Nepotism in Prairie Dogs (Cynomys Ludovicianus) Varies with Competition but Not with Kinship

Anim . Behar ., 1986, 34, 263-270

Nepotism in prairie dogs (Cynomys ludovicianus) varies with competition but not with kinship

JOHN L . HOOGLAND* Department of Biology, Princeton University, Princeton, New Jersey 08544, U .S .A .

Abstract. Behavioural interactions among black-tailed prairie dogs (Cynomys ludovicianus) of the same sex clearly show nepotism (the favouring of kin) . Males and females consistently interact more amicably with kin than with non-kin . Nepotism in this context is striking for two reasons . First, individuals do not interact more amicably with close kin such as offspring and full-siblings than with more distant kin such as half-siblings, full-nieces, half-nieces, and half-nephews . Second, nepotism varies inversely and dramati- cally with changes in competition for either oestrous females (among males) or nesting burrows and breeding rights (among females) .

Nepotism is the preferential treatment of genetic document, has been reported for only a few species relatives (Alexander 1974; Sherman 1980a), and including sweat bees (Lasioglossum °ephyrum : parental care is one obvious expression of nepo- Greenberg 1979 ; Buckle & Greenberg 1981), Beld- tism . Hamilton (1964) predicted that nepotism ing's ground squirrels (Spermophilus beldingi : Sher- beyond parental care should vary directly with the man 1980b), two species of primates (Clutton- coefficient of genetic relatedness (r) under the Brock & Harvey 1976 ; Kurland 1977; Massey appropriate conditions ; that is, individuals should 1977). and humans (Wilson 1978 ; Alaxander 1979; cooperate with close genetic relatives more than Chagnon 1979) . Nepotism evidently does not cor- with distant relatives . Altmann (1979) later pointed relate with r in carpenter ants (Camponotus spp .) or out that if the recipient's benefit varies directly with perhaps in other insect species in which individuals the donor's investment, then individuals should live in huge colonies (Wilson 1971 : Carlin & channel all assistance to closest kin only . However, Holldobler 1983), but failure of nepotism to corre- benefits to close kin do not usually vary directly late with r has not previously been reported for any with investment but rather reach a point of dimi- vertebrate . 1 report here that black-tailed prairie nishing returns, after which individuals will be dogs (Ct'nomys ludovicianus), though nepotistic in selected to start helping more distant kin . Patterns the context of behavioural interactions, do not of nepotism versus r will also be affected by interact more amicably with close kin of the same competition, reciprocity, reproductive value of the sex, such as offspring and full-siblings, than with beneficiary, and the beneficiary's efficiency at using more distant kin such as half-siblings, full-nieces . nepotistic assistance (Alexander 1974; West-Eber- half-nieces, and half-nephews . Further, intrasexual hard 1975 ; Sherman 1980b ; Schulman & Ruben- black-tail nepotism varies inversely in a regular, stein 1983) . While these other factors mean that predictable fashion with competition for either there will be some exceptions, a positive correlation oestrous females (among males) or nesting burrows between nepotism and r is still expected in most and the opportunity to successfully wean a litter cases (Alexander 1979; Schulman & Rubenstein (among females) . 1983). Black-tails are diurnal, colonial, harem-polygy- Nepotism dispensed to kin other than offspring nous, cooperatively breeding squirrels (Rodentia : has been observed in numerous species including Sciuridae) . My study colony in Wind Cave Natio- lions (Panthero leo : Bertram 1976), paper wasps nal Park, South Dakota, occupies 6 .6 ha and in late (Polistes exclamans : Strassman 1981), and acorn spring of each year contains approximately 130 woodpeckers (Melanerpes formicivorus : Koenig et adults (more than 2 years old) and yearlings plus 80 al . 1983) . However, a direct relationship between juveniles arranged into approximately 24 family nepotism and r . perhaps because it is so difficult to groups known as coteries (Hoogland 1979). A typical coterie contains one adult male, three or four adult females, and several offspring which are * Present address: Appalachian Environmental Labor- atory, The University of Maryland, Gunter Hall . either yearlings or juveniles (King 1955). In some Frostburg, Maryland 21532, U.S.A. years as many as 33°,; of all coteries contain more

263

264 Animal Behaviour, 34, l

than one adult male, and the males in these multi- copulate until they reach 2 years of age (Hoogland male coteries are frequently kin (Hoogland 1981 a ; 1982; Hoogland & Foltz 1982), numerous yearling Hoogland & Foltz 1982) . In South Dakota, black- females, but only those yearling males known to tails copulate in February and March, and juve- copulate, were included in dyads . niles first emerge from their natal burrows just To show that nepotism does or does not vary before or at weaning in May and June . Females with r in the context of behavioural interactions usually remain in the natal coterie for life, but requires detailed genealogies and observations of males usually depart permanently 12-14 months numerous interactions. To investigate this question after weaning (Hoogland 1982) ; consequently, the for the black-tails of known ages and genetic females within a coterie are almost always geneti- relationships at my study colony, field assistants cally related . Oestrous females usually mate with and I recorded interactions from three 5-m obser- the adult male(s) resident in the home coterie (Foltz vation towers in February through June of 1979 & Hoogland 1981 ; Hoogland & Foltz 1982) and through 1984. Analyses have been completed for avoid mating with close kin (Hoogland 1982 : Foltz male data from all years, but, because of the large & Hoogland 1983). Coterie members restrict over sample sizes involved (Table 1, Fig . 1), analyses 99°,0 of foraging and other activities to a well- have been completed for female data through 1981 defined coterie territory which is defended by only . We were at the study colony each day for over adults and yearlings of both sexes from individuals 99 of the daylight hours when the prairie dogs of contiguous coterie territories (King 1955 : Hoog- were above ground . Sibling genetic relationships land 1981a). were determined by marking all young from a litter before they mixed with young from other litters METHODS (Hoogland 1981 a, 1982) . Lactating females defend the burrow containing their young from all conspe- Interactions between two black-tails can be cate- cifics during the day and sleep there alone with their gorized as either amicable or hostile. Amicable young at night (King 1955; Hoogland 1983a), so interactions involve a kiss, anal sniff, or allogroom- that maternities could be determined by observing ing in the absence of any aggression (King 1955 ; defensive and sleeping patterns of individual Hoogland 1981a) . Hostile interactions frequently females. Paternities were inferred from behavioural begin with a kiss or anal sniff followed by a fight, observations of oestrous females in combination chase, or territorial dispute (King 1955 ; Hoogland with an electrophoretic analysis of blood samples 1979, 1981a) . Combinations of amicable (e .g. kiss (Foltz & Hoogland 1981 : Hoogland & Foltz 1982) . +kiss or kiss+allogrooming) or hostile (e .g. fight In each coterie each year, interactions were classi- +fight or chase+territorial dispute) interactions fied according to stage of the annual cycle: 'pre- were scored as single interactions . Fights can lead breeding' if before the first copulation in that to serious injury or death, chases sometimes coterie; 'early pregnancy (breeding)' if during the involve more than 500 m of hard running, and first 3 weeks following the first copulation ; 'late territorial disputes can persist for as long as 3 h pregnancy' if during the fourth and fifth weeks (Hoogland 1979, unpublished data) . Thus, because after the first copulation ; 'early lactation' if during hostile interactions are evidently costly to indi- the first 4 weeks after the first parturition (as vidual black-tails, it seems likely that interacting determined from changes in behaviour (Hoogland more amicably with kin than with non-kin (i .e . & Foltz 1982) or by counting either the number of reducing aggression towards kin) would be an days after copulation or the number of days before important expression of nepotism in this species . the first juvenile emergence) ; 'late lactation' if Because black-tail females nurse only their own during the fifth and sixth weeks after the first young, except perhaps just before weaning (Hoog- parturition ; and 'postweaning' if during the first 6 land 1983a), nepotism in this context clearly weeks after the first juvenile emergence . In 1979, favours close kin . In this report I only consider limited data for females were also available from nepotism among adults and yearlings as it applies October. Females within a coterie usually breed to behavioural interactions . A dyad is a pair of synchronously (Hoogland 1981 b), so that all copu- reproductive or potentially reproductive indi- lations in each coterie occurred during the stage viduals of the same sex . Because females frequently labelled early pregnancy (breeding) in Table I and copulate as yearlings while males almost never Fig. 1 .

Hoogland: Nepotism in prairie dogs 265

Although almost all reproductively mature 1983a, in press) . Because interactions between two females at the study colony copulate each year, non-reproductive females are almost always amic- many do not successfully wean a litter (King 1955 ; able and show little variation with stage of the Hoogland 1981a ; Hoogland & Foltz 1982); some annual cycle, I only analysed data from dyads for unsuccessful females never conceive, others abort which at least one of the females successfully their young sometime during pregnancy, and still weaned a litter . For some male and female dyads . others lose their young during lactation (Hoogland data were available for more than 1 year ; in these

Table I. Nepotism for different types of dyad at different stages of the black-tail annual cycle for (A) females and (B) males

Stage

Early Early Late pregnancy Late fact- lact- Post- Dyad Prebreeding (breeding) pregnancy ation ation weaning October

(A) Female dyads Mother-daughter 0.87±0.05 0.43±0-04 0-19+0-04 031-t-0-05 0-36+007 0-83+005 0-671031 216 784 335 656 235 122 3 35 48 44 45 38 32 Z Full sisters 0-94+0 .03 0-28+0-08 0-08+0-05 0 . 13+006 020+0 .07 0 .62+0.08 I0+0 .0 143 537 194 268 160 I05 14 15 15 15 13 1_ Half-sisters 0.90+0.07 0.40+0.08 0 .32+0 .09 028±0 . 09 0. 39±0 . 12 0 .65±0. 10 1 -0-0-0 74 351 259 314 136 62 15 20 19 18 15 14 I Full aunt- 0.95+0 .05 0.26+0 .05 0 . 13+0 .09 0 . 18+0 . 09 0. 32+0 . 12 0 .66+0 14 1 0-1 (P0 niece 50 298 125 262 86 35 6 10 13 12 13 II 10 Half-aunt- 0.96+003 0.52+0 . 10 0 •(14+004 0 . 13+0 . 08 0. 04+004 0 .77_+0 . 15 niece 60 125 44 111 36 9 0 9 11 8 It 6 5 () Full first 0-85+0-0 0.40+0 .0 00+00 00+0-0 0-33+0-0 cousins 20 20 0 5 6 O 1 I 0 1 I (I (B) Male dyads Father-son 0.49+0 .38 0. 17+021 025+0 .43 0 . 25+0 38 0. 36+0.50 0 .46+0. 30 230 135 21 67 29 24 0 6 6 5 6 6 5 0 Full brothers 0.57+0 .44 029+0.41 0 .60+0 . 55 0 . 67+0 . 44 0. 78 + 0 . 44 0 . 67 + 0 . 47 270 229 27 106 82 39 0 6 6 5 5 6 O Half-brothers 0.07+0 . 12 020+021 0 .30+0 . 51 0 . 21+0 . 42 025+0 . 43 0 . 56+0 . 62 131 127 25 103 34 15 n 4 3 3 4 3 ' 0 Full uncle nephew 0 0 0 0 0 fl 0 0 0 0 0 0 (1 0 Half-uncle- 0.29+_0.40 0.0+0.0 0 .65+021 1 .0+00 1 .0+0.0 0. 83+024 nephew 11 20 25 239 76 32 0 2 1 2 2 2 2 n Full first 0.0+0_0 0-0+0.0 0-0+0-0 0-0+0-0 0-0+0-0 0-0+0 . 0 cousins 35 48 3 10 6 12 1) I I I I I I o

For each dyad, at each stage, figures are given for the proportion of interactions that were amicable (mean ± I st_), the total number of observed interactions, and the number of observed dyads . Amicability of interactions did not vary significantly with r at any stage for either sex ; see text for details .

2 66 Animal Behaviour, 34, 1

we observed 11342 interactions involving 156 Id a) FEMALES different dyads (Table I) . 1 .00- 563 I use the terms close kin, for two individuals for f 336 which r is equal to or greater than 0 . 50 (parent- 8

ld offspring, full siblings), distant kin, for two individuals for which 0 .50 > r > 0 .00 (half-siblings, full • Kin, some coterie 2115 0Nonkin, cliff coterie aunt-niece, half-aunt-niece, full uncle-nephew, 0 .40 659 T 08 1616 half-uncle-nephew, full first cousins), and non-kin, 9l57 BI for two individuals for which there is no known 103 '98 270 1545 779 Is kinship. Because of male and female dispersal 0.00 0 0 0 0 patterns, individual black-tails only rarely interact a35 o48 047 47 44 43 7 with kin of the same sex that belong to a different Prebreed Early Late Early Late Fast- October prey prep lactal lactat wean coterie (Hoogland 1981a, 1982) ; for all male and (Breed) female dyads involving kin in this report, individuals were always of the same coterie . In all female dyads, non-kin were always from different 122 coteries; in male dyads, non-kin were either from 227 the same (multi-male) or from different coteries . 0.60- b) MALES All significance levels are for two-tailed statistical 525 16 101 I7 tests. 0.50- 677 1 1

0.40- le 1 RESULTS 119 1 • Kin, some coterie 559 x Nonkin, same coterie Nepotism among black-tail females extends to O Nonkin, dill coterie distant kin such as half-sisters, full nieces, and half- 117 nieces, and nepotism among black-tail males 267 4,12 495 251 26I 9 0 .10- 147~5 extends to distant kin such as half-brothers and 27 6 "29 YC33 ^32 592 YC36 266 26 half-nephews (Table I) . Whereas many of the 84 385 187 8 0 .00- 6 0 0 030 27 30 9 interactions for the single set of female full first cousins were amicable, all of the interactions for Prebreed Early Late Early Late Post- October prep prep loctat lactat wean the single set of male full first cousins were hostile . (Breed) For an investigation of amicability of intrasexual Figure 1 . Nepotism versus competition for (a) females and interactions versus r for males and females, data (b) males . Symbols indicate means ; lines indicate one were available for three levels of r : r= 0 . 50 (parent- standard error (sr); numbers above SE lines indicate numbers of observed interactions ; numbers below SE lines offspring and full siblings), r=025 (half-siblings, indicate numbers of dyads . Note that vertical axes of (a) full aunt-niece or full uncle-nephew), and r = 0 , 125 and (b) differ . (half-aunt-niece or half-uncle-nephew, full first cousins) . Amicability of interactions did not vary significantly with r at any stage of the annual cycle cases, data from the different years were combined for either males or females (P > 0 .050 for all stages . so that each dyad was represented one time only in Kruskal-Wallis ANOVA). Thus, Hamilton's all statistical analyses . The number of observers hypothesis that nepotism should vary directly with often differed among different stages of the annual r is not supported by data from black-tails . cycle, and consequently the number of dyads for Numerous authors have pointed out that nepo- which data were available also differed among tism should vary inversely with competition different stages (Table I) . Dyads containing indi- (Hamilton 1964 ; Alexander 1974 ; West-Eberhard viduals of the same and different ages were consi- 1975). While several studies have demonstrated dered equivalent since, to this point, there is no nepotism under conditions of reduced competition evidence that amicability of interactions among (Rowley 1965 ; Woolfenden 1975 ; Brown 1978) and adults and yearlings varies systematically with age several others have demonstrated an apparent lack for either sex . For males we observed 7765 interac- of nepotism under conditions of extreme competi- tions involving 85 different dyads, and for females tion (Ingram 1959: Hamilton 1972: Eickwort

Hoogland: Nepotism in prairie dogs 267

1973), no previous study has specifically examined coterie was significantly greater during the com- how nepotism among the same individuals varies bined stages of prebreeding and late pregnancy with changes in competition . For black-tail males, through postweaning (when competition for oes- as for males of mammalian species in general trous females was minimal) than during the stage of (Darwin 1871 ; Trivers 1972), the major source of breeding-early pregnancy (when competition for intrasexual competition is almost certainly oes- oestrous females was maximal; P<0.00l, Wil- trous females . It follows that competition among coxon matched-pairs signed-ranks test) . Amicabi- black-tail males should be most extreme, and that lity of interactions among male non-kin of both nepotism should therefore be least extreme, during types did not vary similarly with stage (P > 0 .300 the stage labelled early pregnancy (breeding), when for each type, Wilcoxon matched-pairs signed- all copulations occur . Data in Fig. I support this ranks test) . Further, male interactions among kin prediction . of the same coterie were significantly more amic- Although coterie territories typically contain 30- able than interactions among both types of non-kin 50 burrow systems (King 1955 ; Hoogland 1981b), for all stages (P<0.010 for each stage, Mann-- only some of these systems are evidently suitable Whitney U-test). Male interactions involving non- for rearing offspring since in each territory only a kin of the same coterie were not significantly more small subset of systems consistently produces amicable than interactions involving non-kin of weaned juveniles over the years (unpublished data) . different coteries for any stage (P>0. 100. Mann- Further, perhaps because a colony's resources can Whitney U-test) . support only a limited number of offspring each year, lactating females sometimes try to kill the unweaned offspring of other lactating females of DISCUSSION either the home coterie or adjacent coteries (Hoog- land 1983a, in press) . It follows that competition Figure 1 shows that competition reduces, but does among black-tail females should be most extreme, not eliminate, nepotism . Thus, even when competi- and that nepotism should therefore be least tion is maximal for black-tail males during early extreme, during the stages of early pregnancy pregnancy (breeding), individual males still inter- (when females first begin to defend nesting bur- act more amicably with kin than with non-kin . rows) through late lactation . Data in Fig . I support Similarly, when competition is maximal for females this prediction. The patterns of nepotism versus during pregnancy and lactation, individual females competition for males and females shown in Fig . I still interact more amicably with kin than with non- are evident year after year for both sexes, and can kin. also be seen in the analyses of the same dyads in Changes in black-tail nepotism are sometimes different years (unpublished data) . dramatic . For example, hostile interactions typi- For females, amicability of interactions among cally begin, abruptly, the day after a female kin of the same coterie was significantly greater copulates and end, abruptly, the day that her during the combined stages of prebreeding, post- offspring first emerge from the natal burrow I I weaning, and October (when competition for nest- weeks later; before copulation and after the first ing burrows and breeding rights was minimal) than emergence of her juveniles, a female almost always during the combined stages of early pregnancy interacts amicably with other coterie females . Simi- through late lactation (when competition for nest- larly, in one multi-male coterie containing a father ing burrows and breeding rights was maximal ; and his son and in another multi-male coterie P<0.001, Wilcoxon matched-pairs signed-ranks containing two half-brothers, the two males started test). Amicability of interactions among female interacting amicably, following at least 2 weeks of non-kin of different coteries did not vary similarly almost constant antagonism, on the day after the with stage (P>0-300, Wilcoxon matched-pairs last female in the home coterie copulated . signed-ranks test) . Further, female interactions Unrelated adult males of the same multi-male involving kin of the same coterie were significantly coterie do not interact significantly more amicably more amicable than interactions involving non-kin than unrelated adult males of different coteries of different coteries for all stages (P<0-001 for (Fig. 1) . Thus, for males at least, observed patterns each stage, Mann-Whitney U-test) . For males, of nepotism seem to result ultimately from kinship amicability of interactions among kin of the same rather than from familiarity resulting from mem-

268 Animal Behaviour, 34, 1

bership in the same coterie . A similar comparison is 1973; Davis 1982), arctic ground squirrels (S . not possible for females, since female patterns of parrt •ii: Holmes & Sherman 1982, 1983 ; McLean dispersal and recruitment preclude interactions 1982), yellow-bellied marmots (Marmota ffariren- with female non-kin in the home coterie (Hoogland tris : Armitage&Johns 1982 ; Armitage 1984 . 1985), 1982, 1983b). Data on intrasexual interactions and Belding's ground squirrels (Sherman 1977 . among male and female kin from different coteries 1980b, 1981) . Only for yellow-bellied marmots and are needed for further investigation of the effects of Belding's ground squirrels has nepotism been kinship and familiarity on amicability of interac- documented to the extent reported here and else- tions . Such data sometimes result after a male from where (Hoogland 1983b) for black-tails . Nepotism one coterie disperses to an adjacent coterie and among black-tails differs from nepotism among sires offspring there, and are only now beginning to yellow-bellied marmots and Belding's ground accumulate as my long term study of black-tails squirrels in at least three important ways . First, continues. male-male nepotism is evident among black-tail Patterns of amicability of intrasexual interac- adults but absent among yellow-bellied marmot tions versus r might be biased for black-tails if (Armitage 1984) and Belding's ground squirrel individuals avoid interacting with close kin during adults (Sherman 1981) . This difference probably periods of extreme competition . Females, for results because black-tail males (Hoogland 1982), example. might consistently nest closer to distant unlike yellow-bellied marmot (Armitage & Down- kin rather than close kin, which would lead to more bower 1974) and Belding's ground squirrel males interactions with distant kin during pregnancy and (Sherman 1981 ; Holekamp 1983), sometimes dis- lactation . Biases of this sort evidently do not occur, perse together with a father, son, full brother, or since the number of observed interactions does not half-brother into the same new area, resulting in vary systematically with r for either males or frequent interactions among these kin . Second, females at any stage (P > 0 . 050 for all comparisons. whereas female-female nepotism in yellow-bellied Kendall rank correlation test) . Further, analysing marmots (Armitage 1984, 1985) and Belding's the proportion of interactions that are amicable ground squirrels (Sherman 1980b, 1981) is limited (Table I, Fig . 1) rather than the absolute numbers to mother-daughter, full sister, and half-sister of amicable and hostile interactions would remove dyads, in black-tails it also extends to more distant any biases related to partial avoidance of close kin kin such as full aunt-niece and half-aunt-niece . during periods of intense competition. Female yellow-bellied marmots (Armitage & When two black-tails interact aggressively, it is Downhower 1974) and female Belding's ground usually difficult to determine, from an observation squirrels (Sherman 1981 ; Holekamp 1983) are tower, which individual initiates the aggression . more likely to disperse away from the natal area Also, rather than recording interactions among a than female black-tails (Hoogland 1982) . Thus, small subset of colony residents, field assistants and dispersal is less likely to separate distant female kin I always attempted to record interactions for all for black-tails, and this difference would presum- colony residents with less attention to detail . ably lead to stronger selection for nepotsim among Further, in my analyses, I did not distinguish such distant kin . Third, whereas nepotism in among the different types of aggressive and amic- Belding's ground squirrels (Sherman 1980b, 1981) able interactions (e .g. fight versus chase and kiss and possibly also in yellow-bellied marmots (Armi- versus allogroom) . Even though frequency and tage 1984, 1985) seems to be most pronounced in amicability of interactions do not vary systemati- mother-daughter dyads, less pronounced in full- cally with r for either sex, it is possible that other sister dyads, and least pronounced in half-sister aspects of behavioural interactions (e .g. mean dyads, there is no evidence in black-tails for similar length of each aggressive interaction, ratio of fights consistent variation among the same or other to chases) do vary systematically with r, but this female dyads . In other words, even though genetic seems unlikely . relationships among coterie females vary exten- Among squirrels, preferential treatment of kin in sively (Table I), black-tail females do not seem to the context of behavioural interactions has been discriminate among the various types of kin but reported for round-tailed ground squirrels (S . rather only between kin (members of the home tereticaudus : Dunford 1977), Richardson's ground coterie) and non-kin (members of different coter- squirrels (S. richardsonii : Yeaton 1972 ; Michener ies). Similar patterns of nepotism are evident in

Hoogland: Nepotism in prairie dogs 269

black-tail alarm calling ; individual males and Foundation, The Universities of Michigan, Mary- females with offspring in the home coterie do not land and Minnesota, and Princeton University's call significantly more often than individuals with Whitehall Foundation . For help with the manu- only non-descendant kin in the home coterie script, I thank Richard Alexander, Ken Armitage, (Hoogland 1983b) . These surprising results for Charles Brown, Paul Harvey, Henry Horn, Robert behavioural interactions and alarm calling do not May, Dan Rubenstein, Paul Sherman, George necessarily imply that black-tails do not or cannot Williams and Edward Wilson . discriminate between close kin and distant kin in other contexts, and an investigation of nepotism versus r in other contexts is in progress . REFERENCES As my study of black-tails continues, I am becoming more able to determine distant genetic Alexander, R . D . 1974 . 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For males, on the other hand, the Armitage, K . B . In press . Marmot polygyny revisited : new data suggest that individuals interact with full determinants of male and female reproductive strategies . In : Ecological Aspects of Social Evolution (Ed . first cousins (as suggested in Table I), full first by D . I . Rubenstein & R . W . Wrangham) . Princeton: cousins once removed, half first cousins, and full Princeton University Press . second cousins of the home coterie as though they Armitage, K . B . & Downhower, J . F . 1974 . Demography are non-kin . More data are needed, especially for of yellow-bellied marmot populations . EroloQr . 55, males, on interactions among distant kin of the 1233-1245 . Armitage, K . B . & Johns, D . W . 1982 . Kinship, reproduc- home coterie . tive strategies and social dynamics of yellow-bellied Few hypotheses in behavioural ecology and marmots . Behar . Ecol. Sociohiol.. 11, 55 63 . sociobiology have generated as much theoretical Bertram, B . C . R. 1976 . Kin selection in lions and (e .g . Orlove 1975 ; Milinski 1978 ; Weigel 1981) and evolution. In : Growing Points in Ethology (Ed . by P . P . pp . 281-301 . empirical (e .g . Kurland 1977 ; Greenberg 1979 : G. Bateson & R . A . Hinde), Cambridge: Cambridge University Press . Sherman 1980b: Woolfenden & Fitzpatrick 1984) Brown, J . L . 1978 . Avian communal breeding systems . research as Hamilton's (1964) hypothesis that Ann Rev . Ecol. Syst ., 9, 123-155 . nepotism should vary directly with r . Definitive Buckle, G . R . & Greenberg, L . 1981. Nestmate recogni- field studies are rare, and have uncovered evidence tion in sweat bees (Lasioglo.ssum zephrrum) : does an individual recognize its own odour or only odours of its both for and against Hamilton's (1964) hypothesis . nestmates'' Anim . Below ., 29, 802 809 . Further investigations involving long term field Carlin, N. F . & Holldobler, B . 1983 . Nestmate and kin study seem crucial for a better understanding of recognition in interspecific mixed colonies of ants . nepotism versus r under natural conditions . Science, X . Y ., 222, 1027--1029 . Chagnon, N . A . 1979 . Mate competition, favoring close kin, and village fissioning among the Yanomamo ACKNOWLEDGMENTS Indians . In : Erolutionarv Biology and Human Social Behavior . An Anthropological Perspective (Ed . by N . A . I thank the 94 field assistants who have helped me Chagnon & W . G . Irons) . pp . 86 131 . North Scituate : with my research over the last 12 years . For Duxbury Press . Clutton-Brock, T . H . & Harvey . P . H . 1976 . Evolutionary financial assistance, I thank The National Science rules and primate societies . In : Growing Points in Foundation (grants BNS77-15594, BNS79-24093, Ethology (Ed . by P . P . G . Bateson & R . A . Hinde) . pp . DEB81-02791, and BSR83-07705), The National 195 237 . Cambridge : Cambridge University Press . 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