How is Monarch Mating Behavior Different From Other Butterflies,
and How Might This Behavior Have Evolved?
(Continued)

Abstract  |  Introduction  |  Methods  |   Results  |  Discussion  |  Acknowledgments  |  References   |  Karen's Research Questions

Methods

We studied mating attempts in the Sierra Chincua colony (Calvert & Brower 1986) in Michoacan (Mexico) and Pismo Beach State Park (Frey & Leong 1993) in California (USA). The work took place 24 - 28 February 1996 and 28 February - 4 March 1997 in Mexico (about 3-4 weeks before colony dispersal, Van Hook 1996), and 17 January - 8 March 1996 in California. We observed 276 attempts in Mexico, and 348 in California. We have divided California observations into early (17 Jan - 12 Feb) and late (14 Feb - 8 Mar) attempts because important characteristics (e.g. sex ratio and female mating status) of the colonies change as the season progress. All of these times are during the mass mating period (Van Hook 1993), and our study thus excludes matings before this period.

We studied male-female (all sites and times) and male-male mating attempts (Mexico and late California only) on an opportune basis, waiting for pairs to fall to the ground after contact was made in the air or as the female was resting in the canopy. We timed the total ground phase duration of each attempt and recorded its outcome. In Mexico in 1997 and in California, we placed net cages over pairs so that we could measure several characters of both individuals when an attempt ended. In Mexico, these included right and left forewing length, wing condition (on a scale of 1-5, with one being pristine condition and 5 being the highest level of scale loss), the number of wings with pieces missing (0-4), and an estimate of abdomen girth (on a scale of 1-3, with 1 being emaciated and 3 being very fat). We estimated whether the female had mated previously using abdominal palpation and assigned each female a value of 0 (no spermatophore felt), 1 (a small amount of spermatophore material), or 2 (a large amount of spermatophore material). This technique does not allow us to determine how many times the female has mated, but we can distinguish unmated females from mated females, and females with more than 25-30 mg of spermatophore material in their bursa from those with less material (Oberhauser unpublished, Van Hook 1999). Since spermatophore transfer generally does not begin until nightfall (Svärd & Wiklund 1988, personal observations), our palpations assessed previous matings, not the current one. We also used a non-destructive technique (Altizer et al. 1999, Parasites and natural enemies) to determine whether individuals were infected with the parasite Ophryocyctis elektroscirrha. All butterflies in Mexico were then released. In California, we measured wet mass, right forewing length, the number of damaged wings, and the mass and number of spermatophores (see Frey et. al 1998) in female bursae for 122 pairs that were collected and immediately frozen. If we did not observe the beginning of an attempt, we recorded its outcome and the above individual characteristics, but not the total duration.

We compared the above characteristics of mating individuals to butterflies that were roosting in the trees at the same time and in the same sites. These measurements were made at Sierra Chincua in Mexico in late February and early March, 1996 and 1997, and February 1-6, 1997 at the Ellwood, San Leandro Golf Course, Moran Lake, Morro Bay Golf Course, and Pismo Beach sites in California. We did not compare mating and roosting butterflies late in the winter in California.

Results

There were no effects of year on attempt duration in Mexico, so duration data from 1996 and 1997 are combined. The numbers of attempts observed in each location, and summary statistics on these attempts, are shown in Table 1. The likelihood of successful attempts does not differ with location and time (C ² = 1.90, d.f. = 2, p = 0.386); approximately one third of all male-female attempts result in a mating. The duration of successful and unsuccessful attempts were not significantly different in Mexico, but successful attempts were longer late in the season in California. Male-male attempts made up about one fourth of all attempts in Mexico and late in the season in California (we did not record male-male attempts early in the season in California), and their duration was statistically indistinguishable from heterosexual attempts.

Table 1. Success rate and duration of mating attempts

All durations are given in seconds. Summary statistics on % successful and median durations refer to male/female attempts only. M/M = male/male attempts. We report median durations of attempts due to their skewed distribution (see figure 3). Durations followed by the same letters do not vary at the 0.05 level of confidence (ANOVA of log duration, Bonferroni test).

In California, the mass of the intact bursa copulatrix was positively correlated with the log of attempt duration (n = 122; Spearman Z = 2.2, p = 0.028). In Mexico, durations were longer when attempts involved females in which we palpated a spermatophore (Kruskall-Wallis one-way ANOVA of log duration on female mating status; mean rank unmated females = 16.6, mean rank mated females = 24.0, F = 4.53, p = 0.03, n = 36; figure 2). There was no relationship between duration and female abdomen size, wing condition, or spore load in Mexico; or between duration and female mass, forewing length, or wing condition in California. There were no associations between any of the above traits in males and attempt duration in either Mexico or California.

Figure 2. Distribution of mating attempt durations on a log scale. Successful and unsuccessful attempts are combined for each location, and only male/female attempts are shown. Each point represents the proportion of attempts in a given location that lasted at least the number of seconds shown.

We also looked for associations between characteristics of individuals involved in attempts and the outcome of the attempts. There were no differences between individuals involved in successful and unsuccessful attempts in either location or in either sex.

Table 2 compares mating and roosting butterflies. 1996 and 1997 data from Mexico are combined, since there were no year effects on any measured characteristics. In Mexico, mating males had smaller wings, higher levels of wing damage and wing wear, smaller abdomen girth, and higher incidence of O. electroskirrha infection. In California, mating males were also smaller and more likely to be parasitized than roosting males. Mating males in California tended to have greater wing wear and damage than roosting males, but these differences were not statistically significant. Mating females in Mexico had longer wings than roosting females, and there was a marginally significant tendency for more mating females to have already mated than roosting females. There were no differences in wing condition between mating and roosting females. None of the characteristics we measured differed between mating and roosting females in California.

Table 2. Comparison of monarchs collected mating and roosting

Sample sizes for Mexico: 145 mating and 188 roosting males, 145 mating and 236 roosting females; for California: 86 mating and 154 roosting males, 86 mating and 73 roosting females. "Infected" butterflies had a spore load of 4 or 5 (see Parasites and natural enemies). Forewing is the length of the left forewing in mm. See text for explanation of other characteristics.

Figure 3 shows the distribution of attempt duration (successful and unsuccessful combined, male-female only) in both locations. There is a highly skewed distribution that approximates a negative exponential; most attempts last less than a minute, but some persist for several minutes.

Figure 3a. Relationship between attempt duration (in California) and the mass of the female bursa copulatrix. Females with more material in their bursa are involved in significantly longer attempts. 3b. Box and whisker plot of attempt duration for mated and unmated females in Mexico (mating status determined by abdominal palpation). The boxes enclose the middle half of the data, lines bisect boxes at the median value, and whiskers indicate the range of data.

Discussion

Male coercion in monarch butterflies

The duration and outcome of individual mating attempts in monarchs is affected by how long each individual is willing to persist in its attempt to mate (the male), or not mate (the female). In general, when the male is willing to persist longer, the attempt should result in a mating. Persistence time could be affected by whether assessment by either sex occurs during the struggle. If females use the attempt to assess male quality, they may persist longer with low quality males to avoid matings that could result is less fit offspring. Males might persist longer with high quality females.

The duration and outcome of mating attempts will also be affected by the degree to which each individual controls the struggle. A male clearly has control over an attempt if he forces an actively resisting female to mate. However, when the male ends an attempt without mating, it is difficult to determine which individual controlled the outcome. The male has control if he deserts or rejects a poor quality female. However, a male may also end an attempt because he has reached his persistence limit. In this case, the female has controlled the struggle because she has outlasted the male. One way to help distinguish between male and female control of unsuccessful attempts may be to assess female characteristics. In the case of male control, we would predict that short, unsuccessful attempts should be more common with poor condition females since these females should be most likely to be rejected. We would not expect the same relationship between duration and female condition if females control attempts by outlasting males.

Females clearly have control over attempts if they escape from the male. A successful mating, however, could result from female control if the female chooses or accepts the male because he is of high quality, or from male control if she accepts the mating simply because she has reached her persistence limit. As above, these two possibilities predict different associations between male traits and attempt duration and outcome. If females choose males, short, successful attempts should be more likely with males in good condition.

This study sheds light on how these factors might interact in monarch butterfly mating. Here, we argue that males and females weigh the costs and benefits of mating with little regard to the quality of their potential partner, and that the cost side of the cost/benefit balance is most important to both sexes.

Males with low prospects for future reproductive success, and thus a lower cost of mating, were more likely to be mating during the times that we studied overwintering monarchs. Those in poor condition (more wing damage, higher levels of infection by O. electroskirrha, and smaller abdomens) were over-represented in the mating pool, as were small males (table 2, see also Van Hook 1993, Frey et al. 1998). It is likely that these males would not survive to re-migrate (Alonso 1996), and even if they did, could be at a disadvantage during migration (Van Hook 1993, 1996). The fact that late-season mating attempts in California are longer than earlier ones (table 2, figure 3) supports our cost/benefit explanation, since future reproductive potential should be negatively correlated with male age. The lack of relationship between any potential measure of female quality and attempt duration suggests that the benefits that males can expect to incur from mating do not affect the time they are willing to struggle. However, longer struggles late in the season in California could result from higher expected payoffs to males; egg laying is likely to occur sooner after late season matings due to host plant availability.

Figure 4a illustrates the cost/benefit trade-off for overwintering males. M1, M2 and M3 represent males in progressively poorer condition. We have set the benefits of mating equal for all three males, but the costs they would incur differ due to variation in future prospects. M1 should delay mating until it would result in higher payoffs, but the net value of mating is positive for M2 and M3, since their future prospects are lower. M3 should struggle longer than M2, since he has the least to lose.

Figure 4a. Male 1 should not attempt to mate, since his costs outweigh his benefits. Male 2 will try to mate, but not for very long, since he would gain only a small net benefit from mating. Male 3 should be willing to struggle for longer. Each male expects to gain the same benefits, but they pay different costs in terms of compromised future reproductive success. They could represent overwintering males in progressively poorer condition. 4b. Female 1 should struggle to avoid mating, but not for long, since the costs of mating do not outweigh the benefits by much. Female 2 would benefit from mating, so should not struggle. Females 1 and 2 could represent unmated females (hence low cost of mating) in overwintering and breeding populations, respectively. Female 3 should struggle harder to avoid mating, since she would suffer a large net cost; she could represent a mated female in an overwintering population.

The fact that previously-mated females and females with more material in their bursae were involved in longer attempts (figure 2) suggests that costs of mating are also important to females. Mated females can incur a ruptured bursa copulatrix that will result in death when they remate (Oberhauser 1989a, Goehring & Oberhauser unpublished). We propose that this cost makes mated females willing to struggle to avoid mating. This, along with decreased costs of mating for late-season males (see above), could explain the longer late-season mating attempts in California (table 1), when more females have mated (Leong et al. 1995, Frey et al. 1998). Another possible, but untested, cost for females is the additional weight of an unnecessary spermatophore during re-migration. Several lines of evidence suggest that the benefit side of the cost/benefit trade-off is not important to overwintering females. Females might be expected to benefit most from mating with a large male in good condition, due to a larger nutrient donation (Oberhauser 1988), or because these males might transmit higher fitness to their offspring (e.g. Charlesworth 1987). However, male condition was correlated with neither the duration nor the outcome of attempts (see also Van Hook 1993), and mating males represented a small, poor-condition subset of the male population (table 2, Van Hook 1993, Frey et al. 1998). Another benefit that may be important to female is the male nutrient donation; Wells et al. (1990, 1993) suggested that an increase in female lipid reserves in late winter was due to male-derived nutrient. However, Van Hook (1996) presents evidence that increased female lipid levels are not due to the observed level of mating, but instead are more likely to result from differences in energy budgets or nectaring behavior (Van Hook 1996 and personal communication). Additionally, if male-derived nutrients are important, thin females should be over-represented in the mating pool, since they should benefit most from receiving lipids from males. If anything, the opposite is true (table 2, Van Hook 1993). Finally, it is probably not critical that females obtain sperm during the overwintering period, since they are likely to have ample opportunity to mate when they are ready to lay eggs.

Our results suggest that males do not have complete control over the outcome of mating, as previously implied by many authors (Urquhart 1960, Pliske 1975, Rothschild 1978, Van Hook 1993). Females often exhibit behaviors that decrease the likelihood that the attempt will end in coupling (Frey 1999), and approximately 70% of all attempts do not end in coupling (table 1 and Frey 1999). In addition, male mate choice does not appear to be important during mating attempts. The only female characteristic correlated with attempt duration was mating history, with mated females more likely to be involved in long attempts. If anything, mating with a previously-mated female might be expected to result in lower payoffs due to sperm competition. Traits that might indicate female quality, such as size (e.g. Oberhauser 1997, Alonso et al. 1997) and wing condition, were not correlated with attempt duration or outcome (see also Van Hook 1993). The fact that mating females were larger and fatter than roosting females in Mexico (table 2, Van Hook 1993) could result from variation in female activity or apparency, or active male discrimination (see Van Hook 1993). In any case, the duration and frequency of male-male attempts suggests that males do not carefully assess their partners before or during attempts.

Overwintering and the evolution of male coercion

Boppré (1993, p. 38) said that "we have as yet no meaningful hypothesis as to what might have caused the American monarchs to adopt such a modified mating strategy." We suggest that this strategy evolved in the context of overwintering, in which there is a prolonged adult non-reproductive period followed by costly re-migration. Male coercion should only evolve when the net gain to males of mating with reluctant females is greater than the net loss of unwanted matings to these females. If this condition is not met, selection on females to avoid mating will be stronger than that on males to mate, and females should evolve effective ways to avoid unwanted matings (e.g. Parker 1984). We propose that it is in the context of overwintering that this condition is most often met. At the overwintering sites, especially at the end of the season, many butterflies have used much of their lipid reserve, and there is little chance that they will survive to re-migrate and reproduce (Wells et al. 1993, Alonso et al. 1997). When this is true of males, their best strategy may be to attempt to mate at the overwintering sites. Even though the fitness gains they can expect from these matings are likely to be low, their poor condition means that the net benefit of mating will be relatively high. The fact that sperm survive for several weeks in the female (Oberhauser 1997) means that there is a chance that some sperm from early matings may be used to fertilize eggs once females become reproductive.

Females may not gain a great deal from winter matings, but they also may not lose a great deal, unless they have a large amount of spermatophore material already present in their bursa copulatrix. We suggest that overwintering females are, in general, reluctant to mate because they receive few benefits, and incur some costs. Thus, many overwintering females are like F1 in figure 4b; they do not struggle very long because the costs of the struggle soon outweigh the costs of mating. In the summer, females are more likely to either benefit from mating (since they use sperm and male-derived nutrients in reproduction, e.g. F2), or to incur very high costs, since mating when they need neither sperm nor nutrients results in a cost of lost time for egg-laying in addition to the risk of a ruptured bursa copulatrix (e.g. F3). The condition required for the evolution of male coercion may not be met often in the summer when females are more likely to be either willing to mate or would lose a great deal by mating. We propose that the overwintering co-occurrence of females with cost/benefit balances like F1 and males like M3 in figure 4 fulfill this condition. It is only in the overwintering colonies that reluctant, but fertilizable females with little to gain by mating, but often relatively little to lose either, co-occur with males with few future reproductive options. Once coercion evolved in this species, it became a mating strategy that was used in both overwintering and summer generations, and the dependence on chemical cues was lost.

Future research directions and implications for conservation

Many predictions of our hypothesis are untested, and we would like to suggest research directions for monarch biologists interested in reproductive behavior. Our hypothesis predicts that payoffs to either sex from mating during the overwintering period will be low, but almost nothing is known about these payoffs. They will depend on the magnitude of nutrient donations by overwintering males, the ability of females to utilize male-derived nutrients for increased survival or fecundity, mating opportunities for females after they leave the overwintering colonies, and the extent to which females use sperm received during the overwintering period. In addition, we do not know the proximate causes for the variation in the timing of mating among males, nor the relationship between oogenesis and female mating in the overwintering colonies. Finally, we need to make the same kinds of observations as described above and by Frey (1999) in breeding populations, even though low population densities will make these observations more difficult.

Our results and proposed research directions may seem to have little relevance to conserving this amazing butterfly and the endangered phenomenon of its migration (Brower & Malcolm 1991), but we argue that they do. If our hypothesis is correct and mating in the winter is costly to females, increased mating frequency will result in decreased average female fitness, and the health of a population will suffer if mating by overwintering butterflies becomes more common. Males in poor condition are overrepresented in the overwintering mating pool (Van Hook 1993, Frey et al. 1998, this study), suggesting that a decrease in average male condition is likely to lead to more early mating. The frequency of mating during the overwintering period may be both an indicator of overall population health and a cause of compromised population health; there may be a cascading series of linked conditions beginning with compromised male condition leading to increased mating in the overwintering colonies, decreased female fitness, and finally a compromised spring re-migration. This suggests another productive avenue for future research—determining why mating occurs with greater frequency in California overwintering sites, and how mating affects the timing of female dispersal. The above scenario would predict that butterflies in the western population are in poorer condition. They certainly have higher parasite burdens (see Parasites and natural enemies), and it could also be that warmer average conditions throughout the overwintering period accelerate lipid use and butterfly aging (Chaplin & Wells 1982, Alonso et al. 1997). In any case, it is possible that the increasingly male-biased sex ratios in California colonies result from females leaving the colonies sooner that they would otherwise due to male harassment. We do not know where females go when they depart from the colonies, nor how fitness is related to the timing of female departure.

Many factors will affect male condition, including the abundance and quality of larval food supply, nectar availability during the fall migration, and conditions in the overwintering sites. These factors are likely to be linked in a myriad of ways to overall population health, making every bit of knowledge potentially important in informing monarch conservation efforts.

Acknowledgements

We thank Sonia Altizer, Lisa Falco, Liz Goehring, Kari Geurts, Eneida Montesinos-Patiño, Michelle Prysby, Eduardo Rendon-Salinas, and the docents at Pismo Beach State Park for help in the field; members of Ejidos Los Remedios and Cerro Prieto for access to their land in Mexico; the California Parks and Recreation Department, California Polytechnic State University, and the National Science Foundation (ESI 9554476 to KO) for financial support; Stuart Wagenius for suggesting the balance; Tonya Van Hook, Kingston Leong, and Steven Price for helpful comments on the manuscript; and the Commission on Environmental Cooperation, the Organizing Committee for the North American Monarch Butterfly Conference, and attendees of this conference for providing a stimulating and productive venue for understanding issues connected with monarch butterfly conservation.

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