutionary precursor. In entognathan “B1” blastokinesis (Fig. 6a), the ventrally convex, superficial germband ducks into the yolk, resulting in a ventrally concave posture as the embryo doubles over on itself (Ikeda and Machida, 1998, 2001; Jura, 1967, 1972; Machida, 2006; Uemiya and Ando, 1987). The primary dorsal organ, an entognathan- specific structure distinct from the dorsal organ of hemimetabolous insects (Fig. 4h), is required for B1:ifitis ablated, the germband persists in the ventrally convex position and cannot hatch (Table 2; Jura, 1967). The role of the primary dorsal organ in effecting B1 is unclear, although it may alter the yolk such that the embryo can push into it (Jura, 1967). AB1-like postural change occurs in some holometabolous insects (Anderson and Lawson-Kerr, 1977; Kobayashi, 1998; Kobayashi and Ando, 1981, 1990; Kobayashi et al., 2002; Patten, 1884; Storch and Krysan, 1980), and even in some crustacean embryos (Browne et al., 2005). The authors of these studies variously referred to it as “revolution,”“a blastokinetic movement,” or simply as “ventral flexure.” This trait contains no phylogenetic signal and probably only represents initially convex growth over the yolk surface followed by later folding of the developed embryo within a restrictive egg space. Across the Holometabola there is no correlation of the timing of this folding with either extraembryonic membrane rupture/contraction or dorsal closure. In Archaeognatha, the early egg surface consists of the embryonic rudiment, a pro-amnion, and a pro-serosa; the latter two are distinguished by differing nuclear densities (Jura, 1972; Machida et al., 1994). Archaeognathan “B2” blastokinesis (Fig. 6b) involves a folding movement that tucks the early embryo into the yolk at a large crease in the egg surface (Heymons and Heymons, 1905; Jura, 1972; Larink, 1997; Machida, 1981; Machida et al., 1994). The tissue on the same wall of the crease as the embryo is the pro- amnion while the tissue on the opposing wall may be the pro-serosa (Heymons and Heymons, 1905) or more of the pro-amnion (Machida et al., 1994). B2 differs from membrane formation in other insects, as the pro- amniotic and pro-serosal regions are relatively static while shape changes result from yolk folds. Also, B2 does not create a discrete amniotic cavity, since the space within the crease is continuous with the external space. Interspecific differences in B2 concern the stage of embryonic development when it occurs, the number of yolk folds produced, and the extent to which the pro-serosa is involved. This variation is in marked contrast to the coordination of extraembryonic membrane formation with anatrepsis in other insects (‘Relationship of the extraembryonic membranes to blastokinesis’ section), and may represent an evolutionary stage before these events became so tightly coupled and precise in execution.

Fig. 6. Other movements known as blastokinesis, illustrated by schematic cartoons of topographical changes of the embryo (grey), amnion (orange), serosa (light blue), and primary dorsal organ (dark blue), for (a) “B1” in collembolans and (b) “B2” in archaeognathans, after Uemiya and Ando (1987) (and my unpublished observations) and Heymons and Heymons (1905), respectively. Images are in the lateral aspect with egg-anterior up and egg-dorsal right. The embryo's head is the enlarged region in dark grey. To convey the relative size and ventral side of older embryos, dark grey lines denote the three leg pairs and the antennae and light grey space-filling areas are used in some image panels. Black arrows indicate the direction of motion, including the reverse of ‘pro-anatrepsis’ in the final panel for B2. K.A. Panfilio / Developmental Biology 313 (2008) 471–491 483 occurs, katatrepsis must also occur (see the following two extraembryonic membranes’ section, above). Alternatively, sections), (ii) katatrepsis may occur without anatrepsis if the some authors have suggested that immersion (via anatrepsis) germband is inverted with respect to the egg anyway, and (iii) at may facilitate yolk “mobilization” by the germband stage the time of dorsal closure the embryonic body must be(come) embryo, perhaps by increasing the surface area of embryo in roughly one egg length. contact with the yolk (Heming, 2003; Miura et al., 2003). However, in both the superficial and immersed situations, the Why does blastokinesis occur? presumptive dorsal side of the embryo is in contact with the yolk and the amnion serves as an intervening cover on its Although anatrepsis and katatrepsis are usually classed as ventral side. Thus it is not apparent that immersion increases the morphogenetic movements, the general consensus–as true now surface area of embryonic tissue in direct contact with its as it was over 100 years ago–is that “nobody knows what these nutrient source, and these arguments do not account for movements are good for” (Sander, 1976). The Holometabola superficial anatrepsis. demonstrate that blastokinetic movements and even the extraembryonic membranes can become dispensable over How does it occur?: Insights from experimental data evolutionary time, and throughout the Insecta the extraem- bryonic tissue is a temporary attribute of the egg (but see the As is often the case, when the “why” questions are presently ‘Future directions and questions’ section). Nonetheless, given intractable, the “how” questions are a good way to proceed. how striking and taxonomically widespread blastokinesis or Happily for research on extraembryonic specification and membrane overgrowth+uncovering are, invariably questions of morphogenesis, steps have already been taken in this direction adaptive, functional, or mechanical significance arise. (Table 2). In the pre-developmental genetics era of experimental There are numerous speculations on possible functions of embryology, various means of poking and prodding the blastokinesis. These usually concern anatrepsis, as katatrepsis embryos identified some relevant experimental tools and is less problematic. There is a yin and yang aesthetic to uncovered possible components to extraembryonic morphogen- anatrepsis followed by katatrepsis, with a sense of balance esis. Often the experimental phenotypes generated by these implicit in the literature. What anatrepsis does, katatrepsis then manipulations were variable. In the last few years, the un-does. Katatrepsis has been described as “an active possibilities for selective, genetic manipulation by RNA restorative movement” (Anderson, 1972a), “when the more interference (and transgenesis) have been–and continue to mature germband retraces the route it took earlier” (Sander, be–extended to an increasing number of species representing 1976). Thus, insofar as the germband stage position resulting several orders, including the Orthoptera, Hemiptera, Coleop- from anatrepsis is untenable for future development, kata- tera, Hymenoptera, Lepidoptera, and Diptera (e.g., Amdam et trepsis can easily be explained. One consideration, already al., 2003; Brown et al., 1999; Bucher et al., 2002; Dong and mentioned, is that incorporation of yolk into the developing Friedrich, 2005; Huang et al., 2007; Hughes and Kaufman, gut requires a position external to it. More generally, the 2000; Konet et al., 2007; Liu and Kaufman, 2004; Lynch and germband stage embryo consists largely of external, ectoder- Desplan, 2006; Meyering-Vos et al., 2006; Mito et al., 2005; mal structures. A surface position then creates space into Miyawaki et al., 2004; Sanchez-Vargas et al., 2004). Phenotypic which organs and other internal structures can grow during the data from RNAi have already identified several genes relevant second half of embryogenesis. Anderson (1972a) also points to extraembryonic developmental processes in two species. out that in many species the ventral surface of the egg is These genetic data, coupled with awareness of other relevant convex, whereas the dorsal surface is concave, such that manipulative techniques and with candidate gene information coincidence of egg and embryo ventral surfaces “most from Drosophila studies, provide an ample foundation for economically” accommodates the elongation of the appen- future research. dages. Anterior–posterior orientation may also matter: the cuticular “egg burster” employed by some embryos during Early extraembryonic development hatching develops on the head, and in some species it is most effectively applied to a structurally weaker area of the chorion, At present, little is known about the molecules involved in which is usually at the anterior end of the egg (Cobben, 1968). extraembryonic membrane specification. Outside of extensive Thus katatrepsis may be seen as an “accommodatory move- studies on genes necessary for Drosophila amnioserosa ment” (Anderson, 1972a, p. 131). formation and differentiation (e.g., Hamaguchi et al., 2004; Why, then, does anatrepsis occur in the first place? Some Irish and Gelbart, 1987; Reim et al., 2003; Rusch and Levine, arguments for the occurrence of anatrepsis are based on 1997; Wakimoto et al., 1984), the only functional data to date physiological considerations. Uniquely, Wheeler (1893) sug- come from RNAi studies on the zen1 gene, which encodes a gested that blastokinesis comprises the movements of the homeodomain transcription factor, in the beetle Tribolium developing embryo away from localized regions of yolk castaneum. After knockdown of Tc-zen1, the presumptive pollution from metabolism (anatrepsis), and later aeration of serosal tissue becomes transformed to a more ventral/posterior the yolk bodies when churned up by the older, larger embryo fate as embryonic tissue (van der Zee et al., 2005). This is (katatrepsis). However, regulation of metabolic wastes is now similar to the phenotype obtained in Drosophila zen mutants attributed to the amniotic cavity (‘Proposed functions of the (Wakimoto et al., 1984). 484 K.A. Panfilio / Developmental Biology 313 (2008) 471–491

Box 2 Innovations in the Holometabola: Monster cells and more

Holometabolous insects are non-blastokinetic but exhibit an array of innovations in extraembryonic development. Membrane reduction and varied deployment during rupture/contraction are discussed in the main text (‘Proposed functions’ and ‘Variations on katatrepsis’ sections). A few additional intriguing examples are mentioned here. Apoditrysian Lepidoptera (higher moths, butterflies) have a unique movement known as blastokinesis, here designated B3 (Fig. 7; Anderson and Wood, 1968; Okada, 1960; Reed and Day, 1966; Riddiford and Williams, 1967). The immersed germband completes dorsal closure within the amnion, and has a ventrally convex flexure. The embryo then sucks the amniotic fluid into the body from the mouth, expanding the body's volume and producing a ventrally concave flexure. This postural change is reminiscent of that achieved in entognathan blastokinesis (B1, Box 1), but by an entirely different process. Similar to hemimetabolous katatrepsis, this type of blastokinesis is perturbed by treatment with ectopic juvenile hormone (Table 2; Erezyilmaz et al., 2004; Riddiford and Williams, 1967). Although typically the serosa degenerates or is simply shed at hatching, parasitoid Hymenoptera (wasps) have found a postembryonic use for serosal cells. The eggs and larvae of these species develop inside a host animal, an environment that poses certain challenges. After the embryonic stage, the serosa dissociates into individual cells–termed teratocytes (literally “monster cells”)–that circulate in the host's hemocoel (Danyk and Mackauer, 1996; Pedata et al., 2003; Pennacchio et al., 1994; Rouleux-Bonnin et al., 1999). Functions of the teratocytes may include sequestration of the host's: nutrients (aids parasitoid feeding/causes host attrition), hormones (altering host development in a manner favorable to the parasitoid), or immune factors (suppressing a response to the parasitoid) (Dahlman, 1990). Within the Diptera (flies), some species have both amnion and serosa, while the Cyclorrhapha, including Drosophila, have the single amnioserosa (Schmidt-Ott, 2000). Recent findings on extraembryonic membrane specification in the (non-cyclorrhaphan) mosquito Anopheles gambiae (Goltsev et al., 2007) imply that changes occurred in the developmental process itself, enabling such a reduction. In Anopheles, some genes are expressed in either the amnion or the adjacent serosa. The Drosophila orthologues of these genes are expressed uniformly throughout the amnioserosa. The authors suggest that the distinction of amnion and serosa became lost in the Cyclorrhapha when these genes became expressed in overlapping domains (Goltsev et al., 2007). In most insects, tissue territories become distinguished in the order [serosa, germ rudiment [amnion, embryo]] (Roth, 2004). The Anopheles data imply that this sequence has changed within the flies, with the specification sequence [embryo, extraembryonic [amnion, serosa]]. Restructuring of genetic regulation, such that the serosa and amnion derive from a common field of cells, would represent a profound change in the developmental process itself. If this is the case, the dipteran amnion may be unrelated to the amnion of most insects.

Data on the impetus for anatrepsis come primarily from implicate the yolk system (consisting of various types of yolk physical manipulation studies, and suggest that it may be, in granules as well as a cytoplasmic net and nuclei) in effecting part, a byproduct of various physical forces acting in the early anatrepsis. The germ rudiment is passively pulled into the yolk egg. A number of early studies (described in Heming, 2003; and at the posterior pole as a consequence of concentric, anteriorly in Sander, 1976), such as Sander's (1959, 1960, 1967) work on directed contractions of the yolk system, these contractions anatrepsis in the leafhopper Euscelis plebejus (Hemiptera), being associated with cleavage of the yolk in some species. The

Fig. 7. “B3” blastokinesis in higher Lepidoptera, illustrated by schematic cartoons of topographical changes of the embryo (grey), amnion (orange), and serosa (blue), after Anderson and Wood (1968). Images are in lateral aspect with egg-anterior up and egg-dorsal right. The embryo's head is the enlarged region in dark grey. To convey the relative size and ventral side of the embryo, dark grey lines denote the three leg pairs and the antennae and light grey space-filling areas are used. Black arrows indicate the direction of motion, including ingestion of egg contents by the embryo in the third panel (the portion of the amnion over the mouth has already been consumed in this image). K.A. Panfilio / Developmental Biology 313 (2008) 471–491 485

Table 2 Summary of functional perturbations of extraembryonic morphogenesis (in species other than Drosophila melanogaster), with manipulations listed in order of the developmental timing of the affected event Treatment Affected event Phenotype Order: Species References Affecting extraembryonic tissue formation Tc-zen1 RNAi Serosa differentiation Tissue transformation to embryonic fate: Coleoptera: Tribolium van der Zee et al., 2005 no serosa, temporarily enlarged head castaneum

Affecting early extraembryonic morphogenesis Encasement in glass Blastoderm differentiation; Failed blastoderm differentiation and Hemiptera: Gerris paludum Mori, 1985 (anoxia? pressure?) anatrepsis incomplete invagination insularis Ligation (constriction) Anatrepsis Incomplete invagination of germ rudiment; Hemiptera: Euscelis plebejus Sander, 1959, 1960, 1967 dissociation of material separated by ligature Of-dpp RNAi Anatrepsis/germ rudiment Failure of germ rudiment invagination or Hemiptera: Oncopeltus Angelini and Kaufman, differentiation morphological differentiation fasciatus 2005 Transverse cutting of the Anatrepsis Continued migration of the posterior portion Orthoptera: Acheta domesticus Vollmar, 1972 embryo only; anterior portion no longer moves

Affecting late extraembryonic morphogenesis Gene-targeted treatments: Tc-zen2 RNAi Membrane rupture/ Complete or partial eversion Coleoptera: Tribolium van der Zee et al., 2005 contraction castaneum Of-zen RNAi Katatrepsis Complete eversion Hemiptera: Oncopeltus Panfilio et al., 2006 fasciatus Of-hb RNAi (phenotypic Katatrepsis/dorsal closure Partial eversion, small body, Hemiptera: Oncopeltus Liu and Kaufman, 2004 class V) unincorporated yolk fasciatus Chemical and hormonal treatments: Actinomycin D Katatrepsis Complete or partial eversion; anterior– Isoptera: Odontotermes badius Truckenbrodt, 1979 (inhibition of posterior inversion, inability to hatch; transcription) death at an earlier developmental stage Various juvenile hormone Katatrepsis; dorsal Failed or prematurely arrested movements: Orthoptera: Acheta domesticus, Erezyilmaz et al., 2004; (JH) mimics closure; lepidopteran small body size, aberrant body shape, Locusta migratoria, Kidokoro et al., 2006;

blastokinesis (B3) open body walls and unincorporated yolk Schistocerca gregaria Novák, 1969; Riddiford Lepidoptera: Hyalophora and Williams, 1967 cecropia, Antheraea pernyi, Manduca sexta Other treatments: Ligation (constriction) Katatrepsis Complete or partial eversion Odonata: Calopteryx atrata, Ando, 1955; Mori, 1975; Cercion hieroglyphicum Sander, 1959, 1960 Hemiptera: Gerris paludum insularis, Euscelis plebejus Cauterization Katatrepsis; entognathan Complete or partial eversion; failure Hemiptera: Gerris paludum Mori, 1975; Jura, 1967

(heat ablation) blastokinesis (B1) of movement insularis Collembola: Tetrodontophora bielanensis Cold treatment Katatrepsis Anterior–posterior inversion: Phasmida: Bacillus libanicus Moscona, 1950 inability to hatch Note that a “complete eversion” phenotype also implies anterior–posterior inversion in katatreptic species. main site of activity has been described as an “anatrepsis external mass at the posterior pole of the egg. The cells have center,” and visible foci fitting this description have been seen some degree of embryonic identity, as in older eggs this tissue and/or experimentally demonstrated in hemipterans (reviewed acquires pigmentation typical of the embryo (Panfilio et al., in Heming and Huebner, 1994). Of course, this is an explanation 2006), but there is no apparent morphological differentiation. for the immersion type of anatrepsis only. However, the yolk The cells are also capable of initial morphogenetic movements, system is also thought to contribute to the dorsal shift occurring as posteriorward migration and condensation occur in a fashion in superficial anatrepsis, via peristaltic contractions, in con- similar to wild type, but the tissue does not then enter the yolk. junction with the crawling action of filopodia on the posterior of The serosa appears unaffected. The site of the Of-dppRNAi defect the germ rudiment (Vollmar, 1972). correlates with the site of Of-dpp expression at the posterior pole A recent contribution to the body of experimental data on (Angelini and Kaufman, 2005). Thus the TGF-beta/Dpp anatrepsis comes from maternal RNAi of the signaling molecule signaling pathway is implicated in this morphogenetic event, decapentaplegic (dpp) in the bug Oncopeltus (Angelini and although the exact role of dpp in invagination remains unknown. Kaufman, 2005). Depletion of Of-dpp in this manner results in a This role for Dpp signaling is distinct from its role in Drosophila failure of germ rudiment invagination (=immersion anatrepsis) in dorsal tissue specification, which includes specification of the or differentiation: cells of the germ rudiment form a round, amnioserosa (Irish and Gelbart, 1987; Rusch and Levine, 1997). 486 K.A. Panfilio / Developmental Biology 313 (2008) 471–491

Late extraembryonic development contraction–or of contextual factors–as an important focus for future research. Most functional data to date for extraembryonic develop- Partial eversion may result from several different defects. If ment pertain to late morphogenetic events, especially kata- amnion–serosa fusion is incomplete or if amniotic membrane trepsis or non-blastokinetic membrane rupture/contraction integrity is compromised, the amnion may tear during serosal (Table 2). As most of the manipulations employed in these contraction and leave the embryo partially covered by studies were open-ended regarding which developmental stage membrane. The position of tearing then corresponds with the would be affected, these results do not reflect a popular interest demarcation between uneverted and everted portions of the in katatrepsis or the non-blastokinetic equivalent a priori. embryo (Truckenbrodt, 1979). Partial eversion could also result Rather, the fact that multiple manipulations specifically perturb from inappropriate timing of dorsal closure with respect to this event suggests that it is a particularly sensitive stage. For katatrepsis, for example, arrest in the U-shaped, mid katatrepsis example, in one species, half of all spontaneously occurring position (Fig. 3d), leaving the posterior portion of the embryo in embryonic defects involve defective katatrepsis (Panfilio et al., the amniotic cavity to become everted (e.g., Novák, 1969). In 2006). There is also anecdotal evidence that environmental ligatured dragonfly eggs, interference with the normal pressures stress may impair katatrepsis (Ando, 1955). These observa- in the egg may have caused cessation of contraction during tions correlate with the fact that the katatrepsis or membrane katatrepsis (Ando, 1955). On the other hand, in Oncopeltus, rupture/contraction stage is a period of high activity and hunchbackRNAi-mediated partial eversion results from a mole- change within the egg, including de novo transcription cular cause and likely has a specific effect on different portions (Truckenbrodt, 1979) and synthesis of new classes of proteins of the egg and/or embryo (Liu and Kaufman, 2004). (Handley et al., 1998). Partial eversion due to arrest at the mid katatrepsis position The most commonly observed phenotype for perturbed occurs after orthopteran embryos are treated with juvenile katatrepsis or membrane rupture/contraction is eversion of the hormone (JH) mimics (Erezyilmaz et al., 2004; Kidokoro et al., embryo. That is, the embryo completes development in an 2006; Novák, 1969). However, this phenotype is just one of the inside-out fashion, with the organ tissue outside and the diverse array of defects that ectopic JH activity can produce, appendages inside of the body wall. Such a striking phenotype depending on the particular substance used, concentration, and results from a failure of extraembryonic membrane rupture/ timing of treatment. For example, in the cricket Acheta contraction, which leaves the embryo in its germband position domesticus, early JH treatment (egg age 0–5 days) can lead to (Fig. 1), surrounded ventrally by the amnion. At the time of arrest at mid katatrepsis (on day 7), but treatment during the body flank outgrowth for what ought to be dorsal closure, the 2 days prior to katatrepsis does not have an effect (Erezyilmaz et embryonic lateral flanks grow in a direction dictated by the al., 2004), suggesting that hormone levels indirectly affect inner surface of the amnion, such that the appendages are katatrepsis. Similarly, the effects were seen several days after JH enclosed ventrally. treatment in Locusta migratoria, where treatment suppressed Everted insect embryos have been produced experimentally the completion of katatrepsis while other developmental events since the 1950s, and recent RNAi data contribute to this body of proceeded (Kidokoro et al., 2006). One of the JH mimics up- work. Various treatments have induced eversion in species regulated MAPK/ERK signaling (Kidokoro et al., 2006), representing several insect orders: by ligation in dragonflies although it is unclear whether this signaling pathway is relevant (Odonata); by actinomycin D inhibition of transcription in for katatrepsis or other events. In general, hormone levels termites (Isoptera); by treatment with ectopic juvenile hormone represent an additional factor that affects extraembryonic mimics in locusts (Orthoptera); by ligation, zenRNAi,or morphogenetic movements, though hormonal changes are hunchbackRNAi in bugs (Hemiptera); and by zen2RNAi in the unlikely to be involved on the short-term time scale in the red flour beetle (Coleoptera) (Ando, 1955; Erezyilmaz et al., initiation of events. 2004; Kidokoro et al., 2006; Mori, 1975; Novák, 1969; Panfilio Overall, successful membrane rupture and subsequent et al., 2006; Sander, 1959, 1960; Truckenbrodt, 1979; van der repositioning of membranes and embryo are crucial for normal Zee et al., 2005). In sum, mechanical manipulation of the egg, development, and these developmental events are sensitive to inhibition of transcription (of all genes), inhibition of translation perturbation. It has been recognized for some time that, “study of (of targeted genes), or inappropriate hormone levels can lead to everted embryos might produce very useful information about eversion. Thus although dramatic, the phenotype of eversion is the mechanism of katatrepsis, one of the most characteristic not uncommon. features of insect embryogenesis” (Mori, 1975). Induced Eversion can be complete or partial. Complete eversion may eversion has even been employed as a means of studying the be due to a failure of initiation of membrane contraction/rupture development of usually internal anatomical structures (Mori, events (Panfilio et al., 2006; van der Zee et al., 2005). 1977). In practical application, widespread susceptibility to Alternatively, complete eversion may result from a delay that eversion makes extraembryonic membrane rupture/contraction misses the correct developmental time window, resulting in late an attractive target for insect pest control via specific, molecular serosal contraction that leaves the amnion and embryo behind strategies (Wimmer, 2005). Conservation of zenRNAi-induced (Ando, 1955; Truckenbrodt, 1979). In either situation, the eversion across representatives of the Hemiptera and Coleop- proximate cause of membrane rupture has yet to be determined. tera–species-rich orders containing many agricultural and some The latter situation highlights the timing of membrane rupture/ pathogenic pests–immediately suggests one possible target. K.A. Panfilio / Developmental Biology 313 (2008) 471–491 487

RNAi of specific genes–which causes consistent developmental and for what purpose (cytoskeletal regulation and cell shape failure at a particular step–offers the least complicated approach changes, changes in cell polarity)? More generally, what is the for future studies, as the technique produces one or only a few trigger for membrane rupture? As rupture is a rapid process that phenotypes and avoids possible confounding factors for egg occurs within minutes (Cobben, 1968, p. 33), perhaps it is pre- health that physical manipulations cause. The toolkit will expand cipitated by a physiological signal such as intracellular calcium as additional genes are characterized, building a molecular release, which is involved in vertebrate morphogenesis (Slusarski understanding of the basis of these morphogenetic events. and Pelegri, 2007). Equally, the proximate triggers for membrane outgrowth as folds, invagination for immersion anatrepsis, or Future directions and questions migration for superficial anatrepsis are largely unknown. Insect extraembryonic morphogenesis provides subject Insect extraembryonic development is a wide-open field that matter for research on diverse epithelial morphogenetic is tractable for future research. Presently, we have individual processes: folding, invagination, dissociation to create free data points for physical, molecular, and endocrine factors edges, fusion, rupture, contraction, and reorganization during involved in some processes, but linking these points into a degeneration. As cells are constrained by their positions within larger framework is still to come. There are also some the epithelium and have defined cell neighbors, the diversity of outstanding questions from twentieth century work, as well as movements achieved by the amnion and the serosa are all the new considerations in light of recent studies. more impressive. As many morphogenetic events involving the As enigmatic as ever are the developmental origin and final membranes occur on the egg surface and within a few hours, fate of the amnion. Which cells on the surface of the blastoderm they are accessible and ideal for live imaging, a technique that is contribute to the amnion? The location and number of domains already regularly used in Drosophila dorsal closure studies. comprising the germ rudiment differ between species, and remain Fundamental aspects of cell shape changes, establishing polarity unclear in others (e.g., Butt, 1949; Mellanby, 1935; Sarashina et for directed movements, and intercellular communication at al., 2005; Seidel, 1924), and this has implications for where tissue boundaries have yet to be explored. Parameters of a presumptive amniotic cells are located. Alternatively, in some mechanical or physical nature are virtually unknown and await species, the amnion may not be prefigured in the blastoderm but characterization for these movements. The identification of rather arise de novo during invagination or fold formation some transcription factors and extracellular signaling molecules (Machida et al., 1994; Tojo and Machida, 1997; Woodland, 1957). necessary for these morphogenetic events provides a promising These hypotheses are based on classical observation and starting point. histology. There is a substantial need for the definition of molecular markers for the amnion and, more generally, for fate Acknowledgments mapping and lineage tracing of early stages in diverse insects. It is not merely a polite euphemism to say that the amnion is I would like to thank the Zoology Balfour and Central “replaced” by the embryonic flanks during dorsal closure (e.g., Science Libraries of the University of Cambridge for maintain- ‘Variations on katatrepsis’ section). In fact, there are no data to ing excellent entomological holdings and assistance with provide a more explicit account of the tissue's fate. During searching them; the several Japanese researchers who kindly dorsal closure, does it contract toward the midline to aid closure made their work available to me; the Journal of Morphology for (Dorn, 1976; Woodland, 1957) like the Drosophila amnioserosa making their entire back archive beautifully and freely (Kiehart et al., 2000), migrate anteriorly to join the serosa in the available; Franz Kainz, Martin Jaekel, and Friedemann Linsler dorsal organ (Kershaw, 1914; Patten, 1884), remain in situ? for assistance with translation of German texts; Michael Akam, Subsequently, where does the amnion go—degenerate into the Bárbara Negre, and two anonymous reviewers for constructive yolk (Machida et al., 1994) or contribute to the embryonic comments on the manuscript; Gary Wessel in his capacity as epidermis (Truckenbrodt, 1979; Woodland, 1957)? The latter reviews editor; and those who encouraged the production of this question especially has troubled researchers throughout the past review. This work was prepared during support from a Howard century (e.g., Jura, 1972, p. 90). Again, suggested possibilities Hughes Medical Institute Predoctoral Fellowship. are based on inspection of fixed specimens. In Drosophila it is only recently that fluorescent live imaging analyses conclusively References showed that the amnioserosa degenerates after dorsal closure (Reed et al., 2004; contra Technau, 1987). Abbassy, M.M., Helmy, N., Osman, M., Cope, S.E., Presley, S.M., 1995. Between blastokinetic events, the posited functions of the Embryogenesis of the sand fly Phlebotomus papatasi (Diptera: Psychodi- dae): organogenesis including segmentation, blastokinesis, mouthparts, and membranes when they are static and cover the developing alimentary canal. Ann. Entomol. Soc. 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