Male-male competition and reproduction in wild blue monkeys

FINAL REPORT: MALE-MALE COMPETITION AND REPRODUCTION IN WILD BLUE MONKEYS Su-Jen Roberts Ph.D. Candidate, Department of Ecology, Evolution, & Environmental Biology, Columbia University INTRODUCTION Beginning with Darwin’s theory of sexual selection (1871), research on intrasexual competition has focused on male-male competition for mating opportunities (Andersson 1994, Clutton-Brock 2007). If a single male can exclude other males from a group of females, then theory predicts that both selection pressure on male fighting abilities and variance in male reproductive success should be extreme (Clutton-Brock 1989). Indeed, in species that live in one-male groups (from here, “one-male species”), males are observed to fight each other for residency, sometimes risking mortal injury (Lindenfors & Tullberg 2011), and sexual dimorphism in body size and weaponry is often pronounced (Clutton-Brock et al. 1977). Variance in male reproductive success is also observed to be high in one-male species (Clutton-Brock 1988, Le Boeuf & Reiter 1988, Struhsaker & Pope 1991) and in some cases, resident males monopolize within-group reproduction completely, meaning that lifelong bachelors do not sire any offspring (Pope 1990, Launhardt et al. 2001).

Blue monkeys (Cercopithecus mitis stuhlmanni) are an interesting species in which to study the effect of male-male competition on reproduction because they have an unusually dynamic social organization. Although groups typically include only one resident male, some groups in some mating seasons experience influxes of bachelor males, which temporarily transform one-male groups into multi-male groups with changing male membership (Cords 2002). During both influx and non-influx years, competitors mate with females (Cords et al. 1986, Cords 1988, Pazol 2003) and likely sire offspring (Hatcher 2006), so it appears that residency neither guarantees high siring success nor is it the only successful reproductive tactic.

My research explored patterns of resident and bachelor male reproduction in a population of blue monkeys in the Kakamega Forest, a rainforest located in western Kenya.

Specifically, I used molecular data to determine the number of offspring sired by individual males present in the study population and demographic and behavioral data to identify the factors correlated with high siring success. Using rates of reproduction and home range overlap from the long-term study population, I estimated and compared the lifetime reproductive success of residents and bachelors, thereby contributing to our understanding of the role of intrasexual competition in the evolution of alternative reproductive tactics for males.

SUMMARY OF METHODS AND MAIN RESULTS In the field, I collected fecal samples from 126 offspring conceived in 8 study groups over a 10-year period and 60 adult males, including 11 resident males from the study groups. In the lab, I extracted DNA from the samples and genotyped individuals at 14

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microsatellite loci. These genotypes plus maternal genotypes from earlier work allowed me to assign or exclude males as the father of the offspring.

Resident Male Reproduction I was able to conclusively assign or exclude the resident male as the father of 111 offspring; the resident was the father of 68 of the offspring (61%) and was not the father of 36 of the offspring (39%). A value of 61% is low compared to resident siring success in other one-male species, a difference that may be related to the large female group size or the occurrence of influxes in blue monkeys.

On average, a resident male blue monkey was the father of 58% ± 34% of the offspring conceived in his study group (N=11 resident males), but residents sired as little as 0% and as much as 100% of within-group offspring (Figure 1). I used long-term demographic records to explore the drivers of variation among residents. I predicted that a resident was less likely to be the father of an offspring if the offspring was conceived when many females in the group were fertile and mating at the same time, because it would be more difficult for the resident to monopolize access to multiple females simultaneously (Altmann 1962). I also predicted that a resident was less likely to be the father of an offspring if the offspring was conceived when many competitors were present – such as during an influx – because there would be stronger competition for a limited number of reproductive opportunities (Chism & Rogers 1997, Carlson & Isbell 2001). Finally, I predicted that a resident would be less likely to sire an offspring if he had been in the group for many years, because some evidence from other primates suggests that females prefer to mate with novel males (Inoue & Takenaka 2008, Weingrill et al. 2011).

Figure 1: Offspring conceived during the observed tenures of 11 resident males, with those sired by the resident in gray and those sired by other males in white.

Parentheses indicate the number of mating seasons during which each male was resident.

I extracted measures of female reproductive synchrony, the number of competitors present, and resident tenure length from demographic data collected during the entire study period and used a generalized linear mixed model to assess their effect on the probability that a resident sired an offspring conceived in his group. Both female reproductive synchrony and the number of competitors had a significant negative effect on the probability that a resident sired an offspring, with the number of competitors having a slightly stronger effect (Figures 2 and 3).

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Figure 2: Probability that a resident sired an offspring in his group as a function of the number of females who were fertile and mating (i.e., in conceptive estrus) determined by the logistic regression (line) and the actual binned data (circles).

Parentheses indicate the number of data points per bin.

Figure 3: Probability that a resident sired an offspring in his group as a function of the number of competitor males determined by the logistic regression (line) and the actual binned data (circles).

Parentheses indicate the number of data points per bin.

I found that a resident’s ability to monopolize access to his females decreased when more competitor males were present and when more females were fertile and mating; these results are similar to those found in studies of multi-male species in which the siring success of the alpha male was lower in groups with more males (Cohas et al. 2006, Alberts 2012, Kutsukake & Nunn 2009, Gogarten & Koenig 2012, Lardy et al. 2012) or higher reproductive synchrony (Say et al. 2001, Ostner et al. 2008, Gogarten & Koenig 2012). Earlier work in the study population found a positive relationship between the number of fertile and mating females and the number of males in a group and has furthermore suggested that the presence of many mating females attracts outside males (Cords 2002, Mugatha et al. 2007). When many males are present, a resident blue

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monkey has to spend more time defending his position as resident and limiting other males’ sexual access to his females. Spending more time being vigilant for and aggressive towards intruding males may reduce the resident’s opportunities to mate and increase the chance that an intruder sneaks matings with unguarded females.

Contrary to our prediction, the number of years a resident had been in a group did not affect the probability that he sired an offspring. Female choice for novel males may be relatively unimportant in blue monkeys because sex-biased dispersal and rates of resident turnover make it unlikely that females will mate with close relatives. Female choice for novel mates may also be a strategy to reduce the probability of infanticide (Palombit 2012), which sometimes occurs when a new resident male enters a group (Cords & Fuller 2010). Although females in groups with long-term residents may be particularly motivated to mate with other males who are probably imminent challengers to the current resident, the lack of a tenure effect in this population may indicate that takeovers by infanticidal males are too unpredictable for females to adjust their attraction to nonresidents so precisely (Cords & Fuller 2010).

Bachelor Male Reproduction Of the 36 offspring that were sired by extra-group males, neighboring residents sired 12 and bachelors sired 24. I predicted that when a resident male is unable to monopolize within-group paternity, extra-group males that spend more time in a group should be more likely to sire an offspring in the group because their consistent presence will increase their chances of encountering conceptive females. Additionally, I predicted that high-ranking extra-group males should be more likely to sire offspring than low-ranking males. I used demographic data to calculate the proportion of days each male was observed in the group during the period in which each offspring was conceived and behavioral data to rank extra-group males according to outcomes of agonistic interactions. I then used a generalized linear mixed model to test the effect of both variables on the probability that an extra-group male sired an offspring.

Time spent in group was not a significant predictor of whether an extra-group male sired an offspring, indicating that extra-group males that are consistently present in a group are not more likely to sire an offspring than males that are present infrequently. This lack of effect may occur if males present in the group are unable to effectively monitor group females. Blue monkey groups spread out over a large area in the forest, which may make it difficult to track the location of individual females, thereby reducing the predictive effect of time in group. Blue monkeys mate infrequently, so even males who are present and vigilant for reproductive opportunities may miss these rare mating events.

In contrast, rank had a significant effect on extra-group male siring success: being higher ranking than an additional male resulted in a 78% increase in the odds of siring the offspring. Higher-ranking males were usually neighboring residents, suggesting that when a resident does not monopolize all reproduction in a group, neighboring residents have first access to females, followed by bachelors.

When the data set was limited to offspring sired by bachelors only, however, neither predictor was significant. This lack of a rank effect suggests that bachelor blue monkeys probably use an opportunistic tactic to reproduce, mating when they encounter an estrous female rather than queuing for reproduction (Alberts et al. 2003). Opportunistic matings

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may be more likely to occur in forest-dwelling species like blue monkeys than in species living in open habitats because limited visibility decreases the chance that a higherranking competitor would directly or indirectly interfere with mating (Rowell 1988).

Observations of bachelors mating with females near to but on the other side of vine tangles from a resident suggests that limited visibility may allow bachelors to steal some copulations. The dense forest habitat may similarly negate any effect of dominance rank on siring success among bachelors, allowing low-ranking bachelors to mate and reproduce opportunistically, despite the presence of higher-ranking bachelors in the vicinity of the group.

Comparing Male Reproductive Tactics Theoretical studies usually assume that resident males have a reproductive advantage over bachelors because they have more access to females (Clutton-Brock 1989). There are, however, relatively few studies that compare the lifetime reproductive success of resident and bachelor tactics in long-lived mammals, likely because these studies would require tracking individual males over many years. I developed a simple calculation using rates of resident and bachelor siring success in the study groups, average tenure length, and patterns of home range overlap to determine how long a bachelor would have to pursue the bachelor tactic to sire as many offspring as a resident with a single period of tenure. Although my paternity data set spans multiple years and groups, some parameters were not directly measured and had to be inferred based on known patterns of reproduction in study groups. As such, these calculations are exploratory and set up a framework for future work comparing alternative reproductive tactics.

Resident siring success equaled the annual siring rate (number of offspring) in his group plus the annual siring rate per outside group multiplied by the number of outside groups.

This annual output was then summed over the resident’s tenure. Annual bachelor siring success equaled the annual siring rate per group multiplied by the number of groups contacted. I used the paternity data set, demographic records, and location data recorded for 5 bachelor males followed during the 2011 mating season to calculate minimum, mean, and maximum values for each parameter.

I calculated the number of offspring sired by the average resident by plugging mean values into the equation for resident siring success, finding that the average resident in a small group (<15 adult females) sired 5.0 offspring during a period of tenure of average length. The average resident in a large group sired 9.2 offspring during a period of tenure of average length. Similarly, plugging mean values for annual siring rate and number of groups encountered into the equation for bachelor siring success indicated that the average bachelor sired 0.3 offspring per year. Plugging maximum values into the equation indicated that the best bachelor sired 1.1 offspring per year.

These simple calculations showed that it will usually take many years for a bachelor to sire as many offspring as sired by a resident during one period of tenure and in most circumstances, a bachelor is unlikely to live long enough to sire as many offspring as a resident. Despite my general conclusion that a male who incorporates a period of residency into his reproductive lifetime has higher fitness than one who does not, I did identify some plausible circumstances under which a bachelor may sire the same number of offspring as sired by a resident during one period of tenure. Specifically, a bachelor

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siring offspring at the maximum rate in the maximum number of groups (i.e., the best bachelor) for 4.9 years will be able to sire the same number of offspring as a resident in a small group who is siring offspring at the average rate for an average length of tenure.

This estimate increases to 8.9 years when comparing the best bachelor to the average resident in a large group with an average length of tenure, however, this estimate remains lower than the likely male reproductive lifespan. These calculations thus lead me to question the presumed advantage of residency under all circumstances, though more data are needed to verify this conclusion. Following males over the course of their lives would allow us to estimate of the length of a maleâ&#x20AC;&#x2122;s reproductive lifespan. Additionally, my comparative analysis suggests that a large determinant of lifetime reproductive success is the amount of time that a male spends as a resident or as a bachelor. Long-term tracking data would indicate how often males switch among tactics and thereby allow the inclusion of sequential periods of bachelorhood and residency in the calculation.

CONCLUSIONS Although many mammals live in one-male/multi-female groups, there have been relatively few studies that quantify resident siring success in species with this social organization and fewer still that use demographic and social data to identify drivers of variation in among residents or among bachelors. This study population of blue monkeys provided a unique opportunity to test predictions about how the strength of male-male competition for a limited number of reproductive opportunities affects siring success. The large paternity data set, which included genetic data from 126 offspring conceived over 10 years in 8 study groups, combined with high-resolution data on mating behavior and male presence and interactions allowed a robust analysis of the factors affecting patterns of male reproduction.

My results challenge the presumed reproductive monopoly of resident males living in one-male groups, as resident blue monkeys lose a substantial percentage of offspring to outside males. Even though rival males are, by definition, less often in proximity in one male groups than in multi-male groups, they still pose a competitive threat to resident males. When a resident was unable to monopolize reproduction in his own group, highranking outside males, which were usually neighboring residents, were more likely to sire an offspring than low-ranking bachelors. However, when bachelors competed among themselves, neither rank nor time spent in group was a significant predictor of siring success, suggesting that bachelor siring success may reflect a highly opportunistic mating tactic, which succeeds in a visually opaque habitat where estrous females may be widely dispersed. Comparing the success of alternative reproductive tactics provides a more complete understanding of the evolution of mating systems. These results suggest that a bachelor that sires offspring at the maximum rate in in the maximum number of groups for several years may be able to be as successful as a resident with one period of tenure.

This study calls for future research that tracks individual males over the course of their lifetime to determine how often males switch between residency and bachelorhood, to estimate the length of male reproductive lifespans, and thus to assess variance in lifetime reproductive success.

SUMMARY OF PUBLICATIONS Â

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My examination of resident male siring success is currently in press at Behavioral Ecology and is titled “Factors affecting low resident male siring success in one-male groups of blue monkeys” (DOI: 10.1093/beheco/aru060). I am preparing a second manuscript that focuses on bachelor male siring success and the comparison of resident and bachelor reproduction.

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