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Flight Muscles Degeneration, Oogenesis and Fat Body in Lasius Niger and Formica Rufa Queens (Hymenoptera: Formicidae)

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Flight Muscles Degeneration, Oogenesis and Fat Body in Lasius Niger and Formica Rufa Queens (Hymenoptera: Formicidae) Russian Entomol. J. 29(4): 410–420 © RUSSIAN ENTOMOLOGICAL JOURNAL, 2020 Flight muscles degeneration, oogenesis and fat body in Lasius niger and Formica rufa queens (Hymenoptera: Formicidae) Äåãåíåðàöèÿ êðûëîâîé ìóñêóëàòóðû, îîãåíåç è æèðîâîå òåëî ó ñàìîê Lasius niger è Formica rufa (Hymenoptera: Formicidae) Elena B. Fedoseeva1, Natalya A. Grevtsova2 Å.Á. Ôåäîñååâà, Í.À. Ãðåâöîâà 1 Zoological Museum of Lomonosov Moscow State University, Bolshaya Nikitskaya Street 2, Moscow, 125009 Russia. E-mail: [email protected] 2 Dept. of Entomology, Faculty of Biology, MSU, 1–12 Leninskie Gory , GSP-1, Moscow, 119991 Russia. E-mail: [email protected] 1 Зоологический музей МГУ им. М.В. Ломоносова, Большая Никитская ул., 2, Москва, 125009 Россия. 2 Каф.энтомологии, Биологический ф-т, МГУ им. М.В. Ломоносова, Ленинские горы, 1, стр. 12, ГСП-1, Москва, 119991 Россия. KEY WORDS: comparative anatomical, colony founding, Formica rufa, indirect flight muscles, hystolysis, adipogenesis, ovary, egg. КЛЮЧЕВЫЕ СЛОВА: сравнительно-анатомическое, основание семьи, крыловые мышцы непрямого действия, гистолиз, адипогенез, яичник, яйцо. ABSTRACT. Queens of Lasius niger with their young red wood ant queens lay their first eggs after independent mode of colony founding have a much nuptial flight no earlier than following spring. higher fat content than red wood ants queens, which create new colonies either via budding or through tem- РЕЗЮМЕ. Самки Lasius niger, с их независимым porary social parasitism. After nest foundation, an L. способом основания семьи, по содержанию жира niger queen will never leave it to forage. Therefore, значительно превосходят самок рыжих лесных мура- until workers appear, vital activities of the queen re- вьев, семьи которых возникают либо путём почкова- quire reserves that are within the extremely well-devel- ния, либо в результате временного социального па- oped gaster fat body, and later, the degeneration of the разитизма. После закладки гнезда самка L. niger не flight muscles. This comparative anatomical research покидает его для фуражировки, так что до выхода demonstrated that both alate and dealate young queens первых рабочих её жизнедеятельность обеспечива- of red wood ants collected in nature have no such gaster ют запасы чрезвычайно развитого в брюшке жирово- reserves. During nuptial flight and a month after wings го тела, а позднее — дегенерация крыловых мышц. shedding the gaster of the ants remained compact and Сравнительно-анатомическое исследование показа- free of the massive fat body that is specific to L. niger ло, что собранные в природе как крылатые, так и queens. Ovarian development in young queen red wood бескрылые молодые самки рыжих лесных муравьёв ants is closely dependent on the degeneration of indirect таких запасов в брюшке не имеют. Во время брачно- flight muscles. The process of degeneration includes го лёта и спустя месяц после сбрасывания крыльев их two distinguishable stages: progressive and active hys- брюшко остается компактным и свободно от массив- tolysis of muscle fibers, and two stages of fiber sheaths ного жирового тела, присущего L. niger. Развитие adipogenesis. Ovarian growth in queen red wood ants яичников у молодых самок рыжих лесных муравьёв takes place during the active hystolysis of muscles, but тесно связано с дегенерацией крыловых мышц не- the oogenesis of the first eggs produced occurs during a прямого действия. Процесс дегенерации включает long period of muscle fiber sheaths adipogenesis. Ant явственно отличающиеся стадии: прогрессивного и workers likely play a key role in providing provisions активного гистолиза мышечных волокон, а также две for the queen in the final stage of initial egg develop- стадии адипогенеза волокон. Рост яичников у самок ment. In contrast, in young L. niger queens, the first рыжих лесных муравьёв проходит на стадии актив- batch of eggs is formed much earlier, in the first days ного гистолиза мышц, но оогенез первой порции яиц after wings shedding, when external manifestations of завершается в период адипогенеза оболочек мышеч- flight muscle hystolysis are absent, and the abdomen ных волокон. Рабочие муравьи, по-видимому, игра- contains a fat body. It is assumed that, unlike L. niger, ют решающую роль в обеспечении cамки на заклю- How to cite this article: Fedoseeva E.B., Grevtsova N.A. 2020. Flight muscles degeneration, oogenesis and fat body in Lasius niger and Formica rufa queens (Hymenoptera: Formicidae) // Russian Entomol. J. Vol.29. No.4. P.410–420. doi: 10.15298/rusentj.29.4.08 Flight muscles degeneration, oogenesis and fat body in Lasius niger and Formica rufa 411 чительном этапе развития первых яиц. Напротив, у their derivatives (adipocytes, uratocytes, etc.), and the молодых самок L. niger первая порция яиц формиру- latter are made up of enocytes [Chapman, 1998]. The ется гораздо раньше, в первые дни после сбрасыва- bulk of the fat body consists of adipocytes. Studies of ния крыльев, когда ещё нет внешних проявлений Attini ants have demonstrated the presence of lipid гистолиза крыловых мышц, а брюшко заполнено vesicles and protein granules in fat body cells both in жировым телом. Предполагается, что в отличие от L. queens and workers, as well as the activity of cellular niger, молодые самки рыжих лесных муравьёв спо- structures required for the production of these substanc- собны отложить свои первые после брачного лёта es [Roma et al., 2010]. яйца не ранее весны следующего года. The fat body contains numerous lobes and clusters of cells. Its periphery is comprised of a parietal layer Introduction adjacent to the body wall, and a layer that surrounds internal organs called the perivisceral layer [Schwan- witsch, 1949]. The fat body is most conspicuous in the In the temperate zone, the first young workers appear abdomen, but some portions of the organ extend into the within Lasius niger (Linnaeus, 1758) nests in June, while thorax and head [Chapman, 1998]. In imagoes, perhaps the nuptial flight period lasts from early July to Septem- this is the most dynamic organ since its content and size ber. After insemination, queens shed their wings and changes throughout the life of an insect. Differences in immediately initiate nest founding [Zakharov, 2015]. the wintering weight and summer ant workers have been Hatching of the first generation after wintering in Formi- demonstrated in individuals of F. polyctena, due to ca rufa (Linaeus, 1876) and F. polyctena Forster, 1850 changes in the volume of fat body reserves [Kneitz, ants occurs earlier, in May. Further, in addition to work- 1967]. In ant queens, the most significant fat body ers, viable colonies of F. rufa and F. polyctena produce reorganization that occurs is associated with flight mus- sexual individuals. Nuptial flight in red wood ants takes cle degeneration after wings shedding. place earlier than it does in L. niger, and its duration is In the early 19th century Charles Janet studied micro- shorter, occurring from early May to early June [Za- scopic changes in the flight muscles of ant queens after kharov, 2015]. Young queens, after mating and wing the nuptial flight [Janet, 1907]. He identified two interre- shedding, have two options: to remain at the natal anthill lated processes that occurred in the musculature: a) hys- or independently search for a new one, for which they tolysis, which results in degeneration so that only sheaths employ colonies of Serviformica ants. In the former case, of muscle fibers (sarcolemma) and tracheal structures the queen may become a member of a new colony via that serve muscle remain; and b) adipogenesis, in which maternal anthill budding, and in the latter, she progresses hemolymph cells penetrate the gradually emptying sarco- with the support of the unrelated colony [Dlussky, 1967]. lemma of muscle fibers, where they turn into new adipo- In either case, the queen requires the participation of ant cytes. The nutrients released during hystolysis support workers. This type of colony founding is called ‘depen- the growth of adipocytes, which synthesise both protein dent’. In contrast, independent colony founding typically granules and lipid vesicles. Hystolysis starts prior to occurs in L. niger and many Formicidae species [Höll- adipogenesis, which follows and develops as nutrients dobler, Wilson, 1977; Keller, Passera, 1989]. accumulate within fiber sheaths and the surrounding Lasius niger and red wood ant queens also differ hemolymph. Janet remarked that the rates of hystolysis physiologically at hatching. It was determined that the are not the same in the fibers of different muscles. In fat content in dry weight of queen L. niger after emerg- particular, the indirect flight muscles are the first to ing from the pupa is 22±2%. In contrast, the fat content undergo hystolysis, while direct muscles are last. Both in dry weight of red wood ant species was determined to processes have been described and illustrated in detail be 8±2–12±1% [Keller, Passera, 1989]. Even more using specimens that differed in periods after nuptial significant differences in fat content were observed flight (from several days to one year and 10 months old). between queens at the time of mating in which L. niger According to Janet [1907], in the first days after the and red wood ants were reported to have a fat content of wings shedding, the flight muscles of dealate queens 51±1% and 10±2–13±2%, respectively [ibid.]. Howev- display no external signs of degeneration despite the fact er, the glycogen content in the dry weight of alates was that necrosis has been initiated. The external manifesta- greater in queens of red wood ant species (5.85–8.27%) tion of progressive hystolysis involves the narrowing of than in those of L. niger (4.5%) [Passera, Keller, 1990]. the muscle fibers and the formation of gaps between The fat body of insects is both a storage and source fibers, which is caused by the detachment of the myo- of lipids, proteins and carbohydrates, which serve as fibrillar mass from sheaths and the exit of hystolysis fluid precursors for the metabolism of various substances.
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