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TEM micrograph of a young follicle of a primary reproductive. A monolayer of symbiotic bacteria (arrows) is observable in the follicular cell-oocyte interface. bm, base- ment membrane; fc, follicular cell; o, oocyte. Bar ϭ 2, 5 m.
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Intracellular symbiotic bacteria in specialized cells (bacteriocytes) of the fat body are found in all cockroaches and in the termite Mastotermes darwiniensis Froggatt. DNA sequence analysis of the bacteria in the two taxa shows them to be phylogenetically related; thus, it has been suggested that the bacteriocyte symbiosis was established in an an...
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... 13 December 1996. This is relatively late in the ßight season of the species, and the terminal oocytes of these females were well developed. We assumed that these primary reproductives were unmated, because copula- tion in termites generally does not occur until after males and females pair and begin nest construction (Nutting 1969). Neotenic reproductives were taken from an es- tablished laboratory colony held at the Division of Entomology, Commonwealth ScientiÞc and Industrial Research Organization, in Canberra, Australia. Trans- mission electron microscopy (TEM) observations were carried out in specimens Þxed for 4 h in 2.5% glutaral- dehyde solution in 0.1 M cacodylate buffer (pH 7.2), postÞxed for 2 h in 1% OsO 4 in the same buffer, dehy- drated in ethanol, and embedded in Epon 812. Thin sections were stained with uranyl acetate and lead citrate and examined with a Zeiss EM 900 electron microscope. Scanning electron microscopic (SEM) observations were performed on specimens Þxed for 12 h in glutar- aldehyde, as described above, washed in cacodylate buffer, dehydrated in ethanol, and arranged on cover- slips previously coated with a 1% aqueous solution of poly-L-lysine. The specimens were processed by the critical point drying method in a Bomar SPC-900 Ex apparatus and examined with a Philips KL20. Primary Reproductives. The ovaries of primary re- productives are composed of a series of ovarioles, each individually enveloped by a thick sheath of tracheae (Fig. 1A). Transverse sections of the apical region of the ovarioles show, at the ultrastructural level, oogonia enveloped in a basement membrane and surrounded by tracheae and fat body cells: no bacteria are ob- served at this level of the ovarioles (Fig. 1 A and B). Bacteria appear in the region of the ovarioles contain- ing growing oocytes, which are arranged in a linear pattern (Fig. 2). A monolayer of bacteria is observable in the follicle cell-oocyte interface (Fig. 3). In transverse section, this region of the ovariole is surrounded by the fat body containing bacteriocytes (Fig. 4). The above observations suggest that the bacteria leave the intrao- varic bacteriocyte, cross the ovariole sheath and later the follicular epithelium. Indeed, some bacteria are present in the cytoplasm of the follicle cell and in the narrow intracellular space of the follicular epithelium (Fig. 5). In the ovariole region containing previtellogenic eggs, the symbiont population of the follicle increases and the bacteria appear enmeshed in a microvillar net (Fig. 6). In the vitellogenic egg, conspicuous caps of bacteria are observable at the poles (Fig. 7A). In this phase of oogenesis the microvillar border disappears and the bacteria are located in a wide intercellular space between follicle cells and the vitellogenic egg (Fig. 7B). The symbionts then adhere to the egg sur- face, and pseudopod-like formations arise from the oolemma and envelope the symbionts (Fig. 8). As a consequence of this endocytic process, the ...
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... The earliest-diverging lineage among modern termites is the once cosmopolitan family Mastotermitidae, which includes a single extant species, the Australian Mastotermes darwiniensis [77]. Mastotermes darwiniensis displays several roach-like features, such as eggs laid in an ootheca-like structure [78] or the association with the intracellular endosymbiont Blattabacterium [79]. It also displays a bifurcated developmental pathway with a true worker caste [80], a partially subterranean lifestyle [30,81], and is the only termite species known to explore its environment individually or in tandems instead of following trails with a large number of foragers [82]. ...
Termites are a clade of eusocial wood-feeding roaches with > 3000 described species. Eusociality emerged ~ 150 million years ago in the ancestor of modern termites, which, since then, have acquired and sometimes lost a series of adaptive traits defining of their evolution. Termites primarily feed on wood, and digest cellulose in association with their obligatory nutritional mutualistic gut microbes. Recent advances in our understanding of termite phylogenetic relationships have served to provide a tentative timeline for the emergence of innovative traits and their consequences on the ecological success of termites. While all “lower” termites rely on cellulolytic protists to digest wood, “higher” termites (Termitidae), which comprise ~ 70% of termite species, do not rely on protists for digestion. The loss of protists in Termitidae was a critical evolutionary step that fostered the emergence of novel traits, resulting in a diversification of morphology, diets, and niches to an extent unattained by “lower” termites. However, the mechanisms that led to the initial loss of protists and the succession of events that took place in the termite gut remain speculative. In this review, we provide an overview of the key innovative traits acquired by termites during their evolution, which ultimately set the stage for the emergence of “higher” termites. We then discuss two hypotheses concerning the loss of protists in Termitidae, either through an externalization of the digestion or a dietary transition. Finally, we argue that many aspects of termite evolution remain speculative, as most termite biological diversity and evolutionary trajectories have yet to be explored.
... There are many histological descriptions of the symbiotic bacteria and the bacteriocytes, ranging from classic hand-drawn sketches to more recent light and electron microscopic observations (Blochmann, 1887;Wheeler, 1889;Gier, 1936;Koch, 1949;Bush and Chapman, 1961;Walker, 1965;Milburn, 1966;Cochran et al., 1979;Sacchi et al., 1993Sacchi et al., , 1996Sacchi et al., , 1998aSacchi et al., , b, 2000Laudani et al., 1995;Lambiase et al., 1997;Park et al., 2013). The vertical transmission processes of the symbiotic bacteria and formation processes of the bacteriocytes were histologically described in detail, particularly focusing on the processes during embryogenesis (Gier, 1936;Koch, 1949;Sacchi et al., 1996Sacchi et al., , 2000Lambiase et al., 1997). Many researches attempted to cultivate the symbiotic bacteria in vitro, but, despite an array of erroneous reports of success (e.g., Mercier, 1907;Gropengiesser, 1925;Glaser, 1930;Hoover, 1945;Pierre, 1964), the attempts finally turned out to be in vain (Gier, 1947;Brooks and Richards, 1966). ...
Having been reported in 1898 for the first time from Japanese waters, the lineid heteronemertean Lineus longifissus auct. is known to inhabit tidal flats under the influence of the warm Kuroshio Current along the coasts of Honshu and southwestward, characteristically with a uniformly raisin-colored to black body lacking a caudal cirrus. The taxonomic identity of the Japanese L. longifissus auct. has been questioned by specialists because of some obvious morphological differences between Lineus longifissus (Hubrecht, 1887) s.str. (now in Heteronemertes Chernyshev, 1995), originally described from the subantarctic region. In the present study, we describe the Japanese L. longifissus auct. as Corsoua takakurai sp. nov. Before the present study, the genus Corsoua Corrêa, 1963 had been monotypic with the type species Corsoua kristenseni Corrêa, 1963 from the Caribbean. We infer the phylogenetic position of Corsoua takakurai within Lineidae based on the mitochondrial 16S rRNA and cytochrome c oxidase subunit I, and the nuclear 18S rRNA, 28S rRNA, and histone H3 genes.
... There are many histological descriptions of the symbiotic bacteria and the bacteriocytes, ranging from classic hand-drawn sketches to more recent light and electron microscopic observations (Blochmann, 1887;Wheeler, 1889;Gier, 1936;Koch, 1949;Bush and Chapman, 1961;Walker, 1965;Milburn, 1966;Cochran et al., 1979;Sacchi et al., 1993Sacchi et al., , 1996Sacchi et al., , 1998aSacchi et al., , b, 2000Laudani et al., 1995;Lambiase et al., 1997;Park et al., 2013). The vertical transmission processes of the symbiotic bacteria and formation processes of the bacteriocytes were histologically described in detail, particularly focusing on the processes during embryogenesis (Gier, 1936;Koch, 1949;Sacchi et al., 1996Sacchi et al., , 2000Lambiase et al., 1997). Many researches attempted to cultivate the symbiotic bacteria in vitro, but, despite an array of erroneous reports of success (e.g., Mercier, 1907;Gropengiesser, 1925;Glaser, 1930;Hoover, 1945;Pierre, 1964), the attempts finally turned out to be in vain (Gier, 1947;Brooks and Richards, 1966). ...
Cockroaches are commonly found in human residences and notorious as hygienic and nuisance pests. Notably, however, no more than 30 cockroach species are regarded as pests, while the majority of 4,500 cockroaches in the world are living in forest environments with little relevance to human life. Why some cockroaches have exceptionally adapted to anthropic environments and established pest status is of interest. Here we investigated the German cockroach Blattella germanica, which is a cosmopolitan pest species, and the forest cockroach Blattella nipponica, which is a wild species closely related to B. germanica. In contrast to easy rearing of B. germanica, laboratory rearing of B. nipponica was challenging—several trials enabled us to keep the insects for up to three months. We particularly focused on the distribution patterns of specialized cells, bacteriocytes, for harboring endosymbiotic Blattabacterium, which has been suggested to contribute to host's nitrogen metabolism and recycling, during the postembryonic development of the insects. The bacteriocytes were consistently localized to visceral fat bodies filling the abdominal body cavity, where a number of single bacteriocytes were scattered among the adipocytes, throughout the developmental stages in both females and males. The distribution patterns of the bacteriocytes were quite similar between B. germanica and B. nipponica, and also among other diverse cockroach species, plausibly reflecting the highly conserved cockroach-Blattabacterium symbiotic association over evolutionary time. Our study lays a foundation to experimentally investigate the origin and the processes of urban pest evolution, on account of possible involvement of microbial associates.
... There is general agreement that Mastotermes represents a good example of primitive relict anatomy (McKittrick 1965;Emerson 1965;Nalepa and Bandi 2000). Mastotermes shares many primitive features with cockroaches such as endosymbiotic flavobacteria in the fat body, packaging of eggs in an oothecal mass, well-developed anal lobe in the hind wing, and similarities in the structure of reproductive organs (McKittrick 1965;Baccetti 1987;Watson and Gay 1991;Nalepa and Lenz 2000;Sacchi et al. 2000). Historically, Mastotermitidae has been considered as a sister family to all other termites (Engel et al. 2009;Engel and Delclòs 2010). ...
The first representative of the genus Mastotermes Froggatt, 1897 from the Cenozoic of the South America is described here based on seven specimens from the Fonseca Formation, Eocene-Oligocene boundary, Minas Gerais State, southeastern Brazil. Today, Mastotermes is geographically restricted to northern Australia, with only one relict species, Mastotermes darwiniensis Froggatt, 1897. However, its fossil record clearly shows a global distribution, with species ranging from the Cretaceous of Myanmar, Russia, Mongolia and China, throughout Cenozoic of mainland Europe and Miocene of Africa, Mesoamerica and the Caribbean. Along with Spagotermes costalimai Emerson, 1965, Mastotermes brasiliensis sp. n. is the second fossil termite recorded in the Fonseca strata. This discovery extends the paleo-distribution of this genus into Neotropical South America during the Paleogene.
... Cysts became largely defunct for intergenerational transmission at the onset of anal trophallaxis in the ancestral hosts, but the flagellates could not revert to a functional two-stage life cycle via horizontal transmission because of the concomitant change in host social structure (Figure 2). Nonetheless, vertical transmission of flagellates in Cryptocercus is unlikely to be as tightly coordinated as vertically transmitted, obligate intracellular symbionts (e.g., Sacchi et al., 2000;Arab et al., 2020). There may always be some noise in a transmission system that relies on host behavior, and vertical transmission in Cryptocercus should be considered high fidelity but not perfect (Tai et al., 2015). ...
Lower termites, as well as their sister group, the subsocial wood-feeding cockroach Cryptocercus, rely on flagellated eukaryotic symbionts in the hindgut to cooperatively digest their wood diet. In Cryptocercus these flagellates undergo encystment cycles tightly coordinated with the molting cycle of their host, yet the resultant cysts play no demonstrated role in their transmission to neonates; the trophozoite stage of the flagellates is passed directly from parents to offspring via hindgut fluids (proctodeal trophallaxis). This pattern suggests that encystment is a vestige from a gregarious cockroach ancestor, when the flagellates had a functional, two-stage life cycle and the cysts were horizontally transmitted among hosts via coprophagy. The strong integration between flagellate encystment cycles and host developmental physiology in Cryptocercus indicates that the relationship of the flagellates with their proposed gregarious cockroach ancestor was not commensal, but parasitic, with flagellates likely obtaining benefits by taking advantage of host gut metabolites and ingested plant debris. When vertical transmission evolved the parasites were ‘captured,’ and their fitness became inescapably embedded in the fitness of their host. The vertical transmission of gut flagellates and the origin of host subsociality via proctodeal trophallaxis can be considered two sides of the same coin. From the host point of view proctodeal trophallaxis marks the origination of parental care by provisioning neonates with nourishment, metabolites and beneficial microbiota. From the flagellate point of view, proctodeal trophallaxis was a shift from horizontal to vertical transmission, pushing them from the parasitic to the mutualistic end of the symbiotic spectrum, arguably making this host behavioral change the most critical juncture in the evolutionary trajectory of the termite lineage.
... Not all are observed in all castes and species of termites. Mycetocytes have been reported only in the fat body of Mastotermes darwiniensis (Grassé, 1982;Sacchi et al., 2000). ...
... The most common cells of termite fat body are adipocytes or trophocytes and urocytes or urate cells, although mycetocytes had been described in the termite Mastotermes darwiniensis (Grassé 1982;Sacchi et al. 2000). Adipocytes primarily contain lipid droplets, whereas urocytes function in the storage of uric acid, often in the form of spherocrystals (Grassé 1982;Sacchi et al. 2000;Costa-Leonardo et al. 2013). ...
... The most common cells of termite fat body are adipocytes or trophocytes and urocytes or urate cells, although mycetocytes had been described in the termite Mastotermes darwiniensis (Grassé 1982;Sacchi et al. 2000). Adipocytes primarily contain lipid droplets, whereas urocytes function in the storage of uric acid, often in the form of spherocrystals (Grassé 1982;Sacchi et al. 2000;Costa-Leonardo et al. 2013). ...
Termites are social insects with well-defined castes: workers, soldiers and reproductives. The soldier is a terminal stage and originates from either larvae or workers after two molting processes that include an intermediate presoldier instar. The present study followed the occurrence and morphological changes of the fat body during the soldier ontogeny in the neotropical termite Heterotermes tenuis. Workers and soldiers collected in the field and presoldiers obtained in laboratory were fixed in FAA fixative and embedded in resin for light microscopy. The histological sections were submitted to histochemical tests for protein and urate detection. The fat body in all the individuals showed only two cellular types: adipocytes and urocytes. The adipocytes of presoldiers displayed some lipid droplets, and a large amount of acidophilic granules interpreted as proteins because they were strongly stained by xylidine Ponceau. In soldiers, the fat body was deprived from proteins and showed a higher quantity of urocytes with many urate spherocrystals compared with those present in workers and presoldiers. The results were consistent with metamorphosis process and with the possibility of presoldiers being at the beginning of molting stage. The occurrence of many protein granules suggests uptake and consumption of protein storage during the whole development of the presoldiers into soldiers. The dynamic transformations of the fat body enable the individuals of different phenotypes to accomplish their role in the termite colony.
... Not all are observed in all castes and species of termites. Mycetocytes have been reported only in the fat body of Mastotermes darwiniensis (Grassé, 1982;Sacchi et al., 2000). ...
The functions of the fat body in the different castes of termites, and accumulation of energy reserves, proteins and urates within this organ, are reviewed. The termite fat body is involved in multiple metabolic activities, including recycling of nitrogen. Termite fat body showed three different types of cells: adipocytes, urocytes and mycetocytes, the latter restricted to the species Mastotermes darwiniensis. Adipocytes synthesize and store lipids, glycogen and several proteins. These cells also elaborate important peptides, including some that act in immune processes. Urocytes are responsible for the storage of spherocrystals of urates, which vary quantitatively among the termite castes. The different metabolic functions of the fat body in the several castes and stages of termites are associated with specific adipocyte morphologies. The synthesis and storage of different compounds modify the structure of the fat body; this differentiation is coordinated by hormones involved with molting and reproductive cycles.
... Basic features of adipocytes and urocytes are the same as those described in termites and cockroaches (Han and Bordereau, 1982;Hyatt and Marshall, 1985;Polver et al., 1986). In contrast to some termite species (Sacchi et al., 2000), oenocytes and mycetocytes are lacking in the fat body of the two cave crickets. ...
The cave crickets Troglophilus cavicola and Troglophilus neglectus are the most widely distributed European species of the family Rhaphidophoridae. Their life cycles span two years. They overwinter twice in caves in 4-6 months lasting diapause, T. cavicola in warmer microhabitats. In caves, older T. cavicola undergo sexual maturation, while T. neglectus do not. We hypothesized that the use of energy-supplying compounds and reserve proteins in the fat body is more extensive in T. cavicola than in T. neglectus. We analyzed the contents and morphology of lipid droplets, glycogen rosettes and protein granula at the beginning, the middle and the end of overwintering applying optic, TEM and biochemical methods. In all individuals, the fat body is composed of about 40 oval ribbons consisted of gradually changing adipocytes and urocytes. T. cavicola use glycogen continuously, and stop using lipids in the middle of overwintering, while this is inverse in T. neglectus. Till the middle of overwintering, all individuals exploit proteins, afterwards they are unevenly exploited. We found that the fat body is differently engaged in metabolism of both cave crickets during overwintering, supporting a more glycogen-dependent metabolism in T. cavicola, and a more lipid-dependent one in T. neglectus.
... ms that are essential for the digestion of cellulose. Presence of Lactobacillus in the spermatheca may be beneÞcial, just as lactic acid bacteria are considered important for the ecological balance in termite gut. Bauer et al. (2000) postulated that lactic acid bacteria act as an antagonist against colonization of the gut by opportunistic bacteria. Sacchi et al. (2000) reported transovarial transmission of symbiotic bacteria present in the bacteriocytes in ovarian fat body of Mastotermes darwiniensis Froggatt. It has been stated earlier that the nutrients produced by the secretory cells and released into the lumen of the spermatheca may help in long-term storage of sperm. The bacteria found in the spe ...
Primary reproductives of the Formosan subterranean termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae), complete their first reproductive cycle in ≈60 d after nest formation. During this period, the pairs mate several times. The spherical, aflagellate sperm, after transfer by the male, are stored in the female’s spermatheca. Sperm numbers in the spermatheca increase significantly between day 20 and 40, and thereafter they show a steep decline, indicating that the pairs may not be mating after day 40. The spermatheca is bean shaped with an extremely narrow duct. The thick wall of the spermatheca consists mainly of type 3 cells made up of secretory and duct cells. Cuticle-lined ducts are interspersed throughout these cells. Finger-like extensions of the cuticle-lined interior wall project into the spermathecal lumen. The secretory cells presumably provide nutrition for the sperm during their long storage. Eleven anaerobic and six aerobic species of bacteria were cultured and identified from the spermatheca. The role of these bacteria is unknown.
