Entomology 3rd edition - C.Gillott - Chapter 19 ppsx

III R e p ro d uction an d Deve l o p ment 19 R e p ro d uction 1 . Introductio n As was discussed in Chapter 2 (Section 4.1), an important factor in the success of the I nsecta is their hi g hre p roductive ca p acit y , the abilit y of a sin g le female to g ive rise to m an y o ff s p r i n g ,are l at i ve ly l ar g e p ro p ort i on o f w hi c h ma y reac h sexua l matur i t y un d er f av ff o ra bl e con di t i ons. As re p ro d uct i on i sa l most a l wa y s sexua li n i nsects, t h ere ar i se w i t hi n i nsect populations large numbers of genetic combinations, as well as mutations, which can b e tested out in the prevailing environmental conditions. As these conditions change with t ime, insects are able to ada p t readil y , throu g h natural selection, to a new situation. Over the s h ort term t h e i r high re p ro d uct i ve ca p ac i t y ena bl es i nsects to ex pl o i t tem p orar ily f avora bl e con di t i ons, f or exam pl e, ava il a bili t y o f su i ta bl e f oo dpl ants. T h e l atter re q u i res t h at b ot h t he ti m i ng o f mat i ng, egg pro d uct i on, an dh atc hi ng, an d t h e l ocat i on o f asu i ta bl e egg- l ay i n g site must be carefully “assessed” by an insect. Like other terrestrial animals insects have had to solve two ma j or p roblems in con- n ect i on w i t h t h e i rre p ro d uct i ve bi o l o gy , name ly ,t h e b r i n gi n g to g et h er o f s p erm an d e gg i nt h ea b sence o f surroun di n g water an d t h e p rov i s i on o f asu i ta bl e water y env i ronment i n whi c h an em b ryo can d eve l op. T h eso l ut i on to t h ese pro bl ems h as b een t h eevo l ut i on o f i nternal fertilization and an egg surrounded by a waterproof cover (chorion), respectively. The latter has itself created two secondar yp roblems. First, because of the g enerall y im- p ermea bl e nature o f t h ec h or i on, structura l mo di ficat i ons h ave h a d to evo l ve to ensure t h at a d e q uate g aseous exc h an g e can occur d ur i n g em b r y on i c d eve l o p ment. Secon d ,t h ec h or i o n i s f orme d w hil eanegg i sst ill w i t hi nt h eovar i an f o lli c l e, t h at i s, pr i or to f ert ili zat i on, w hich has necessitated the development of special pores (micropyles) to permit entry of s p erm. 2 . S tructure and Function of the Reproductive Sy ste m The external structure of male and female reproductive systems has been dealt with in Cha p ter 3 (Section 5.2.1), so that onl y the structure of internal re p roductive or g ans will b e d escr ib e dh ere . 5 6 1 56 2 C HAPTER 19 2. 1 . Female F unctions of the female reproductive system include production of eggs, includin g y olk and chorion formation, reception and storage of sperm, sometimes for a considerable p eriod, and coordination of events that lead to fertilization and ovi p osition. Th ou gh d eta il svar y ,t h e f ema l es y stem (F ig ure 19.1) essent i a lly i nc l u d es a p a i ro f ov ar i es f rom eac h o f w hi c h runs a l atera l ov id uct. T h e l atera l ov id ucts f use i nt h em idli ne , an d t h e common ov id uct typ i ca ll y enters a sac lik e structure, t h evag i na. In some spec i es the vaginal wall evaginates to form a pouchlike structure, the bursa copulatrix, in which F I G URE 19.1 . Representat i ve f ema l e repro d uct i ve systems (not to sca l e). (A) M e l anop l us san g uinipes (Ortho p tera); (B) R hodnius p rolixu s (Hemi p tera); (C) P eri p laneta american a (Dict y o p tera); and (D ) N a so n i a vi tr ip enn is ( Hymenoptera). Abbreviations: BC, bursa copulatrix; CA, calyx; CG, collateral (accessory) glands; CO, common ov id uct; DG, Du f our’s gl an d ; LCG, l e f tco ll eter i a lgl an d ; LO, l atera l ov id uct; OV, ovar i o l e; PCG, p seudocolleterial g land; RCG, ri g ht colleterial g land; SP, s p ermatheca; SPG, s p ermathecal g land; VG, veno m g land; VGR, venom gland reservoir. [A, C, D, from C. Gillott, 2002, Insect accessory reproductive glands: Key pl a y ers i n p ro d uct i on an dp rotect i on o f e gg s, i n: C h emoeco l og y o f Insect Eggs an d Egg Deposition (M. H ilk er and T. Meiners, eds.), B yp ermission of Blackwell Verla g , Berlin; B, from R. P. Rue gg , 1981, Factors influencin g reproduction in R hodnius p rolixus (Insecta: Hemiptera), Ph.D. Thesis, York University, Canada.] 5 63 REPR O DUCTI ON spermatophores and/or seminal fluidis deposited during copulation. Also connected with the va g ina are the s p ermatheca in which s p erm are stored and various accessor yg lands. In some s p ec i es p art o f t h es p ermat h eca ta k es t h e f orm o f a di vert i cu l um, t h es p ermat h eca lgl an d . I t i s notewort hy t h at t h eovar i es t h emse l ves l ac ki nnervat i on t h ou gh t h e d ucta l com p onent s of the system receive nerves from the terminal abdominal ganglion (Sections 5 and 7.2) . The ovaries are usually dorsolateral to the gut, and each comprises a number of tubula r o v a rioles ensheathed b y a network of connective tissue in which numerous tracheoles an d m usc l es are em b e dd e d .T h e num b er o f ovar i o l es p er ovar y ,t h ou gh a pp rox i mate ly constant wi t hi nas p ec i es, var i es w id e ly amon g s p ec i es. For exam pl e, i n some v i v ip arous a phid san d i n d ung b eet l es t h ere i s one ovar i o l e per ovary i n contrast to t h e more t h an 2000 ovar i o l es per ov a ry in some higher termite queens. The wall of each ovariole includes an outer epithelial sheath and an inner acellular, elastic layer, the tunica propria. Each ovariole (Figure 19.2) F I GU RE 19 . 2 . T yp es of ovarioles. The u pp er p ortion of each fi g ure is enlar g ed to a g reater extent than the lower in order to make details of germarial structure clear. [After A. P. Mahowald, 1972, Oogenesis, in : D evelo p menta l Sy stems: Insect s ,V ol. I (S. J. Counce and C. H. Waddington, eds). By permission of Academic Press Ltd., and the VV a uthor. ] 564 C HAPTER 19 c onsists of a terminal filament, germarium, vitellarium, and pedicel (ovariole stalk). The terminal filaments ma y fuse to form a sheet of tissue attached to the dorsal bod y wall or d orsa ldi a ph ra g m by w hi c h an ovar yi s sus p en d e d w i t hi nt h ea bd om i na l cav i t y .W i t hin t h e g ermar i um, oo g on i a, d er i ve df rom p r i mar yg erm ce ll s, gi ve r i se to ooc y tes an d , i n some types o f ovar i o l es, a l so to nutr i t i ve ce ll s (see b e l ow). As oocytes mature an d enter the vitellarium they tend in most insects to become arranged in a linear sequence alon g the ovariole. Each ooc y te also becomes enclosed in a one-cell-thick la y er of follicula r e pi t h e li um d er i ve df rom meso d erma lp re f o lli cu l ar t i ssue l ocate d at t h e j unct i on o f t h e g ermar i um an d v i te ll ar i um. As i ts name i n di cates, t h ev i te ll ar i um i st h ere gi on i nw hi c h an oocyte accumu l ates yo lk , a process k nown as v i te ll ogenes i s (Sect i on 3.1.1). Norma ll y v itellogenesis occurs only in the terminal oocyte, that is, the oocyte closest to the latera l o viduct, and during the process the oocyte’s volume may increase enormously, for example , by as muc h as 10 5 ti m es in D rosophila. Eac h ovar i o l e i s connecte d to a l atera l ov id uct by at hi n-wa ll e d tu b e, t h e p e di ce l ,w h ose l umen i s i n i t i a lly occ l u d e dby e pi t h e li a l t i ssue. T hi s pl ug o f t i ssue i s l ost d ur i ng ovu l at i on (movement o f a mature oocyte i nto a l atera l ov id uct) and replaced by the remains of the follicular epithelium that originally covered the oocyte. O varioles ma yj oin a lateral oviduct linearl y , as in some a p ter yg otes, E p hemero p tera an d O rt h o p tera, or, more o f ten, o p en con fl uent ly i nto t h e di sta l ex p an d e dp ort i on o f t h eov id uct, t h eca ly x . Th ree types o f ovar i o l es can b e di st i ngu i s h e d (F i gure 19.2). T h e most pr i m i t i v e type, found in Thysanura, Paleoptera, most orthopteroid insects, Siphonaptera, and som e M ecoptera, is the panoistic ovariole in which specialized nutritive cells (trophocytes) are absent. Tro p hoc y tes occur in the two remainin g t yp es, the p ol y tro p hic and telotro p hic ovari - ol es, w hi c h are somet i mes g rou p e d to g et h er as mero i st i covar i o l es. In p o ly tro phi covar i o l es, s evera l trop h ocytes (nurse ce ll s) are enc l ose di n eac hf o lli c l ea l ong w i t h an oocyte. T h e trophocytes and oocyte originate from the same oogonium. Polytrophic ovarioles are foun d in most endopterygotes, and in Dermaptera, Psocoptera, and Phthiraptera. In Hemipter a and Coleo p tera telotro p hic (acrotro p hic) ovarioles occur in which the tro p hoc y tes form a sy nc y t i um i nt h e p rox i ma lp art o f t h e g ermar i um an d connect w i t h eac h ooc y te by means of a trop hi c cor d . T he lateral oviducts are thin-walled tubes that consist of an inner epithelial layer set on a basal lamina and an outer sheath of muscle. In many species they include both mesodermal and ectodermal com p onents. In almost all insects the yj oin the common oviduct mediall y b eneat h t h e g ut, b ut i nE ph emero p tera t h e l atera l ov id ucts rema i nse p arate an d o p en t o t h e exter i or i n d e p en d ent ly .T h e common ov id uct, w hi c hi s li ne d w i t h cut i c l e, i s usua lly more muscu l ar t h an t h e l atera l ov id ucts. Poster i or l y, t h e common ov id uct i s con fl uent w i t h the vagina that, as noted above, may evaginate to form the bursa copulatrix. In some species the bursa forms a diverticulum off the oviduct. In nearl y all Le p ido p tera the bursa is p h y si - c a lly di st i nct f rom t h eov id uct an d o p ens to t h e outs id ev i at h evu l va (F ig ure 19.3). A narro w sp erm d uct connects t h e b ursa w i t h t h eov id uct an df orms t h e route a l on g w hi c h t h es p erm m i grate to t h e spermat h eca. U sually a single spermatheca is present in which sperm are stored, though in some higher Diptera up to three such structures occur. The spermatheca and the duct with which i t j o i ns t h e b ursa are li ne d w i t h cut i c l e. T h e cut i c l e over l a y s a one-ce ll -t hi c kl a y er o f e pi t h e li um w h ose ce ll s are gl an d u l ar an d assume d to secrete nutr i ents f or use by t h e store d s perm. Typ i ca ll y, a l so, t h ece ll s h ave a muc hf o ld e d ap i ca l p l asma l emma, a dj acent to w hi c h are many mitochondria, features characteristic of cells involved in ion exchange (compar e the structure of Malpighian tubule and rectal epithelial cells, Chapter 18, Sections 2.1 5 6 5 REPR O DUCTI ON F IGURE 19. 3. R eproductive system of female Lepidoptera-Ditrysia. [After A. D. Imms, 19 5 7, A G enera l Te xtbook of Entomology e e , 9th ed. (revised b y O. W. Richards and R. G. Davies), Methuen and Co.] and 4.1). These features ma y indicate that the s p erm stored in the s p ermatheca re q uire an i on i cm ili eu diff erent f rom t h at o f t h e surroun di n gh emo ly m ph. Var i ous accessor ygl an d s(a l so ca ll e d co ll atera l or co ll eter i a lgl an d s) ma yb e p resent an d u sua ll y open i nto t h e b ursa. However, i n Acr idid ae (Ort h optera) t h eg l an d s, k nown as pseu- d ocolleterial glands, are anterior extensions of the lateral oviducts (Figure 19.1A). Normally, t here is one p air of g lands, which secrete materials that form a p rotective coatin g aroun d th ee gg sorst i c k t h ee gg stot h esu b strate d ur i n g ov ip os i t i on. Less common ly t h e gl an ds p ro d uce ant ib acter i a l su b stances t h at coat t h ee gg s, tox i ce gg p rotectants, an d ov ip os i t i on- st i mu l at i ng or ov i pos i t i on- d eterr i ng p h eromones (G ill ott, 2002). In some spec i es t h eg l an d s m ay be structurally distinct bi- or multipaired structures, each pair presumed to have dis - crete functions. In Hymenoptera, the glands are single, not paired, and produce the venom u se di nt h est i n g , secrete tra il -orov ip os i t i on s i te-mar ki n gph eromones, or l u b r i cate t h e ov ip os i tor va l ves (F ig ure 19.1D) . 2. 2 . Mal e Funct i ons o f t h ema l ere p ro d uct i ve s y stem i nc l u d e p ro d uct i on, stora g e, an d , fina lly, d e li very to t h e f ema l eo f sperm. In some spec i es, t h e system pro d uces su b stances trans- ferred during copulation that regulate female receptivity and fecundity (Gillott, 199 5 , 2003; W olfner, 1997, 2002). An additional function ma y be to su pp l y the female with nutrients th at can b e i ncor p orate di nto d eve l o pi n g ooc y tes, t h ere by i ncreas i n g t h e rate an d num b er o f e gg s p ro d uce d . T h ema l e system i nc l u d es pa i re d testes ( i n Lep id optera t h ese f use to f ormas i ng le m edian organ), paired vasa deferentia and seminal vesicles, a median ejaculatory duct, an d various accessory glands (Figure 19.4). The testes, which lie either above or below the gut, com p r i seavar i e d num b er o f tu b u l ar f o lli c l es b oun d to g et h er by a connect i ve t i ssue s h eat h. T h e f o lli c l es ma y o p en i nto t h evas d e f erens e i t h er con fl uent ly or i na li near se q uence. T h ewa ll o f eac hf o lli c l e i sa l ayer o f ep i t h e li um set on a b asa ll am i na. W i t hi nt h e f o lli c l es several zones of development can be readily distinguished (Figure 19. 5 ). The distal zone i s the germarium in which spermatogonia are produced from germ cells. In Orthoptera, 566 C HAPTER 19 F IGURE 19.4. Examp l es o f ma l e repro d uct i ve systems (not to sca l e). (A) Me l anop l us san g uinipes (Ort h optera) ; ( B ) L y tta nutta lli ( Co l eo p tera); (C ) Ana g asta k uhniella ¨ (Le pid o p tera); an d (D) D rosop h i l ame l ano g aster (D ip tera). In M . sangu i n i pe s 1 6 pairs of tubules make up each collateral gland (CG). There are 4 white tubules (WT) , 10 s h ort h ya li ne tu b u l es (SHT), an d a l ong h ya li ne tu b u l e (LHT). T h e1 6 t h tu b u l e serves as a sem i na l ves i c le ( SV ) .InL. nutta lli th ere are t h ree tu b u l es i n eac h co ll atera lgl an d ;as pi ra l tu b u l e(S p T), s h ort tu b u l e (ST), an d a long tubule (LT) . O ther abbreviation s : CED, cuticular ejaculatory duct; D, duplex; EB, ejaculatory bulb; ED, ej acu l atory d uct; LVD, l ower vas d e f erens; MED, meso d erma l e j acu l atory d uct; T, test i s; TF, test i s f o lli c l e; UVD, u pp er vas d e f erens; VD, vas d e f erens. (A, f rom C. G ill ott, 2002, Insect accessor y re p ro d uct i ve gl an d s: Ke ypl a y er s i n production and protection of eggs, in : Chemoecology of Insect Eggs and Egg Depositio n ( M. Hilker and T . M e i ners, e d s.). By perm i ss i on o f B l ac k we ll Ve r l ag, Ber li n; B, f rom G. H. Ger b er,N.S.C h urc h ,an d J. G. Rempe l, 1971, T h e anatom y , hi sto l o gy ,an d phy s i o l o gy o f t h ere p ro d uct i ve s y stems o f L y tta nutta ll i Sa y (Co l eo p tera : M eloidae). I. The internal genitalia , C an. J. Zool . 49 :523–533. By permission of the National Research Council of C ana d a; C, f rom a di agram supp li e db y Dr. J. G. R i emann; D, f rom E. Ku bli , 199 6 ,T h e D rosop h i la sex-pept id e : A p e p t id e ph eromone i nvo l ve di nre p ro d uct i on , Ad v. Dev. Bioc h em . 4 : 99–128. B y Perm i ss i on o f JAI Press, I nc.) 5 6 7 REPR O DUCTI ON F I G URE 19 . 5 . ( A) Section throu g h testis to show arran g ement of follicles; and (B) zones of maturation in testi s follicle. [A, from R. E. Snodgrass , Principles o f Insec t M orphology. Copyright 1935 by McGraw-Hill, Inc. Used with p ermission of McGraw-Hill Book Com p an y . B, after V. B. Wi gg lesworth, 196 5 , Th e Princip l es o f Insect Physiolog y , 6th ed., Methuen and Co. B yp ermission of the author. ] Dict y o p tera, Hemi p tera, and Le p ido p tera a p rominent a p ical cell is also p resent whose p re- sume df unct i on i stosu pply nutr i ents to t h es p ermato g on i a. As eac h s p ermato g on i um moves prox i ma ll y i nto t h e zone o f growt h , i t b ecomes enc l ose d w i t hi na l ayer o f somat i cce ll s, forming a “cyst.” Within the cyst, the cell divides mitotically to form a varied number (usu - ally 64–2 5 6) of spermatocytes. In the zone of maturation, the spermatocytes undergo two m aturation divisions, so that from each s p ermatoc y te four ha p loid s p ermatids are formed . I nt h e p rox i ma lp art o f t h e f o lli c l e, t h e zone o f trans f ormat i on, s p ermat id s diff erent i ate i nto fl a g e ll ate d s p ermatozoa. At t hi st i me t h ec y st wa ll norma lly h as ru p ture d ,t h ou gh o f ten t h e sperm w i t hi na b un dl e (spermato d esm) rema i n h e ld toget h er b yage l at i nous cap t h at covers t heir anterior end. This cap may be lost as the sperm enter the vas deferens or persist until t he s p erm have been transferred to the female . I nLe pid o p tera two t yp es o f s p erm occur. P y rene (nuc l eate) s p erm are t h ose t h at f ert ili ze egg s, w hil ea py rene (anuc l eate) s p erm are s p ecu l ate d to h ave severa lf unct i ons, i nc l u di n g ass i st i ng i nt h e movement o f pyrene sperm f rom t h e testes to t h e sem i na l ves i c l es, prov idi ng n ourishment to the pyrene sperm, and destroying sperm from previous matings (Silberglie d e ta l. , 1984). In each species within the Drosop h i l a obscur a c omplex two size classes of 56 8 C HAPTER 19 nucleated sperm are produced, which differ in head and tail lengths. Snook and Karr (1998) c onfirmed that onl y the lon g -s p erm t yp e fertilize e gg s, thou g h the function(s) of the short s p erm rema i nun id ent i fie d. Sperm are move df rom t h e testes to t h e i rs i te o f storage (norma ll y, t h e sem i na l ves i c l es) by peristaltic contractions of the vas deferens. The seminal vesicles are dilations of the vasa deferentia. Their walls are well tracheated and frequently glandular, which may indicate a p ossible nutritive function. In Acrididae (Ortho p tera) s p erm are stored in a p air of hi g hl y mo di fie d accessor ygl an d tu b u l es (F ig ure 19.4A). In man y Le pid o p tera t h em ig rat i on o f s p erm f o ll owsac i rca di an r hy t h m(G i e b u l tow i c z e t al. , 1989). T ypi ca lly s p erm are re l ease d f rom the testes into the upper vasa deferentia shortly before or just after dark, and the n are moved into the seminal vesicles during the next light phase. However, they quickly l eave this site, bein g moved into the du p lex re g ion of the re p roductive tract (Fi g ure 19.4C), wh ere t h e y rema i n unt il t h enextco p u l at i on occurs. T h et i m i n g o f s p erm movement i s suc h t h at t h es p erm p ro d uce d eac hd a y move i nto t h e d u pl ex a f ew h ours a f ter t h ema l e’s d a ily p er i o d o f recept i v i ty to f ema l ep h eromone. T hi s ensures t h at w h en t h ema l enext h as an o pportunity to mate, a substantial amount of new sperm will be available for insemination . T he vasa deferentia enter the anterior ti p of the e j aculator y duct, an ectodermall y d er i ve d tu b e li ne d w i t h cut i c l ew h ose wa ll s norma lly are h eav ily muscu l ar i ze d . Poster i or ly, t h ee j acu l ator yd uct ma y run t h rou gh an eva gi nat i on o f t h e b o dy wa ll ,w hi c h t h us f orms an i ntrom i ttent organ. In i nsects t h at f orm a comp l ex spermatop h ore, su bdi v i s i on o f t he ejaculatory duct into specialized regions may occur. In Ephemeroptera no ejaculatory duc t is p resent, and each vas deferens o p ens directl y to the exterior . Th e accessor ygl an d sma yb ee i t h er meso d erma l (mesa d en i a) or ecto d erma l (ecta d en i a) i nor igi nan d are connecte d w i t h e i t h er t h e l ower p art o f t h e vasa d e f erent i aort h eu pp er en d o f t h ee j acu l atory d uct. In some spec i es cons id era bl e morp h o l og i ca l an df unct i ona l differentiation of the glands occurs. Essentially, however, their secretions may contribute to the seminal fluid and/or form the spermatophore. In some species the glands produc e substances that, when transferred to the female durin g insemination, cause increased e gg p ro d uct i on (Sect i on 3.1.3) an d/ or d ecrease d rece p t i v i t y (w illi n g ness to mate su b se q uent ly ) (G ill ott, 1988, 2003). 3 . S exual Maturatio n Most male insects eclose (emer g e as adults) with mature s p erm in their seminal vesicles. In d ee d , i na f ew i nsects, f or exam pl e, some Le pid o p tera, P l eco p tera, an d E ph emero p tera, b ot h egg an d sperm pro d uct i on occur i nt h e fina ll arva l or pupa li nstar to ena bl e mat i ng an d egg laying to take place within a few hours of eclosion. Generally, however, after eclosion, a period of sexual maturity is required in each sex during which important structural, p h y siolo g ical, and behavioral chan g es occur. This p eriod ma y extend from onl y afewda ys u p to severa l mont h s i ns p ec i es t h at h aveare p ro d uct i ve di a p ause (Sect i on 3.1.3) . 3 .1. Female Among the processes that occur as a female insect becomes sexually mature are vitello- genesis, development of characteristicbody coloration, maturationof pheromone-producing g lands, g rowth of the re p roductive tract, includin g accessor yg lands, and an increase in 5 69 REPR O DUCTI ON r eceptivity. These processes are controlled by the endocrine system whose activity, in turn, i s influenced b y various environmental stimuli . 3 .1.1. Vitellogenesis As note d a b ove, v i te ll o g enes i s occurs, by an dl ar g e, on ly i nt h e term i na l ooc y te w i t hin an ovar i o l e, yet i n many spec i es t h e process i s hi g hl y sync h ron i ze d among ovar i o l es an d b etween ovaries; that is, the eggs are produced in batches. Why vitellogenesis does not occu r t o any great extent in themore distal oocytes isunclear, though various suggestions have been m ade. One su gg estion is that the terminal ooc y te, as the first to mature, that is, to become ca p a bl eo f v i te ll o g enes i s, s i m ply outruns t h e com p et i t i on. In ot h er wor d s, once t h e ooc y t e b eg i ns v i te ll ogenes i san d growt h , i ts i ncreas i ng sur f ace area ena bl es i t to capture v i rtua lly all of the available nutrients. This, however, cannot be the complete answer because in man y female insects vitellogenesis in the penultimate oocyte appears to be inhibited even after the t erminal ooc y te has com p leted its y olk de p osition and become chorionated, p rovided that the m ature e gg i s not l a id .Twoex pl anat i ons h ave b een p ro p ose d .A d ams an d co-wor k ers (see A d ams, 1970, 1981) s h owe d , in Mu s ca d o me s tic a at l east, an ovar y conta i n i n g mature e gg s produces an oostatic hormone that prevents release of the ovarian ecdysiotropic hormone n ecessary for vitellogenesis (Section 3.1.3). In contrast, in Rh o d nius p ro l ixu s an d L ocusta migratori a an anti g onadotro p ic hormone is p roduced b y the abdominal p eris y m p athetic or g ans an d t h orac i c g an gli a, res p ect i ve ly ,w h en t h eovar i o l e conta i ns a mature e gg .T he f unct i on o f t hi s h ormone, i t i s p ro p ose d , i sto bl oc k t h e act i on o fj uven il e h ormone on t h e f o lli c l ece ll s (Sect i on 3.1.3), aga i n prevent i ng v i te ll ogenes i s (Hue b ner an d Davey, 1973 ; Da vey a a e ta l ., 1993). Remarkably, the metacestode stage of the rat tapeworm , H ymeno l epis d iminut a , which infects female mealworm beetles ( T enebrio mo l ito r ), also p roduces an ant ig ona d otro pi n. T hi s acts s i m il ar ly to t h at o f Rh o dniu s , t h us a ll ow i n g t h e p aras i te to m a k e use o f resources or igi na lly i nten d e df or e gg p ro d uct i on (Hur d , 1998) . As yo lk appears, i t i s seen to b ema d eupa l most ent i re l yo f roun di s h granu l es o r vacuoles known as yolk spheres. Within the yolk spheres, protein, lipid, or carbohydrat e can be detected. The membrane-bound protein yolk spheres are most abundant, followe d by li p id dro p lets that are not membrane-bound. Relativel y few g l y co g en-containin gy ol k s ph eres are usua lly p resent. Sma ll amounts o f nuc l e i cac id s are norma lly d etecta bl e, b ut th ese are not w i t hi nt h eyo lk sp h eres. T h e source o f some o f t h ese mater i a l s i s diff erent i n t he various types of ovarioles. I n all ovarioles, however, almost all yolk protein is extraovarian in origin. In most insect s t he p roteins are accumulated from thehemol y m p h. The source of these p roteins, as was note d i n Cha p ter 16, Section 5.4, is the fat bod y , which, durin g vitello g enesis, s y nthesizes ∗ a n d re l eases l arge quant i t i es o f a f ew spec i fic prote i ns (v i te ll ogen i ns or f ema l e-spec i fic prote i ns ) t hat are selectively accumulated by the terminal oocytes. The higher Diptera are a notable e xce p tion in that the follicular e p ithelium is also a ma j or source of y olk p roteins; indeed, i nt h e sta bl e fly , S tomox y s calcitrans,a ll y o lk p rote i n p ro d uct i on occurs h ere (Ke lly , 1994). S h ort ly b e f ore v i te ll o g enes i s,as p ace a pp ears b etween t h e f o lli c l ece ll san d t h e term i na l o ocytes, an di nterce ll u l ar spaces d eve l op i nt h e f o lli cu l ar ep i t h e li um (patency), so t h at t h e o ocytes become bathed in hemolymph. The tunica propria appears to be freely permeabl e t o all solutes within the hemolymph. Electron microscopic and other studies have shown ∗ In i nsects t h at h ave f u ll y d eve l ope d eggs at ec l os i on, t h e prote i ns are synt h es i ze d (an d store d ) b yt h e f at b o d y d ur i n gl arva ld eve l o p ment, to b ere l ease dd ur i n g t h e p u p a l sta g ew h en v i te ll o g enes i s occurs . [...]... Davey (196 5, 198 5a,b), Engelmann (197 0), and de Wilde and de Loof (197 4a) Highnam and Hill (197 7), Koeppe et al (198 5), Hagedorn (198 5), Raabe (198 6), Nijhout (199 4), and Belles (199 8) discuss the endocrine control of reproduction Reviews of other aspects of insect reproduction are given by Phillips (197 0), Baccetti (197 2), and Jamieson (198 9) [sperm]; Dumser (198 0) [spermatogenesis]; Cade (198 5),... Cade (198 5), Bailey and Ridsdill-Smith (199 1), and Gillott et al (199 1) [sexual behavior]; King (197 0), Mahowald (197 2), Telfer (197 5), and King and B¨ ning u (198 5) [ovarian development]; Margaritis (198 5) [vitelline membrane and chorion;]; Chen (198 4), Gillott (198 8, 2003), and Kaulenas (199 2) [male accessory reproductive glands]; and Hinton (198 1) [eggs] Adams, T S., 197 0, Ovarian regulation of the... the female may not lay if she detects the oviposition-deterring pheromone that coats the eggs deposited by a prior female (Schoonhoven, 199 0) Culex mosquitoes assess a potential egg-laying site using tarsal 589 REPRODUCTION 590 CHAPTER 19 sensilla that determine water quality (salinity, pH, and amount and type of organic matter present) Oviposition-aggregation pheromone released from previously deposited... adjacent to the vitelline membrane and an exochorion (Figure 19. 6) In some insects, for example, Acrididae, the shell takes on a third layer, the extrachorion, 572 CHAPTER 19 FIGURE 19. 7 Diagrammatic sagittal section through an egg at oviposition [After R F Chapman, 197 1, The Insects: Structure and Function By permission of Elsevier/North-Holland, Inc., and the author.] as an oocyte moves through the... important The importance of the corpora allata in egg development first became apparent in 193 6 when Wigglesworth and Weed-Pfeiffer (cited in de Wilde and de Loof, 197 4b) demonstrated independently that in Rhodnius and Melanoplus, respectively, allatectomy (removal of the 575 REPRODUCTION 576 CHAPTER 19 FIGURE 19. 8 Endocrine control of egg development (A) Schistocerca gregaria and other locusts; (B)... Gillott, C., and Friedel, T., 197 6, Development of accessory reproductive glands and its control by the corpus allatum in adult male Melanoplus sanguinipes, J Insect Physiol 22:365–372 Gillott, C., and Friedel, T., 197 7, Fecundity-enhancing and receptivity-inhibiting substances produced by male insects: A review, Adv Invert Reprod 1 :199 –218 Gillott, C., and Gaines, S B., 199 2, Endocrine regulation of... Berlin Pener, M P., 198 3, Endocrine research in orthopteran insects, Occ Pap Pan Am Acridol Soc 1:42 pp Phillips, D M., 197 0, Insect sperm: Their structure and morphogenesis, J Cell Biol 44:243–277 Raabe, M., 198 6, Insect reproduction: Regulation of successive steps, Adv Insect Physiol 19: 29–154 Ramaswamy, S B., Shu, S., Park, Y I., and Zeng, F., 199 7, Dynamics of juvenile hormone-mediated gonadotropism... in the “collar” 571 REPRODUCTION FIGURE 19. 6 Egg of Locusta (A) General view; (B) enlargement of posterior end; (C) section through chorion along micropylar axis; and (D) details of chorion structure [A, after R F Chapman, 197 1, The Insects: Structure and Function By permission of Elsevier/North-Holland, Inc., and the author B, C, after M L Roonwal, 195 4, The egg-wall of the African migratory locust,... (Figure 19. 8D) In mosquitoes, JH controls only the previtellogenic growth of the primary follicles and is not required for vitellogenesis (Figure 19. 8C) (Dhadialla and Raikhel, 199 4; Klowden, 199 7) Originally, it was believed that JH probably triggered the synthesis of yolk precursors in the follicle cells, which then passed these materials on to developing oocytes However, 577 REPRODUCTION FIGURE 19. 8... the hemolymph, which serves as a reservoir for materials synthesized in the fat body In the early to mid -1 96 0s, evidence was collected that suggested a 578 CHAPTER 19 hormone from the median neurosecretory cells of the brain regulated protein synthesis in the fat body (references in Highnam and Hill, 197 7) Only later came the realization that the neurosecretion does not act directly on the fat body, but . to three such structures occur. The spermatheca and the duct with which i t j o i ns t h e b ursa are li ne d w i t h cut i c l e. T h e cut i c l e over l a y s a one-ce ll -t hi c kl a y er. a dj acent to w hi c h are many mitochondria, features characteristic of cells involved in ion exchange (compar e the structure of Malpighian tubule and rectal epithelial cells, Chapter 18, Sections. Abbreviations: BC, bursa copulatrix; CA, calyx; CG, collateral (accessory) glands; CO, common ov id uct; DG, Du f our’s gl an d ; LCG, l e f tco ll eter i a lgl an d ; LO, l atera l ov id uct; OV, ovar i o l e;