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Ecological and evolutionary change is generated by variation in individual performance (Coulson et al. 2006). Yearly reproductive success (YRS) can be defined as the total number of offspring produced in a year by each member of a set of known individuals (Grafen 1988). Analysing the factors related to individual variation in YRS, and identifying the characteristics of successful individuals, provides insight into the selective pressures affecting evolutionary processes, especially if summed over a lifetime (but see also Coulson et al. 2006). YRS is not usually easy to study in natural populations of large mammals, as it requires accurate measures of the number of offspring produced per individual. This is especially difficult in species that occur at low densities and are difficult to observe and capture. However, molecular techniques can be used to determine paternity (Clutton-Brock 1988; Clutton-Brock, Albon & Guinness 1988; Clapham & Palsboll 1997; Coltman et al. 2001).
Due to the absence of paternal care in most mammals, male reproductive success is constrained only by the ability to sire offspring (Trivers 1972). Thus, male mammals usually compete intensely for mates, creating the potential for a high variance in male mating success (Emlen & Oring 1977) and thus an opportunity for sexual selection (Wade & Arnold 1980; Arnold & Wade 1984), but only if variation in mating success is correlated with phenotypical variation (Andersson 1994).
Intrasexual selection favours traits that confer an advantage on males in access to females (Andersson 1994), such as large body size, because of its advantage during combat and endurance rivalry (Andersson 1994). When male mating success is influenced strongly by fighting, sexual selection promotes sexual size dimorphism, with larger males. Male reproductive success is then expected to be biased towards a few large adults with superior competitive abilities. Large male size may also be favoured if females prefer large males (Andersson 1994). Body size has often been found to be a major contributing factor to male reproductive success (e.g. red deer Cervus elaphus, Clutton-Brock, Guiness & Albon 1982; Clutton-Brock et al. 1988; bridled nailtail wallaby Onochyogalea fraenata, Fisher & Lara 1999; common brushtail possum Trichosurus vulpecula, Clinchy et al. 2004), but not always (harbour seal Phoca vitulina, Coltman, Bowen & Wright 1998; Coltman et al. 1999).
Population density may influence YRS, with mating skew increasing or decreasing with density (Kokko & Rankin 2006). In red deer male lifetime breeding success was correlated positively with the local female density (Clutton-Brock et al. 1988). In an expanding population of brown bears (Ursus arctos), the relative female population density declined more rapidly than for males from the centre of the distribution towards the edge (Swenson, Sandegren & Söderberg 1998a; Swenson et al. 1998b), which may affect male YRS.
Superior reproductive competitors may have greater multilocus heterozygosity, which is often correlated with fitness-associated traits (David 1998; Hansson & Westerberg 2002). Significant correlations between multilocus heterozygosity and fitness have been found in birds (Hansson et al. 2001) and mammals (Coltman et al. 1998; Slate et al. 2000). Brown (1997) suggested that the expression of vigour, condition-sensitive ornaments and symmetry in males may directly reflect individual heterozygosity at key loci or many loci.
Here we evaluate YRS and its determinants in male brown bears using genetic paternity analysis in an 18-year study of two bear populations in Sweden. To our knowledge, this is the first report of male reproductive success in a wild non-social large carnivore. The brown bear is thought to be a non-social and non-territorial species, exhibiting a sequentially polygynous and promiscuous mating system, in which males compete for access to individual oestrous females (Schwartz, Miller & Haroldson 2003). Our objectives were to estimate the influence of phenotypical factors, age and population density on variation in YRS of males. We predict that (a) body size, (b) age and (c) population density are correlated positively with male YRS, and that (d) internal relatedness (a measure of genetic heterozygosity; Amos, Worthington Wilmer & Kokko 2001) is correlated negatively with male YRS.
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During 1984–2001, we obtained reproductive data from 68 males (24 in the north, 44 in the south) for 417 individual mating seasons (the number of mating seasons the males in our sample were alive during the 18-year study period). Males were spatially stable over time, because the mean distance between male annual home range centres was shorter than both the mean and median home range diameters of adult males in both areas (Table 1). Male age ranged from 3 to 30 years, and ages of successful males ranged from 3 to 27 years. The male age structure differed between the areas (Fig. 1), with mean age significantly higher in the south than in the north (South: X̄ = 9·55 years ± 5·93 (SD), North: X̄= 6·88 years ± 4·51, t58 = 2·08, P = 0·042). Mean YRS was significantly higher in the north than in the south (North: X̄ = 1·02 ± 1·59, South: X̄ = 0·42 genetically detected offspring per year ± 0·95, t134 = 3·69, P < 0·001). There was also a statistically significant difference in the proportion of reproductively successful males per age class (3 years of age and older) between the study areas (south: age classes 3–30, X̄ = 21·4% ± 32·6, north: age classes: 3–24, X̄ = 56·8% ± 42·1, t38 = 2·56, P = 0·014, Fig. 2).
Table 1. Comparison of mean and median home range diameters and the mean distance between adult male brown bear annual home range centres in two study areas in Scandinavia in the period 1984–2001. Males were aged 3–30 years (north: 22 males with radio-locations from together 74 years; south: 34 different males with radio-locations from together 126 years). Home range sizes are in km2, the distances calculated are in km. Median diameter = median home range diameter as calculated from the median home range. Mean diameter = mean home range diameter as calculated from the mean home range. Mean distance = the mean distance between male annual home range centres
|Study area||Median home range||Mean home range||Range||Median diameter||Mean diameter||Mean distance|
|North|| 833 km2*||1137 km2*||245–2029 km2*||16·28 km||19·02 km||12·7 km**|
|South||1055 km2*||4289 km2*||314–8264 km2*||18·33 km||36·95 km||11·6 km**|
Figure 1. Proportions based on the composite age structure of marked adult (≥ 3 years) male brown bears in two study areas in Scandinavia from 1984 to 2001. The thick solid line represents males in the north and the thin solid line males in the south. Due to capture methods a relatively lower proportion of 3- and 4-year old males are represented in the figure.
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Figure 2. Proportion of adult (≥ 3 years) male brown bears reproducing annually per age class in two study areas in Scandinavia from 1984 to 2001. The black bars represent the south, the white bars the north.
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The area-specific von Bertalanffy curves (based on 74 individuals in the north and 152 in the south) were not significantly different (Table 2, Fig. 3) and were used to calculate the body size of the individuals in further analyses. The overall model showed that YRS was significantly lower in the south (Table 3). Age and population density were positively related, and internal relatedness was negatively related to YRS. The interaction study area × body size suggested that body size was more important in the south, whereas the interaction study area × age showed that age was more important in the north (Table 3). The separate analysis of the study areas showed that YRS was related significantly to age and population density in the north and related significantly to body size and tended to be related to population density in the south (Table 4).
Table 2. Parameter estimates for the von Bertalanffy size-at-age curves for head circumference of male Scandinavian brown bears (± SE) in two study areas in Scandinavia. S: asymptotic head circumference; K: size growth constant; A: theoretical age at which the animal would have size zero; n: sample size
|Study area||S (cm)||K (year−1)||A (years)||n|
|North||78·28 ± 1·81||0·384 ± 0·047||−3·25 ± 0·48|| 74|
|South||77·68 ± 0·80||0·335 ± 0·018||−3·83 ± 0·24||152|
Figure 3. The von Bertalanffy growth curve fitted to age and head circumference of male Scandinavian brown bears. The thick solid line and the circles represent males in the north (n = 74) and the thin solid line and triangles males in the south (n = 152).
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Table 3. A global generalized mixed linear model explaining the detected number of offspring produced annually by a male brown bear in two study areas in Scandinavia in the period 1984–2001. Variables included are study area, age, body size, internal relatedness, density and relevant interactions. Male identity was included as a random effect. After a successive exclusion of the least significant terms, the final model is shown in the table; d.f.: degrees of freedom, β: logistic regression coefficient, SE: standard error; t: t-value; P: significance level; n = 417, number of groups: 68
|Study area|| 66|| || ||−2·284||0·026|
| South|| ||−6·086||2·665|| || |
| North|| ||0||0|| || |
|Study area × body size||343|| || ||1·954||0·051|
| South × body size|| ||0·079||0·041|| || |
| North × body size|| ||0||0|| || |
|Study area × age||343|| || ||−2·007||0·046|
| South × age|| ||−0·104||0·052|| || |
| North × age|| ||0||0|| || |
Table 4. Separate global generalized mixed linear models explaining the detected number of offspring produced annually by a male brown bear in two study areas in Scandinavia in the period 1984–2001. Variables included are age, body size, internal relatedness, population density and relevant interactions. Male identity was included as a random effect. After a successive exclusion of the least significant terms, the final models are shown in the table; d.f.: degrees of freedom; β: logistic regression coefficient; SE: standard error; t: t-value; P: denotes the significance level. North: n = 108, number of individuals = 24; south: n = 309, number of individuals = 44
|Study area||Explanatory variables||d.f.||β||SE||t||P|
| ||Age|| 82||0·063||0·024||2·632||0·010|
|Population density|| 82||0·039||0·016||2·399||0·019|
| ||Body size||263||0·063||0·022||2·841||0·005|
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YRS measures an individual's short-term (seasonal) production of offspring. In general, YRS in this study might be underestimates, because males could have sired offspring outside the study area or produced young within the study area that were not detected. Age patterns or spatial organization in natural, non-hunted brown bear populations and the importance of some factors influencing male YRS may differ between unhunted and hunted populations. We studied hunted (legally and illegally) populations; in Sweden no age or sex classes, except females with young, are protected and bear hunters show little selection (Fujita 2000).
YRS was significantly lower in the south (Table 3, Fig. 2), due perhaps to better sampling in the north. However, this should affect only the absolute but not the relative measures of YRS. Another explanation may be the lower operational sex ratio in the south (fewer adult females per adult male; Swenson et al. 2001). Due to illegal killing, especially in spring, only one old and reproductively dominant male and several young adult males were present in the north for several years (Swenson et al. 2001). Males ≥ 9 years were largely missing (Fig. 1). This uneven age distribution apparently enabled a relatively higher proportion of young males (3–4 years) to gain reproductive success in the north, and achieve relatively higher YRS than in the south (Fig. 2). In the south bears were usually killed during a regulated autumn hunting season. This resulted in a more evenly distributed age structure and increasing YRS with age classes (Figs 1 and 2).
Generally, YRS was correlated positively with age. We found no evidence of reproductive senescence in male brown bears, as occurs in male red deer (Clutton-Brock et al. 1988) and female brown bears (Schwartz et al. 2003b), because all males over 20 years reproduced regularly. Females of many species choose to mate with old males, possibly because they pass superior genes to their offspring (Brooks & Kemp 2001). Male age may reflect genetic quality (the viability selection hypothesis, Trivers 1972), and/or older males may be more selected by females (the good gene hypothesis, Brown 1997). However, this latter hypothesis (Brown 1997) may not be applicable to our study, because both study populations were under heavy hunting pressure and therefore survival may not depend on genetic quality. Additionally the mortality rates of adult bears (≥ 3 years) are independent of age (Sæther et al. 1998).
The brown bear mating system is based on male contest competition for females (Schwartz et al. 2003a), which is also indicated by the large sexual size dimorphism (Andersson 1994). As predicted, age-corrected male body size was correlated positively with YRS. This suggests that larger males are able to dominate and exclude smaller males physically when competing for oestrous females, as has been found in several other species (Clutton-Brock et al. 1988; Le Boeuf & Reiter 1988; McElligott et al. 2001; Wilson et al. 2002). An alternative explanation is that females select larger males, as suggested for brown bears (Bellemain et al. 2006). An advantage of body size in endurance competition may also be involved. In general, energy storage capacity should increase with body size more rapidly than metabolic costs (Andersson 1994). Large size and stored energy may enable a male to roam wider and longer in search of females. In bighorn sheep (Ovis canadensis) younger or subdominant males that were not able to attend an oestrous female employed alternative mating tactics more often than adult males, which successfully attended oestrous females (Hogg 1984). However, to our knowledge, no alternative mating tactics have been observed in brown bears, although some young males may mate with an unguarded oestrous female.
The separate analyses of the study areas and the interactions of study area × age and study area × body size suggest that age was more important for YRS in the north and body size was more important in the south. Body size and age are highly correlated in our study areas (Bellemain et al. 2006). These study-area differences are probably related to the aforementioned differences in male age structure due to human-caused mortality. A single old male dominated the reproduction in the north during the study period (Fig. 2), which resulted most probably in the relatively higher importance of age there. In the south, with a more even male age structure, no single male dominated. This resulted most probably in a more intense competition among males, with body size as the deciding factor.
As predicted, population density had a positive effect on YRS. The Scandinavian bear population is expanding in size and range (Swenson et al. 1995), and Swenson et al. (1998a,b) showed that the relative density of females declined more rapidly than for males from the centre of the distribution towards the edge, and that males dominated low-density areas into which bears are expanding. The declining female density towards the population edge decreases the chances to obtain mating opportunities and therefore also their YRS (Swenson et al. 1998b).
As predicted, IR was correlated negatively with YRS. Negative values suggest relatively outbred individuals, whereas high positive values suggest inbreeding. The negative correlation in our results suggests that outbred individuals have higher YRS. IR was probably not correlated significantly with male YRS when the study areas were analysed separately because of sample size, because the effects of measures of heterozygosity are typically evident only with large sample sizes (David 1998). Individual heterozygosity at key or many loci may be reflected in male physical qualities and condition-sensitive traits (Brown 1997), which may directly benefit males in competition. However, heterozygosity may also be selected via female choice; a female might choose the most heterozygous male through physical cues because it may favour the production of diverse and superior offspring. In brown bears, females seem to select genetically diverse males for mating (Bellemain et al. 2006), as also suggested in grey seals (Halichoerus grypus) (Amos et al. 2001). In red deer male and female lifetime breeding success was correlated positively with heterozygosity (Slate et al. 2000). Less inbred, and thus more heterozygous, males may also have an advantage in sperm competition (Andersson 1994). Multiple paternities are frequent in Scandinavian brown bears, occurring in 14·5% litters with ≥ 2 and 28% of litters with ≥ 3 (Bellemain, Swenson & Taberlet 2005b). Internal relatedness as a measure of heterozygosity probably reflects male quality due to the functional overdominance hypothesis (Bellemain et al. 2006).