How is Monarch Mating Behavior Different From Other Butterflies, and How Might This
Behavior Have Evolved?
(see also Oberhauser and Frey 1999)
Karen Oberhauser
University of Minnesota
And
Dennis Frey
Biological Sciences Department
California Polytechnic State University
San Luis Obispo, CA 93407 USA
dfrey@calpoly.edu
Abstract | Introduction |
Methods | Results |
Discussion | Acknowledgments |
References | Karen's Research Questions
Abstract
We studied two aspects of mating behavior in overwintering monarch butterflies:
their coercive courtship behavior, and the occurrence and timing of mating during
the overwintering period.
Approximately one third of male-female mating attempts resulted in coupling, and
the duration of attempts ranged from one second to over 30 minutes. About one quarter
of all attempts involved two males, and male-male attempts were as long as male-female
attempts. Mating attempts involving previously-mated females were longer than those
involving unmated females. Mating males were in poorer condition than roosting males,
and mating females in Mexico were larger than roosting females. We use a cost/benefit
model to interpret these results. We argue that the payoff of winter mating is probably
low for both sexes. There is a good chance that females will remate, and last-male
sperm precedence in monarchs means that sperm transferred during winter matings
are likely to be superseded by subsequent matings. From the female perspective,
the costs of mating (carrying the additional mass of a spermatophore and possible
physical damage) may not be offset by benefits of winter matings. We suggest that
females that could suffer the cost of a ruptured bursa copulatrix from mating too
often or too soon after a previous mating are likely to struggle longer in a subsequent
mating, and that males in poor condition are more willing to mate and thus incur
reduced future fitness since they have a smaller chance of surviving to mate later.
Males in Mexico may be selecting large females, although the prevalence of male-male
attempts argues that males are not very discriminatory. We propose that male coercion
in monarchs evolved in the context of overwintering. At overwintering sites, males
with low prospects for future reproductive success co-occur with females that have
little to gain by mating, but less to lose from unwanted matings than summer females
who face the pressure of needing to maximize time for oviposition.
Introduction
Male coercion
Mating behavior in monarchs, especially the coercive behavior of males, presents
a puzzle for biologists. This behavior has been described in detail elsewhere (e.g.
Pliske 1975, Boppré 1993, Van Hook 1993, Frey et al. 1998, Frey 1999). Briefly,
pre-copulatory courtship (behaviors that occur after
the male has located the female and before the pair has coupled or separated without
mating) has two phases. During the first phase males either pursue females in flight
or pounce on resting females. During the second phase the male is in physical contact
with the female and attempts to couple with her. The second phase can involve prolonged
contact, during which females often show resistance behavior (Frey 1999). Unsuccessful
mating attempts end when one individual leaves the attempt. Successful attempts
result when the female stops using resistance behaviors or when the male succeeds
in coupling with the female despite active resistance (Frey 1999). Copulations last
up to sixteen hours and females cannot end a copulation once it has begun (Oberhauser
1989b). Monarchs are one of only a few lepidopteran species in which coercive mating
has been described; most female Lepidoptera can reject courting males successfully
and quickly (review in Rutowski 1982). The monarch is also unusual among its close
relatives. Whereas most Danainae (milkweed butterflies) secrete pheromones (chemical
signals) from hairpencils and alar wing pockets, and engage in complex courtship
rituals, male monarchs employ a ‘take-down’ strategy in which ritual behaviors
and chemical cues appear to be unnecessary (Pliske 1975, Boppré 1993).
Courtship in the queen butterfly (Danaus gilippus). The male hovers over
the female, releasing pheromones in an attempt to convince her to mate with him.
Male queen butterflies, unlike monarchs, do not force females to mate.
Intersexual conflict over mating has attracted both empirical and theoretical attention
(e.g. Parker 1979, 1984; Hammerstein & Parker 1987, Clutton-Brock & Parker
1995, Choe & Crespi 1997). The conflict is manifested between individual males
and females when females try to reject males because they have already mated, or
could increase their fitness by mating with a different male or at a different time.
However, the outcome of intersexual conflict is an evolutionary one. Males have
won the evolutionary conflict when coercion, the use of force or threat of force
by males to overcome female reluctance to mate (Smuts & Smuts 1993), is a mating
strategy in a species. Once coercion evolves, females must either accept matings
that could have negative effects on their fitness, or engage in costly behavior
to reject males. Females have won the conflict when males respond to female signals
of non-receptivity by giving up courtship attempts. Male coercion generally either
occurs or doesn’t occur in species, even though individuals may differ in the
degree to which they use coercion as a mating strategy.
Figure 1a is a schematic presentation of the costs and benefits involved in matings.
Males should only attempt to mate with unwilling females if the benefits of mating
are likely to outweigh the costs. These benefits are the number and viability of
offspring that are likely to result from mating, and their magnitude depends on
female age, size and condition, and the probability and timing of female remating.
Young females in good condition are likely to lay more eggs than older females (Oberhauser
1997), whereas a subsequent mating by the female will result in decreased male fitness,
due to last-male sperm precedence (Whose sperm fertilize the
female’s eggs if she mates more than once?). The cost of mating for a
male is any decrease in future reproductive success that results from the mating.
Potential costs include lost time (while a male is mating with one female, he cannot
mate with another, possibly more receptive or fertile, female), the possibility
of contracting sexually transmitted diseases (e.g. Altizer et al. 1999,
Parasites and Natural Enemies), the male’s material investment, and increased
risk of predation during mating. Because costs are weighed against future reproductive
success, they will be relatively more important to males with higher future reproductive
potential; selection favors investment in current reproduction over conserving resources
for later reproduction when individuals have a low probability of surviving to reproduce
later (Williams 1966).
Females should struggle to avoid mating when the costs of mating outweigh the benefits
they expect to gain (figure 1a). Female benefits include the
sperm and nutrients passed in the spermatophore, and their magnitude will depend
on the amount of nutrients received, the female’s nutritional state, whether
she has eggs ready to fertilize, and possibly the male’s genetic quality. Potential
costs include the time involved in mating (during which she cannot lay eggs or nectar),
potential disease transfer, and risk of predation. In addition, females can suffer
costs from mating too often; they can actually be killed if they receive so much
spermatophore material that their bursa copulatrix ruptures (Oberhauser 1989a, Goehring
& Oberhauser unpublished).
Mating attempts have costs for both individuals (e.g. energy, wing damage, predation
risk, and time), which are separate from the costs of mating itself. The magnitude
of these costs should increase in a roughly linear way with the time spent in the
attempt. Males should desist in an attempt when its costs outweigh the expected
net benefit of mating. Females should stop struggling and give in to the male when
the costs of resisting the attempt outweigh the expected net cost of the mating
itself (for a game theory approach to this process, see Clutton-Brock & Parker
1995). The more the male balance is tipped to the left (higher benefit to cost ratio),
the longer the male should be willing to struggle to mate (figure
1b). The further the female balance is tipped to the right (higher cost to
benefit ratio), the longer the female should be willing to struggle (figure
1c).
Figure 1a. The male should attempt to mate, even if the female is unwilling, since
the benefits he would gain from mating outweigh the costs. The female should struggle
to avoid mating, since the costs she would incur outweigh the benefits. Potential
costs and benefits are represented in the figure (STD’s = sexually transmitted
diseases) 1b. Male 1 should be willing to persist longer in a mating attempt than
Male 2, since his benefits outweigh his costs by more. 1c. Female 1 should be willing
to struggle longer to avoid mating than Female 2, since her costs outweigh her benefits
by more.
Mating during the overwintering period
The timing of mating during the overwintering period presents an additional puzzle
for monarch biologists. Individuals in summer generations begin reproducing about
five days after eclosion (Oberhauser and Hampton 1995, Does
mating cause eggs to mature?), whereas reproductive tract development in the
late summer/early fall generation is minimal and most individuals will not mate
for several months (Herman 1985, Goehring and Oberhauser 1999, Diapause in monarch
butterflies). After a period of reproductive dormancy during the fall migration
and overwintering period, diapause is terminated and a mass mating period is followed
by remigration and reproduction in summer breeding grounds (e.g. Herman 1973, Brower
1985). Many of the hormonal and environmental cues that trigger these reproductive
changes have been determined (Barker & Herman 1973, Goehring & Oberhauser
1999). However, there is both between- and within-population variation in the timing
of diapause termination. The mass mating period in California appears to begin earlier,
relative to dispersal from the colonies, and involve more individuals and more matings
per individual than in Mexico (e.g. Tuskes & Brower 1978, Leong et al. 1995,
Van Hook 1996). Some individuals begin mating sooner than others at the overwintering
grounds (Van Hook 1993), and some mating occurs throughout the overwintering period
in both Mexico and California (Van Hook 1996, 1999). Since mating incurs costs for
both sexes, its occurrence days and even months before oviposition presents a puzzle.
Previous workers have addressed the puzzle of the timing of mating during the overwintering
period. Van Hook (1993) suggested that males in poor condition begin mating first
because they would have little chance of re-migrating. Alternatively, Wells et al.
(1993) proposed that large colonies are actually an adaptation that increases the
chances that females will survive the winter by facilitating nutrient transfer from
males to females. Male monarchs, like other Lepidoptera, transfer a protein-rich
spermatophore during mating (Spermatophores,
Boggs & Gilbert 1979, Oberhauser 1989a, 1992). The spermatophore is stored in
the bursa copulatrix, a muscular organ within the female (Rogers & Wells 1984),
and broken down by mechanical and chemical means into nutrients that have been traced
to both female somatic tissue and eggs (Boggs & Gilbert 1979, Wells et al. 1993).
Receiving nutrients from more than one male results in increased fecundity (Oberhauser
1989a, 1997, What factors affect the number of eggs that females
lay?), but male-derived nutrients have not been shown to increase survival
prospects for overwintering females.
Here, we argue that it is likely that sexual coercion by male monarch butterflies
evolved under the conditions experienced in the overwintering colonies, and that
the solutions to the puzzles of male coercion and mating during the overwintering
period are causally linked.
Continue to Methods and Results