The relationship between mating and oogenesis in monarch butterflies (Lepidoptera: Danainae)

Journal of Insect Behavior, Vol. 8. No. 5, 1995

The Relationship Between Mating and Oogenesis In Monarch Butterflies (Lepidoptera: Danainae)

Karen S. Oberhauser 1'2 and Rachel Hampton I

We studied the relationship between the timing of mating and oogenesis in monarch butterflies (Danaus plexippus) to determine (1) the potential for male nutrient input into eggs and (2) whether mating stimulates egg development. Most females mated soon after they started maturing eggs. One and 2 days after mating, females contained the same number of mature oocytes as virgin females of the same age, while 3 days after mating they contained more mature oocytes than did virgins. These results confirm the potential for male-derived nutrients to augment oocyte production, but indicate that mating is not required for oocyte maturation to occur.

KEY WORDS: Danaus plexippus; monarch butterflies; spermatophores; stimulation of oogenesis; vitellogenesis; mating age.

INTRODUCTION

In many Lepidoptera, fecundity appears to be limited by nitrogenous nutrients obtained as larvae; females deplete both nutrients and oocytes throughout their adult lives, and die with few oocytes left (Norris, 1932; Labine, 1968; Dunlap- Pianka et al., 1977). However, some species obtain nitrogenous nutrients as adults, and their fecundity need not be restrained by larval reserves (Gilbert, 1972; Duntap-Pianka et al., 1977; Boggs, 1990). These species might be expected to show more indeterminate oogenesis. One source of nitrogenous nutrients is the adult food supply. For example, Heliconius butterflies extract

~Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, Minnesota 55108-6097.

"To whom correspondence should be addressed.

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702 Oberhauser and Hampton

amino acids from the pollen on which they feed (Gilbert, 1972; Boggs et at. , 1981; Boggs, 1987). In addition, many female Lepidoptera obtain nitrogenous compounds from the spermatophores transferred by males during mating (Boggs and Gilbert, 1979; Boggs, 1981; Boggs and Watt, 1981; Greenfield, 1982; Boggs, 1990; Wells et al. , 1993), and in some species there is a positive relationship between the amount of spermatophore material received and fecundity (Rutowski et al. , 1987; Watanabe, 1988; Oberhauser, 1989a; Tarnhankar et al., 1993; Wiklund et al. , 1993). Of the above studies, only Rutowski et al. (1987) compared females that obtained either one large or one small spermatophore. The others compared singly to multiply mated females, and the increased fecundity observed in these studies could be due to a hormonal or mechanical stimulation of mating itself, rather than nutrient effects.

Allocation of male-derived nutrients to egg production will depend, in part, on the state of oocyte development when they are received (Boggs, 1990). If females mate after most oocytes have been yolked, there is less potential for male nutrient input than when females mate before many of their oocytes are mature. The timing of vitellogenesis (deposition of yolk in the oocyte) and that of mating vary widely in the Lepidoptera. In some species, females eclose with a full complement of oocytes, many of which are already yolked, while in others they eclose without apparent oocytes (e.g., Norris, 1932; Labine, 1968; Dunlap- Pianka et al. , 1977). Some females mate while still in the pupal stage or as teneral adults, while others remain virgins for several days after eclosion (Gil- bert, 1976; Ehrlich and Ehrlich, 1978).

In this study we examined the relationship between the timing of mating and oocyte development in the monarch butterfly. This relationship is relevant to several questions about the role of mating and male-derived nutrients in oocyte maturation. First, it will determine the potential for male-derived nutrient input into eggs. Several lines of evidence indicate that male-derived nutrients are important to female monarchs. Monarch spermatophores contain large quantities of nitrogen (Oberhauser, 1992) that can be traced to both reproductive and somatic tissue in the female after mating (Boggs and Gilbert, 1979; Wells et al., 1993), and these nutrients probably contribute to female reproductive output (Oberhauser, 1989a; but see Sv~ird and Wiklund, 1988b). Captive monarchs show a fecundity pattern similar to that found in Heliconius butterflies that obtain protein as adults from pollen, despite the fact that their adult food source (nectar) contains little protein (Baker and Baker, 1973). They have high lifetime fecundities, show a relatively steady output of eggs over a 3- to 4-week period, and die with oocytes remaining in their ovaries (Oberhauser 1989a,b, and unpublished). A second issue related to the potential for male-derived nutrient input into eggs is the question of how these nutrients fit into female nutrient budgets. If females mate long before their eggs are matured, male-derived nutrients are more likely to become part of the overall nutrient budget than if they delay

Mating and Oogenesis in Monarch Butterflies 703

mating until they begin maturing eggs. In the latter case it seems likely that the nutrients females receive from males are more important in egg production than in other activities. A third question is whether there is a causal relationship between mating and oogenesis. Virgin female monarchs captured in the wild usually have no visible oocytes (Ehdich and Ehrlich, 1978; and personal observations), and some authors have suggested that mating is required to stimulate egg production in this species (Ehrlich and Ehflich, 1978; Drummond, 1984). Our study also tests this hypothesis.

METHODS

Experimental butterflies w e r e F 2 offspring of wild females caught in Ten- nessee in April 1993. Larvae were reared on cuttings of common milkweed (Asclepias syriaca) in screen cages kept outdoors in St. Paul, Minnesota. All adults were weighed to the nearest 0.1 mg the morning after they eclosed, before being fed for the first time. At this point, the meconium has been discharged and masses remain relatively constant (Oberhauser, unpublished). Females that eclosed over a 4-day period (t8-21 July 1993) were assigned to mating and nonmating treatments, with sample sizes of 60 and 49, respectively. All females were kept in walk-in screen cages (2 m x 2 m x 2 m) from the day of eclosion until they were dissected at various ages. They were removed for 1-2 h every morning to be fed a 1 : 4 honey : water solution ad libitum. No males were ever put into the cage with nonmating females. Mating cages contained equal numbers of 4- to 6-day-old virgin males and experimental females. We controlled male age and mating history to eliminate the possibility that female mating age was affected by the type of male in the cage and to control spermatophore size. Male age, mating history, and size all affect spermatophore size, with most variation being explained by age in virgin males (Oberhauser, 1988). Densities in mating cages were 25 or fewer of each sex.

No host plants were available to females in either treatment to control for any effects of oviposition (virgins rarely lay eggs and oviposition does not occur in the absence of host plants; personal observations). Previous work on monarchs has shown that host-plant availability is not required for oogenesis to occur; females held in glassine envelopes from the day of eclosion produce mature oocytes (Herman and Barker, 1977; and personal observations).

We checked for mating pairs at 2-h intervals throughout the day. This frequency ensured observation of all matings because monarchs begin mating in mid to late afternoon and remain in copula for several hours, rarely separating before 0200 h (Sv/ird and Wiklund, 1988a; Oberhauser, 1989b). After mating, females were kept in the cage with nonmating females until they were dissected. Due to environmental factors we stopped measuring the timing of mating after females had been in mating cages for 8 days; cool, wet weather for the following


2 days made mating unlikely, and the timing of later matings could have been due to weather conditions and not female receptivity.

From ages 1-I0 days we dissected six nonmating females every day under 6 × and 12 x magnification on a Wild dissecting microscope and counted mature oocytes (oocytes that are both yolked and have a ridged chorion) in the ovaries and common oviduct. We did not make total egg counts because immature oocytes, especially at the tops of ovarioles, are tiny and hard to count accurately. We noted the presence of visible immature oocytes, distinguishing between those that were not yolked and those that were yolked, but on which the chorion had not been deposited.

Females in the mating treatment were dissected after mating. We deter- mined that matings had been successful by checking the bursa copulatrix for the presence of a spermatophore. Oocytes were counted as described above. We initially planned to limit these dissections to 1 and 2 days after mating, but it was clear after 5 days that these females did not differ in oocyte development from virgin females of the same age. We then dissected additional females 3 days after mating. Times of dissection refer to the number of days after the day mating began.

RESULTS

Timing of Oocyte Development

Table I summarizes the state of oocyte maturation in both virgin and mated females. Egg maturation takes from 2 to 3 days; at age 1 day no oocytes were visible in any females, by age 3 days half of the females had yolked oocytes, and by age 4 days some females had mature oocytes. We used a log-linear model to test for independence of oocyte development state and mating treatment. For this test, we combined ages 4 and 5 days, 6 and 7 days, 8, 9, and 10 days to make three age categories. Females dissected at ages 1, 2, and 3 days were not included in the test, because of the small number of mated females dissected at these ages. Given age, oocyte development state is independent of mating treatment (Pearson X 2 coefficient = 5.28, df = 9, p = 0.809).

Figure 1 shows the number of mature oocytes as a function of virgin female age. Females continue to produce mature oocytes over their first 10 days, even when they do not mate. A linear regression of number of mature oocytes on female age and mass (Table IIA) indicates that oocyte number increases with age. The effect of virgin females mass on oocyte number is not significant at the 0.05 level of confidence. We tested for effects of female age, mass, and the number of days that had elapsed since mating on mature oocyte number in mated females. Time since mating was included in the model in two different ways; once with 1, 2, and 3 days separated (Tabel liB), and once with 1 and 2 days


Table I. State of Oocyte Development I

Mating Number with Number with Number with treatment Number with unyolked yolked mature and age ~ no oocytes b oocytes' oocytes 't oocytes ~

V1 6 0 0 0 V2 4 0 2 0 V3 2 l 3 0 V4 0 0 3 2 V5 0 1 I 3 V6 0 0 I 5 V7 0 1 3 2 V8 0 2 1 2 V9 0 0 0 6 VI0 0 0 0 6

M2 2 0 0 0 M4 0 0 3 0 M5 0 1 1 1 M6 0 1 2 5 M7 0 2 0 4 M8 0 1 0 8 M9 0 0 0 7 M10 0 0 0 3

"v, Virgin; M, mated; numbers refer to age in days at dissection. bNo oocytes could be detected under 12 × magnification. ~Visible, but with no or little vitellogenin deposited. dContain vitellogenin, but no chorion. ~Femates were categorized according to their most mature oocytes; for example, those with mature oocytes also contained yolked and unyolked oocytes.

combined (Table IIC). This was done because visual (see Fig. 2) and statistical (see below) analyses of the data suggested that, for a given age, there is no

difference in the number of mature oocytes in mated females dissected 1 or 2 days after mating. Again, there is a strong effect of female age on mature oocyte

number (see also Fig. 2). Initial female mass had a small, but statistically

significant, negative effect. Time since mating had a positive effect in both models, but the adjusted R 2 value for the model that combined 1 and 2 days is higher.

There is no difference between the number of mature oocytes in mated females dissected I or 2 days after mating and in virgin females dissected at the

same age (Fig. 2; p > 0.15 for ages 4 -10 days, t-tests for unequal sample sizes

and variances). However, females dissected 3 days after mating (at ages 8, 9, and 10 days) had more mature oocytes than both virgin females and mated

females of the same age dissected 1 or 2 days after mating (p < 0.02 for all

ages; t-tests for ages 8 and 9 days, sign test for age 10 days).

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Fig. 1. Number of mature oocytes as a function of virgin female age. Stars indicate means, which were calculated using both zero and positive values. Sym- bols at zero include females with both no oocytes and only immature oocytes, and some represent more than one female (see Table I).

Table 2, Effects of Age," Female Mass, and Time Since Mating on Number of Mature Oocytes

i i / / iii i i iiiiiii i i i i i i i i

Predictor Coet~cient Standard error P Adj. R 2~'

A. Virgin females

Age 6.71 1.75 0.0005 0.541 Female mass - 0 . 0 5 2 0.0256 0.0562 0.572

B. Mated females (I, 2, and 3 days after mating separate)

Age 8.35 2.81 0.0053 0.640 Female mass - 0 . 1 0 0.0336 0.0040 0.690 TSM'- 17.5 6.76 0.0138 0.732

C. Mated females (1 and 2 days after mating combined) a

Age 8.31 2.36 0.0012 0.644 Mass - 0 . 1 4 0.032 0.0001 0.694 TSM (dummy) 43.3 10.9 0.0003 0.782

i i i

"Only females aged 4 days and older were included in regressions, since no eggs are mature before this age.

hAdjusted R 2 from stepwise analysis of variance. '-Time since mating; number of days after mating that female was dissected. aTSM included as dummy variable, with I and 2 days combined.

Mating and Oogenesis in Monarch Butterflies

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Fig. 2. Number of mature ooeytes as a function of mated female age. Stars indicate means for virgin females of the same age for comparison. Other symbols refer to the number of days after mating that females were dissected.

We observed no oviposition behavior on the part of mated females before they were dissected, nor did we detect any eggs on either the sides of the cage or non-host plants (mostly grass) in the cage. While it is possible that some oviposition on inappropriate substrates did occur, we have no evidence of this.

Timing of Mating

Forty-two of the mating-treatment females (86%) had mated by age 8 days, when we stopped putting males in the mating cage. The percentage of females that mated at each age is shown in Fig. 3. Before age 4 days, when no females had mature oocytes, only 14% of the total number of females had mated. By age 6 days, when all virgin females had either yolked or mature oocytes, 70% of the females had mated.

DISCUSSION

Effects of Mating on Oocyte Development

Experimental virgin females contained mature eggs (Table I and Fig. 1), clearly indicating that mating is not required to stimulate oogenesis in monarchs.

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This is contrary to Ehrlich and Ehrlich (1978), who reported an association between virginity and immature oocytes in their survey of lepidopteran mating frequencies and suggested two possible explanations: (1) new females need time to begin maturing eggs, during which they reject courting males, and (2) insemination is required to induce oogenesis. Ehrlich and Ehrlich (1978) and Drum- mond (1984) incorrectly cited monarchs as an example of the latter explanation, after a study by Herman and Barker (1977). However, Herman and Barker (1977) found means of up to approximately 140 mature oocytes/g female wet weight (approximately 70 mature oocytes/female) in virgin females held inside at 25°C, and we found a mean of 55 mature oocytes in 10-day-old females kept in outdoor cages and never allowed to mate. Our results do not tell us what does stimulate oogenesis in monarchs. However, other workers have shown that the induction of oogenesis in Lepidoptera is complicated; in many species, vitellogenin production and oocyte maturation are stimulated by juvenile hormone (e.g., Sroka and Gilbert 1971; Pan and Wyatt, 1971, 1976; Herman and Bennett, 1975; Herman and Barker, 1977; Hagedorn and Kunkel, 1979; Less- man et al. , 1982), but how and when the corpora allata are activated to release juvenile hormone are not clearly understood. There are often complex relation- ships between oocyte development and several factors, including female nutri-


tion, the presence of a spermatophore and viable sperm, and oviposition (e.g., Benz, 1969; Sasaki and Riddiford, 1984).

While there was no detectable increase in the rate of oocyte maturation for 2 days after mating, 3 days after mating females contained more mature oocytes than did virgin females of the same age. Herman and Barker (1977) also found more mature oocytes in mated than in virgin females, although their difference was greater than ours. Their data included combined egg counts from wild- caught females dissected 12 days after capture and laboratory-reared females dissected 5-7 days after mating, versus 3 days in our study, which could account for the greater difference. The inclusion of wild-caught females in their study could also explain the higher mature oocyte number in mated females observed by Herman and Barker (1977); wild-caught females had presumably oviposited before capture, and oviposition (or host-plant presence) stimulates oogenesis in monarchs (Herman and Barker, 1977).

The increase in mature oocyte number after mating in monarchs suggests two (nonexclusive) explanations: (1) mating provides a hormonal or mechanical stimulus to mature additional oocytes, and (2) females utilize nutrients from spermatophores to augment vitellogenin production. It will be difficult to distin- guish between these two processes. However, the fact that the stimulus of mating is not required for continued oocyte maturation over 10 days argues against the primary importance of a mechanical or hormonal effect. We think that the second explanation is likely to be important in monarchs for several reasons. Monarch spermatophores contain nitrogenous compounds (Oberhauser, 1992) which limit reproduction in many Lepidoptera (Norris, 1932; Labine, 1968; Dunlap-Pianka et al. , 1977). Labeled amino acids from spermatophores are incorporated into eggs (Boggs and Gilbert, 1979) and other female tissues (Wells et al., 1993) after mating, and females that receive more spermatophore material show higher fecundity over the time that they are degrading this male-derived material (Ober- hauser, t989a, 1992). It is likely that the effect of these nutrients could take 3 days to be manifested in a statistically detectable increase in the number of mature oocytes, given the rate at which oocytes are matured (Table I) and the high variance in oocyte development. There is some correspondence between this period and the results of Boggs and Gilbert (1979), who found peak incorporation of male-derived material into monarch eggs 2-4 days after mating in one of the two matings they analyzed. Wiklund et al. (1993) also found that the peak incorporation of male-derived materials occurred 3-4 days after mating in Pieris napi.

The lack of a positive effect of initial female mass on number of mature oocytes in both treatments is consistent with previous work on monarchs (Ober- hauser, 1989a) that showed no effect of female mass on lifetime fecundity. Fecundity in insects is often correlated with mass [Suzuki (1978), Lederhouse (1981), and Cushman et al. (1994) include data on Lepidoptera], but this effect


should be less important with increasing dependence on adult, rather than larval, nutrient sources for egg production (Boggs, n.d.). This provides further support for the importance of male-derived nutrients to female monarchs.

Timing of Mating and Oocyte Development

Our results support three conclusions about the relationship between the timing of mating and oocyte maturation in monarchs. (1) Females mate for the first time early in the process of vitellogenesis, when they have a few mature oocytes ready to be fertilized. This supports Ehrlich and Ehrlich's (1978) first explanation for the relationship between virginity and immature eggs in the Lepidoptera, that females reject courting males before they have begun to mature eggs. (2) Because females delay mating until vitellogenesis has begun, male- derived nutrients are likely to be more important for vitellogenesis than for other activities, such as somatic maintenance and foraging activity. This makes sense from a resource allocation viewpoint. Yolk is protein rich, making male-derived nutrients likely to be important in vitellogenesis, while sugars in the adult diet may suffice for activities such as somatic maintenance and foraging (Boggs and Ross, 1993). (3) The number of mature oocytes at the time of a female's first mating is small relative to average daily fecundities (Oberhauser, 1989a,b; and unpublished), so while the first eggs laid after mating utilize nutrients obtained solely from larval reserves, male-derived nutrients can be used to augment these reserves early in egg laying. The high degree of polyandry in monarchs (Pliske, 1973; Suzuki and Zalucki, 1986; Oberhauser, 1989a) results in constant replen- ishment of male-derived nutrients during egg laying.

The timing of mating could have fitness implications for both sexes, but because females seem to be able to avoid unwanted matings in most Lepidoptera (e.g., Wildund, 1977, 1982; Wildund and Forsberg, 1985), female interests probably control timing in most species. We think that females often control the timing of mating in monarchs as well; even though aerial takedowns by male monarchs sometimes result in forced copulation (Pliske, 1975; Rothschild, 1978; Oberhauser, 1989a; Van Hook, 1993), females often appear to evade unwanted males (Pliske, 1975; Oberhauser, 1989a; Frey, unpublished; Jessup and Oberhauser, unpublished; but see Van Hook, 1993). While females could potentially benefit from receiving male-derived nutrients at any time, there might be a cost to mating too early. Spermatophores can represent 5-10% of adult mass (Oberhauser, 1988; Svfird and Wildund, 1989), and degrade over a period of several days after mating (Oberhauser, 1992). This means that mated females have an increased flight load that could make flying energetically more expen- sive, or decrease their ability to avoid predation. Other potentially relevant costs include the time spent mating, increased predation during mating itself, or sex- ually transmitted disease, although these would seem to be equally costly at any


time. If females delay mating until they are ready to reproduce, they avoid costs associated with early mating while still obtaining nutrients to augment larval reserves early in the process of egg maturation. I f this scenario is common in the Lepidoptera, it could account for the association between virginity and immature eggs in other species as well (Ehrlich and Ehrlich, 1978).

The timing of egg maturation could also have important fitness implications for females. An obvious strategy is to link egg maturation to host-plant presence; it may be costly to divert resources to egg production before oviposition is possible. In some Lepidoptera egg maturation has been shown to be dependent on host-plant access (McNeil and Delisle, 1989; McNeil, 1991; Tamhankar et

al . , 1993). Monarchs, however, lack a linkage of egg maturation and mating to host-plant presence. Females probably find oviposition sites easily due to the abundance of host plants throughout monarch summer ranges and their ability to fly long distances. Overwintering in large congregations in sites without host plants could also uncouple mating and egg production from host-plant presence. Females usually mate before they leave these congregations (Hill et al . , 1976; Brower, 1985; Van Hook, 1993; Wells et al . , 1993). This allows them to take advantage of the presence of many males; population densities o f the first butterflies to recolonize summer habitat might be low enough to make it risky to migrate before mating.

A C K N O W L E D G M E N T S

We thank Don Alstad, Sarah Stai, and Liz Goehring for help making cages and rearing, dissecting, and observing butterflies; and Don Alstad, Carol Boggs, Dennis Frey, Sonia Altizer, Liz Goehring, Dann Siems, Christer Wiklund, and an anonymous reviewer for comments on earlier versions of the manuscript. Research was supported by NSF DEB-9220829 to K.S.O.

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The relationship between mating and oogenesis in monarch butterflies (Lepidoptera: Danainae)

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