The collapsed eggs found in the bursa copulatrix of a plum moth, Illiberis rotundata Jordan (Zygaenidae: Procridinae): An unusual egg resorption system?

4 Pages·2002·2.1 MB·English

by  Chiharu Koshio

JournaloftheLepidopterists'Society
56(2),2002,62-65
THE COLLAPSED EGGS FOUND IN THE BURSA COPULATFJX OF A PLUM MOTH, ILLIBERIS
ROTUNDATA JORDAN (ZYGAENIDAE: PROCRIDINAE): AN UNUSUAL EGG RESORPTION SYSTEM?
Chiharu Koshio, Yoshihisa Tanaka and Shin-ichi Kudo
Naruto UniversityofEducation, Takashima, Naruto 772-8502,Japan
ABSTRACT. Inaplum moth, llliberis rotundataJordan (Zygaenidae),collapsedeggsandemptychorionswereusuallyfoundinthebursa
copulatrix. Effects ofthe numberofthese eggs on female longevitywere analyzedwitii female bodyweight, bodyweight ofhermate, andfe-
male iecundity. The results ofmultiple regression analysis showedthat females with more eggs in the bursacopulatrix lived longer. It is most
likelythat eggs are resorbed in the bursacopulatrix andused forthe survival ofthe females. This moth seems have an unusual eggresorption
system.
Additional keywords: oocyte, longevity.
Eggresorption, a specific type ofreproductive tactic male longevity: female body weight (body weight of
in which oocytes degenerate instead of being laid as each female when she emerged), male body weight
eggs, has been reported in manyinsects (Bell & Bohm (body weight of her mate when he emerged), fecun-
1975), including lepidopteran species from groups dity (total number ofeggs each female laid during her
such as Heliconiinae (Dunlap-Pianka et al. 1977) and lifetime) anddie numberofeggs (in anycondition, see
&
other Nymphalidae (Boggs Ross 1993). results) in the bursa copulatrix. Before further analy-
llliberis rotundata Jordan (Zygaenidae) is a univol- ses, each value of female body weight, male body
tine and diurnal moth. Larval host plants include cher- weight, fecundity and the number ofeggs (+1) in the
ries, plums and other Rosaceae trees. Adults emerge bursa copulatrixwas log-transformed.
from May to June in western Japan, and copulate and We analyzed correlation structures between these
oviposit repeatedlyalmost fora month, takingonlywa- factors and longevity. Multiple regression analysis was
ter (CK unpublished data). During the process of a also used to estimate only the direct effects of each
study on mating behavior of I. rotundata, we found factor on female longevity, using female longevity as
manycollapsedeggs in the bursacopulatrix offemales. die dependent variable, and the four factors as the in-
In this paper, we describe this unusual phenomenon dependent variables. Data were analyzed using the
and suggest a possible function ofthese eggs. StatView5.0 (SAS Institute Inc.).
Materials and Methods Results
We collected pupae ofllliberis rotundata in Naruto We dissected 22 laboratory females and 21 ofthem
City (34°11'N, 134°35'E) in May 2000. Each indi- (95.5%) had eggs in dieirbursa copulatrix (Fig. 1). We
vidual was kept separately in a paper cup (7 cm diam- found a few spheroid shaped eggs, several collapsed
eter, 7 cm depth) placed in a constant condition room eggs, and many empty eggs including fragmented
at 21 + 1°C with a 15L:9D photoperiod. After emer- chorions (Fig. lb). The spheroid eggs were observed
gence, all adults were weighed using an electric bal- nearthe ductus bursa, whereas the emptyeggs were at
ance (Sartorius AG) with an accuracy of 0.01 mg. the bottom ofthe bursa. In one female, a spheroid egg
Nineteen females were allowed to copulate once one was also observed in the ductus seminalis. We could
day after emergence and five females were kept un- not recognize any distinct spermatophore. The fat
mated through their lives (the laboratory females). bodyhad almost been depleted at death.
Each mated female was moved to and kept in aplastic The number ofeggs, including spheroid, collapsed
case (9 cm diameter, 5 cm depth) supplied with a and empty eggs, in the bursa copulatrix varied from
single fresh cherry leaf (Prunus x yedoensis) and wa- zero to 52 in the laboratory females (Mean ± SD =
ter. These females were allowed to lay eggs until 11.4 + 12.8, N = 19). In many cases, the bursa con-
death. Each cherryleafwas renewed everyevening af- tained some othersmall fragmentedchorions, thus the
ter the number ofeggs laid by the female on that day counted number ofeggs seems to be underestimated.
had been checked. We dissected these females soon Amongthose 19 females, longevitywas 23.6 + 6.0 days
after their deaths and examined the contents of the (Mean ± SD), fecundity was 461.1 ± 177.3, body
bursa copulatrix. In 2001, we also collected and dis- weight was 53.7 ± 8.8 mg, and body weight of their
sected females from the field (the wild females). mates was 31.6 ± 3.4 mg.
In order to reveal the function of the eggs in the The number ofeggs in the bursa copulatrix and fe-
bursa copulatrix, we examined their effects on female male body weight were positively correlated with fe-
longevity. We selected fourfactors that might affect fe- male longevity (Table 1, Fig. 2), but fecunditywas neg-
Volume 56, Number 2 63
Fig. 1. Thebursacopulatrixcontainingeggsin the laboratoryfemales, (a) Manyeggscontainedarevisible throughthetranslucentwallof
thebursa(BC, bursacopulatrix; OV, oviduct; SP, spermatheca). Afterdissectionofthisbursa, 9collapsedand 18emptyeggswerecounted, (b)
Spheroid, collapsedoremptyeggs from thebursaofanotherfemale.
ativelycorrelatedwith female longevity. Fecunditywas retainedeggs found inwild females (Mean ± SD = 0.64
also positivelycorrelatedwith female bodyweight (r = ± 0.75, N = 14) was smaller tiian that ofthe laboratory
0.46, P = 0.046). Fecundity and number ofeggs in the females (Mann-Whitney's [/-test, U = 13.5, P < 0.0001).
bursa, however, showed no significant correlation (r =
Discussion
-0.36, P = 0.13).
The total multiple regression model was highly sig- Resorption usuallyoccurs inimmature eggs (oocytes)
nificant (R2 = 0.82, F = 15.5, P < 0.0001; Table 1). within the ovarioles (Bell & Bohm 1975). On the other
Both the numberofeggs in the bursa and female body hand, the resorption of mature eggs (chorionated
weight positively influenced female longevity. Fecun- eggs) has been reported in Heliconiine butterflies
dity negatively affected female longevity, suggesting a (Dunlap-Pianka et al. 1977) andotherinsects (see Bell
phenotypic cost of reproduction (see Reznick 1985). & Bohm 1975).
Male bodyweight had no effect on female longevity. In most laboratory females of 7. rotundata, col-
There is no significant correlation between fecun- lapsed eggs with chorions were found in their bursa
dity and the number of eggs in the bursa, partialling copulatrixat death. To the best ofourknowledge, such
out longevity (partial r = 0.129, P = 0.59, N = 20). a phenomenon has never been documented in Lepi-
Nine out of16wild females that had been collected doptera. At this point we might ask, what is the func-
in the field also had collapsed eggs or chorions in their tion of these eggs? Eberhard (2000) found a mature
bursacopulatrix. Seven ofthe nine females had one or egg or a larva just hatched from the egg in the bursa
two eggs, while two females had highly degenerated copulatrix in some female Microsepsis armillata
chorions that could not be counted. These observa- (Diptera: Sepsidae) flies, and he also reported the
tions indicate that retention ofeggs in the bursa copu- same phenomenon in other flies. He suggested that
latrixis not caused artificiallybykeeping females in the the egg orlarvawould prevent intromission by a male,
laboratory for long periods. However, the number of even though in these species females are immune to
Table 1. Results ofcorrelation and multiple regression analysis forfemale longevityandfactors potentiallyaffectingthelongevity. The total
multipleregression modelwashighlysignificant(seetext), r: correlationcoefficient. (3: standardizedpartialcorrelationcoefficient.
Correlation Mijltiple regression
Factor r P P f P
Femalebodyweight 0.29 0.232 0.49 3.55 0.003*
Malebodyweight 0.21 0.391 0.06 0.53 0.607
Female fecundity -0.52 0.023 -0.55 -3.68 0.003*
Numberofeggs inbursa 0.76 <0.001* 0.50 3.81 0.002*
:Significantafterusingthe sequential Bonferronicorrection.
— — — —
* i
64 Journal of the Lepidopterists' Society
40 In some insects oocytes are quickly resorbed in the
10 35 - absence ofmating. Illiberis rotundata females usually
CD mate repeatedly under field conditions (CK unpub-
-a
_c 30 - lished data). In our experiment, however, females
>> 25 - • were allowed to mate only once. When females are
->•— • prevented from mating, they may consume some of
CDD) 20 - their eggs in order to live longer and possibly achieve
c
_o 15 -i • additional matings. Through multiple matings, these
CD females might gain additional nutritional and/or ge-
10 -
CO & &
E netic benefits (Arnqvist Nilsson 2000, Jennions
CD 5 - Petrie 2000).
— — — — — Besorption can occur in Lepidoptera in response to
I i i i
10 20 30 40 50 60 qualitative or quantitative nutrient deficiencies (Dun-
&
lap-Pianka et al. 1977, Boggs Boss 1993). Adults of
Number of eggs in bursa copulatrix 7. rotundata take only water, and thus no additional
nutrients from food are available for survival. Never-
Fig. 2. The relationship between the number of eggs in the theless they can live for relatively long periods, some-
bursacopulatrixandfemalelongevity.
times more than three weeks. Egg resorption in this
rape. In I. rotundata, females are usually polyandrous species seems to be an effective system for obtaining
and these eggs in the bursa copulatrix would not pre- additional nutrients at the expense ofreproduction.
vent intromission by males. Wild females also had collapsed eggs or degener-
The result ofmultiple regression analysis shows that ated chorions in theirbursacopulatrix, butthe number
females which had more eggs in their bursa copulatrix ofthese eggs and chorions was very low. Two reasons
lived longer. It is most likely that females consume for this are to be considered: first, the age ofthe wild
eggs in the bursa copulatrix and use them to survive, females is uncertain and diey mayhave been dissected
that is, they re-allocate resources from reproduction to at a younger age than the laboratory females, which
survival. There are two pieces ofindirect evidence to were dissected after living out their lives. Ifthere is a
support our hypothesis for I. rotundata. First, most of positive correlation between the number of eggs in
the eggs in the bursa copulatrix were highly degener- bursa copulatrix and female age, youngerwild females
ated. We could see many empty eggs or fragmented would have less eggs in the bursathan older laboratory
chorions at the bottom of the bursa, whereas some females. Second, wild females may have copulated re-
spheroid shaped eggs were observed near the ductus peatedlyuntil the point ofcollection, while the labora-
bursa. These suggest that egg contents were digested tory females mated only once. Ifmales provide nutri-
and resorbed during retention in the bursa copulatrix. tional investment to females duringcopulation, mating
The fact that a spheroid egg was in the ductus semi- frequencywill have an effect on egg resorption by fe-
nalis of a female suggests that eggs were transferred males.
from the ovary to the bursa copulatrix via the ductus Why, then, do I. rotundata females resorb eggs in
seminalis. Second, it is reported that many lepi- their bursa copulatrix not in ovarioles like other in-
dopteran females can consume male spermatophores sects? One possible reason could be to eliminate re-
in their bursa copulatrix as nutrition for their eggs mains after egg resorption. If resorption of chorion-
&
and/or themselves (Boggs Gilbert 1979, Boggs ated eggs occurs in ovarioles, the remains ofresorbed
1981). In I. rotundata, no distinct spermatophores eggs, such as chorions, should be eliminated to facili-
were detected in the bursa copulatrix ofthe laboratory tate the passage of the following eggs. Some wasps
females. It is possible that not onlyspermatophores but oviposit emptychorions to solve this problem (see Bell
chorionated eggs are also degenerated in the bursa. & Bohm 1975). Disposal ofthe remains in the bursa
Bell and Bohm (1975) listed many factors promot- copulatrix seems to be less costlythan in ovarioles, be-
ing oosorption. For example, the restriction of the cause remains can be left in the bursa copulatrix. But
ovipositional site sometimes increases resorption of it is still unknown whythey resorb chorionated eggs.
eggs. In our experiment, each female was restrainedin
a small plastic case with a leafofthe host plant. These Acknowledgments
unnatural conditions might inhibit theiroviposition, al-
We thankA. R. Chittenden forhis suggestionsimprovingan ear-
though they laid eggs readily on the leafor the wall of lierdraftofdiispaper.WealsothankC. L. Boggsforherconstructive
the case. commentsandC. M. Penzforhereditorialhelponthemanuscript.
Volume 56, Number 2 65
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