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Behavioral Ecology Vol. 11 No. 2: 220-227
© 2000 International Society for Behavioral Ecology
Female spadefoot toads compromise on mate quality to ensure conspecific matings
Department of Ecology, Ethology, and Evolution, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA
Address correspondence to K. S. Pfennig at the Department of Biology, CB#3280, Coker Hall, University of North Carolina, Chapel Hill, NC 27599-3280, USA. E-mail: kpfennig{at}email.unc.edu .
Received 10 February 1999; revised 27 August 1999; accepted 4 September 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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When high-quality conspecifics resemble heterospecifics, females may be unable to engage effectively in both species recognition (identification of conspecifics) and mate-quality recognition (identification of high-quality mates). Consequently, females that engage primarily in mate-quality recognition may risk heterospecific matings, and females that engage primarily in species recognition may risk mating with low-quality mates. I examined the evolutionary consequences of this conflict between species and mate-quality recognition in spadefoot toads, Spea multiplicata. I compared mate preferences and the fitness consequences of these preferences in spadefoot toad populations that did and did not overlap with congeners. In non-overlapping populations, S. multiplicata females preferred an extreme call character resembling that of heterospecifics, and they had more eggs fertilized. In overlapping populations, S. multiplicata females preferred those call characteristics that were closest to the norm for their population, and they did not receive the benefit of enhanced fertilization success. Thus, S. multiplicata females appear to trade off species and mate-quality recognition, such that those co-occurring with heterospecifics forgo the benefits of high-quality matings to ensure conspecific matings. These results suggest that the interaction between species and mate-quality recognition may influence mate choice decisions in important and nonintuitive ways.
Key words: mate choice, mate-quality recognition, species recognition, Scaphiopus couchii, Spea bombifrons, Spea multiplicata.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Mate choice often requires that individuals engage in both species recognition (identification of conspecifics) and mate-quality recognition (identification of high-quality mates) (Sherman et al., 1997
).
Because the types of traits used for each form of recognition potentially
differ, a conflict may often exist between species and mate-quality
recognition (Gerhardt, 1982;
Pfennig, 1998;
Ryan and Rand, 1993). This
potential for conflict has important implications for the evolution of mate
choice.
Females potentially face a conflict between species and mate-quality
recognition whenever high-quality conspecifics resemble heterospecifics. To
illustrate this conflict, consider that when engaging in mate-quality
recognition, females often prefer those males with the most extreme secondary
sexual characters (reviewed in Andersson,
1994; Ryan and Keddy-Hector,
1992). Because such traits are often costly to produce, they
potentially serve as reliable signals that a male is of high quality in that
he can provide either direct fitness benefits to the female or indirect
fitness benefits to her offspring (reviewed in
Andersson, 1994; e.g.,
Møller, 1990;
Petrie, 1994;
Reynolds and Gross, 1992).
However, preferences for extreme traits may increase the likelihood that a
female will mistakenly mate with heterospecifics, if heterospecifics resemble
high-quality conspecifics (Gerhardt,
1982; Pfennig,
1998; Ryan and Rand,
1993). In contrast, when engaging in species recognition, females
often prefer those males with secondary sexual characters closest to the
population norm, presumably because such traits may best indicate species
identity (Andersson, 1994;
Gerhardt, 1991;
Pfennig, 1998; e.g.,
Butlin et al., 1985;
Gerhardt, 1991;
Kyriacou and Hall, 1982;
Waage, 1975). However,
preferences for average traits may prevent females from identifying
high-quality mates if these traits do not reliably indicate quality. Thus,
when high-quality conspecifics resemble heterospecifics, females that engage
primarily in mate-quality recognition risk heterospecific matings, and females
that engage primarily in species recognition risk matings with relatively
low-quality males (Gerhardt,
1982; Pfennig,
1998; Ryan and Rand,
1993).
To mitigate this conflict between species and mate-quality recognition,
selection should favor female preferences that minimize the costs and
likelihood of mistakenly mating with heterospecifics or low-quality
conspecifics (Pfennig, 1998).
As a result, females may engage in one form of recognition at the expense of
the other. For example, females that do not co-occur with heterospecifics may
prefer extreme secondary sexual characters and benefit by selecting
high-quality mates. Females co-occurring with heterospecifics, in contrast,
may prefer typical values and therefore possibly forgo the fitness benefits of
high-quality matings.
My study was designed to evaluate the above prediction in southern spadefoot toads (Spea multiplicata). I first asked whether secondary sexual characters (male calls) of S. multiplicata resembled those of two closely related sympatric species with which S. multiplicata occasionally mismates. I then compared mate preferences and the fitness consequences of these preferences in S. multiplicata populations that did and did not overlap with congeners. The results indicate that S. multiplicata females do indeed face a conflict between species and mate-quality recognition. The results further suggest that the interaction between these two processes may influence the evolution of mate choice in important and nonintuitive ways.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study species, field sites, and laboratory culture
Spea multiplicata co-occurs with the plains spadefoot toad, Spea bombifrons, and Couch's spadefoot toad, Scaphiopus couchii, in southeastern Arizona, USA, although S. bombifrons is restricted to lower elevations (Simovich, 1985
). Mismatings occasionally occur between all three species
(Pfennig KS, personal observation;
Simovich, 1985). Matings
between the Spea species are more common (10-30% of matings may be
mismatches; Pfennig KS, personal observation;
Simovich, 1985) because these
species usually occur in the same breeding aggregations. Matings between the
Spea species produce sterile males and females that are less fecund
than either parent type (Simovich,
1985). Matings between S. couchii and Spea are
rare (Pfennig KS, personal observation), in part because S. couchii
does not always occur in the same breeding aggregations with Spea.
When matings between S. couchii and Spea do occur, they
produce inviable eggs (Tinsley RC, personal communication).
Female spadefoots have ample opportunity to choose mates (Pfennig KS,
personal observation; Sullivan and
Sullivan, 1985; Tinsley,
1990) and can use male call features to assess species identity
and quality of potential mates. In other anuran species, females use
species-specific values of call pulse rate (number of pulses within a call per
second; Gerhardt, 1988,
1991) or call frequency
(Gerhardt, 1988;
Rand et al., 1992) to identify
conspecific mates. They also use characters such as long call duration
(Gerhardt, 1988;
Taigen and Wells, 1985;
Welch et al., 1998), fast call
rate (Bevier, 1997;
Cherry, 1993;
Gerhardt, 1988;
Grafe, 1996;
Prestwich et al., 1989;
Taigen and Wells, 1985) and
frequency as indicators of male quality
(Robertson, 1990;
Ryan, 1980). Call frequency
can be used to indicate body size
(Robertson, 1990;
Ryan, 1980), and both long
call duration and fast call rate require greater investment of energy into
calling (Bevier, 1997;
Cherry, 1993;
Grafe, 1996;
Prestwich et al., 1989;
Taigen and Wells, 1985),
thereby potentially serving as reliable indicators of male quality
(Cherry, 1993;
Grafe, 1996;
Welch et al., 1998).
I conducted field research near the American Museum of Natural History's Southwestern Research Station at Portal, Arizona, USA, where all three spadefoot species co-occur. In addition, S. multiplicata females were collected from the Altar Valley, Arizona, where S. bombifrons does not occur (area of allopatry; Figure 1).
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Females used in phonotaxis experiments were transported to the University of Illinois or the University of North Carolina. There they were housed in 4-1 buckets filled with dirt and fed nutrient-dusted crickets ad libitum. The animals were housed under a reverse light-dark cycle of 14 h light:10 h dark. During the fall months, the temperature in the room was cooled from a holding temperature of 25.6°C to approximately 17°C. The cooler temperatures were maintained for approximately 3 months, then returned to 25.6°C. All phonotaxis experiments were conducted during the spring following this cool-down period.
Male call characters
Males of all three spadefoot species, along with several S.
bombifrons x S. multiplicata hybrid males, were recorded
in 2 separate years at four natural mixed-species ponds. I also recorded the
pond temperature in which the males were calling because temperature can
affect male call characters. I analyzed the recordings of the calls using
sound analysis software to determine call rate, call pulse rate, call dominant
frequency, and call duration for each species. Where temperature affected a
call character, the characters were corrected to 20.4°C (the most common
recording temperature) based on the regression relationship between
temperature and the call character (Sokal
and Rohlf, 1995; e.g.,
Gerhardt, 1991;
Wagner and Sullivan,
1995).
Phonotaxis experiments
To determine what aspect (if any) of conspecific calls S.
multiplicata females prefer, I collected females from both areas of
sympatry and allopatry (i.e., where S. bombifrons is absent;
Figure 1). Using these females,
I then conducted two-speaker phonotaxis experiments in which females were
presented alternative calls using standard procedures (e.g.,
Gerhardt, 1991;
Wagner and Sullivan,
1995).
Each female was initially placed in the center of a wading pool equidistant
between two speakers set 180° and 1.4 m apart. From each speaker I
broadcast one of two stimuli (see below). Each female was initially placed in
an opaque container for an acclimation period of 15 min. I began to play the
stimuli at the start of this interval. At the end of the acclimation interval,
the female was released and allowed to move freely about the pool, while the
stimuli continued to play. Each female was watched continuously by a hidden
observer for 30 min or until she approached within 10 cm (approximately two
body lengths) of a speaker, whichever came first. Upon release, most females
spent time orienting their head or body toward a speaker before actually
approaching the speaker (i.e., females did not move randomly through the arena
until they bumped into a speaker). I scored a female as preferring a stimulus
when she approached the speaker broadcasting that stimulus (e.g.,
Gerhardt, 1991;
Wagner and Sullivan, 1995).
This is an appropriate bioassay of female mate preference because spadefoot
females initiate amplexus by closely approaching and/or touching a male
(Pfennig KS, personal observation). If a female had not approached a speaker
within the 30-min observation interval, the female was considered
nonresponsive and excluded from analysis.
In four separate experiments, I presented the sympatric S. multiplicata females with the following alternative call types differing in only one parameter: high versus low dominant frequency calls (see below for stimuli values used), long (1.26 s) versus short (0.91 s) duration calls, average (25.2 pulses/s) versus fast (26.4 pulses/s) call pulse rate, and average (31 calls/min) versus fast (37 calls/min) call rate. In each experiment, all call features (including volume) were kept constant at typical conspecific values, except for the character being manipulated.
To create the sound stimuli for each experiment (except dominant frequency, see below), I randomly chose 3-10 S. multiplicata calls from a collection of digitized recordings (from the recordings above). Each call was then manipulated using sound editing software to create the alternative stimuli given above. In the case of the dominant frequency experiment, three sets of two calls (i.e., calls from six different males) were chosen from the digitized recordings. Two of these sets consisted of male calls at 1.25 kHz and 1.42 kHz, and a third set consisted of alternative male calls at 1.22 kHz and 1.38 kHz. These calls were then manipulated so that they consisted of typical species values for all other call characters. For each experiment (except for the call rate experiments), the manipulated calls were then repeated onto separate tracks of an audio tape at an average call rate. Thus, females presented a given tape heard alternative versions of the same male's call (except in the case of dominant frequency).
The females were randomly assigned to three to ten approximately
equal-sized groups of 6-18 females. The number of groups and the number of
females within groups depended on the experiment and the number of females
available for testing when the experiment was conducted. I injected females
with 0.1 ml 36.0 µg/ml luteinizing hormone-releasing hormone to bring them
into reproductive condition (e.g.,
Semlitsch and Schmiedehausen,
1994). I tested the females in each experiment within 12 h of
injection once they were in reproductive condition (eggs were readily visible
through the skin of their abdomens). Each female within a group was tested on
the same day and was presented the same tape. Thus, all females in a given
experiment were presented the same stimuli sets (except dominant frequency;
stimuli values are given above), but the male call that was used in making
those stimuli differed between the groups. This procedure of presenting
multiple representations of the stimuli ensured that females were responding
to the values of the call stimuli per se rather than to an uncontrolled
variable in a natural male recording
(Kroodsma, 1989).
All of the above stimuli values were within the natural range of variation for sympatric S. multiplicata males and were appropriate for the temperature (20.6°C) at which the females were tested. High and low values represented extremes within this range of variation for a given character. Females were used only once for a given set of stimuli. I switched the stimuli between speakers after each female to control for position effects.
I also tested 18 allopatric S. multiplicata females for their preferences of call rate. These females were presented the same average versus fast call rate stimuli as given above. They were not tested for any other stimuli.
I analyzed the preference data for each experiment by first determining if females could be pooled across groups using heterogeneity chi-square tests. Where there was no significant heterogeneity among groups, I pooled all of the females and, using log-likelihood ratio (G) tests, determined if female preferences deviated from 1:1 random expectation.
Benefits of female mate choice
To determine if S. multiplicata females benefited from mate choice
when S. bombifrons were absent but not when they were present, I
collected S. multiplicata pairs (before gamete release) from a high
elevation, pure-species pond (~1650 m elevation) and from three lower
elevation, mixed-species ponds (~1200 m elevation) within 10 km of each
other near Portal, Arizona (S. bombifrons does not occur above 1500 m
elevation; Simovich, 1985).
The pairs were separated and the male designated as that female's
"preferred" mate. Unmated calling males from the same breeding
aggregation were collected and designated "nonpreferred"
males.
I brought these animals into the laboratory and placed each female in
13.5-1 dechlorinated water with either her preferred mate or a randomly chosen
nonpreferred male from her breeding aggregation (order randomized). After each
female released half her clutch (Spea have external fertilization), I
separated her from her first mate, rinsed her with water to remove residual
sperm, and placed her with her second mate. Once mating was completed, I
counted the proportion of fertilized eggs (the animal pole of fertilized eggs
rotates upward and is easily identified with the unaided eye;
Nace et al., 1974). I compared
the proportions of each female's eggs fertilized by preferred and nonpreferred
males using two-tailed paired t tests.
I removed a random subset of hatchlings from each clutch and reared them to
metamorphosis in 1.8-m diameter wading pools
(Pfennig et al., 1991). Within
each wading pool, I placed two mesh-sided boxes (1 mx0.7 mx0.2 m)
containing 25 offspring from the same female sired by either her preferred
male or a nonpreferred male. This density fell within the range of densities
in natural ponds (Pfennig et al.,
1991). I fed tadpoles in each box rabbit chow three times for a
total of 10.59 g, thereby simulating detritus on which tadpoles feed in
natural ponds (Pfennig et al.,
1991). This food amount was low and was meant to maximize
potential differences between the offspring of preferred and nonpreferred
males. I measured age, mass, and snout-vent length at metamorphosis and
calculated mean values per box. These measures are important because age and
size at metamorphosis correlate with adult survival in this species
(Pfennig et al., 1991). I then
compared these measures for the offspring of preferred males versus those of
nonpreferred males using two-tailed paired t tests.
I measured the mass and snout-vent length of the preferred and nonpreferred
males. I controlled for snout-vent length in these mass measurements by
correcting mass to the average male snout-vent length using the regression
relationship between mass and snout-vent length
(Sokal and Rohlf, 1995). This
technique allowed me to compare mass for a given body size between preferred
and nonpreferred males and allowed me to assess male condition (heavier males
for a given body size are likely to have greater energy stores, a potential
indicator of male condition). Larger, heavier males may produce better quality
offspring (Reynolds and Gross,
1992; Woodward,
1986), better quality sperm, or higher sperm counts
(Berrigan and Locke, 1991;
Pitnick and Markow, 1994).
I repeated the collection and pairing procedures with S. bombifrons from two mixed-species ponds where the S. multiplicata were collected. The proportion of fertilized eggs was counted for females paired with their preferred mates and with the nonpreferred males as for S. multiplicata. However, the offspring from these crosses were not reared to metamorphosis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Male call characters
Spea multiplicata calls overlap with at least one other species for two call characters: call duration and call dominant frequency (Figure 2). Two other call characters, call pulse rate and call rate, are distinct among all three species and the hybrid males (Figure 2).
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Phonotaxis experiments
Sympatric S. multiplicata females did not express any clear
preference for an extreme value of either call duration (CD) or dominant
frequency (DF). Of the 30 females presented the dominant frequency stimuli, 27
responded by approaching one of the two stimuli. There was significant
heterogeneity among the three S. multiplicata female groups tested
for dominant frequency (
2 = 7.24, df = 2, p <.05),
so that females could not be pooled across groups. One group of females
(presented 1.25 kHz versus 1.42 kHz) showed significant preference for high DF
(seven preferred high DF, whereas one preferred low DF; G = 5.06, df
= 1, p =.025). However, the remaining groups did not show this
tendency to prefer high DF. The second group (presented 1.25 kHz versus 1.42
kHz) was evenly split (five preferred high DF and five preferred low DF) and
the third group (presented 1.22 kHz versus 1.38 kHz) showed the opposite trend
(two preferred high DF and seven preferred low DF; G = 2.94, df = 1,
p =.086).
Of the 31 sympatric S. multiplicata females tested for their
preferences of call duration, 29 responded to the test. There was no
significant heterogeneity among the female groups tested for call duration
(2 = 7.89, df = 4, p >.05), so the groups were
pooled for analysis. These females were nearly evenly split between the long
and short call duration stimuli: 13 females preferred long CD and 16 preferred
short CD.
In contrast to the results for dominant frequency and call duration, S.
multiplicata females expressed clear preferences for values of pulse rate
and call rate. Of the 42 sympatric S. multiplicata females tested for
their preferences of pulse rate, one female did not respond and was excluded
from analysis. The females were pooled across groups for analysis
(heterogeneity 2 = 2.02, df = 2, p >.25). These
S. multiplicata females preferred calls with an average pulse rate to
those of a fast pulse rate (27 females preferred average pulse rate versus 14
that preferred fast; G = 4.19, df = 1, p =.041).
Spea multiplicata females also expressed a preference for call
rate, but whether females preferred average or fast call rate depended on
whether they were from populations in sympatry or allopatry with S.
bombifrons (Figure 1). Of
18 allopatric S. multiplicata females presented the alternative call
rate stimuli, all responded and were pooled across groups for analysis
(heterogeneity 2 = 0.48, df = 2, p >.75). These
females showed a significant preference for conspecific calls at the faster
than average call rate (Figure
3). In contrast, S. multiplicata females from sympatry
significantly preferred the average call rate stimulus to the faster than
average call rate stimulus (Figure
3). Of the 67 sympatric S. multiplicata females available
for testing, 54 approached one of the two call rate stimuli (13 were
nonresponsive and excluded from analysis). These females were pooled across
groups for analysis (heterogeneity 2 = 11.08, df = 9,
p >.25). Thus, preferences by S. multiplicata females for
call rate significantly differed in sympatry and allopatry
(Figure 3): females in
allopatry preferred extreme values of call rate, whereas females in sympatry
preferred average values of call rate.
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Benefits of female mate choice
Preferred (P) S. multiplicata males did not sire larger or faster
developing offspring than did nonpreferred (NP) males at either the pure- or
mixed-species ponds (Table 1).
However, in the pond where S. bombifrons was absent, S.
multiplicata females had significantly higher fertilization success with
preferred males than with nonpreferred males
(Figure 4), receiving 3.5% more
offspring with their preferred mates. Moreover, these preferred males tended
to be heavier for a given body size and were therefore likely in better
condition than the nonpreferred males
(Figure 5). In contrast, S.
multiplicata females from the three mixed-species ponds did not receive
this benefit; there was no difference between preferred and nonpreferred males
in terms of ability to fertilize a female's clutch
(Figure 4) or in terms of mass
(Figure 5).
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Contrary to the S. multiplicata females from the mixed-species ponds, S. bombifrons females had considerably higher fertilization success with their preferred mates as opposed to nonpreferred males (Figure 4). Moreover, preferred S. bombifrons males tended to be heavier for a given body size than the nonpreferred S. bombifrons males (although the difference was not significant; Figure 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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I compared mate preferences and the fitness consequences of these preferences in spadefoot toad populations that did and did not overlap with congeners. In non-overlapping populations, S. multiplicata females preferred an extreme call character resembling that of heterospecifics, and they had more eggs fertilized. In overlapping populations, S. multiplicata females preferred average call characteristics, and they did not benefit in terms of enhanced fertilization success.
The finding that sympatric S. multiplicata females prefer average
call rate is unusual. Although anuran females often use species-typical values
of pulse rate to identify conspecific males
(Gerhardt, 1988), anuran
females generally prefer faster call rates to slower values (e.g.,
Cherry, 1993;
Dyson et al., 1998;
Gerhardt, 1987;
Lopez and Narins, 1991;
Passmore et al., 1992;
Sullivan, 1983;
Wagner and Sullivan, 1995).
Call rate is a condition-dependent character (i.e., the ability to call
rapidly requires greater energy; Bevier,
1997; Grafe, 1996;
Prestwich et al., 1989;
Taigen and Wells, 1985) so
that fast call rates are potentially reliable indicators of male quality
(Cherry, 1993;
Grafe, 1996).
Gerhardt (1991) suggested
that anuran females may glean multiple messages from male calls, such that one
trait (e.g., pulse rate) may indicate species identity and other traits (e.g.,
call duration or call rate) may indicate male quality. Moreover, females may
weight the importance of this information differently depending on whether
they are in sympatry or allopatry (e.g.,
Gerhardt, 1994). Why then do
sympatric S. multiplicata females not use an average value of pulse
rate to identify conspecific males and exaggerated values of call rate to
identify high-quality mates (e.g.,
Gerhardt, 1994)? One possible
explanation is that backcross hybrid males (which can occur in mixed-species
ponds; Simovich, 1985) may
possess calls that overlap with or are similar in pulse rate and/or call rate
to calls of pure S. multiplicata males. Thus, sympatric S.
multiplicata females may need to use species-specific values of both
characters to identify conspecific mates. The need to avoid F1 and
backcross hybrid males may also explain female avoidance of a fast call rate
(37 calls/min) that is still well below the average for S.
bombifrons. To evaluate this hypothesis, it will be necessary to fully
describe the call characters of F1 and backcross hybrid males. It
would also be interesting to determine how S. multiplicata females
(both from sympatry and allopatry) react to simultaneous variation in both
pulse rate and call rate (e.g., Gerhardt,
1994). Such experiments would provide a better understanding of
how S. multiplicata females use the information in both
characters.
In contrast to the call rate preferences of sympatric S.
multiplicata females, allopatric S. multiplicata females
preferred an exaggerated, faster than average value of call rate to the
average value (Figure 3). Thus,
S. multiplicata females appear to use exaggerated values of a
condition-dependent trait when S. bombifrons is absent. These
findings are based on females collected from one population in sympatry and
one population in allopatry, however, so it will be necessary to compare
female mate preferences from additional sympatric and allopatric populations
to generalize beyond these two populations. Nevertheless, female mate
preferences often differ between populations in sympatry and allopatry (e.g.,
Gerhardt, 1994;
Markow, 1981;
Márquez
and Bosch, 1997; Noor,
1995; Ratcliffe and Grant,
1983; Waage,
1975), such that individuals in sympatry are more selective
against heterospecifics than are individuals in allopatry.
By preferring an average call rate to a faster call rate, sympatric S.
multiplicata females appear to sacrifice information on male quality to
avoid mismating with S. bombifrons and sterile hybrid males, which
possess fast call rates (Figure
2). Indeed, S. multiplicata females had enhanced
fertilization success only when S. bombifrons were absent (i.e., in
the pure-species pond; Figure
4). That S. multiplicata females benefited from mate
choice when congeners were absent, but not when they were present, supports
the prediction that females engaging primarily in species recognition forgo
benefits of mate choice (Pfennig,
1998). Thus, S. multiplicata females apparently emphasize
species recognition when risk of heterospecific matings is high and
mate-quality recognition when such mismatings are unlikely. Note that,
although S. multiplicata females from the Altar Valley co-occur with
S. couchii, their preference for faster-calling conspecific males
(Figure 3) potentially allows
them to select against both low-quality conspecific mates and heterospecifics
(i.e., S. couchii). This preference for an exaggerated value of call
rate allows Altar Valley S. multiplicata females to select against
heterospecifics because S. couchii males call more slowly than S.
multiplicata males (Figure
2). Thus, in this situation, species and mate-quality recognition
may reinforce one another (i.e., by selecting high-quality conspecifics,
females also avoid heterospecifics).
Once a female is freed from having to engage primarily in species
recognition, the benefits of mate-quality recognition can be substantial. For
example, S. multiplicata females at the pure-species pond had 3.5%
more offspring with preferred males versus nonpreferred males. Because this
3.5% is an increase in the number of offspring females receive, it is an
estimate of the strength of selection on female preferences. Using the
standard equation for the spread of a favorable allele
(Ridley, 1996), an allele
encoding a preference that yields 3.5% more offspring will go from being rare
(1%) to common (>50%) in fewer than 200 generations.
The mechanism by which S. multiplicata females benefited from
enhanced fertilization success with preferred males is unclear, but likely
involves male condition. Females at the pure-species pond preferred mates that
were heavier for a given body size than were nonpreferred males
(Figure 5), suggesting that the
preferred males were in better condition. In other species, larger males
produce better quality ejaculate and higher sperm counts
(Berrigan and Locke, 1991;
Pitnick and Markow, 1994).
Thus, spadefoot males that are heavier for a given body size may produce more
or better quality sperm, thereby enabling them to better fertilize a female's
clutch.
It might be contended that an unidentified environmental variable in the mixed-species ponds prevented S. multiplicata females from selecting high-quality mates. Yet, S. bombifrons females from these same ponds had substantially higher fertilization success with preferred males (Figure 4). This finding illustrates an important point: females that do not face a conflict between species and mate-quality recognition are not expected to compromise on mate quality, even when hetero-specifics are present. Such is the case with S. bombifrons females that can potentially use extreme values of fast call rate to select high-quality conspecific mates without risking heterospecific matings (Figure 2).
It is possible that S. multiplicata females did not benefit in mixed-species ponds because S. multiplicata males at these ponds were unable to provide females with enhanced fertilization success. For example, mixed-species ponds, which are typically at lower elevations, may be in marginal habitat for S. multiplicata such that S. multiplicata males at mixed-species ponds are in poor condition and therefore unable to provide females with enhanced fertilization success. However, the mean fertilization success among males at each pond type is similar, thereby mitigating against this hypothesis (mean fertilization success at pure-species pond ± SE = 90.29 ± 0.03; mean fertilization success at mixed-species ponds = 92.78 ± 0.01; t = 0.92, df = 62, p =.36). Moreover, although this hypothesis explains why S. multiplicata females would not receive benefits from males at the mixed-species ponds, it does not explain why sympatric (as opposed to allopatric) S. multiplicata females would prefer males with an average value of a condition dependent character (call rate).
It is also possible that a more complex acoustic environment at
mixed-species ponds may have prevented S. multiplicata females (but
not S. bombifrons females) from identifying high-quality mates
(Gerhardt and Klump, 1988;
Wollerman, 1999). However,
this hypothesis also does not necessarily explain why sympatric S.
multiplicata females prefer an average call rate. All else being equal,
faster call rates contain more energy than slower values, so faster-calling
males might be more easily detected against a background chorus sound. Thus,
chorus noise per se potentially should select for preferences of fast call
rates rather than average call rate.
Compromising on mate quality to ensure conspecific matings is not
necessarily a long-term solution to a conflict between species and
mate-quality recognition. Such a trade-off between species and mate-quality
recognition may most likely occur when ranges of species that use similar
secondary sexual signals have overlapped recently (as may be true of S.
multiplicata and S. bombifrons in southeastern Arizona;
Simovich, 1985). Ultimately,
selection may favor females that use multiple characters that enable them to
assess mate quality and species identity simultaneously, or selection may
favor high-quality males that produce signals distinct from heterospecifics
(Pfennig, 1998).
In general, females may engage in species recognition over mate-quality
recognition whenever sympatric species use similar secondary sexual signals.
However, although this study has emphasized how species recognition may be
expressed at the expense of mate-quality recognition, the converse may also
hold. In particular, selection may favor an emphasis on mate-quality
recognition over species recognition if the costs or risks of heterospecific
matings are low (Pfennig,
1998). Such an emphasis on mate-quality recognition over species
recognition may explain situations where mate preferences for exaggerated
traits lead to preferences for traits of heterospecific males
(Basolo, 1990;
Jones and Hunter, 1998;
McClintock and Uetz, 1996;
Moodie, 1982;
Morris and Fullard, 1983;
Ryan and Wagner, 1987).
In sum, the interaction between species and mate-quality recognition can affect the evolution of individuals' abilities to detect mates, sexually selected characters, and, ultimately, mate choice behavior in important and seemingly nonintuitive ways. By establishing how these recognition processes interact, we will better understand why and how individuals choose certain mates.
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ACKNOWLEDGEMENTS |
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I am grateful to David Pfennig, Regan McNatt, Katrina Rapa, Beatrice Trentinella, Tony Frankino, and the staff and volunteers at the South-western Research Station for lab and field assistance. Many thanks also to David Pfennig, Jeff Brawn, Jeff Conner, David Enstrom, Bob Podolsky, George Batzli, Scott Robinson, Paul Sherman, Kern Reeve, and two anonymous reviewers for helpful comments on the manuscript, Dan Buchholz for providing allopatric females, and the Arizona Game and Fish Department for collecting permits. This research was supported by grants from the American Museum of Natural History's Roosevelt and Southwestern Research Station Student Support funds, the Animal Behavior Society, the Francis M. and Harlie M. Clark Fund (University of Illinois), the Graduate College of the University of Illinois, and Sigma Xi.
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