How is Monarch Mating Behavior Different
From Other Butterflies,
and How Might This Behavior Have Evolved?
(see also Oberhauser and Frey
1999)
by 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
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during winter matings are likely to be superseded by subsequent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.
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
|
