Early development of the anterior body region of the grey widow spider Latrodectus geometricus Koch, 1841 (Theridiidae, Araneae)
Introduction
Crown-group chelicerates (=Euchelicerata, following the system proposed by Chen et al., 2004) have a specific body tagmosis not found in other euarthropods (trilobites, crustaceans, myriapods and insects): the anterior region, prosoma, comprises seven segments, and the posterior region, opisthosoma, 13 segments. The prosoma encompasses the ocular segment, and the segments carrying chelicerae, pedipalps and the other four pairs of limbs. Like the head of other arthropods, the prosoma is a character-rich region for reconstructing relationships, in this case amongst chelicerates (Anderson, 1973, p. 442). Early embryos show striking similarities between the prosoma of chelicerates and the head of other arthropods (Anderson, 1973). This provides an opportunity to compare the developing morphology and topology of structures of the anterior region of the embryos across arthropods. These embryological data can contribute to our understanding of arthropod phylogeny.
Among the crown-group chelicerates, embryos of spiders have played an important role in recent studies about arthropod evolution. For example, numerous molecular studies on the embryos of Cupiennius salei Keyserling, 1877 (Ctenidae, Entelegynae) make this animal a well-established model species (Stollewerk et al., 2001, Damen, 2002, Schoppmeier and Damen, 2005, Janssen et al., 2008, Stollewerk and Seyfarth, 2008, McGregor et al., 2008). Historically, basic studies on the embryonic development of spiders, focusing on morphogenesis, have been carried out since the 19th century (e.g. Herold, 1824, Claparède, 1862). This early research remained of interest until well into the second half of the 20th century (see Anderson, 1973). Surprisingly, subsequent to the review of Anderson (1973), interest in this issue declined significantly with the exception of a brief paper by Marechal (1994) that paid special attention to the visual system of a mygalomorph spider, Ischnothele guyanensis (Walckenaer, 1837).
Existing knowledge about spider embryonic development can be briefly summarised as follows. Once cleavage has finished, the yolk-rich spider eggs enter a blastula stage, at which most of the blastoderm cells begin to converge at one side of the egg to form the germ disc (Holm, 1952, Holm, 1954, Rempel, 1957, Suzuki and Kondo, 1995). The centre of the germ disc then has a bulged appearance due to the development of the caudal cumulus underneath the germ cells (Holm, 1952, Holm, 1954, Rempel, 1957, Suzuki and Kondo, 1995, Akiyama-Oda and Oda, 2003). The caudal cumulus later on migrates to the periphery of the egg and its migrating route finally splits the germ disc (Akiyama-Oda and Oda, 2003). The two separated parts of the germ disc migrate away from each other until the whole germinal area is band-like in shape (Holm, 1952, Holm, 1954, Rempel, 1957, Suzuki and Kondo, 1995, Akiyama-Oda and Oda, 2003). Thereafter, the germinal area is called germ band. The germ band elongates itself around the egg and stops elongating when its anterior and posterior ends almost touch (Holm, 1952, Rempel, 1957, Chaw et al., 2007, McGregor et al., 2008). In some species, the distance between the two ends is not that short, because the second half of the opisthosoma does not attach to the egg surface but folds anteriorly (e.g. Holm, 1940, Yoshikura, 1955). At this time in development, a process called ‘inversion’ (or reversion) begins. This process occurs in most spiders except those of the Mesothelae and certain species from the Orthognatha (Foelix, 1996, p. 216). The inversion in spider embryology means that the germ band, which is initially situated on one side of an egg, is separated into two halves longitudinally by a furrow appearing in the midline of the germ band. The furrow was termed a ‘ventral sulcus’ by various embryologists (see Anderson, 1973). The two halves of the germ band are then pushed away from each other by the widening of the ventral sulcus, and they finally reach a position on the lateral side of the egg (Holm, 1952, Holm, 1954, Rempel, 1957, Yoshikura, 1954, Yoshikura, 1955, Yoshikura, 1958, Yoshikura, 1961, Yoshikura, 1972, Suzuki and Kondo, 1995). Thereafter, a thin epidermal layer starts to grow on the ‘dorsal’ side of the egg to connect the two halves of the germ band. This process is called ‘dorsal closure’, at the end of which the body form of the hatchling, resp. the adult spider emerges (Holm, 1940, Holm, 1952, Holm, 1954, Rempel, 1957, Yoshikura, 1954, Yoshikura, 1955, Yoshikura, 1958, Yoshikura, 1961, Yoshikura, 1972).
In order to understand the development of the prosoma of chelicerates, and to compare it with the head formation of other arthropods, we employed scanning electron microscopy to investigate embryos of the grey widow spider Latrodectus geometricus Koch, 1841 (Theridiidae, Araneae) at an ultrastructural level. Several details found herein are first documented for spider embryos: (1) a ventro-median bridge connecting the pre-cheliceral lobes and its development; (2) three pores being arranged like the mathematical ‘because’ sign (∵) in the prospective mouth region; and (3) the prosomal shield is developed from the fusion of the anterior margin of the pre-cheliceral lobes and the tergal portions of the four posterior-most prosomal segments. We discuss our data in the light of earlier investigations on the embryogenesis within the Chelicerata. Common features found in early embryos of various chelicerates are further discussed. Such discussion provides preliminary information for mapping the embryonic features into ground pattern conditions, as what has been briefly carried out by Anderson (1973) and Yoshikura (1975).
Section snippets
Materials and methods
Living material of Latrodectus geometricus was kindly provided by Martin Thierer-Lutz from the born to be eaten Insektenzucht GmbH, Schnürpflingen, Germany. The selection of this species is mainly based on three reasons: (1) easy lab culture of the adults; (2) the large amount of eggs produced by the females all through the year; and (3) the embryonic development of this species has never been described before. Eggs were removed from the cocoons and fixed with Carnoy's fixative (100% alcohol:
Results
The current work mainly presents investigations on the post-germ disc development of the anterior region of the widow spider embryos (Figs. 2A and Fig. 3, Fig. 4, Fig. 5; see the supplementary data for brief observations on the germ disc phase). The dorsal side of the embryos at selected steps is presented in order to document the formation of the prosomal shield (Fig. 5). Two diagrams are provided to explain the details (Fig. 6, Fig. 7). In total, 16 embryonic steps are recognised with
Pre-cheliceral lobes
In embryos of L. geometricus, each of the pre-cheliceral lobes can be recognised as two areas: (1) a marginal region that later on becomes the anterior part of the prosomal shield; and (2) a central area that is subdivided into two portions that later fuse and separate from the marginal region by three furrows. The central area of each pre-cheliceral lobe finally gets internalised. Similar findings have been reported and discussed by several previous authors. Pross (1966) recognised two pairs
Conclusions and outlook
The detailed investigation on the embryonic development of Latrodectus geometricus enables a comparison between our data and those from existing literature. We are now able to characterise several features found in the embryos of various chelicerates and to further achieve new understanding of the phylogenetic status of those features. New understanding are: (1) in the pre-cheliceral lobes, the two subdivisions and their later internalisation, as well as the associated furrows are currently
Acknowledgements
We are grateful to Martin Thierer-Lutz, Schnürpflingen and his colleagues from born to be eaten for providing us all living material used herein. Professor Ryuichiro Machida, Sugadaira, Japan and his students, and Professor Roger Farley, Riverside, USA are thanked for sharing their experience of preparing arthropod embryos for SEM observations to one of the authors (YL). Joachim T. Haug, Ulm, Viktoria Linne, Mainz, and Angelika Stollewerk, London, provided valuable, still unpublished
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2017, Arthropod Structure and DevelopmentCitation Excerpt :Although the structural identity of the labrum has also been historically problematic (reviewed in Haas et al., 2001; Scholtz and Edgecombe, 2006; Bitsch and Bitsch, 2010), its bilobed nature and the activity of various limb-pattering genes (e.g. wingless, decapentaplegic, Distal-less, dachshund, extradenticle, reversed polarity) argue in favour of its origin as a fused pair of appendages (Popadic et al., 1998; Boyan et al., 2002; Browne et al., 2005; Kimm and Prpic, 2006; Posnien et al., 2009, 2010, 2011; Treffkorn and Mayer, 2013). In the adult form, the labrum is usually expressed as a flap-like structure (labrum/clypeolabrum in Mandibulata) (see Møller et al., 2003, 2004; Posnien et al., 2009, 2011; Wolff, 2009; Bitsch and Bitsch, 2010; Liu et al., 2010) or it becomes reduced and practically inconspicuous as a component of the mouth opening (upper-lip or “rostrum” in Euchelicerata) (see Farley, 2001, 2005; Liu et al., 2009; Wolff and Hilbrant, 2011; Mittmann and Wolff, 2012). Intriguingly, the labrum appears to be absent in Pycnogonida (Machner and Scholtz, 2010), although it is possible that it has become secondarily fused with the large anterior proboscis that characterizes this bizarre group (see Scholtz and Edgecombe, 2006; Edgecombe, 2010).
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