Killing males from rival communities can provide male chimpanzees with clear reproductive benefits, including improved access to feeding territory for themselves, their mates, and offspring12-14. Within-community killing of males, on the other hand, is puzzling, because these males can provide benefits, such as increasing the chances of winning inter-community contests8,15 and expanding territory14. Previous studies have hypothesized that within-community killing in chimpanzees is (1) a non-adaptive byproduct of generalized aggression7; (2) a consequence of decreased inter-community threat5,7,9; or (3) the result of reproductive competition intensified by male-biased operational sex ratios4-5,9. Previous analysis also indicates that killing in chimpanzees occurs more frequently at high population densities8. Here, we test these hypotheses, as well as a fifth: within-community killings function to eliminate rivals, which is more likely to benefit attackers when females are few in number, and thus more readily monopolized. Evolutionary game theory predicts that fatal fighting should be most likely when the value of a contested resource is large relative to expected future payoff16. Thus, when a large share of reproductive opportunities is at stake, males should be more willing to engage in fatal fighting. The share of reproductive opportunities available depends on the degree to which fertile females can be monopolized by the highest-ranking male. Nunn11 proposed an index of monopolizability, which is higher when females are few in number and/or cycle asynchronously11. Nunn found that this index predicted traits associated with contest competition in male primates better than the operational sex ratio17. Following this logic, we propose that in groups with many males and females, killing rival males is unlikely to benefit attackers, because the degree to which the remaining females can be monopolized remains low. In smaller groups, however, killing rivals can enable attackers to greatly increase their share of reproductive opportunities.
We tested these hypotheses using data from the Mitumba (median = 3 males, 9 females ≥12 years old) and Kasekela (median = 12 males, 23 females ≥12 years old) communities at Gombe (1997–2018). During this study period, we infer that fighting among males led to 5 deaths in Mitumba and 1 in Kasekela (Table S1). The killings in Mitumba began in 2004, when alpha male Vincent was injured in a fall. During the subsequent three months, Vincent avoided the other two adult males of Mitumba, Rudi and Edgar, but when these two males encountered Vincent in December 2004, they attacked and killed him. In January 2005, Edgar’s 8.2 year-old brother Ebony was found dead with injuries consistent with attack by chimpanzees. Circumstantial evidence indicates Ebony was likely killed by a Mitumba male, as most of the Kasekela males were under observation 2.5 km away at the likely time of Ebony’s death. Rudi then became alpha male, but Edgar challenged Rudi repeatedly, severely injuring Rudi in 2007. Edgar became alpha male in 2008. Rudi disappeared in 2013; as he had not recently been injured, and also was positive for SIVcpz, we infer that he died from disease. Edgar injured three other males in severe attacks: Forest (2012), Apple (2015), and Fansi (2017). Forest and Apple disappeared soon after the attacks; we infer they died from injuries inflicted by Edgar. In 2017, observers found Edgar displaying near Fansi’s freshly killed body; we infer Edgar was the killer. In Kasekela, one male, Kris, disappeared after an attack by the alpha male, Ferdinand; we infer Kris died from the resulting injuries. Controlling for population size in the manner commonly used for homicide data (killings per year per 100,000 individuals18,19) yields rates of 2859 (Mitumba) and 242 (Kasekela) killings per 100,000 weaned males per year, much higher than the median rate across long-term chimpanzee studies, which is 0 (Table S2).
Ranging and male coalition strength
We examined both the potential costs and benefits of killing males from one’s own community. We began by exploring the impact of male coalition size on effectiveness in competition for territory. Mitumba had a smaller home range than Kasekela (1997-2016, n=20 years; Mitumba: median=5.13 km2, range=3.51—8.03; Kasekela: median=16.5 km2, range= 10.9—19.4). The Mitumba community’s range size increased when they had more adult males relative to the number of males in the neighboring community (Pearson correlation; t=2.6, df=18, n=20, p=0.02, r=0.52, 95% CI=0.11—0.79) but Kasekela’s did not (t=1.42, df=18, n=20, p=0.17, r=0.32, 95% CI=-0.15—0.67; Figure S1), probably because when Kasekela chimpanzees lost range to Mitumba, they were able to expand their range to the south at the expense of the declining Kalande community20. Kasekela’s annual range center shifted south by 585 m during the study period (1997: 9482903 m N; 2016: 9482318 m N; UTM 35S). The annual locations of the two communities’ range centers were positively correlated (Pearson Correlation, t=2.74, df=18, n=20, p=0.01, r=0.54, 95% CI=0.13—0.79), indicating that Kasekela shifted southward to avoid Mitumba chimpanzees as the number of mature males in Mitumba increased.
We examined use of the ‘contested area,’ which we defined as the area of overlap in range used by each community over the study period, using 99% minimum convex polygons (Figures S2-3). The proportion of time that chimpanzees spent in the contested area each year increased with increasing number of males for Mitumba (Pearson correlation, t=5.3, df=18, n=20, p<0.01, r=0.78, 95% CI=0.51—0.91; Figure S4), but not for Kasekela (Pearson correlation, t=-0.4, df=18, n=20, p=0.70, r=-0.09, 95% CI=-0.51—0.37). Both Mitumba and Kasekela used the contested area more in years when they had a higher ratio of males in their community to males in the neighboring community (Pearson correlation; Mitumba, t=5.7, df=18, n=20, p<0.01, r=0.80, 95% CI=0.55—0.92; Kasekela, t=3.9, df=18, n=20, p<0.01, r=0.68, 95% CI=0.34—0.86; Figure S4). Thus, having more males improved access to territory. To be adaptive, within-community killing of males would need to provide killers with sufficient benefits to offset the costs resulting from reduced coalition size.
Rates of male aggression
If within-community killings occurred as a byproduct of overall higher rates of aggression, then these rates should be higher in Mitumba than in Kasekela. However, controlling for individual identity and observation time, Kasekela and Mitumba males did not differ in their rate of aggression, considering either all aggressive acts (mixed Poisson regression, β=0.64, 95% CI=-0.31—1.55, z=1.43, p=0.152), or only instances of higher-cost aggression (chasing and/or physical contact: mixed Poisson regression, β=-0.30, 95% CI=-0.98—0.42, z=-0.90, p=0.37; Table S3). Even Edgar, who was observed attacking four of the five victims in Mitumba, nonetheless did not have an exceptionally high rate of aggressive behavior overall (Figure S5). These findings indicate that the higher rate of killings in Mitumba did not result from simply from a higher rate of aggression in that community. Moreover, in the observed case, Edgar and Rudi continued attacking Vincent until he was dead, suggesting that killing was intentional. The many wounds found on Fansi’s freshly killed body also appear consistent with intentional rather than accidental killing.
Intercommunity threat
If within-community killings resulted from chimpanzees being faced with a low level of intercommunity threat, then we would expect (1) that more within-community killings would occur in the community facing a lower level of inter-community threat and (2) that within-community killings would occur more often in years with few intercommunity incursions. The Mitumba chimpanzees faced a high level of inter-community threat, as they had a smaller range than Kasekela (1997–2016; t-test, t=21.0, df=30.8, nKK=nMT=20 years, p<0.01, 95% CI= 9.96—12.11, d=6.64) and fewer males to defend it (1997–2018; t test, t=20.3, df=41.0, nKK=nMT=22 years, p<0.01, 95% CI= 7.57—9.26, d=6.12; Figure S6). Kasekela had a nearly 4:1 numerical advantage over Mitumba (median male ratio=3.67, range=1.80—7.00). Kasekela males killed infants from Mitumba in 1993 (Rejea21) and 2005 (Andromeda22), and likely killed an adolescent male in 2002 (Rusambo21), while Kasekela suffered a single inter-community killing in 2004 (Patti8). The mean rate at which individuals died from intercommunity killing was higher in Mitumba (404 victims per year per 100,000 individuals) than Kasekela (175 victims per year per 100,000 individuals), though this difference was not statistically significant; t-test, t=-0.75, df=28.6, nKK=nMT=22 years, p=0.46, 95% CI=-851.47—393.16, d=-0.23). As a finer scale metric of intercommunity threat, we examined the number of days per year when Kasekela males traveled north of a major ridge between the communities (Figure S2; median=13.5 days/year, range = 0–99). Within-community killing did not occur more often in Mitumba in years when Kasekela males crossed this boundary less frequently (Poisson regression; β=0.016, 95% CI=-0.03—0.04, z=0.91, n=20 years, p=0.36).
Population density
We previously found that high population density correlated with higher rates of killing overall (including within- and between-communities)8. If within-community killings occur due to increased competition for resources resulting from high population density, such killings should occur more often in more densely populated communities. Population density was greater in Mitumba than Kasekela (1997-2016, Mitumba mean=4.91, Kasekela mean= 3.40, t-test, t=-5.37, nKK=nMT=20, df=31.2, p<0.01, 95% CI=-2.09—-0.94, d=-1.70). However, the years in which within-community killings took place did not have higher population density than years with no killings (1997-2016, Mann-Whitney U, U=88, n0=36, n1=4, p=1, A=1).
Operational sex ratio
Previous studies have suggested that within-community killings in chimpanzees occur when a highly male-biased operational sex ratio increases intensity of competition among males4,5,9. However, we found that the operational sex ratio was less male-biased in Mitumba than Kasekela (1997-2018; Mitumba mean=10.52; Kasekela mean=14.92; t-test, t=4.18, df=41.9, nKK=nMT=22 years, p<0.01, 95% CI=2.27—10.52, d=1.26, Figure S6).
Monopolizability
Following Nunn11, we propose that the intensity of competition among males is best predicted, not by operational sex ratio, but by the degree to which males can monopolize fertile females. When many females are present, the probability that only one female is fertile — and is thus monopolizable by the top-ranking male — decreases. We calculated predicted annual monopolizability of fertile females for both communities and compared these with observed values determined via observations of female sexual swelling (Figure S7, Table S4). Predicted and observed monopolizability were positively correlated (linear regression, β=1.41, 95% CI=1.01—1.81, t=7.11, p<0.01, R2=0.60). Each day, Mitumba had fewer cycling, parous females than Kasekela (Mitumba mean=1.05; Kasekela mean=5.90; t-test, t= 173.43, df=8137.1, n1=n2=6574 days, p<0.01, 95% CI= 4.80—4.91, d=3.03; Figure 1) and as a result, Mitumba exhibited a greater proportion of days with only one female observed mating (𝛸2=23.59, df=1, p<0.01, Φ=0.05; Figure S8).
Attackers are those listed in Table S1 as known or inferred attackers in fatal cases. Non-attackers are all other mature males (i.e., those that were observed mating in periods before and after violent events). Error bars represent one standard deviation of uncertainty.
Reproductive consequences for attackers
Known and suspected attackers from both communities increased their share of observed mating following severe within-community attacks (Figure 2, Figure S9; Binomial glmm, Attack Order*Attacker, β=0.62, 95% CI=0.42—0.81, z=6.2, p<0.01). Paternity data also indicated that community size affected the extent to which attackers gained benefits from intra-community killing (Figure 3). In the small Mitumba community, the alpha male sired 80% of infants born in Mitumba, but only 18% of infants born in Kasekela (1997-2018). In 2002, Mitumba had three adult males: alpha-male Vincent, Rudi, and Edgar. Genetic data indicate that prior to Vincent’s killing, he sired 66.7% (n=4) of Mitumba infants with known paternity while Rudi and Edgar sired only one infant each (16.6%). After killing Vincent in December of 2004, Rudi and Edgar increased their share of paternity (𝛸2=8.19, df=2, p=0.016, Φ=0.74; Figure 3A). In 2009, Kasekela’s alpha-male, Ferdinand, similarly increased his share of conceptions after attacking Kris, an adult male who subsequently disappeared. Ferdinand’s share of paternities increased from before his attack on Kris (6.3%, n=2) to after (15.4%, n=2); however, this change was not statistically significant (𝛸2=0.16, df=1, p=0.70, Φ=0.15; Figure 3B). Both Mitumba attackers fathered more infants than all but three Gombe males (Figure 3C-D), making them exceptionally successful even after taking into account the death of Andromeda (sired by Edgar), whose killing by Kasekela males might have been averted if Vincent had survived. After Rudi died, Edgar obtained 72% of observed matings (Figure S9A). Edgar likely has sired even more offspring; 14 Mitumba infants remain un-genotyped, with only one conceived before Rudi’s death.
Cross-site analysis
Using the Gombe data presented here, together with published data from long-term chimpanzee field sites8 (Table S5), we employed an information-theoretic model selection approach to test which of three factors best predicted rates of within-community killing: operational sex-ratio, population density, and monopolizability. The best model included only monopolizability (model weight w = 0.70), and only for monopolizability did the 95% confidence interval of the model-averaged parameter value exclude zero (Table 1). These results support the view that within-community killing of male chimpanzees results from male reproductive competition4-5,9, and that monopolizability provides a better predictor than sex ratios. High monopolizability of fertile females can make it worthwhile for males to eliminate rivals.
Table 1. Summary of information-theoretic model averaging: within-community killings of weaned males.
Model
|
Intercept
|
Monopolizability
|
Operational Sex Ratio
|
Population Density
|
K
|
Δi
|
wi
|
1
|
-9.65
|
4.64
|
|
|
2
|
0.00
|
0.70
|
2
|
-11.49
|
6.59
|
-0.05
|
0.22
|
4
|
2.80
|
0.17
|
3
|
-5.97
|
|
|
|
1
|
4.49
|
0.07
|
4
|
-6.47
|
|
|
0.12
|
2
|
5.96
|
0.04
|
5
|
-6.19
|
|
0.02
|
|
2
|
6.90
|
0.02
|
Model-Averaged Parameter
|
-9.50
|
5.03
|
-0.04
|
0.21
|
|
|
|
2.5%
|
-14.26
|
0.26
|
-0.15
|
-0.06
|
|
|
|
97.5%
|
-4.75
|
9.80
|
0.07
|
0.47
|
|
|
|