Behavioral Ecology Vol. 10 No. 2: 161-168
© 1999 International Society for Behavioral Ecology
Mating success of male bushy-tailed woodrats
when bigger is not always better
Ecology and Evolution Group, Department of Zoology, University of Western Ontario, London, Ontario, Canada
Address correspondence to M. G. Topping, Department of Zoology, Miami
Received 7 June 1998; accepted 29 August 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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To determine the factors that regulate mating opportunities of male bushy-tailed woodrats (Neotoma cinerea), we used stepwise multiple regression on measurable morphological and behavioral traits. DNA fingerprinting was used to determine the paternity of juveniles, allowing mating success (the number of females mated with), and reproductive success (the number of offspring fathered) to be quantified. Both measures of male success were significantly related to the growth rate of males while reproductively active. The most successful males were those that had higher growth rates, indicating that there is relatively little cost (weight loss) associated with successful mating in male woodrats. Our findings demonstrate that although this species is highly sexually dimorphic, large body size does not influence mating success. In addition, it appears that male mating success cannot be predicted from morphological measures and may instead be determined by behavioral or olfactory cues.
Key words: bushy-tailed woodrats, growth rate, mating success, Neotoma cinerea, promiscuity, reproductive success.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The energetics of reproduction, involving differential patterns of parental investment between males and females, have often led to markedly different reproductive strategies between the sexes (Clutton-Brock, 1989
;
Ridley, 1978). This
differential parental investment was first addressed by Trivers
(1972), who suggested that in
species where one sex invests more (e.g., female mammals, which undergo
gestation and lactation), members of the opposite sex will compete for access
to them (Trivers, 1972;
Williams, 1966). As a
consequence, the more successful competing individuals will be those that gain
a greater reproductive success. Individuals that possess a competitive
advantage due to a particular trait will thus have greater fitness as a result
of the expression of the particular trait. The establishment and maintenance
of such traits may be favored through sexual selection
(Andersson, 1994).
Determining the factors that influence mating success may be difficult when
dealing with species that are not readily observable (i.e., nocturnal or
inconspicuous). Laboratory studies can often reveal the mechanisms of male
competition in otherwise unobservable animals
(Baker et al., 1986;
Shapiro and Dewsbury, 1986),
but a trade-off may exist in such studies between the ability to accurately
record all interactions among members of a population and attempts to make
conditions in the laboratory as close to the normal environment as possible.
An alternative to laboratory studies of intrasexual competition is to measure
the effects of competition in a field setting by recording parentage of
offspring and therefore obtaining information on mating success after
competition has occurred (Boellstorff et
al., 1994; Lacey et al.,
1997; Travis et al.,
1996).
Previous investigations into the effects of intrasexual competition in
natural populations have revealed that a variety of morphological and
behavioral traits improve mating success through intrasexual competition (see
Andersson, 1994, for review).
In small mammals, traits that appear to confer an advantage include body size
(Schwagmeyer and Brown, 1983;
Solomon, 1993), nest quality
(Brandt, 1989), and size of the
occupied area (Schwagmeyer,
1988). However, many of these studies only record mating success
as individuals gaining copulations or proximity to members of the opposite sex
and do not necessarily record the reproductive success of individuals because
there is no means to confirm parentage in such situations.
The advent of molecular technology in behavioral and ecological studies has
allowed parentage to be reliably assigned. Now, reproductive success and the
number of members of the opposite sex that each individual mates with can be
unambiguously quantified. These techniques have been used to investigate
mating success and mating systems of a variety of vertebrates, including
investigations into the male mating success of mammals. In the few studies
that have combined genetic analyses of parentage and field observations, body
size appears to exhibit a positive correlation with male success. Studies on
Clethrionomys rufocanus bedfordiae
(Kawata, 1988) and
Spermophilus tridecemlineatus
(Foltz and Schwagmeyer, 1989)
have demonstrated that larger or heavier males are more successful. Additional
studies on Spermophilus brunneus
(Sherman, 1989) and Sorex
araneus (Stockley et al.,
1994) have suggested that body size may confer some advantage in
male success.
The bushy-tailed woodrat (Neotoma cinerea) is the largest and most
northern-living species of the genus Neotoma, distributed from the
southern Yukon to northern New Mexico, generally following the Rocky Mountains
(Burt and Grossenheider, 1976).
It is a nocturnal, nonhibernating herbivore that feeds on a variety of plant
material (Finley, 1958). Local
distributions of N. cinerea are limited by the availability of
suitable den sites, located in fissures within rocky outcrops, caves, or
rockpiles, resulting in an aggregation of den sites on suitable habitat
(Escherich, 1981;
Finley, 1958;
Hickling, 1987). Reproduction
is highly seasonal, with a short breeding season (April-August) in Canada
(Hickling, 1987;
Moses, 1992). Females produce
one to two litters per season and may survive through 3 years of breeding
(Egoscue, 1962). Male
bushy-tailed woodrats are not known to provide any parental investment, and
therefore have the potential to mate with more than one female
(Egoscue, 1962;
Escherich, 1981). In addition,
females show asynchrony in their estrus periods, resulting in a male-biased
operational sex ratio (Egoscue,
1962; Finley,
1958), which presents the opportunity for males to mate with more
than one female during a breeding season
(Emlen and Oring, 1977).
Bushy-tailed woodrats exhibit a mating system that can best be described as
roving male promiscuity, where males and females occupy large, overlapping
home ranges during the breeding season
(Topping and Millar, 1996).
There is a high degree of intersexual and intrasexual home range overlap for
both males and females (Topping and
Millar, 1996). DNA fingerprinting of litters has demonstrated that
males gain exclusive access to individual females during each period of
estrus, resulting in no multiple paternity within litters and similar variance
in male and female reproductive success
(Topping and Millar, 1998). As
such, N. cinerea represents an ideal species with which to
investigate the factors that influence male breeding success. The mating
success of a male can be determined as the number of females with which he is
able to successfully produce offspring. Because there are no confounding
factors, such as sperm competition, we are presented with a species in which
males exhibit a direct link between success in intrasexual competition and
genetic fitness.
The purpose of this study was to identify the factors associated with male mating success in N. cinerea. Correlations were made between male mating success (defined as the number of females that a male successfully mated with) or male reproductive success (defined as the number of offspring fathered by a male that subsequently survived until weaning) and measurable traits that could be correlated with mating success. The degree to which mating success is related to such traits will provide information on which traits are important in predicting mating success of male N. cinerea.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Livetrapping and tissue collection
This study was conducted in the Kananaskis Valley, southwestern Alberta, Canada (51° N, 115° W), from late April to August, 1992-1994. Reproduction by woodrats is highly seasonal in this location, with females producing one or two litters per year between May and August (Hickling, 1987
;
Moses, 1992). We monitored
woodrats from four adjacent rocky outcrops by mark-recapture livetrapping and
radiotelemetry (Topping and Millar,
1996). To gather information about the relative locations of the
outcrops and trapping stations, permanent markers were placed at 25-m
intervals across the study area. Seven lines, running east to west across the
study area and separated by 50 m were established. The entire study area (1000
m x 300 m) was marked in this way. As such, the locations of trap
stations and den sites could then be identified by triangulating from two
permanent markers. The study area included all four outcrops monitored during
the study; the next suitable habitat for woodrats was approximately 1.5 km
away.
All animals were marked with uniquely numbered ear tags (National Band and
Tag model 1005-1). We determined age by trapping history or weight and pelage
color (grey-buff = yearling, buff = adult). Weight (g), total length (mm), and
reproductive status were recorded at each capture. We classed males as scrotal
or nonscrotal and females as pregnant (weight gain of >15 g), lactating
(raised nipples with dried milk), pregnant and lactating, or postreproductive
(nonperforate vaginas and no indication of pregnancy or lactation). Estrus was
not determined by field observation but was estimated using data on
parturition date, which was calculated as either (1) the point midway between
last capture as pregnant and first capture as nonpregnant, or (2) using
juvenile growth rate regressions developed by Moses
(1992). From this estimate,
conception date was calculated as 30 days before parturition
(Egoscue, 1962). As a
conservative estimate, females were assumed to be in estrus for 5 days
(Egoscue, 1962), with
conception occurring on day 5. Radio collars (model no. PD-2C, Holohil Systems
Ltd., Ontario, Canada) were fitted to all reproductively active, resident
males and females in April and early May each year. We classed residents as
overwintered animals from the study area or animals captured at least three
times in the first 2 weeks of study of each year. Data were collected from the
onset of reproductive activity (males having scrotal testes and females
becoming perforate) until the end of the breeding season (males having
abdominal testes and females no longer lactating). Tissue samples were taken
from each ear of all individuals captured during the course of this study and
used for genetic analysis of paternity.
DNA fingerprinting protocol
Tissue samples (20-55 µg) were digested following Topping and Millar
(1998). Genomic DNA was
isolated by a series of phenol:chloroform extractions, then precipitated in
100% ethanol, pelleted out via centrifugation, and suspended in 50 µl of 1X
TBE. Samples were stored at 4°C. We subsequently digested 10 µg of
genomic DNA by adding AluI to a restriction solution containing 10 mM
spermidine (Maniatis et al.,
1982). Differential sized fragments within each digested sample
were separated by electrophoresis (Thorne,
1967) on a 15 cm x 20 cm 0.8% agarose gel for 18-20 h at 2
V/cm. Gels were washed twice in denaturing solution (1.5 M NaCl, 0.5 M NaOH),
resulting in single-stranded DNA. This was followed by three washes in
neutralizing solution (2.5 M ammonium acetate), after which the DNA was
transferred to a nitrocellulose membrane (Schleicher and Schuell) by Southern
transfer (Southern, 1975)
using 1 M ammonium acetate, 0.02 M NaOH.
We used an RNA template ([AGGGCUGGAGG]54) analogous to probe
33.6 (Jeffreys et al., 1985)
in the hybridization reactions (Ribble,
1991). The probe was radiolabeled with 32P during a
transcription reaction (Ribble,
1991). We used phenol:chloroform and chloroform extractions to
remove any nonspecific transcription. Membranes were exposed to a
hybridization solution (5x SSPE, DI formamide, 1x Denhardts
solution, 12,000 µg tRNA and dextran sulfate) containing the radiolabeled
probe for 18-24 h. Membranes were then washed in 2x SSPE, 0.2% SDS at
55°-65°C until background counts reached 1-3000 cpm, after which they
were exposed to X-ray film (Kodak X-OMAT AR) with intensifying screens for
5-25 days.
Due to the large number of males in 1992 and 1994, we ran multiple gels for
each maternal lineage to compare the fingerprints from mother and juveniles
with all potential fathers (i.e., all males captured at least once during the
breeding season for each year). Bands were scored between 23 and 2 kb on all
radiographs. Bands in the juveniles' lanes were assessed as either maternally
or paternally derived, based on position and intensity
(Burke and Bruford, 1987). For
the purpose of paternity identification, we considered only those bands that
did not derive from the mother (i.e., all bands that were either maternally
inherited or shared by the father and the mother). By considering only those
bands that could only have been transmitted from the father (diagnostic
paternal bands), we identified a putative father. Males were considered
fathers if they possessed all or all but one of the diagnostic bands. Males
could be assessed as putative fathers if they possessed all but one band
because bands in the juveniles' fingerprint may arise through mutation. The
mutation rate recorded in this study was 8.7 x 10-3
(Topping, 1996). In cases
where juveniles possessed a band that arose by mutation, we did not assign a
father unless the next most likely male shared <65% of diagnostic bands. By
adapting this protocol, we were able to identify putative fathers, while
allowing for a normal mutation rate within the population.
We defined a successful mating as a male-female pair producing at least one offspring that survived until weaning. Mating success was defined as the number of litters produced (females) or fathered (males). Reproductive success of an individual was defined as the total number of offspring born or fathered in a given year.
Identification of traits associated with mating success
Statistical analysis was performed using Minitab for Windows
(1993). We used separate
multiple regression analyses to derive a predictive equation for the factors
influencing reproductive success and mating success. We used stepwise multiple
regression and set F (enter) = F (remove) = 3.0. This means
that a variable was not added to the regression equation unless the calculated
F statistic for that variable 
3.0. Similarly, a variable already
in the equation was removed from the regression equation if its F
statistic fell below 3.0, due to the addition of another variable. We chose to
set F (enter) = F (remove) = 3.0 because this represents a
relatively high F value, ensuring that the resulting multiple
regression equation will be significant. Because more than one variable was
entered into the resulting equation, partial correlations were calculated to
describe the relationship between success and each variable while controlling
for the effects of the other variables
(Zar, 1984). Variables with
nonsignificant partial correlations are those that only influence male success
in combination with other variables. In contrast, if a variable has a
significant partial correlation, this means that the variable has a direct
influence on male success, even when controlling for the other variables.
Under these conditions, the variable is described as being uniquely
significant, as it influences male success regardless of the impact of other
variables. Multiple regression analysis, rather than regression of
reproductive success and mating success on single traits was used because it
may provide a more accurate representation of the factors that determine
reproductive success and mating success. Because male reproductive success and
mating success is likely the result of a combination of factors, stepwise
multiple regression allows identification of all traits relating to
reproductive success and mating success as well as determining the relative
importance of each trait.
Morphological traits that had been shown to relate to reproductive success and mating success in other vertebrate species were recorded. We used mean weight and mean body length while reproductively active as measures of male body size during the breeding season. In addition, we calculated growth rates of all males by regressing weight against Julian date while the male was reproductively active and taking the slope of the regression as the growth rate. Growth rate was used in this analysis to examine whether there were physiological costs associated with mating (i.e., greater reproductive success and mating success at the expense of reduced opportunity for growth).
Although many studies have found a relationship between male territory or
home range size and male success, we were unable to use such a measure in this
study. Because stepwise regression is most effective when each animal has all
variables recorded, we were unable to use variables that, although meaningful
and relevant to such a study, would reduce the sample size available for
analysis. Therefore, only variables that could be measured for the majority of
males (90%) were used in the multiple regression analysis. Because home
range size was measured for 17 of 27 males (63%) used in this analysis
(Topping and Millar, 1996),
the missing data would have greatly reduced the effectiveness of the stepwise
regression analysis. However, home range size for the 17 available males
showed no relationship with mating success (r =.03; p =.509)
or reproductive success (r =.04; p =.447). Therefore, the
exclusion of home range data is unlikely to affect the results from the
multiple regression analysis. Bushy-tailed woodrats have large home ranges
that overlap considerably with multiple animals of the same and opposite sex.
No evidence of territoriality has been found in this species
(Topping and Millar, 1996),
and home range size did not differ between animals of different ages
(Topping, 1996). We therefore
decided against using home range size as a predictive variable and instead
used other, more readily measurable behavioral and ecological traits. The
degree to which males were subject to local competition for resources was
described by traits that reflected the local distribution of males, assuming
that the greater the local competition, the lower the chance of a given male
being able to gain exclusive access to females. Therefore, the number of other
males resident on each outcrop, along with the distance to the nearest male's
den site, and the mean distance to the two nearest males' den sites were
calculated for each male. In addition, we determined the local distribution of
females for each male by considering three measures: the number of females on
the same outcrop, the distance from the male nest to the nearest female nest,
and the mean distance between the male nest and the nearest two females. The
locations of woodrat dens were identified by either radiotelemetry during the
day or by considering the proximity of den sites to livetrapping capture
locations.
Finally, we considered the length of time that the male was present on the study area during the breeding season. The time from first capture to the time when the male was last known to be alive (as indicated by trapping the male or recording a dynamic radiotelemetry fix) were taken as the total length of time that the male was active during the breeding season. This measure of time spent on the study area was only measured for males while in reproductive condition (i.e., having scrotal testes). In addition, any effect of age on male reproductive or mating success was examined using chi-square analysis on the frequencies of mating success and reproductive success within each year, where each male was classed as either a yearling (1 year old) or an adult (2+ years old).
Statistical significance was accepted at p 
.05. All values are
reported in the text as means ±1 SD.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We recorded 27 resident males in breeding condition on the study area from 1992 to 1994. However, five males were recorded on the study area in more than 1 year, so to avoid any potential problems associated with pseudoreplication, only 1 year of data was used for each male, with the removal of additional years for these five males being determined by random numbers. Therefore, we had 34 "male-years" of data, but eliminated 7 "male-years" from animals that were present in >1 breeding season. The number of resident animals contributing data for analysis in each year was 11 in 1992, 7 in 1993 and 9 in 1994. The ratio of adult: yearling males (binomial test) did not differ significantly from 1:1 in 1992 (eight adults, three yearlings, p =.113), 1993 (four adults, three yearlings, p =.499), or 1994 (two adults, seven yearlings, p =.090). Similarly, the ratio of adult: yearling females did not differ significantly from 1:1 in 1992 (six adults, ten yearlings, p =.227), 1993 (eight adults, three yearlings, p =.113), or 1994 (four adults, five yearlings, p =.499).
Variation in reproductive success in relation to age was examined for males
and females separately. The reproductive success of adult males, yearling
males, adult females and yearling females in each year is shown in
Figure 1. Males showed no
age-related differences in reproductive success during, 1992
(
2 = 7.22, df = 6, p >.25), 1993
(2 = 7.0, df = 4, p >.10), and 1994
(2 = 1.29, df = 4, p >.75). Similarly, females
showed no age-related differences in reproductive success during 1992
(2 = 3.2, df = 4, p >.50), 1993 (2
= 3.44, df = 4, p >.25), and 1994 (2 = 6.98, df =
4, p >.10).
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The mating success of males and females was analyzed separately, in
relation to age. The mating success of adult and yearling males, along with
the number of litters produced by adult and yearling females are shown in
Figure 2. Males showed no
age-related differences in mating success during 1992 (2 =
2.18, df = 3, p >.50), 1993 (2 = 2.24, df = 3,
p >.50), or 1994 (2 = 0.52, df = 2, p
>.75). Females showed no age-related differences in the number of litters
produced during 1992 (2 = 0.64; df = 2; p >.50),
1993 (2 = 2.36, df = 2, p >.25), or 1994
(2 = 0.9, df = 2, p >.50).
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The 10 variables used in the multiple regression analysis were measured for all 27 males, with the following exceptions. The growth rate of 26 males was measured due to a low number of captures of one animal in 1992. In addition, tenure was measured for 25 of the 27 males. The remaining males did not have tenure recorded because they were not resident for the entire breeding season. The mean (±SD) and range of all variables analyzed in relation to mating and reproductive success are shown in Table 1. A significant, positive correlation between mating success and reproductive success was found (r =.910; p <.001).
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Stepwise multiple regression analysis resulted in a two-factor multiple
regression equation, relating reproductive success to growth rate and mean
body length:
 | (1) |
(F = 6.00, df = 2, 23, p =.008). The coefficient for growth rate indicated a positive relationship between reproductive success and growth rate. However, the coefficient for body length was small and showed a negative relationship between mating success and body length.
Multiple regression analysis on mating success resulted in a two-factor
regression equation, including growth rate and distance to the nearest male in
the equation:
 | (2) |
(F = 6.13, df = 2, 23, p =.007). The coefficients for both variables demonstrated a positive relationship between mating success and each measure.
It may be expected that higher growth rates are attributed to younger or smaller males in other species. However, there was no significant difference between the growth rates of adult (0.16 ± 0.22 g/day, n = 13) and yearling (0.66 ± 0.17 g/day, n = 13) males (t test: p =.083, power analysis = 0.86). Furthermore, there was no significant correlation between male body size and growth rate (r =.056, p =.787, power analysis = 0.96), or male weight and growth rate (r = -.276, p =.173, power analysis = 0.73), indicating that males were equally likely to gain or lose weight, regardless of age or size.
Partial regression analysis revealed a significant relationship between mating success and growth rate, while controlling for nearest male distance (p =.044). However, the relationship between distance to the nearest male and mating success, controlling for growth rate was not significant (p =.084). Similarly, there was a significant relationship between reproductive success and growth rate, while controlling for body size (p =.007), but the relationship between reproductive success and body size while controlling for growth rate was not significant (p =.063).
Chi-square analysis revealed no difference in the relative numbers of
occupied den sites on each of the four hills among years (2 =
4.93, df = 6, p >.50). The distribution of occupied and unoccupied
den sites over the study period is shown in
Figure 3. Although there was a
positive relationship between the number of males and females on each outcrop
(pooling data among years), there was no significant correlation (r
=.40, p =.110).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Partial regression analysis of Equation 1 revealed that although both growth rate and body size were related to reproductive success, only growth rate was uniquely significant in determining reproductive success (p =.007). This means that male body size has an effect in determining male reproductive success, but only when considered in conjunction with growth rate. Similarly, partial regression analysis of Equation 2 showed that growth rate is uniquely significant in determining mating success (p =.044), whereas distance to the nearest male nest is only significant when considered together with growth rate.
The positive relationship between male growth rates and both reproductive
and mating success reveals two points of interest related to the reproductive
ecology of male woodrats. First, successful males do not appear to suffer any
costs in terms of loss of condition (body weight) as a result of seeking,
courting, and copulating with females. Such an observation is in direct
contrast to studies on primarily polygynous mammals, which demonstrate that
males may experience substantial weight loss due to the energetic costs of
male-male rivalry (Anderson and Fedak,
1985; Clutton-Brock et al.,
1982; Deutsch et al.,
1990). Second, growth rate in male woodrats is a more reliable
predictor of mating success than morphological measures such as body size or
weight. The finding that more successful males were those who gained weight
during the breeding season may indicate that growth rate is an indicator of
quality. Males that are able to gain weight while searching and competing for
females are potentially in better condition (and therefore can be considered
higher quality) than those males that did not gain weight. Due to the novel
relationship outlined in this study (increased growth rate = more successful
males), such a relationship may be considered as a spurious correlation.
However, the relationship between growth rate and male quality is supported
when the relationship between growth rate and survival is considered. Males
with high growth rates have a greater probability of survival to the next
breeding season, even when controlling for age (t = 2.43, df = 29,
p =.022) than males with low growth rates. Therefore, it appears that
high, or at least positive, growth rates during the breeding season increases
the chance of survival to the next year. Males with higher growth rates may
therefore be in good condition.
Although male growth rate shows strong positive correlations with mating success and reproductive success, it is unlikely that growth rate per se is the male attribute that is important in male intrasexual competition. Because males and females would not be able to assess growth rates in the field, it seems extremely likely that the characteristic(s) that ultimately determines mating success exhibits a significant relationship with growth rate. Growth rate is the only measurable variable that we found to be correlated to male success, but this does not imply that it is the only important variable or that woodrats are able to use this measure. We believe that an additional variable (or variables) that could not be measured under this current study (e.g., vigor or quality of display, olfactory cues) is likely to be the male characteristic that ultimately determines mating and reproductive success. This suggestion is supported by the finding that growth rate is related to survival in male woodrats and therefore is likely to be correlated with a measure of male quality.
Male mating success also showed a positive relationship with the local distribution of males, in that males with their nearest competitors at greater distances had greater mating success. The most likely explanation for this relationship is that males with no close competitors are likely to suffer lower levels of local competition. Whether the advantage to males with no close neighbors is a result of lack of interference when courting receptive females (i.e., reduced mating competition from other males), or simply increased access to other resources (i.e., food), cannot be determined from this study. However, regardless of how males gain such an advantage, the inclusion of the distance to the nearest male in the stepwise regression equation, coupled with the positive correlation coefficient, reveals that the distance to the nearest male's nest has large implications for the resulting mating success of male woodrats.
Although body length was included in one of the multiple regression equations, it is noteworthy that (1) body length was not uniquely significant in determining reproductive success, and (2) the correlation coefficient for body length was negative, indicating that smaller, rather than larger, males may experience increased reproductive success. The significance of this is unclear because weight (which is correlated with body size) has no effect on male success.
Traits that confer a mating success advantage in other species, such as the
local distribution of females, were not included in either of the resulting
multiple regression equations and are therefore not significant predictors
when considering male mating success in N. cinerea. The lack of
correlation between female distribution and male mating success is also
surprising, given the asynchrony of estrus and the clumped nature of female
nest sites (Escherich, 1981).
Because male mating success is dependent on the local distribution of males,
rather than on the distribution of females, this may suggest a possible
mechanism by which males establish themselves in suitable habitat. The
relationship between proximity of competitors and mating success may be
influenced by the fact that suitable nest sites for bushy-tailed woodrats
consist of crevices in rocky outcrops or bluffs and cannot be constructed by
the woodrats (Escherich, 1981;
Finley, 1958). The
availability of suitable crevices places an upper limit on the number of nest
sites on a particular outcrop. Males are not able to dictate the location of
their nests, so they are unable to locate themselves in close proximity to
females unless a suitable nest site is available. Because nest sites are a
limiting resource for N. cinerea
(Hickling, 1987), and
obtaining shelter is vital due to an enhanced ability to conserve energy while
in a nest (Brown, 1968),
individuals are presumably under pressure to locate a suitable nest as quickly
as possible. Therefore, rather than gauging the location and population
density of females before choosing a nest site, males may choose a nest site
based on a lack of immediate competitors. The availability of nest sites may
facilitate such behavior because there are available den sites on all outcrops
in all years (Figure 3).
Weight was not included in either equation, and the only relationship with
body size indicated a slight advantage for smaller males. Because previous
studies on small mammals have demonstrated that body size is often a
significant predictor of mating success
(Ribble, 1992;
Solomon, 1993), it is perhaps
surprising that larger body size is not related to male success in N.
cinerea, given that it is the most sexually dimorphic species within the
genus (Escherich, 1981).
Pooling data for all years of this study
(Topping, 1996), there was
significant difference in body weight between males (360 ± 58 g) and
females (287 ± 25 g) when females were not pregnant (t = 6.78,
df = 45, p <.0001). Little evidence (lack of wounding) for male
competition through fighting was found in this study (Topping M, personal
observation), suggesting that males may compete instead through displays,
perhaps when courting females. Despite the level of dimorphism in this
species, there may be no advantage to large body size in terms of competing
for mates or gaining reproductive success. As a result, it is interesting to
speculate about factors relating to the evolution of sexual dimorphism in this
species. Clearly, there is no advantage in terms of mating success because
males weighing 243 and 510 g were both able to mate successfully with females
during 1993 (Topping,
1996).
There was no obvious pattern to male-female pairings in relation to
proximity on the outcrops. Over all years, 65.7% of litters were produced by a
male and a female from the same outcrop, with the remaining litters made up of
animals from neighboring outcrops (Topping
and Millar, 1998). Females mated with the nearest male (straight
line distance) in only 10 of 35 cases, and, on average, females mated with the
third closest male (range 1-10; Table
2).
|
Given that a strong relationship exists between growth rate and male success, it must be noted that females that produce two litters in a season have different partners for each litter. This switching of mates initially appears to contradict the notion that females may choose males based on particular characteristics. However, when growth rates and behavior of males that father first and second litters are analyzed, a pattern emerges. There were two females in each year that successfully produced two litters (Figure 2). This results in a small sample size (n = 6) for this analysis, yet the results are noteworthy. In two cases, the male that fathered the first litter had died before the time of conception of the second litter. Three cases were characterized by the first male mating with another female at the same time that his previous mate was in estrus. This again supports the idea that males must guard or attend females to ensure paternity of the litter. The situation with the final female was unclear, as the second male had a lower growth rate. Therefore, it appears that switching mates between litters may be due more to the fact that the first mate is either not alive, or is not available to mate with, since he is involved in attending another female at the time of his first mates' estrus. The fact that females do not mate with the same males from one breeding season to the next may be explained by females attempting to maximize the genetic diversity of their offspring, or alternatively that the criteria for female choice depend only on the present condition of a male.
In conclusion, the information presented in this paper has demonstrated
that there is no significant relationship between male success and male body
size or weight in bushy-tailed woodrats. In general, body size is usually
associated with greater mating success, particularly in sexually dimorphic
species, and therefore these results are surprising, given the level of sexual
dimorphism in this species. Although there are species where a relationship
between male size and mating success has been demonstrated through the
application of molecular genetics
(Craighead et al., 1995;
Wickings et al., 1993),
clearly, the results of this investigation show that this rule does not always
apply (see also Spencer et al.,
1998). As more studies incorporating genetic analyses of parentage
are documented, we may have to reevaluate a number of long-held assumptions
regarding the relationship between characteristics of individual males and
their resulting reproductive success.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We thank James Goddard, Jean-Philippe Bechtold, and Nicole Swerhun for their valuable assistance in the field. The University of Calgary Kananaskis Field Station provided facilities that permitted the undertaking of this study. For review and discussion of earlier drafts of this manuscript, we thank Margo Chase, Matina Kalcounis, Paul Handford, Terence Laverty, Neala MacDonald, Andrew McAdam, Robert Tamarin, and Taye Teferi. We are also grateful for the expert statistical advice and assistance offered by Paul MacDonald. The final version of the manuscript was improved by the comments of two anonymous referees. This study was supported by a Commonwealth Scholarship to M.T. and a Natural Sciences and Engineering Research Council of Canada grant to J.M.
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