Top-down regression of the avian oviduct during late oviposition in a small passerine bird

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1 The Journl of Experimentl Biology 27, Pulished y The Compny of Biologists 24 doi:1.1242/je Top-down regression of the vin oviduct during lte oviposition in smll psserine ird T. D. Willims* nd C. E. Ames Deprtment of Biologicl Sciences, Simon Frser University, 8888 University Drive, Burny, V5A 1S6, Cnd *Author for correspondence (e-mil: tdwilli@sfu.c) Accepted 3 Octoer 23 Egg production in oviprous vertertes is ssumed to e costly ut the physiologicl sis of ny costs remins unknown. The vin oviduct is highly differentited liner orgn, with five functionlly specific regions. Here we show tht the oviduct regresses rpidly from the top down s soon s the more proximl regions hve completed their function ut while the distl regions still retin n oviductl egg. In zer finches Teniopygi guttt, oviduct mss did not differ etween erly lying irds t the 1-egg stge compred with lte-lying irds (with one remining yolky follicle; dry mss, mg). However, in irds with no remining yolky follicles ut with n oviductl egg, oviduct mss decresed to 94 mg (44%). Regression occurred uneqully mong different regions of the oviduct, with significnt decreses in the Summry proximl infundiulum/mgnum nd isthmus regions (59% nd 4%, respectively), ut no chnge in distl shell glnd/vgin mss. The shell glnd did not regress until fter the lst oviposition. Thus, the vin oviduct hs highly regulted size function reltionship consistent with high mintennce energy cost for this orgn. We suggest tht oviduct function is significnt contriutor to the physiologicl costs of egg production nd might medite individul vrition in mternl effects ssocited with non-yolk components of egg qulity (e.g. immunogloulins, lysozyme). Key words: cost of egg production, oviduct, orgn size-function reltionship, mternl effect, Teniopygi guttt. Introduction Egg production in irds is widely ssumed to e energeticlly costly (e.g. Stevenson nd Brynt, 2; Nger et l., 2; Nilsson nd Rerg, 21; Visser nd Lessells, 21) ut currently little is known out the specific processes, or components of the reproductive xis, which form the physiologicl sis for these costs (Crey, 1996; Monghn nd Nger, 1997; Nilsson nd Rerg, 21; Vézin nd Willims, 22). Most studies to dte hve focussed on ovrin processes in reltion to differentil ptterns of femle reproductive effort, e.g. follicle development, yolk precursor synthesis nd uptke (Chllenger et l., 21; Christins nd Willims, 21), or trnsfer of steroid hormones from mother to offspring vi yolk (e.g. Schwl, 1993, 1996; Muller et l., 22). In contrst, the reltive importnce of extr-ovrin components of the femle reproductive system hve rrely een considered in reltion to prent offspring interctions or in mediting vrition in mternl effects (however, see Sino et l., 21, 22). Recent studies hve suggested tht the oviduct might hve high energy costs for growth nd/or mintennce, contriuting sustntilly to the energetic cost of reproduction. For exmple, in reeding Europen strlings Sturnus vulgris egg production ws ssocited with 22% increse in resting metolic rte (RMR; Vézin nd Willims, 22; see lso Nilsson nd Rerg, 21), nd oviduct mss ws the only orgn tht explined vrition in RMR mong lying femles (Vézin nd Willims, 23). Similrly, in house sprrows Psser domesticus, Chppell et l. (1999) found tht sl metolic rte (BMR) ws positively correlted with comined dry ovry nd oviduct mss. While these studies suggest potentil costs to individuls with lrge oviducts, Christins nd Willims (1999) reported positive reltionship etween lumen protein content of eggs nd oviduct mss, i.e. individuls with lrger oviducts might enefit in eing le to produce higher qulity eggs (Willims, 1994). Given these identifile costs nd enefits, this predicts tht oviduct size should e tightly coupled to the functionl demnds of this orgn (sensu Dimond nd Hmmond, 1992). In support of this ide, Vézin nd Willims (23) found tht totl oviduct mss decresed y 47% immeditely following ovultion of the lst ovrin follicle even though n oviductl egg ws still present t this point (though they did not identify which component(s) of the oviduct ccounted for this decrese in mss). The oviduct of oviprous vertertes is highly differentited orgn, with five ntomiclly nd functionlly distinct regions (King nd McLellnd, 1984; Plmer nd Guillette, 1988). In poultry, n egg tkes pprox. 25 h to pss down the entire length of the oviduct, ut spends most time

2 264 T. D. Willims nd C. E. Ames (pprox. 2 h) in the distl shell glnd nd reltively little time in the proximl mgnum nd isthmus regions where lumen nd shell memrne formtion occur (Solomon, 1983; Bkst, 1998). Here, in zer finches Teniopygi guttt, we demonstrte tht the oviduct does hve highly regulted size function reltionship. Specificlly, this liner orgn regresses very rpidly t the end of egg-lying from the top down s soon s the more proximl regions hve completed their function ut while the distl regions re still functionl. This would minimize the time tht the different components of this orgn re mintined in functionl stte, nd thus reduce the energy cost of mintining the complete oviduct. Mterils nd methods Animls nd husndry Zer finches Teniopygi guttt Vieillot were mintined in controlled environmentl conditions (temperture C; humidity 35 55%; constnt light schedule of 14 h:1 h L:D, lights on t 7: h). All irds hd ccess d liitum to mixed seed diet (Pnicum nd white millet, 5:5 w/w, pproximtely 12.% protein nd.6% lipid nd 84% crohydrte y dry mss), wter, grit nd cuttlefish one (clcium), nd were given multivitmin supplement once per week. Birds were kept in single-sex cges when not eing red (pprox. 35 irds/triple cge). Breeding pirs were housed individully in single cges (61 cm 46 cm 41 cm), ech with n externl nest ox (11.5 cm 11.5 cm 11.5 cm). Most reeding pirs (N=58) were given n egg-food supplement from piring throughout lying (high-qulity diet or HQD; 6 g dy 1 ; 2.3% protein nd 6.6% lipid). The remining reeding pirs (N=6) were not given egg food during lying (low qulity diet or LQD). The HQD is the stndrd reeding diet in our lortory, ut we included the LQD tretment to llow direct comprison to the study of Houston et l. (1995). Experiments nd niml husndry were crried out under Simon Frser University Animl Cre Committee permit (no. 558B), in ccordnce with guidelines from the Cndin Committee on Animl Cre (CCAC). Experimentl tretments Birds were ssigned to reeding pirs rndomly nd ll mles nd femles used in this experiment hd red previously. Nest oxes were checked dily etween 9: h nd 11: h nd ny newly lid eggs were weighed (±.1 g) nd numered. Lying femles were collected for ody composition nlysis etween 7: h nd 7.15 h on the dy fter lying specific numer of eggs. Lying femles were killed y exsnguintion under nesthetic (Rompun/ Ketmine, 1:1 v/v), the oviduct ws dissected out, nd the oviductl egg removed. We chose this collection time ecuse 95% of eggs re lid within 2 h of lights on in zer finches (Christins nd Willims, 21) with ovultion occurring 3 45 min fter oviposition (Etches, 1996). Thus, irds ovipositing on the dy of collection hd n lmost fully formed oviductl egg in the distl shell glnd region. This llowed us to dissect out the oviductl egg without the risk of confounding oviduct mss y the presence of lumenl lumen from developing eggs. Although intr-cellulr lumen content in the oviduct might hve vried with time of dy, since ll irds were collected t the sme time, nd given the short time window of oviposition, this would not confound our susequent nlyses. Femles were then ctegorized into different stges of ovrin (follicle) development, sed on the numer of yolky follicles in their ovry nd the presence of n oviductl egg: (1) 1-egg irds (N=1) tht hd lid only their first egg nd hd full follicle hierrchy of >3 follicles; (2) irds with 2 3 remining yolky follicles tht hd lid 3+ eggs (men=3.8±.8) nd hd n oviductl egg (N=9); (3) irds with only one remining yolky follicle tht hd lid 3+ eggs (men=3.9±.3) nd hd n oviductl egg (N=13); (4) irds with no remining yolky follicles tht hd lid 4+ eggs (men=4.3±.5) nd still hd n oviductl egg (N=15); nd (5) irds t clutch completion with no yolky follicles nd no oviductl egg (N=8; men clutch size 4.8±.9). All femles were weighed (±.1 g) t piring, t the 1-egg stge nd/or on the dy they were collected. In ddition we collected the first nd lst egg tht ech femle lid for nlysis of egg composition (first eggs were replced with dummy eggs to mintin clutch size). Eggs were oiled for 1 2 min nd frozen t 2 C until further nlysis. Susequently ech egg ws seprted into shell, lumen nd yolk, ech component ws dried to constnt weight t 6 C nd weighed (±.1 g). Oviduct nlysis We divided the oviduct into three sections sed on King nd McLellnd (1984): () infundiulum/mgnum: we pooled these sections since the junction etween the infundiulum nd mgnum ws not esily discernle, nd the infundiulum on verge represented only 6.9±.6% of the comined mss; () isthmus: we seprted the proximl end of the isthmus from the mgnum t the shrply distinguished trnslucent nd of tissue, nd the distl end of the isthmus from the uterus t the red region ; nd (c) shell glnd (uterus)/vgin. Ech section ws susequently dried to constnt mss t 6 C nd weighed gin (±.1 g). We report dt for dry oviduct mss throughout: we did not lipidextrct oviduct tissue ecuse this contins negligile mount of lipid (e.g. 3.9%, F. Vézin, unpulished dt; see lso Houston et l., 1995). Results Body mss vried with stge of ovrin development (F 4,54 =4.7, P<.1), decresing from 16.6±.4 g to 14.1±.5 g etween the 1-egg stge nd clutch completion. Dry oviduct mss ws positively relted to ody mss (F 1,54 =34.2, P<.1, r 2 =.39), therefore we controlled for ody mss (minus orgn mss; Christins, 1999) in ll susequent nlyses. Diet hd mrginlly significnt effect on oviduct mss in lte lying irds: LQD, 151±8 mg, N=4, vs. HQD, 17±4 mg, N=16 (F 2,19 =4.18, P=.6; these irds hd ll ovulted 3 eggs nd hd only 1 2 yolky follicles). We only

3 Top-down regression of vin oviduct 265 hd dt from two irds on the LQD with n oviductl egg nd no remining yolky follicles, ut oviduct msses in these irds (73 mg, 112 mg) were similr to those in irds on the HQD t this stge (men 91 mg, rnge mg, N=15). Totl dry oviduct mss vried with stge of ovrin development (F 5,54 =31.9, P<.1, controlling for ody mss; Fig. 1). Oviduct mss did not differ etween irds t the 1-egg stge (with full follicle hierrchy) nd lte-lying irds tht hd ovulted 3 5 follicles nd hd only one yolky follicle remining (153±8 vs. 167±7 mg; P>.9). However, oviduct mss then decresed y 44%, to 94±6 mg in irds with no remining yolky follicles ut still with n oviductl egg (P<.1), nd then decresed further to 55±1 mg in irds with no oviductl egg, i.e. in irds t clutch completion (P<.1). This reduction in oviduct dry mss over the cycle of ovrin development occurred uneqully mong the different regions of the oviduct (Fig. 2). The mss of the proximl infundiulum/mgnum regions nd the isthmus region decresed y 56% nd 38%, respectively, when irds with one yolky follicle were compred with those with no yolky follicles nd only n oviductl egg (Fig. 2A,B; P<.1 in oth cses). In contrst, there ws no chnge in mss of the shell glnd/vgin t this stge (pired contrst, P>.9). Rther, shell glnd/vgin mss only decresed (y 34%) 24 h lter, fter the lst egg hd een lid, i.e. in irds t clutch completion with no oviductl egg (Fig. 2C; P<.1). Thus, regression of the oviduct ws initited first, nd occurred most rpidly, in the proximl regions of the orgn, ut ws delyed in the distl section until fter the lst oviposition. As consequence, the reltive morphology of this orgn chnged with stge of ovrin development. As lying progressed the reltive contriution of the infundiulum/mgnum regions decresed from 66.6±7.1% of totl oviduct mss t the 1-egg stge to 52.5±3.6% in irds tht hd completed their lst ovultion ut still retined n oviductl egg. Conversely, the reltive contriution of the shell glnd/vgin regions incresed from 21.7±4.5% to 34.2±2.9%, respectively. First-lid eggs were significntly lighter thn lst-lid eggs for femles lying 4 eggs (1.42±.115 g vs. 1.93±.83 g, Dry oviduct mss (mg) st egg > F1 foll + F1 foll + foll + Stge of ovrin development foll No Fig. 1. Vrition in dry oviduct mss (mg) during the lying cycle in femle zer finches in reltion to stge of ovrin development. 1st egg, dy first egg ws lid; F1 foll, one or more yolky follicles present; foll, no remining yolky follicles;, oviductl egg present. Columns shring the sme letter re not significntly different (P>.5). pired t-test, t 23 =2.85, P<.1). There ws no difference in the solute, or reltive, dry mss of shell with lying sequence, ut lte-lid eggs hd higher solute, nd reltive, lumen content compred with first-lid eggs (Tle 1). In contrst, the percentge dry yolk mss ws lower in lst lid eggs (Tle 1). Discussion We predicted tht if mintennce of lrge oviduct is energeticlly costly (Vézin nd Willims, in press) then oviduct size should e tightly coupled to the functionl demnds plced on this orgn (s reported for other orgn systems, e.g. Dimond nd Hmmond, 1992; Hmmond nd Dimond, 1994; Hmmond et l., 1996). This prediction ws supported not just t the whole-orgn level (e.g. rpid regression of the oviduct following lst oviposition) ut lso t the intr-orgn level, with rpid regression of the proximl c Tle 1. Comprison of egg composition for first- nd lst-lid eggs in femle zer finches lying 4 5 egg clutches Shell Alumen Yolk Egg order Dry mss (mg) % Dry mss (mg) % Dry mss (mg) % First 6.±6 25.2± ± ± ± ±4.2 Lst 62.1±5 24.7± ±8** 33.5±2.4** 15.7± ±2.4* Dry mss vlues re mens ± S.D. (N=23); % vlues re percentge of totl egg dry mss. Asterisks indicte significnt difference: *P<.5, **P<.1.

4 266 T. D. Willims nd C. E. Ames sections of the oviduct even efore the finl oviposition. In the ~24 h period fter the lst follicle ws ovulted, ut efore this egg ws lid, the proximl infundiulum/mgnum nd the isthmus regions decresed y 56% nd 38%, respectively. Over the sme period there ws no chnge in shell glnd/vgin mss, ut these sections regressed y 34% in mss in the ~24 h fter the lst oviposition. This mintennce of the functionl cpcity of the oviduct until lst oviposition is supported y the fct tht there ws no decrese in solute or reltive mss of oviduct-dependent egg components (shell nd lumen) for lter-lid eggs. The pttern of oviduct regression in our study is very different from tht reported y Houston et l. (1995), lso for Dry infundiulum mgnum (mg) Dry shell glnd/vgin (mg) Dry isthmus (mg) A B C 1st egg > F1 foll + F1 foll + foll + Stge of ovrin development foll No Fig. 2. Vrition in dry mss of infundiulum/mgnum (A), isthmus (B) nd shell glnd/vgin (C) during the lying cycle in femle zer finches in reltion to stge of ovrin development (s for Fig 1). Columns shring the sme letter re not significntly different (P>.5). the zer finch. They suggested tht the oviduct reched pek mss t the 1-egg stge ut then declined in mss linerly through lying, decresing from 12 mg to 4 mg (66%) etween the 1- nd 4-egg stges. Houston et l. (1995) rgued tht this reflected relese of protein from the oviduct for egg formtion, i.e. tht the oviduct cts s storge orgn. We disgree with this conclusion nd suggest tht the result of Houston et l. (1995) ws n rtifct of (1) plotting oviduct mss y egg numer (lying sequence), rther thn the ctul stge of ovrin development, (2) including irds t lter stges of egg-lying tht hd ctully completed egg formtion, nd (3) not using mss-corrected oviduct mss. Indeed, if we nlyze our dt this wy, not ccounting for these confounding fctors, we lso find n pprent decrese in oviduct mss etween the 1- nd 4-egg stge (dt not shown). Although irds in the study y Houston et l. (1995) were mintined on lowqulity seed diet (in contrst to our study), our dt show tht diet per se does not explin the difference in oviduct mss etween studies. Even on seed-only diet in our study, irds lte in lying hd oviducts verging 151 mg, which is much lrger thn the men of 3 5 mg reported y Houston et l. (1995). Thus, we elieve there is currently no evidence to support protein storge function for the vin oviduct in reltion to egg production (cf. Houston et l., 1995; see lso Vézin nd Willims, 23). The results of our study clerly show tht totl oviduct mss remins constnt during egg-lying s long s there is t lest one remining yolky follicle still to e ovulted nd to pss down the oviduct. However, once the lst ovultion hs occurred there is rpid, nd mrked, regression of the proximl regions of the oviduct (the infundiulum, mgnum nd isthmus) s soon s the follicle hs pssed these regions (within 24 h postovultion), ut while the distl shell glnd region is still processing the oviductl egg. Prt of this decrese might e explined y loss of stored secretory products (lumen proteins) from oviductl tissue following the lst ovultion. This does not fully explin the differentil pttern of oviduct regression we report, ut this source of mss loss would still e consistent with rpid downregultion of oviduct function (lthough in the domestic hen, lumen protein content of the mgnum region does not decrese until fter cesstion of lying; Yu nd Mrqurdt, 1973). Our result is very similr to tht reported for lying femle Europen strlings, where oviduct mss lso remins constnt up to the lst ovultion, ut then decreses y 5% following this lst ovultion in irds with only one oviductl egg remining (Vézin nd Willims, 23). Thus, in two smll psserines, the vin oviduct hs highly regulted

5 Top-down regression of vin oviduct 267 size function reltionship consistent with high energy cost of mintennce for this orgn (i.e. high levels of cellulr secretory ctivity). This interprettion is supported y the oservtion tht individul vrition in residul RMR in Europen strlings during egg-lying is positively relted to oviduct mss ut not to other orgns (Vézin nd Willims, 23). There ppers to e little known out the specific mechnisms involved in oviduct regression, ut our study suggests tht these mechnisms must e specific to ech region of the oviduct (e.g. differentil timing of receptor expression) rther thn involving more generic, humorl signl such s downregultion of plsm estrogen or progesterone levels (Burley nd Vdehr, 1989). Although we did not investigte the growth phse, Yu nd Mrqurdt (1973) showed tht the rte of growth of the mgnum during oviduct development is much greter thn tht of more distl sections of the oviduct, i.e. the pttern of growth lso closely reflects functionl demnds. Although mintennce of lrge oviduct would pper to e costly, there re likely dvntges to hving lrge oviduct in terms of oth the quntity, nd potentilly the qulity, of egg lumen. Alumen protein content of eggs is positively relted to oviduct mss (Christins nd Willims, 1999), nd this might e importnt for offspring fitness in terms of structurl growth of the offspring (Willims, 1994; Finkler et l., 1998). In ddition, severl recent studies hve suggested tht mternl effects might include trnsfer of immunogloulins nd nticteril fctors from mother to offspring in egg lumen (Sino et l., 21, 22); thus, oviduct size/function might ply role in mediting these mternl effects. Nevertheless, we consider it unlikely tht oviduct size determines egg size, vi lumen content, independently of ovrin fctors tht determine yolk size (Willims et l., 21). Rther, it seems more likely tht high qulity irds which produce lrge yolks must lso e le to sustin the high costs of oviduct function to deposit the pproprite mount of lumen required y yolks of prticulr size. It is cler tht nimls possess considerle phenotypic flexiility in ody composition, undergoing reversile chnges in orgn size, e.g. in reltion to migrtion (Bttley et l., 2; Guglielmo nd Willims, 23) or reproduction (Vézin nd Willms, 23). However, in generl these studies hve focussed on modultion t the whole-orgn level. We suggest tht the type of intr-orgn structure function reltionship documented here for the vin oviduct might lso occur in other liner orgns with high mintennce energy costs where there is temporl seprtion of function, e.g. in digestive trcts with prolonged pssge times (Secor nd Dimond, 1997). 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