Leave Or Conceive: Natal Dispersal and Philopatry of Female Mountain Gorillas in the Virunga Volcano Region

Animal Behaviour 77 (2009) 831–838

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Leave or conceive: natal dispersal and philopatry of female mountain gorillas in the Virunga volcano region

Andrew M. Robbins a, Tara Stoinski b,1, Katie Fawcett b,1, Martha M. Robbins a,* a Max Planck Institute for Evolutionary Anthropology b Dian Fossey Gorilla Fund International article info Natal dispersal is often attributed to inbreeding avoidance, competition for resources or competition for Article history: mates, but the patterns and frequency of dispersal vary considerably among and even within species. We Received 18 March 2008 examined the possible reasons for dispersal and philopatry of natal nulliparous female mountain gorillas, Initial acceptance 5 June 2008 Gorilla gorilla beringei, in the Virunga volcano region, including comparisons with non-natal and/or Final acceptance 4 December 2008 parous females. Competition among females is generally weak and ineffective in this population, and Published online 28 February 2009 inbreeding avoidance has been considered the ultimate cause of natal dispersal. Yet fewer than half of MS. number: 08-00194R nulliparous females left their natal group when the dominant male was old enough to be their father, so they did not rely entirely upon dispersal to avoid such risk of inbreeding. Almost all natal nulliparous Keywords: females were with at least one sexually active male who was not old enough to be their father, so the female transfer presence or absence of such mating alternatives also did not determine whether they left. Natal Gorilla gorilla beringei nulliparous females were more likely to leave groups with only one adult male, where infanticide losses inbreeding infanticide have been higher than in multimale groups. Thus natal dispersal seemed to be inﬂuenced by infanticide mountain gorilla avoidance, which has been considered the ultimate cause of secondary dispersal. Natal nulliparous natal dispersal females have more time to encounter suitable destinations than other females, which may be a proximate reason why they were more likely to transfer despite having the same ultimate cause of dispersal. Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Inbreeding avoidance is often invoked as an ultimate cause of populations (Keller & Waller 2002; Lehmann & Perrin 2003; Kokko natal dispersal by females, but its full impact remains difficult to & Ots 2006). If dispersal costs are considerable, a female can quantify (Moore & Ali 1984; Perrin & Mazalov 1999; Guillaume & tolerate even greater inbreeding depression within her natal group Perrin 2006). The impact of inbreeding by females can be examined (Waser et al. 1986). by comparing the fitness consequences of breeding with a relative Despite such theoretical predictions that inbreeding may be versus a nonrelative (e.g. Waser et al. 1986; Kokko & Ots 2006). beneficial, the presence of a putative father has been considered From that perspective, inbreeding by a female involves a trade-off one of the proximate causes of natal dispersal by females. Female between the indirect fitness benefits of perpetuating the genes of dispersal is common among polygynous mammals when the a relative versus the direct fitness costs of inbreeding depression. If average age at first conception is less than the average tenure of dispersal costs are negligible, then inbreeding by the female is breeding males (Clutton-Brock 1989). These results were consid- favoured when d(r) < r/(1 þ r), where r is the relatedness between ered evidence of inbreeding avoidance, because without dispersal the female and her mate, and d(r) is the inbreeding depression in females might breed with their father. The Clutton-Brock (1989) comparison to mating with a nonrelative (for derivation and study included species in which females left multimale groups that underlying assumptions, see Waser et al. 1986). Thus, mating with contained natal males spanning a wide range of ages. Thus some a father (r ¼ 0.5) should be preferred to mating with nonrelatives females may emigrate whenever they face any possibility of mating unless d(0.5) > 1/3, which has been considered to be near the with their father, even when younger alternative mates are avail- upper range of reported values for inbreeding depression in wild able within their natal group. Females may also avoid such inbreeding through selective mate choices within their natal group, or through extragroup copulations, delayed conception or if the older males disperse (Clutton-Brock 1989; Pusey & Wolf 1996; Field * Correspondence: M. M. Robbins, Max Planck Institute for Evolutionary & Guatelli-Steinberg 2003). Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany. Our aim in this study was to examine the possible reasons for E-mail address: [email protected] (M.M. Robbins). 1 T. Stoinski and K. Fawcett are at the Dian Fossey Gorilla Fund International, 800 dispersal and philopatry of natal nulliparous female mountain Cherokee Ave SE, Atlanta, GA 30315-1440, U.S.A. gorillas, Gorilla gorilla beringei, in the Virunga Volcano region from

0003-3472/$38.00 Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2008.12.005 832 A.M. Robbins et al. / Animal Behaviour 77 (2009) 831–838

1967 to 2005, using the demographic database of the Dian Fossey transfers are influenced by infanticide protection for their offspring, Gorilla Fund International (DFGFI). Mountain gorillas are an inter- which is considered an ultimate cause of secondary dispersal by esting species for examining the influence of inbreeding, because female mountain gorillas (Watts 2000; Harcourt & Greenberg dispersal and philopatry are common for both sexes (Harcourt et al. 2001; Robbins et al., in press b). Infanticide typically occurs when 1976). Male philopatry has been attributed to the benefits of social the silverback dies in a one-male group, because the remaining queuing for dominant status (Robbins & Robbins 2005), whereas group members are unable to protect offspring from outsider males emigrating males become solitary and attempt to establish their (fully mature silverbacks can be twice as large as adult females and own group (Harcourt et al. 1976). As a result of these two male blackbacks; Watts 1989). Infanticide can also occur during reproductive strategies, both one-male and multimale groups can encounters between groups, as silverbacks risk serious injury and be observed in the same population (median ¼ 40% multimale even death while competing for females (Fossey 1984; Watts 1989). groups, range 8–53%, N ¼ 6 censuses of the entire population: Multimale groups have had a lower frequency of infanticide Kalpers et al. 2003). These two ‘group types’ are defined based upon than one-male groups (known cases equal 1.5% versus 10.4% of all their number of ‘silverbacks’, which are males 12 years old or more births) and lower overall infant mortality (22% versus 42%, M. M. (e.g. Kalpers et al. 2003). Outsider males have not been observed to Robbins et al. 2007; A. M. Robbins et al., in press b). Thus it has been take over established groups (e.g. Watts 1989), and even when proposed that infanticide may contribute to a female preference for a dominant male is usurped by a subordinate within his own group, multimale groups, and the lack of a second silverback could be secondary dispersal generally does not occur (i.e. he remains in the a proximate cause of female dispersal (e.g. Watts 1989, 1990a, group as a past-prime male: Robbins 1995). In contrast with the 2000). Accordingly, parous females have been five times more males, females have both natal and secondary dispersal, and they likely to leave one-male groups than multimale groups (Robbins transfer directly from one group to another without becoming et al., in press b). To test the hypothesis that infanticide protection is solitary (Harcourt et al. 1976). In previous studies of this population, an ultimate cause of dispersal by natal nulliparous females too, we seven of 14 nulliparous females (50%) transferred from their natal examined whether they were also more likely to leave one-male group before giving birth (Watts 1990b, 1991), and 15 secondary groups than multimale groups. transfers occurred among 24 females who were observed for at If infanticide protection is an ultimate cause of dispersal for all least 10 years of their reproductive life (Sicotte 2001). females, and inbreeding avoidance is an additional cause of Inbreeding avoidance has been considered the ultimate cause of dispersal for many natal nulliparous females, then natal nulliparous natal dispersal by female mountain gorillas (Harcourt 1978; Watts females should be more likely to transfer than most other females. 1990a; Sicotte 2001). Extragroup copulations are rare, as is male (If natal parous females faced a substantial risk of breeding with immigration, so dispersal is the main option for a female to avoid their father, they probably would have left already.) Therefore, as an mating with ‘familiar’ males (i.e. a male that has been with her additional test of the hypothesis that natal nulliparous females since his or her birth). Female mountain gorillas mate with half- disperse to avoid inbreeding, we examined whether they were brothers and even full brothers, but it has been considered rare for more likely to transfer than other females. However, this test may them to mate with males who are old enough to be their father not be conclusive, because even if natal nulliparous females do not (Harcourt 1981; Watts 1990b, 1991; Harcourt & Stewart 2007). As disperse to avoid inbreeding, they could still be more likely to a result, Watts (1990b) suggested that the proximate cause of natal transfer than other females. For example, if a nulliparous female female dispersal would be the lack of any sexually active male who chooses the best available destination for her natal transfer, she could not have been her father (i.e. males who had not been may have no incentive to make any subsequent transfers as a non- sexually active in her group when she was born). Therefore, to test natal nulliparous female, and even if some other destinations the hypothesis that inbreeding avoidance is the ultimate cause of eventually become better after she has conceived, she may have natal dispersal by nulliparous female mountain gorillas, we few opportunities to transfer as a parous female. examined whether they were less likely to transfer when their Owing to the risk of infanticide for their offspring, female group contained a potential mate who was not old enough to be mountain gorillas typically do not disperse while lactating or their father. In light of the Clutton-Brock (1989) study of other pregnant (Robbins et al., in press a; but see Sicotte 2000). So after species, we also examined whether natal nulliparous females were the death or weaning of an offspring, parous females have an more likely to transfer when their group contained a male who was average of 3.9 2.6 months of cycling in which to transfer before old enough to be their father. Females could leave when they face conceiving again (Harcourt et al. 1980; Watts 1990b). In contrast, any possibility of breeding with their father, or they could stay nulliparous females can transfer as early as 5–6 years, so they may when they have any opportunity to avoid it. have a few years to transfer before their first conception at 7–12 Male mountain gorillas start to attempt copulations at 8 years, years (Harcourt 1978; Gerald 1995; Robbins et al., in press a). and they have complete copulations by 9–10 years (Watts 1990b, Between their natal transfer and their first conception, females 1991). Therefore, we defined ‘sexually active males’ to include have an average of 15.1 11.1 months for any subsequent transfers blackbacks (8–11 years) as well as silverbacks. The dominant male as a non-natal nulliparous female (Robbins et al., in press a). Thus reportedly allows subordinates to mate with his putative daughters natal nulliparous females may have more time and more oppor- (Watts 1990b; T. S. Stoinski, R. Rosentaum, T. Ngaboyamahina, tunities to transfer than non-natal and/or parous females. V. Vecellio, F. Ndagijimana & K. Fawcett, unpublished data). In summary, we predicted that dispersal of natal nulliparous However, in paternity analyses of 48 offspring, the youngest father females will depend upon whether alternative mates are available was 11 years old, and the dominant male sired 85% of offspring in (i.e. the criteria from Watts 1990b rather than Clutton-Brock 1989), multimale groups (Bradley et al. 2005). Therefore, in addition to because selective mating can allow philopatric females to avoid testing whether the dispersal of a natal nulliparous female depends inbreeding with their probable father. We predicted that these upon the presence or absence of sexually active males who could be alternative mates can include subordinate silverbacks but not her father, we also examined whether the criterion is limited to blackbacks, because dominant males allow their putative daughters silverbacks, or whether it is based solely upon whether the domi- to mate with subordinates, but confirmed siring has been limited to nant male could be her father. males who were near or beyond 12 years. We predicted that natal In addition to examining whether natal nulliparous females nulliparous females will be more likely to leave one-male groups disperse to avoid inbreeding, we also examined whether their than multimale groups, because such a pattern has already been A.M. Robbins et al. / Animal Behaviour 77 (2009) 831–838 833 reported for parous females, and future offspring of natal nullipa- If females were younger than 6 years when their group was rous females would be equally vulnerable to infanticide. We pre- habituated, they were assumed to be in their natal group. Only one dicted that natal nulliparous females would be more likely to of 44 (2%) natal nulliparous females in this study made a voluntary disperse than other females, even if these differences cannot be transfer before that age, and only four of the 139 (3%) females in the conclusively linked to inbreeding avoidance. long-term records were observed in a group disintegration before that age. If females were older than 6 years when their group was METHODS habituated, we assumed that their natal group is unknown, and they were excluded from analyses when necessary. Data Set Fissions and group disintegrations are both excluded from dispersal calculations, which are limited to voluntary transfers. Data were evaluated for the mountain gorilla population of the Among the 61 assumed cases of voluntary transfers in this study, Virunga Volcano region of Rwanda, Uganda, and Democratic 77% were confirmed by locating the female in another group Republic of Congo from 15 September 1967 until 31 December (Table 2). The records refer to a probable destination for another 2005. The data came from 11 groups that have been habituated by 13% of the cases, but they do not explicitly state whether the female DFGFI for long-term research, and from one group that has been was seen there. In the remaining 10% of assumed cases, the female habituated for tourism (Table 1). Each of the current study groups is simply disappeared. No health problems were reported for females generally observed on a daily basis, but before 1980 it was more with unknown fates, and dispersal is more common than death, so typical to monitor only one group per day, and all observations have it is a more probable cause for these disappearances. been interrupted at times (e.g. during the civil unrest in 1997– The voluntary transfers occurred during 46 events when 1998). The identity of the dominant male was not always identified a female left by herself, three events when a non-natal parous for the tourist group (Su), so that group is excluded from analyses female transferred simultaneously with a non-natal nulliparous when necessary. female, one event when a non-natal parous female transferred with The DFGFI Karisoke Research Center has developed a classifica- a natal nulliparous female, one event when a natal nulliparous tion system for the precision of the estimated birth date of each female transferred with a parous female of unknown natality, and gorilla, based upon its condition when first observed (Gerald 1995; one event when five natal nulliparous females transferred together. Williamson & Gerald-Steklis 2003). For 39 of the 44 natal nullipa- Relationships among female mountain gorillas are weak, so rous females in this study (89%), the birth date is known to within 6 simultaneous transfers by multiple females were treated as sepa- months because they were first observed as young infants. Birth rate data points. dates are known to within 1.5 years for the remaining natal nulliparous females, who were first observed as prereproductive Natal Nulliparous Females immatures. For 69 of their 78 potential mates (88%), the birth date is known to within 2 years because they were first observed before For analyses of dispersal versus philopatry by natal nulliparous becoming silverbacks. Birth dates have an estimated precision females, we performed Fisher’s exact tests using Systat 11 (2004, of 4 years for an additional seven males (9%), and 10 years for SYSTAT Software Inc., Richmond CA, U.S.A.). The analyses included the remaining two males (3%). The two males with the least precise one data point for each of the 44 natal nulliparous females who birth dates were both estimated to be older than 30 years, so were observed to transfer or give birth in the study groups. The despite the imprecision of these estimates, we are reasonably dependent variable could have a value of either ‘go’ or ‘stay’, to certain that the males were old enough to be the father of any natal indicate whether the female made a natal transfer or stayed and nulliparous females. gave birth in her natal group. Following the death of its dominant male, one of the research To test the hypothesis that inbreeding avoidance is the ultimate groups split into two nearly equal-sized groups (Robbins 2001). cause of dispersal by natal nulliparous females, we used six inde- Natal females were still with familiar males after the fission, so they pendent variables that could each have a value of ‘yes’ or ‘no’. The were still considered to be in their natal group. Four of the study first two independent variables included all sexually active males as groups disintegrated during the 147 group-years of this study. Their potential mates of a natal nulliparous female, so we assumed that females were with unfamiliar males after the disintegration, so males could be her father if they were at least 8 years older than she these females were no longer considered to be in their natal group. was (i.e. she could have been sired by a blackback). The first

Table 1 Summary of the study groups

Group Years observed Total size AF SB BB MMG (%) Age of dominant male Group-years Female-years Births Emigrations

First Last Min Max am 1971 1971 2.0 1.0 1.0 0.0 0 28.5 28.6 0.2 0.2 1 bm 1985 2005 19.6 6.2 2.9 1.9 95 14.9 31.3 20.4 126.9 29 4 g4 1967 1979 11.0 4.0 1.3 0.8 21 12.6 30.0 11.3 45.8 9 7 g5 1967 1993 17.6 6.6 2.2 0.8 83 12.9 34.7 25.7 168.8 43 11 g8 1967 1974 4.1 0.7 1.7 1.2 60 23.5 29.9 6.7 4.6 1 2 nk 1972 1985 10.6 4.9 1.0 0.0 0 16.0 28.5 11.2 54.2 15 9 pb 1993 2005 40.5 15.6 3.1 2.4 100 15.6 27.0 12.6 196.4 53 5 pn 1975 1992 6.0 0.0 2.2 2.6 74 14.0 0.6 1 sh 1993 2005 21.3 6.2 3.8 2.8 62 16.3 28.8 12.6 78.2 19 2 sm 1971 1976 2.0 1.0 1.0 0.0 0 14.0 18.2 2.8 2.8 1 3 su 1978 2005 26.5 9.1 2.6 2.0 95 17.0 39.5 27.3 248.0 64 15 tg 1984 1987 2.5 1.0 1.0 0.0 0 16.8 19.3 2.1 2.1 1 1

The table gives the ﬁrst and last year of observation for this study, the average composition of each group, that is, the number of adult females (AF), silverbacks (SB) and blackbacks (BB), as well as the percentage of months that it was multimale versus one-male (MMG), the minimum (Min) and maximum (Max) ages (in years) for the dominant male, the number of group-years (excluding time as a solitary male) and female-years observed for each group and the number of observed births and emigrations. 834 A.M. Robbins et al. / Animal Behaviour 77 (2009) 831–838

Table 2 Number of transfers and births within each category of females

Category of female Category of transfer destination Births Transfer percentage

Known Probable Unknown Total Nulliparous Natal 22 2 1 25 (23) 21 (21) 54 Non-natal 4 2 1 7 (7) 29 (29) 19 Unknown 0 1 1 2 (2) 4 (4) 33

Subtotal 26 5 3 34 (29) 54 (54) 39

Parous Natal 2 0 0 2 (2) 25 (9) 7 Non-natal 12 2 3 17 (13) 133 (44) 11 Unknown 7 1 0 8 (5) 22 (7) 27

Subtotal 21 3 3 27 (18) 180 (57) 13

Total 47 8 6 61 (45) 234 (71) 21

Transfers were confirmed by locating the female in another group (known), or the records refer to a probable destination, or the female disappeared (unknown). The ‘total’ column indicates the total number of transfers with known, probable or unknown destinations. Values in parentheses indicate the number of different females who contributed to the number of transfers or births. The table shows 25 transfers by 23 natal nulliparous females because two females left their natal group, returned, and then left again. The ‘transfer percentage’ is the number of transfers divided by the number of transfers plus births. independent variable indicated whether a natal nulliparous female conversely each birth can be considered a decision not to transfer. was with at least one sexually active male who was old enough to Thus we essentially considered the outcome of these decisions be her father (Clutton-Brock 1989). The second independent vari- (leave or conceive). The two main independent variables were the able indicated whether she was with any sexually active male who ‘natality’ (0 ¼ non-natal, 1 ¼ natal) and ‘parity’ (0 ¼ nulliparous, was young enough that he could not be her father (Watts 1990b). 1 ¼ parous) of the female when she transferred or conceived. The third and fourth independent variables excluded blackbacks The comparisons between natal nulliparous females versus as potential mates of a natal nulliparous female, so we assumed other females often involved multiple transfers and/or births by the that males could be her father if they were at least 12 years older same female (Table 2). To control for nonindependence between than she was (i.e. she would have been sired by a silverback). The these data points, the identity of the female was included as third independent variable indicated whether a natal nulliparous a random effect in every GLMM. Multiple data points by the same female was with at least one silverback who was old enough to be female may also be subject to temporal autocorrelation, if, for her father. The fourth independent variable indicated whether she example, females are unlikely to leave a group that they have just was with any silverback who was young enough that he could not chosen to join. We tested for temporal autocorrelation by adding be her father. For both blackbacks and silverbacks, males above a third independent variable (e.g. see Chatterjee & Price 1991). For their age criterion were considered ‘old’, and males below the each data point i, the autocorrelation term equalled: criterion were ‘young’. P The fifth and sixth independent variables excluded subordinate rj= ti tj jsi silverbacks and blackbacks as potential mates of a natal nulliparous P (1) female, and focused solely upon whether the dominant male could 1= ti tj jsi have been her father. The fifth independent variable indicated whether the dominant male was at least 12 years older than the in which rj are the residuals of all other data points by the same female, and the sixth independent variable indicated whether he female (taken from the original model), ti is the date of the data had already been dominant when she was born. point, and tj are dates of all other data points by the same female. To test the hypothesis that infanticide protection is the ultimate Thus we placed greater weight on potential autocorrelation cause of dispersal by natal nulliparous females, we used an inde- between data points that were closer in time. pendent variable that indicated whether or not the female was in We defined the ‘transfer percentage’ as the number of transfers a multimale group when she transferred or conceived (yes or no). within a specified portion of the data set, divided by the number of transfers plus births within that same data subset. We used the Natal Nulliparous Females versus Other Females transfer percentage for discussion purposes only, and it was not a variable in any of the statistical analyses. As an additional test of the hypothesis that inbreeding avoidance is the ultimate cause of dispersal by natal nulliparous females, we examined whether they were more likely to transfer than other RESULTS females. We performed the analyses using generalized linear mixed models (GLMM) with a binomial error distribution, by specifying Natal Nulliparous Females that ‘family ¼ binomial’ in the lmer function of the lme4 package developed for R (version 2.7.0, R Development Core Team 2008, To test the hypothesis that inbreeding avoidance is the ultimate http://www.R-project.org). The analyses included one data point cause of dispersal by natal nulliparous females, we considered for each birth in the study groups, and one additional data point for several potential proximate causes (Table 3). First, we considered each voluntary transfer from the study groups (Table 2). The whether females transferred when they faced any possibility of dependent variable equalled one whenever a female transferred, mating with any sexually active male who was old enough to be and zero whenever she gave birth. Each voluntary transfer can be their father (Clutton-Brock 1989). At the time of their first transfer considered a ‘decision’ not to reproduce in the current group, so or conception, 43 of 44 (98%) females were with at least one A.M. Robbins et al. / Animal Behaviour 77 (2009) 831–838 835

Table 3 the age of the dominant male could be more important when Analyses of dispersal versus philopatry for natal nulliparous females alternative mates are not available. If the analysis is limited to one-

Test NStay NGo Go% P male groups, four of five natal nulliparous females left when the 3.1 Did the group contain an old sexually active male? dominant male was old, and in the fifth case she mated instead Yes 20 23 53 0.477 with a blackback who was ‘verging on sexual maturity’ (so an No 1 0 0 alternative mate was effectively available and that case could 3.2 Did the group contain a young sexually active male? almost be considered a multimale group, Fossey 1983). Yet all three Yes 21 21 50 0.489 females also left one-male groups when the dominant male was No 0 2 100 young, so the age of the dominant male was not necessarily the 3.3 Did the group contain an old silverback? deciding factor for dispersal from one-male groups. Yes 15 20 57 0.272 Forty per cent of natal nulliparous females left the same male No 6 3 33 who had been dominant since their birth, which is not significantly 3.4 Did the group contain a young silverback? higher than the 20% who left a different dominant male (test 3.6). In Yes 20 19 49 0.348 10 of the 15 cases when the dominant male had changed, his No 1 4 80 relatedness with the female was probably still at least 0.25 (e.g. 3.5 Did the group contain an old dominant male? paternal half-siblings, because they had been born in the same Yes 10 9 47 0.723 group while the same male was dominant). Relationships are No 9 5 36 unknown for the other five cases. The female transferred in three of 3.6 Was the same male dominant when the female was born? these 10 known cases. In total, natal nulliparous females trans- Yes 6 4 40 0.378 ferred in seven of 20 (35%) cases in which the dominant male was No 12 3 20 their probable father, paternal brother or a similarly close relative. 3.7 Did the group contain more than one silverback? In summary, none of the preceding results provided significant Yes 20 16 44 0.048 support for the hypothesis that inbreeding avoidance is the ulti- No 1 7 88 mate cause of dispersal by natal nulliparous females. For each of the seven analyses, the table shows the number of natal nulliparous To test the hypothesis that infanticide protection is the ultimate females who transferred (NGo) versus those who stayed and gave birth (NStay), as well as the percentage of females who transferred (Go%). These values are shown for cause of dispersal by natal nulliparous females, we examined females whose group composition fulfilled the specified conditions (yes) versus whether they were more likely to leave one-male groups versus those that did not (no). Sexually active males were considered ‘old’ if they were at multimale groups. Eighty-eight per cent of nulliparous females left least 8 years older than the female, and ‘young’ if they were not. Silverbacks were their natal group when it was one-male, which is significantly considered ‘old’ if they were at least 12 years older than the female, and ‘young’ if higher than the 44% who left when it was multimale (test 3.7). This they were not (see Methods). P values are taken from Fisher’s exact tests. result is consistent with the hypothesis that natal nulliparous females disperse to reduce the infanticide risk for their future sexually active male who was at least 8 years older than they were offspring, which has been significantly higher in one-male groups (test 3.1). Yet only 53% of these females transferred, so the possi- (M. M. Robbins et al. 2007; A. M. Robbins et al., in press b). bility of mating with their potential father did not consistently lead to dispersal. Natal Nulliparous Females versus Other Females Second, we tested whether nulliparous females stayed and conceived in their natal group when they had any possibility of As an additional test of the hypothesis that inbreeding avoid- mating with any sexually active male who was young enough that ance is the ultimate cause of dispersal by natal nulliparous he could not be their father (Watts 1990b). At the time of their first females, we examined whether they were more likely to transfer transfer or conception, 42 of 44 (95%) females were with at least than other females (Fig. 1, Table 4). The GLMM showed that one sexually active male who was less than 8 years older than they dispersal was significantly more likely for both natal and nullip- were (test 3.2). Thus natal nulliparous females almost always had arous females (test 4.1). The higher transfer percentage of natal the possibility to mate with a male who was too young to be their father. Half of those females transferred, so the presence of 60 a ‘young’ male did not consistently lead to female philopatry. 46 Next we considered whether dispersal by natal nulliparous females depended upon the presence or absence of silverbacks rather than any sexually active male. Fifty-seven per cent of nulliparous females transferred when their natal group contained 40 88 at least one silverback who was at least 12 years older than they were, which is not significantly higher than the 33% who left when it did not (test 3.3). Forty-nine per cent of nulliparous females 36 transferred when their natal group contained at least one silver- 20 back who was less than 12 years older than they were, which is not Transfer percentage 150 207 significantly lower than the 80% females who left when it did not 27 (test 3.4). Thus, natal nulliparous females were not significantly more likely to leave when they faced any possibility of mating with 0 an ‘old’ silverback, and they were not significantly less likely to Natal Non-natal Total leave when ‘young’ alternatives were available. Finally, we considered whether dispersal by natal nulliparous Figure 1. Transfer percentages for nulliparous (shaded bars) and parous (unshaded) females depended upon whether the dominant male could have females in their natal and non-natal groups. In each category, the transfer percentage equals the number of transfers divided by the number of transfers plus births. The been their father. Forty-seven per cent of natal nulliparous females number of transfers plus births is shown at the top of each bar. The ‘total’ values do not left an old dominant male, which is not significantly higher than equal the sum of natal plus non-natal females, because it was sometimes unknown the 36% who left a young dominant male (test 3.5). Hypothetically, whether a female was in her natal group. See Table 2 for additional details. 836 A.M. Robbins et al. / Animal Behaviour 77 (2009) 831–838

Table 4 significantly more likely to leave groups that contained a male Results of generalized linear mixed models for the effects of natality and parity upon who was old enough to be their father, even when the male was in dispersal the dominant breeding role, and had already been dominant when Test Data set Variable Coefficient SE P they were born (Table 3). Thus female mountain gorillas do not 4.1 Multivariate analysis base case rely entirely upon dispersal to avoid all risk of inbreeding with Full Natality 1.259 0.409 0.002 such males. Full Parity 1.159 0.397 0.003 Watts (1991) suggested that natal dispersal by female mountain 4.2 Multivariate analysis with an autocorrelation term gorillas could depend upon whether their group contains at least Full Natality 4.072 0.898 <0.001 one sexually active male who was young enough that he could not Full Parity 1.536 0.681 0.024 be their father. In this study, 95% of natal nulliparous females were Full Auto 1.596 0.534 0.003 with at least one such male (including blackbacks), and 89% were Post hoc univariate analyses with at least one such silverback (Table 3). As a result, we could not 4.3 Nulliparous Natality 1.662 0.513 0.001 4.4 Natal Parity 2.557 0.876 0.004 fully evaluate whether dispersal is more common when these 4.5 Non-natal Parity 0.588 0.531 0.269 alternative breeding opportunities are lacking. However, we can 4.6 Parous Natality 0.280 0.928 0.763 conclude that the Watts (1991) criteria do not explain most of the The natality variable equalled 1 when a female was in her natal group and 0 when observed transfers, which occurred even when these alternative she was not. The parity variable equalled 0 for nulliparous females and 1 for parous breeding opportunities were available. females. The dependent variable equalled 1 when a female transferred and 0 when The dispersal patterns of female mountain gorillas are consis- she stayed and gave birth. Test 4.1 is a model that includes both natality and parity, tent with behavioural observations that the dominant male allows and test 4.2 is the same model but with an autocorrelation term added. The last four tests are separate post hoc analyses with subsets of the data. For example, test 4.6 his putative daughters to mate with subordinates, and that females compares natal parous females versus non-natal parous females, because it is do not avoid these breeding alternatives (Watts 1990b). The examining the effect of natality within the data subset for parous females. The subordinates are often half-brothers or other relatives of the natal coefficients for significant results indicate higher transfer percentages for natal or female, so even if she avoids mating with her father, philopatry may nulliparous females. The coefficient for the autocorrelation term indicates that lead to moderate inbreeding (Harcourt 1981; Watts 1990b, 1991; females who recently transferred were less likely to make another transfer soon. All data sets exclude females with unknown natality. All models include the identity of Harcourt & Stewart 2007; Stoinski et al., unpublished data). Such the female as a random effect. moderate inbreeding may optimize her inclusive fitness, as proposed for some rodents and birds (Lehmann & Perrin 2003). If inbreeding depression increases exponentially with relatedness females was expected to reflect inbreeding avoidance, and the (Charlesworth & Charlesworth 1987; Keller & Waller 2002), then its higher transfer percentage of nulliparous females was expected to costs may not become prohibitive unless relatedness is high, and reflect the amount of time available to encounter suitable desti- the costs of breeding with intermediate relatives may be exceeded nations. The effects of natality and parity both remained signifi- by the indirect fitness benefits of increasing the reproductive cant when we added the autocorrelation term (test 4.2). The success of these males (Waser et al. 1986; Kokko & Ots 2006). Even coefficient for the autocorrelation term was negative, which if moderate inbreeding imposes a net fitness cost, females might indicates that females who recently transferred were less likely to tolerate these costs when they are outweighed by other factors make another transfer soon. such as infanticide protection (see below). In post hoc analyses, the GLMM indicated that the effects of natality and parity arose mainly from the transfer percentage of Group Type natal nulliparous females, which was significantly higher than those of both non-natal nulliparous females and natal parous Natal nulliparous female mountain gorillas were significantly females (tests 4.3 and 4.4). These differences suggest that the morelikelytoleaveone-malegroupsthanmultimalegroups(Table 3). influences upon dispersal are different for natal nulliparous females Consequently, this study may have overestimated the extent of versus other females, which would be consistent with factors such philopatry throughout the broader population, where one-male as inbreeding avoidance and/or additional time to encounter suit- groups are more typical. For example, in a census of the entire able destinations. Conversely, the transfer percentage of non-natal population, only 24% of adult females outside of the study groups parous females was not significantly different from those of non- were in a multimale group (C. Sholley, unpublished data), natal nulliparous females or natal parous females (tests 4.5 and compared with 81% of natal nulliparous females during the births 4.6). The latter comparison suggests that natal parous females do and transfers reported in this study. Similarly, the broader pop- not typically have more reasons to transfer than non-natal parous ulation may contain a higher proportion of females in natal groups females (i.e. they do not have a greater need to avoid inbreeding). without ‘young’ males. Overall, the results from the GLMM are consistent with the Hypothetically, the higher natal dispersal from one-male groups hypothesis that natal nulliparous females disperse to avoid could be taken as evidence for inbreeding avoidance, because natal inbreeding, but other factors could be involved. females in these groups have fewer breeding choices. However, the Clutton-Brock (1989) study showed that inbreeding avoidance DISCUSSION typically depends upon male tenure regardless of group type, and in this study natal nulliparous females left one-male groups even Inbreeding Avoidance when the silverback was not old enough to be their father. Higher dispersal from one-male groups has also been observed for parous Despite increasing quantification of inbreeding costs in wild female mountain gorillas, who are less likely to be influenced by populations (Crnokrak & Roff 1999; Keller & Waller 2002; O’Grady inbreeding (Robbins et al., in press b). et al. 2006), its impact upon dispersal is generally inferred by Infanticide protection has been considered the ultimate cause of comparing conditions in which females stay versus leave. Clutton- female mountain gorillas preferring multimale groups, which have Brock (1989) showed that females often disperse when they reach less infanticide than one-male groups and lower overall infant maturity in a group with a male who could be their father. In mortality (M. M. Robbins et al. 2007; A. M. Robbins et al., in press b; contrast, natal nulliparous female mountain gorillas were not see also Watts 1989, 1990a, 2000). Infanticide protection may also A.M. Robbins et al. / Animal Behaviour 77 (2009) 831–838 837 depend upon factors such as male quality, for example, because and parous females will have fewer chances than nulliparous female lowland gorillas have been shown to prefer silverbacks with females. Therefore we cannot exclude the possibility that a 12-fold a larger crest size, longer bodies and more musculature (Caillaud difference in the time for dispersal (a few months versus a few et al. 2008; T. Breuer, M. M. Robbins & C. Boesch, unpublished data). years) could explain the four-fold difference in the transfer Lowland gorillas live almost exclusively in one-male groups percentages of parous versus natal nulliparous females (13% versus (Magliocca et al. 1999; Parnell 2002), and any relationship between 54%, Table 2). male quality and group type is unknown for mountain gorillas. Regardless, when nulliparous females have experienced strong Conclusions infanticide protection in their natal group, moderate inbreeding may be a small price to pay in comparison with the risks of joining We found little evidence that natal nulliparous female mountain a group whose performance is less well known. gorillas disperse to avoid inbreeding, even though it had been Lower female emigration from multimale groups has also been considered the ultimate cause of their transfers (Harcourt 1978; attributed to herding by resident males, which has been reported Watts 1990a; Sicotte 2001). The most compelling evidence for for 18% of intergroup encounters by multimale groups versus only inbreeding avoidance was that they were more likely to transfer 2% for one-male groups (Sicotte 1993, 2001; Robbins et al., in press than non-natal and/or parous females, who will typically have less b). Males are typically considered less sensitive to inbreeding than need to avoid inbreeding. However, these results may arise merely females, because they have less parental investment in the because natal nulliparous females have more opportunities to offspring (Parker 1979; Waser et al. 1986; Kokko & Ots 2006). So encounter suitable destinations, and because females are unlikely even if natal nulliparous females are attempting emigration to to leave a group that they have recently chosen to join. These avoid substantial inbreeding costs, some resident males may have findings are consistent with theoretical predictions that moderate an incentive to retain them. However, natal females have dozens of inbreeding may provide net fitness benefits (Waser et al. 1986; encounters in which to transfer before their first conception (see Kokko & Ots 2006), or that any net costs may be outweighed by below), so the observed herding does not seem frequent enough to other factors. Natal dispersal seemed to be influenced by infanticide prevent emigration, unless it is accompanied by sufficient coercion protection, which has been considered a major reason why female to discourage the female from trying again later (Watts 1992; mountain gorillas stay with males at all (Harcourt & Greenberg Sicotte 1994; Robbins, in press). 2001; Harcourt & Stewart 2007).

Natal Nulliparous Females versus Other Females Acknowledgments Natal nulliparous females were more likely to transfer than non- We appreciate the long-term commitment of the Rwanda Office natal and/or parous females (Table 4), which could indicate that of Tourism and National Parks (ORTPN) for supporting the research they have an additional cause of dispersal. That additional cause activities at the Karisoke Research Center. We are greatly indebted could be inbreeding avoidance, which seems more likely to affect to the many researchers and field assistants who during the past 40 natal nulliparous females than most other females. Thus our results years of research have contributed to the long-term demographic suggest that inbreeding avoidance could still be an ultimate cause and behavioural databases of Karisoke. In particular, we highly of dispersal by some natal nulliparous females, even if this study commend the outstanding and tireless commitment of all Karisoke did not find the proximate basis for such transfers. Such a conclu- and ORTPN field staff to protect the mountain gorillas during the sion is tentative, however, because other factors could also explain last four decades; without their efforts this research would not be the higher transfer percentage of natal nulliparous females. For possible. We thank Maryke Gray, the International Gorilla Conser- example, the statistical significance of the autocorrelation term vation Program, and the Ranger Based Monitoring programme for suggests that females became less likely to transfer after they had the use of the demographic data from the Susa Group. We appre- recently done so (Table 4). This temporal autocorrelation may be ciate the statistical assistance provided by Roger Mundry, including especially relevant for explaining the lower transfer percentage of programming for the GLMM. We are grateful to Roger Mundry, non-natal nulliparous females (19%, versus 54% for natal nullipa- Paula Stockley and two anonymous referees for their helpful rous females, Table 2), who have typically just made their natal comments on the manuscript. We thank the various public and transfer. None the less, the overall effects of natality and parity private agencies, foundations and individuals that have provided remained significant after controlling for such autocorrelation support for the Karisoke Research Center since 1967. The Max (Table 4). Planck Society provided support for data analysis and writing up Natal nulliparous females could also be more likely to transfer the project. than other females because they have more time for dispersal. For example, mountain gorillas typically do not disperse while lactating or pregnant, so parous females have only a few months to References transfer while cycling, versus a few years for natal nulliparous Bradley, B. J., Robbins, M. M., Williamson, E. A., Steklis, H. D., Steklis, N. G., females (Harcourt et al. 1980; Watts 1990b; Robbins et al., in press Eckhardt, N., Boesch, C. & Vigilant, L. 2005. Mountain gorilla tug-of-war: a). The additional time for natal nulliparous females may not silverbacks have limited control over reproduction in multimale groups. always increase their probability of dispersal, if it mainly allows Proceedings of the National Academy of Sciences, U.S.A., 102, 9418–9423. them to encounter repeatedly the same destinations that they have Caillaud, D., Levrero, F., Gatti, S., Menard, N. & Raymond, M. 2008. Influence of male morphology on male mating status and behavior during interunit already chosen not to join. However, some encounters are mere encounters in western lowland gorillas. American Journal of Physical Anthro- auditory interactions at distances up to 500 m, and herding by pology, 135, 379–388. resident silverbacks can further reduce transfer opportunities, so Charlesworth, D. & Charlesworth, B. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics, 18, 237–268. the probability of dispersal may sometimes increase even when Chatterjee, S. & Price, P. 1991. Regression Analysis by Example. New York: Wiley- females encounter the same destinations repeatedly (Sicotte 1993; Interscience. Watts 1994, 1998). Intergroup encounters occur only about once Clutton-Brock, T. H. 1989. Female transfer and inbreeding avoidance in social mammals. Nature, 337, 70–72. a month in this population (Watts 1989), so females may not always Crnokrak, P. & Roff, D. A. 1999. Inbreeding depression in the wild. Heredity, 83, have effective opportunities to join some potential destinations, 260–270. 838 A.M. Robbins et al. / Animal Behaviour 77 (2009) 831–838

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