Proc. Natl. Acad. Sci. USA Vol. 92, pp. 8092-8099, August 1995 Review An evolutionary theory of the family (ecological constraints/kin selection/reproductive skew/step-parent/incest avoidance) Stephen T. Emlen Section of Neurobiology and Behavior, Comell University, Ithaca, NY 14853-2702 Communicated by Thomas Eisner, Cornell University, Ithaca, NY, May 5, 1995

ABSTRACT An evolutionary frame- assumption of sociobiology), while the (i) Ecological constraints theory (11- work for viewing the formation, the sta- second argues that, even if present, heri- 16)-which examines factors affecting dis- bility, the organizational structure, and table aspects of social behavior will be of persal options of sexually maturing off- the social dynamics of biological families minor importance. spring. It specifies the conditions for de- is developed. This framework is based Both criticisms can be easily dispelled. layed dispersal and, hence, the formation upon three conceptual pillars: ecological The condition-dependent expression of of family social units. constraints theory, inclusive fitness the- many social behaviors in no way precludes (ii) Kin selection theory (6, 17, 18)- ory, and reproductive skew theory. I offer them from genetic influence. The work of which helps identify the types and contexts a set of 15 predictions pertaining to living researchers such as Maynard-Smith (2) of social interactions expected among within family groups. The logic of each is and Parker (3) has clarified the relation- family members (most of whom are ge- discussed, and empirical evidence from ship between conditionality and the evo- netic relatives). family-living vertebrates is summarized. I lution of behavior. Indeed, the last decade (iii) Reproductive skew theory (19- argue that knowledge of four basic pa- has seen a marked shift toward viewing 24)-which incorporates and expands on rameters, (i) genetic relatedness, (ii) so- organisms as "decision makers," selected areas i and ii to predict when conflict over cial dominance, (iii) the benefits of group to accurately assess the consequences of reproduction is expected within families living, and (iv) the probable success of different behavioral options available to and when such conflict will result in re- independent reproduction, can explain them and to express those behavioral vari- productive sharing. Such sharing creates many aspects of family life in birds and ants that maximize their fitnesses (e.g., extended family structures. mammals. I suggest that this evolutionary refs. 4 and 5). Depending upon social A set of 15 evolutionary predictions perspective will provide insights into un- circumstances, the optimal choice of be- pertinent to family living is presented be- derstanding human family systems as haviors may vary. But, providing that her- low in Family Formation and Stability, well. itable variation exists in the assessment Family Dynamics, and Family Structure. I algorithms underlying the choices, natural discuss the logic of each prediction and Two decades ago, in the introduction to selection can fine-tune the decision rules provide a synopsis of the relevant litera- his treatise, Sociobiology: The New Synthe- and thereby bring them into the realm of ture from family-dwelling vertebrates. sis, E. 0. Wilson (1) stated that ". . . soci- darwinian predictability. Predictions and data are summarized in ology and the other social sciences ... are The second criticism pertains to the use Table 1. Additionally, I discuss why these the last branches of biology waiting to be of evolutionary models to predict the so- predictions should generalize across taxa, included in the Modern Synthesis." He cial behaviors of higher primates, partic- to all species that live in family groups, was referring to the untapped potential of ularly our own species. The obvious im- including humans. darwinian thinking to provide a concep- portance of cultural influences on our tual framework for better understanding behavior does not negate the probability Definition of Family many aspects of human behavior. In the that we humans also possess a set of intervening years, a small but growing biologically based predispositions for inter- There is no strict consensus among social number of evolutionary anthropologists acting with one another. It is these predis- scientists as to what constitutes a family. and psychologists has begun making in- positions that one attempts to predict from Sociologists typically stress functional as- roads into "darwinizing" the social sci- evolutionary models of behavior. pects of the child rearing unit: families are ences. But their progress has been slow Progress in "darwinizing" the social sci- groups of coresident adults responsible for and has often been met with resistance. ences has also been slowed by the absence the production, socialization, and educa- Two often-cited reasons for such resis- of a general evolutionary theory of the tion of offspring (e.g., refs. 72-74). An- tance are (i) a belief that the tremendous family. The seminal contributions, for ex- thropologists stress kinship and intergen- plasticity that exists in the expression of ample, of Trivers (6) on parent-offspring erational aspects of families: families are social behaviors renders applicability of conflict, of Trivers and Willard (7) on kin groups through which descent lines are biological (genetic) principles unlikely and differential investment in sons and daugh- traced and which consist, at a minimum, of (ii) the view that culture, rather than ters by parents, of Alexander (8) on pa- parent(s) and unmarried offspring (75, genes, is of overriding importance in me- ternity and nepotism, and of Daly and 76). diating such behaviors in our own species. Wilson (9, 10) on the effects of genetic In humans, preferential interactions oc- The first seemingly contradicts the idea of relatedness on child abuse, represent im- cur between offspring and their parents a heritable basis for social behaviors (an portant steps in this direction. even after offspring have established Building on these and other studies, I households of their own. To ease the task a The publication costs of this article were defrayed develop general evolutionary framework of seeking parallels between human and in part by page charge payment. This article must for understanding biological families. This nonhuman species, I restrict the definition therefore be hereby marked "advertisement" in framework is based upon the integration of animal families to those cases where accordance with 18 U.S.C. §1734 solely to indicate of three overlapping conceptual areas of offspring also continue to interact regu- this fact. behavioral ecology: larly, into adulthood, with their parents 8092 Downloaded by guest on September 29, 2021 Review: Emlen Proc. Natl. Acad. Sci. USA 92 (1995) 8093

Table 1. Biological families: Evolutionary predictions and empirical evidence No. Abbreviated prediction Evidence Family formation: The importance of delayed dispersal 1 Family groupings will be unstable, Supportive: avian, Melanerpes formicivorus (25), Picoides borealis disintegrating when acceptable (26), Phoeniculus purpureus (27), Malurus cyaneus (28), Aphelocoma reproductive opportunities materialize coerulescens (29), Nesomimus parvulus (30), and Acrocephalus elsewhere. sechellensis (31); mammalian, Peromyscus leucopus (32) and Dipodomys spectabilis (33) 2 Family stability will be greatest in those Supportive: avian, Melanerpes formicivorus (34, 35), Aphelocoma groups controlling high quality resources. ultramarina (36), Aphelocoma coerulescens (37), Campylorhynchus Dynasties may form. nuchallis (38), and Acrocephalus sechellensis (31) Family dynamics: Kinship and cooperation 3 Help with rearing offspring will be the Supportive: 107 avian species* and 57 mammalian species* norm. Counter: 5 avian species* and 6 mammalian species* 4 Help will be expressed to the greatest Supportive: avian, Merops bullockoides (39), Manorina melanophrys extent between closest genetic relatives. (40, 41), Manorina melanocephala (42), Nesomimus parvulus (43), and Gymnorhinus cyanocephalus (44); mammalian, Hyaena brunnea (45), Helogale parvula (46), and Panthera leo (47) Counter: avian, Aphelocoma ultramarina (36) 5 Sexually related aggression will be Supportive: 18 avian species* and 17 mammalian species* will reduced because incestuous matings Counter: 1 avian and 3 mammalian species* be avoided. Pairings will be exogamous. species* 6 Breeding males will invest less in Supportive: avian, Melanerpes formicivorus (48) (Many additional offspring as their certainty of paternity studies, some supportive, others counter, have been conducted on decreases. nonfamilial species.) Family dynamics: Disruption after breeder loss or replacement 7 Family conflict will surface over filling Supportive: avian, Melanerpes formicivorus (34), Picoides borealis the reproductive vacancy created by the (49), Eopsaltria georgiana (50), Campylorhynchus nuchallis (38), loss of a breeder. Acrocephalus sechellensist, and Turdoides squamiceps (51) 8 Sexually related aggression will increase Supportive: avian, Melanerpes formicivorus (34, 52), and Merops because incest restrictions do not apply bullockoidest, Campylorhynchus nuchalis (53), and Turdoides to replacement mates. Offspring may squamiceps (51) mate with a step-parent. 9 Replacement mates (step-parents) will Supportive: avian, Melanerpes formicivorus (48, 54, 55) and invest less in existing offspring than will Nesomimus parvulus (56); mammalian, for summaries of mammalian biological parents. Infanticide may occur. data, see Hrdy (57) and Hausfater and Hrdy (58) 10 Family members will reduce their Supportive: avian, Aphelocoma coerulescens (59) and Acrocephalus investment in future offspring after the sechellensis (60) repairing of a parent. Counter: avian, Picoides borealis (49) and Campylorhynchus nuchallis (102) 11 Step-families will be less stable than (No data currently available) biologically intact families. Family structure: Reproductive sharing leads to extended families 12 Decreasing ecological constraints will Supportive: avian, Merops bullockoides (14) and Nesomimus parvulus lead to increased sharing of (62) reproduction. 13 Decreasing asymmetry in dominance will Supportive: avian, Malurus splendens (61) and Turdoides squamiceps lead to increased sharing of (51); mammalian, Helogale parvula (69, 70) reproduction. 14 Increasing symmetry of kinship will lead Supportive: avian, Melanerpes formicivorus (63), Merops bullockoides to increased sharing of reproduction. (64), Aphelocoma ultramarina (36), and Turdoides squamiceps (51) 15 Decreasing genetic relatedness will lead Supportive: avian, Poryhyrio poryhyrio (65), Buteo galapagoensis (66), to increased sharing of reproduction. Merops bullockoides (64, 67), Crotophaga sulcirostris (68) and Prunella Reproductive suppression will be modularis (107); mammalian, Helogale parvula (69, 70) and Panthera greatest among closest kin. leo (71) Species listed are those for which available data allow testing of the prediction in question. Numbers in parentheses refer to references. *S.T.E. and N. J. Demong, unpublished compilation. tj. Komdeur, personal communication. tS.T.E., P. H. Wrege, and N. J. Demong, unpublished data.

(16). Typically, this occurs when offspring which only a single female breeds, and the presence or absence of reproductive delay dispersal and continue to reside with extended families, in which two or more males forms the basis of a second parti- one or both parents past the age of sexual relatives of the same sex reproduce. The tioning into biparental, vs. matrilineal, maturity. I distinguish between simple presence of a breeding male is not essen- families. It is useful to further differenti- families (single parent or conjugal pair), in tial to the definition of a family. Rather ate between intact families, those where Downloaded by guest on September 29, 2021 8094 Review: Emlen Proc. Natl. Acad. Sci. USA 92 (1995)

the original breeders are still the repro- what makes for a good situation at home, tition to fill these vacancies will be more ductives, and replacement families where, and vice versa. intense. The result will be prolonged phi- because of death, divorce, or departure, a Consequently, I propose a generalized lopatry and greater temporal stability of breeder has been replaced. For simplicity, economic model of family formation (14, family units controlling high-quality re- I exclude large assemblages in which par- 16) that incorporates aspects of both ar- sources. ents and mature offspring reside but have guments above. It can be stated as follows: Six avian studies allow testing of Predic- no spatial territory of their own (e.g., (i) Delayed breeding occurs when the tion 2; each provides supportive results many troop-living primates and ungulates) production of mature offspring exceeds (31, 34-38). although many of the predictions should the availability of acceptable opportuni- Inheritance of the parental breeding also apply to them. ties for their independent reproduction. position represents a common route to (ii) Under such circumstances, some off- achieving breeding status among many Family Formation and Stability spring must wait until acceptable repro- species of family-dwelling birds and mam- ductive vacancies arise and then compete mals (see refs. 13, 25, and 81-83). The The key to understanding the evolution of to fill them. (iii) Families form when such greater the quality of the resources con- families is understanding the causes of waiting is best done at home, when re- trolled by the family, the greater will be delayed dispersal. One probable reason maining on the natal territory and/or the incentive to remain at home to inherit why families are so rare in nature (only 3% associating with one's family somehow them (see Prediction 7). Few studies have of bird and mammal species are known to augments the offspring's inclusive fitness. proceeded long enough to test this portion be familial) is that delayed dispersal en- Family formation thus can be viewed as a ofPrediction 2. But work on Florida scrub tails an automatic fitness cost. In intact "solution" to the temporary problem of a jays, Aphelocoma coerulescens, has docu- simple families, offspring do not repro- shortage of acceptable reproductive op- mented the continuous occupancy of high duce and in extended families their repro- portunities. This leads directly to my first quality territories by familial lineages over duction is frequently suppressed. Thus the prediction. several generations (G. Woolfenden, per- cost of delayed dispersal is the forfeiture Prediction 1. Family groupings will be sonal communication). I expect family of fitness associated with missed repro- inherently unstable. They will form and dynasties will prove common as long-term ductive opportunities. Families develop expand when there is a shortage of accept- monitoring studies continue. only when offspring that remain with their able reproductive opportunities for mature parents and forego early breeding oppor- offspring, and they will diminish in size or Family Dynamics: Kinship and tunities somehow compensate for this cost dissolve (break up) as acceptable opportu- Cooperation (16). nities become available. Two seemingly opposing schools of Evidence in support of Prediction 1 Family dynamics, the social interactions thought have emerged to explain delayed comes from a number of long-term obser- that occur among family members, are dispersal. Ecological constraints models vational studies and from field experi- expected to differ from the dynamics of (11-16) emphasize the scarcity of accept- ments in which breeding vacancies were other types of social groupings because able reproductive vacancies available to artificially manipulated. Data from five families are largely composed of genetic maturing offspring, as well as the low avian (25, 27, 29-31) and two mammalian relatives. Hamilton's theory of kin selec- success often associated with early, or (32, 33) species provide especially con- tion (17) revolutionized evolutionary unaided, breeding attempts by such indi- vincing evidence that families form only thinking about social behavior by stressing viduals. The automatic cost is low because when acceptable breeding opportunities that individuals contribute genetically to the fitness benefit associated with leaving are limited. Experimental verification of future generations both directly, through home is low. The "missed reproductive this causal link has been obtained in three the production of their own offspring, and opportunities" are nonexistent or of poor bird species (26, 28, 31). For each, breed- indirectly, through their positive effects quality. ing vacancies were created where none upon the reproduction of relatives. The In contrast, benefits-of-philopatry mod- previously existed. The effects on family sum of these two effects constitutes an els (35, 77-79) emphasize the fitness ben- stability were striking. In each case, ma- individual's inclusive fitness. By virtue of efit gained by staying with one's parents ture offspring living within their parents' common descent, both one's offspring and on the natal territory. Benefits may in- territories left home to fill the vacancies, the offspring of relatives have predictable clude enhanced survivorship while waiting causing the dissolution of family groups. probabilities of carrying alleles that are for outside reproductive opportunities to Prediction 2. Families that control high identical to one's own. The closer the arise, improved abilities to compete when quality resources will be more stable than genetic relationship, the greater the fre- they materialize, and the possibility of those with lower quality resources. Some quency of such shared alleles. sharing or inheriting the natal breeding resource-rich areas will support dynasties in Kinship is thus predicted to influence position itself. Also included are any in- which one genetic lineage continuously oc- the types of behaviors exhibited within direct benefits gained by helping parents cupies the same area over many successive families. Predictions 3 and 4 derive directly or other kin while staying home. generations. from kin selection theory. I have argued elsewhere (refs. 14 and Prediction 2 follows from the realization Prediction 3. Assistance in rearing off- 16; see also refs. 15 and 80) that these two that what constitutes an acceptable repro- spring (cooperative breeding) will be more models represent two sides of a semantic ductive opportunity for one individual prevalent in family groups than in otherwise coin. Both assume that maturing offspring may be quite unacceptable to another. comparable groups composed of nonrela- assess the profitabilities of two options: When the fitness associated with staying at tives. dispersing early and attempting to breed home varies with the quality of the natal Cooperative breeding occurs when an independently (B) vs. delaying dispersal territory or the composition of the family adult member of a social group provides and staying at home (S). Both further group, the quality of the reproductive regular care to offspring that are not ge- assume that offspring remain with their opportunity that will be sufficient to favor netically its own. It typically involves pro- parent(s) only when the expected inclusive dispersal also will vary. Specifically, off- visioning and defending such offspring for fitness benefit of doing so exceeds that spring from high quality natal situations a prolonged period of time. expected by leaving (i.e., when S - B > 0). will be more choosy in their dispersal A survey of the literature provides And both emphasize similar interrelated decisions (15, 16, 77). A smaller fraction of strong support for Prediction 3. More than variables: having poor options for inde- available breeding vacancies will be ac- 90% of both family-living birds and mam- pendent breeding is an integral part of ceptable to such individuals, and compe- mals (excluding primates) exhibit cooper- Downloaded by guest on September 29, 2021 Review: Emlen Proc. Natl. Acad. Sci. USA 92 (1995) 8095

ative breeding (Table 1). Cooperative data are available show strong tendencies when resources controlled by the family are breeding also occurs in familial species of to pair exogamously (Table 1). of high quality. both eusocial insects (84, 85) and social Incest avoidance is not universal among If family formation is a "solution" to the spiders (86, 87). Assistance in the rearing vertebrates, however (see refs. 93 and 94). problem of a shortage of acceptable of young appears to be the norm within Neither is Prediction 5 an absolute. As breeding vacancies and if one route to family-structured societies. ecological constraints on the option of becoming a breeder is to inherit the natal In contrast, such assistance is rare in independent breeding become increas- breeding position, then the loss of a parent nonfamilial species. Of all the birds and ingly severe, a point may be reached where creates an excellent opportunity for an mammals known to exhibit cooperative it is better to breed incestuously than to offspring (or another subordinate kin in breeding, fully 88 and 95% of those for risk not breeding at all. These conditions the case of extended families) to ascend to which social organization is known live in have been modeled by Bengtsson (95) and breeding status on its home territory. The family groups (107 of 121 and 57 of 60 Waser et al. (96). higher the quality of the family resources, species, respectively; S.T.E. and N. J. De- Prediction 6. Breeding males will invest the more intense the expected competi- mong, unpublished compilation). Coopera- less in offspring as their certainty ofpater- tion to fill the breeding vacancy. tive breeding as a reproductive system thus nity decreases. Offspring of most species, however, will is largely restricted to familial societies. This prediction is not restricted to familial not pair with a parent (Prediction 5). Con- Predition 4. Assistance in rearing offspring species but will apply to any situation where sequently, an offspring can only secure the (cooperative breeding) will be expressed to the males provide care for dependent young. breeding vacancy for itself if it obtains an greatest e-xtent between thosefamily members Parental care is a form of kin assistance. unrelated mate from outside the group. In that are the closest genetic relatives. Offspring share-half their genes with each simple families (in which only one female The clearest tests of Prediction 4 come parent, providing that the social parent is breeds), the offspring must also prevent from cooperatively breeding species that actually a biological parent. When a breeder continued reproduction by its surviving par- live in extended families, those in which has been cuckolded, however, its related- ent. Such prevention can include resisting multiple individuals (or pairs) are breed- ness to the offspring is zero, and the fitness the settlement of a replacement mate, be- ers. This situation provides potential allo- benefit accrued by caring for such offspring haviorally suppressing breeding by the sur- parents with choices, making it possible to largely disappears. viving parent, or physically evicting the par- ask whether they preferentially aid their For most vertebrate species, parental ent from the group. Without such action, the closest kin. In studies conducted to date, uncertainty is primarily a male problem. surviving parent will recruit a new mate of five of six bird species (39-44) and three We thus should expect males to be sensi- its own and continue as sole breeder. of three mammals (45-47) show the pre- tive to their risk of cuckoldry and to adjust In most vertebrate species, dominance is dicted preferential allocation of aid. their behaviors accordingly (97). Recent influenced by gender and age. Males typi- Prediction 5. Sexually related aggression models (e.g., ref. 98) suggest that cuck- cally are dominant over females, and older will be less prevalent in family groups than olded males should reduce or terminate individuals are dominant overyounger ones. in otherwise comparable groups composed their investment in current young when Thus when a breeding female dies, a surviv- ofnonrelatives. This is because opposite-sex continued care is costly and when there is ing daughter will rarely challenge her father closegenetic relatives will avoid incestuously a sufficiently high probability of their for breeder status. However, challenges are mating with one another. achieving greater assurance ofpaternity in expected between sons and mothers (and Prediction 5 derives from the fact that future breedings. sons and potential step-fathers) after the incestuous matings between close relatives Only one study of a familial species has loss of a father. often have deleterious genetic conse- tested Prediction 6. By varying the timing Note that an offspring will be less re- quences in normally outbred populations. of temporary removal experiments, Koe- lated to future young produced by a sur- Inbreeding causes an increased frequency of nig (48) showed that breeding male viving parent and step-parent (its half- homozygosity that results in the phenotypic Acorn woodpeckers, Melanerpes formi- siblings) than to its own future offspring expression of recessive alleles whose nega- civorus, indeed vary their nurturing be- should it become a breeder. This provides tive effects are otherwise masked. Delete- haviors according to their probability of an additional evolutionary "incentive" for rious effects of inbreeding have been docu- siring offspring. attempting to usurp the breeding position mented in many (but not all) vertebrate after the disappearance of a parent (see species examined (e.g., refs. 88-92). Family Dynamics: Disruption After also Prediction 10). Natural selection is thus expected to Breeder Loss or Replacement The literature is full ofvivid accounts of foster the evolution of inbreeding avoid- within-family power struggles for breeding ance mechanisms. These mechanisms will The death, divorce, or departure of a status after a parental loss (e.g., refs. 34, lead to decreased tendencies to pair with, breeding parent, and its replacement from 38, 50, and 51). And in simple conjugal or to show sexual interest in, close genetic outside the group, will alter the basic family species, sons replace their deceased relatives of the opposite sex. Conse- genetic structure of the family unit. Such fathers as breeders much more often than quently, sons will rarely compete with loss of a parent is expected to profoundly daughters replace their deceased mothers their father and daughters will rarely com- alter the social dynamics of the family (see refs. 13 and 82). To cite one example, pete with their mother for sexual access to group and, potentially, its stability as well. in Red-cockaded woodpeckers, Picoides the parent of the opposite sex. Neither will Predictions 7-11 pertain to these changes. borealis, in each of 23 instances after the siblings compete for sexual access to one These predictions are phrased in terms of death of a father, sons assumed breeder another. The result will be a reduced biparental families, but all except Predic- status and mothers dispersed (49). incidence of mate guarding and other tion 8 are applicable, with slight modifi- Prediction 8. Sexually related aggression forms of sexually related harassment and cations, to matrilineal families as well. will increase after the re-pairing ofa parent. aggression within family groups. Prediction 7. The loss of a breeder will In the specific case ofsimple conjugalfam- A literature survey (S.T.E. and N. J. result infamily conflict over thefilling ofthe ilies, the surviving parent and its mature Demong, unpublished compilation) indi- resulting reproductive vacancy. In the spe- same-sex offspring will now compete for cates that, despite frequent opportunities cific case of simple conjugal families, the sexual access to the replacement mate (step- to interact sexually with other family survivingparent and its mature opposite-sex parent). This conflict will be especially se- members, incestuous matings are exceed- offspring will now compete for breeder sta- vere when the asymmetry in dominance ingly rare. Fully 18 of 19 avian, and 17 of tus. The conflict will be especially severe between the surviving breeder and its same- 20 mammalian, family species for which when offspring are ofthe dominant sex and sex offspring is small. Downloaded by guest on September 29, 2021 8096 Review: Emlen Proc. Natl. Acad. Sci. USA 92 (1995) If a divorced, widowed, or abandoned ditions under which an incoming mate is Prediction 11 has yet to be tested rigor- parent takes a new mate, the replacement is expected to adopt, ignore, or destroy any ously. However, in three avian species almost invariably from outside the family current dependent young. offspring of the same sex as the step- group (Prediction 5). Parental re-pairing Prediction 10. Nonreproductive family parent are more likely to leave their family thus provides a mating opportunity that is members will reduce their investment in group after the re-pairing of a parent than exempt from incest restrictions for mature future offspring after the replacement of a are their opposite-sex siblings (34, 103, offspring of the same sex as the remaining closely related breeder by a more distantly or 104). parent. This opens an avenue for such off- unrelated individual. spring to gain direct fitness by reproducing This prediction follows directly from Family Structure: Reproductive Sharing with the new unrelated breeder. kin selection theory. Natal family mem- Leads to Extended Families Shared reproduction, however, typically bers will be only one-half as related to will have detrimental fitness conse- future offspring produced by a parent and Much of the previous discussion has dealt quences for the surviving parent. Thus an unrelated replacement mate as to with simple families (single parents or while the appearance ofsexual behavior in former offspring produced by both bio- conjugal pairs and their grown offspring) previously nonsexual offspring is expected logical parents. The indirect benefit real- in which reproduction is monopolized by after the re-pairing of a parent, so too is an ized by helping to rear such future off- the single dominant female. Sometimes, accompanying increase in sexual conflict spring will be correspondingly decreased. however, two or more relatives of the (e.g., mate guarding, intrasexual aggres- Surprisingly few vertebrate studies have same sex breed, giving rise to extended sion, and attempted reproductive suppres- tested this prediction. Two avian reports family structures. In vertebrates, this most sion) between family members. (49, 102) provide contrary evidence (non- typically occurs when offspring reproduce In one of the few studies to examine breeders provisioned full- and half- concurrently with their parent(s). Ex- Prediction 8, Piper and Slater (53) con- siblings equally), whereas two others (59, tended families may be matrilineal or bi- trasted behavior in intact vs. replacement 60) demonstrate support (the proportion parental. They generate assemblages of families of Stripe-backed wrens, Campy- of family members assisting in rearing relatives that may include grandparents, lorhynchus nuchalis. Sons displayed no young decreased significantly when a step- aunts, uncles, cousins, 'and in-laws, in ad- sexual interest in their mothers, but they parent assumed a breeding role and dition to simply parents and offspring. frequently courted their step-mothers. Pa- dropped to near zero when both parents The fundamental challenge in explaining ternity data showed that while sons never were replaced). the diversity of family structures lies in iden- sired offspring with their biological moth- Prediction 11. Replacement (step-) fam- tifying the conditions under which repro- ers, they did so with their step-mothers. ilies will be inherently less stable than bio- duction becomes shared. Several models, Replacement families also showed logically intact families. This will be espe- collectively known as reproductive skew the- marked increases in father-son aggres- cially true when offspringfrom the originally ory, have addressed this question (19-24). sion. Analogous results are reported in intact family are of the same sex as the Reproductive skew refers to the distributio'n three other avian studies (34, 51, 52). step-parent. of direct reproduction among same-sex Prediction 9. Replacement breeders (step- I have argued that the replacement of a members of a group and can vary from a parents) will invest less in existing offspring parent by an unrelated breeder will have value of 1 (when reproduction is totally than will biological parents. They may in- negative consequences on the fitness of off- monopolized 'by a single individual) to 0 fanticidally kill current young when such spring that continue to reside with their (when reproduction is distributed equitably action speeds the occurrence, or otherwise replacement families. Offspring of both among all mature individuals) (20, 21). All increases the success, oftheir own reproduc- sexes suffer a reduction in future indirect models assume that dominant individuals tion. This will be more likely when the benefits available from helping rear young control the reproduction of subordinates. replacement mate is of the dominant sex. ofthe new breeding pair (Prediction 10), and All further assume that, all else being equal, This prediction builds on Prediction 6. all risk possible reduction in investment in dominant individuals will maximize their Because replacement mates typically will them by the replacement breeder (Predic- own fitness by monopolizing breeding them- be unrelated to current family members, tion 9). These factors are predicted to make selves. they will gain no clear fitness benefit from replacement families less stable than intact The central idea of skew theory is that helping to rear dependent offspring from families because a reduction in the fitness when dominants in the group benefit from previous breedings. Such help is not ex- associated with staying at home lowers the the continued presence of subordinates, pected unless the replacement mate ben- quality of the outside reproductive oppor- dominants may, under certain circum- efits in some other way from its actions. tunity sufficient to favor offspring dispersal stances, share reproduction in order to In circumstances where the continued (which leads to family dissolution). induce the subordinates to remain. Alex- care of extant offspring delays reproduction In biparental families, these negative con- ander (18) and Emlen (19) call such in- by the replacement mate, conflict is ex- sequences may be offset for a mature off- ducements "fitness forfeiting"; Reeve and pected. The abandonment, eviction, or in- spring of the same sex as the surviving Ratnieks (23) call them "staying incen- fanticidal destruction of such offspring may biological parent. With incest inhibitions tives." Provided that the dominant, while result. Given the typical dominance asym- lifted, such an offspring might reproduce sharing reproduction, still realizes a metries between the sexes, such forcible with the replacement mate (Prediction 8). If higher inclusive fitness than it would in the actions will occur more frequently with this occurs, the offspring will gain direct absence of the subordinate, the result can male, than with female, replacement mates. fitness through personal reproduction. be a "win-win" situation for both partic- The hypothesis of adaptive sexually se- Should the surviving biological parent die, ipants. The sequence of decisions leading lected infanticide was first proposed by the offspring iswell-positioned to inherit the to various types of family structures is Hrdy (57) and has received support from primarybreeding spot because it already has shown in Fig. 1. numerous studies of rodents, carnivores, a suitable mate. The stability of the new Skew models identify four parameters and primates (for review, see ref. 58). family unit will depend, in part, upon the that specify the conditions under which re- Among birds, there is a growing literature specifics of these fitness trade-offs. productive sharing should occur and the documenting cases of rejection or destruc- Neither of these potential benefits is amount of sharing expected. These are (i) tion of eggs and young by avian step- available to offspring of the same sex as the magnitude of any benefit realized by the parents (e.g., refs. 48,54-56, and 99-101). the step-parent, who are, therefore, pre- dominant if the subordinate should stay, (ii) These trade-offs are discussed more fully dicted to be more likely to leave the family the expected success of the subordinate if it by Rohwer (100) who examines the con- unit after a parental replacement. should leave, (iii) the relative asymmetry in Downloaded by guest on September 29, 2021 ReVieW: Emlen Proc. Natl. Acad. Sci. USA 92 (1995) 8097

Does subordinate remain in group without direct reproduction?

Does dominant forfeit some direct reproduction to induce subordinate to stay?

FIG. 1. Reproductive skew theory depicts the formation of extended family structures as the compromise resolution to family conflict over the dispersal decisions of subordinates. Shared reproduction is predicted when the dominant benefits from the continued retention of the subordinate within the family group, but the subordinate, in the absence of any direct reproduction, would realize greater fitness by leaving. Extended families are more reproductively egalitarian than simple families (patterned after figure 3.1 of ref. 23). dominance between the potential cobreed- Reproductive sharing thus is expected are more likely to become cobreeders than ers (the dominant and subordinate), and (iv) primarily at intermediate levels of severity are individuals more dissimilar in age. the genetic relatedness between them (19- of ecological constraints, when conditions Prediction 14. Reproduction within a 24). Each parameter influences the relative afford viable reproductive opportunities family will be shared more equitably when payoffs of staying vs. leaving for the differ- for subordinates, but are not so benign the potential cobreeders consist of siblings ent participants. Collectively, they deter- that the benefits of continued group living than when they consist of parent(s) and mine the leverage that the dominant has in for dominants disappear altogether. grown offspring. "withholding," and the subordinate has in Familial species that exhibit variable In some extended families, same-sex sib- "demanding," (anthropomorphically speak- levels of reproductive skew are ideal sub- lings will be potential cobreeders. When this ing) a share of reproduction. jects for testing Prediction 12. In both occurs, the genetic relatedness between The interaction of these four factors de- White-fronted bee-eaters, Merops bullock- each sibling and the offspring of the other is termines the outcome of reproductive com- oides, and Galapagos mockingbirds, Neso- symmetrical (r = 0.25 for each). All else petition within the family. A necessary pre- mimus parvulus (the only two vertebrate being equal, under conditions where repro- condition for reproductive sharing is that species for which requisite data are avail- ductive sharing is favored by one sibling, it the dominant must benefit from its contin- able), the frequency of shared breeding will also be favored by the other. ued association with the subordinate; only was greatest in seasons when ecological In contrast, mothers and daughters (or then will extended family structures de- constraints were most benign (12, 62). fathers and sons) typically are asymmetri- velop. The remaining three parameters Prediction 13. Reproduction within a cally (unequally) related to one another's form the bases for the final four predictions. family will become increasingly shared as future offspring. Assuming mate fidelity the asymmetry in social dominance between on the part of the parents, an offspring will Prediction 12. Reproduction within a potential cobreeders decreases. be more closely related to its parents' family will become increasingly shared as the severity of ecological constraints de- A subordinate always has the option of future offspring (its full siblings, r = 0.5) directly challenging the dominant for re- than the parents will be to the offspring's creases, that is, as the expected profitability of the subordinate's option ofdispersal and productive rights within the group. A suc- offspring (their grand-offspring, r = 0.25). cessful challenge can result in the domi- The parent thus has more to gain from independent reproduction increases. nant's overthrow and the subordinate's withholding shared reproduction than the The leverage that a subordinate can assumption of breeder status. The costs offspring does from demanding it. This wield depends both on the profitability of can be high for both participants. Fights will lead to greater reproductive skew in its and on the dispersal option magnitude may lead to injury, eviction, or even death. parent-offspring, compared with sibling- of the benefit to the dominant of continu- All else being equal, the benefits of such sibling, associations (105). This will only ing its association with the subordinate. challenges for a subordinate, as well as the be true, however, provided that no paren- The profitability of the subordinate's dis- risks for a dominant, will be greatest when tal mate-change or extra-pair fertilization persal option, in turn, depends on the the disparity in their fighting abilities is least has occurred. Reeve and Keller (105), who number and quality of available breeding (23). It may then be advantageous for the recently modeled this comparison, cite vacancies, as well as the expected success dominant to share reproduction. Such shar- several species that breed in extended of unaided breeding attempts. These are ing will increase the profitability for the families of variable composition and show the same factors that define the severity of subordinate of staying and continuing to the predicted shift in reproductive skew the ecological constraints on independent cooperate, thereby reducing the magnitude (36, 51, 63). I would add one more (64). breeding (12-14). of any gain to be realized by challenging the Prediction 14 will be difficult to test Interestingly, if conditions become too dominant. Reeve and Ratniecks (23) call definitively because two additional fac- benign (e.g., if the advantages of large such fitness forfeiting a "peace incentive." tors, the age-related dominance asymme- group size, or cooperative rearing of off- Several studies provide suggestive sup- try typical between parents and offspring spring, decrease sufficiently), the impor- port for Prediction 13. For example, in (Prediction 13) and the avoidance of in- tance of subordinates to the inclusive fit- Splendid fairy-wrens, Malurus splendens cestuous matings between parent and off- ness of the dominant may cease. When this (61), Arabian babblers, Turdoides squami- spring (Prediction 5), yield the same ex- occurs, subordinate dispersal will be in the ceps (51), and Dwarf mongooses, Helogale pectation of greater reproductive skew in best interest of all parties, and families will parvula (69, 70), family members close to the matrifilial/patrifilial groupings than in dissolve (Prediction 1). dominant in age (and thus in dominance) sibling-sibling associations. Teasing apart Downloaded by guest on September 29, 2021 8098 Review: Emlen Proc. Natl. Acad. Sci. USA 92 (1995) the relative contributions of these three by considering all four together in the share reproduction with those family mem- factors will depend upon close examina- analysis of any particular society. bers to whom they are genetically the least tion of the degree of reproductive skew in closely related. different types of familial associations. Conclusions Social vertebrates, and particularly Prediction 15. Reproduction will be birds, are excellent subjects for generating shared most with those family members to I have attempted to demonstrate that and testing darwinian hypotheses about whom the dominant breeders are least many aspects of family life, ranging from living with relatives. The variations in closely related. In species in which domi- the formation and stability of family their family structures, and the tactics they nants actively suppress reproduction by sub- groupings, to the roles that different fam- demonstrate in interacting with one an- ordinates, such suppression will be greatest ily members adopt in their interactions other, often have direct parallels in human in those subordinates to whom the dominant with one another, to the structural form of society. Their social behaviors, while com- is most closely related. the family unit itself, can be understood plex enough to be inherently interesting, This counterintuitive prediction was within a darwinian framework. This are simple in the sense of being relatively first proposed over a decade ago (19-22). framework is based upon three major free of complex cultural influences. Ani- It follows from the fact that subordinates concepts ofbehavioral ecology: ecological with a valuable differ in' the magnitude of the indirect constraints theory, inclusive fitness the- mal studies thus provide us benefits that they obtain by remaining and ory, and reproductive skew theory. Each window through which we can more easily helping in their family groups. All else assumes that individual behaviors are view the fundamental biological rules that being equal, these benefits are propor- based, at least partially, on adaptive deci- govern social interactions within family tional to the subordinates' degree of ge- sion rules shaped by natural selection. groups. By looking within this window, we netic relatedness to the breeders. Subor- From these basic tenets of evolutionary can gain insights into noncultural factors dinates to whom the dominant pair is most biology, I have distilled a set of 15 predic- that affect our own social behaviors. closely related receive the largest amount tions that provide an integrated frame- Human behavior, while highly flexible, is of indirect benefit from helping (Predic- work for considering the workings of the not infinitely malleable. While agreeing that tion 4). They therefore are predicted to family and other kin associations. Abbre- human behavior is strongly shaped by the require the smallest "staying incentives" viated versions of the predictions appear cultural environment, I argue that humans to keep them in the family group. In in Table 1, along with relevant nonhuman also possess a set of biologically based pre- contrast, distantly or nonrelated subordi- examples from the vertebrate literature. dispositions for interacting with relatives, a nates gain little or no indirect benefits Predictions 1 and2 forecast the conditions biological heritage based on flexible deci- from staying and helping and, thus, re- under which families originate and discuss sion rules thatwere adaptive during our long quire a greater amount of personal repro- how stable these families are likely to be. evolutionary history of living in extended duction to be induced to remain. Stability depends on the trade-offs between family groups. It is these predispositions that Several recent studies provide clear tests the fitness benefits available from staying I attempt to predict in this paper. of Prediction 15. Both pukekos, Porphyrio home vs. those available from dispersing to This view of family systems is very dif- porphyrio (an Australasian gallinule), and attempt reproducing elsewhere. ferent from that adopted by many social lions, Panthera leo, form extended families Predictions 3-5 discuss the extent to scientists. The adaptive framework pre- in which the group males may or may not be which reproductive cooperation (helping sented here in no way contradicts, but closely related to one another. Copulation behavior and reduced sexual competition) rather supplements, studies of the proxi- and paternity data confirm that reproduc- can be expected among family members. mal and developmental mechanisms that tion is shared quite equitably among males Prediction 6 introduces family conflict, in influence the behavior of human family when the groups are composed ofunrelated the form of reduced paternal investment members. The adaptive and mechanistic individuals, but dominants monopolize re- by males that may have been cuckolded. viewpoints are not mutually exclusive. production when the potential mate-sharing Predictions 7-11 pertain to the disrup- Rather they constitute paradigms reflect- groups are composed ofclose male relatives tive effects on family dynamics that result different levels of analysis (106, 108). (65, 71). from the disappearance of a biological ing Reproductive competition often takes parent and its subsequent replacement by Each stands to benefit by incorporating the form of disruption or suppression of a step-parent. The death of a father in a elements of the other into its approach. the breeding attempts of subordinates. In simple conjugal family, for example, will I dedicate this paper to my father, J. T. the extended families of White-fronted lead to conflict between a mother and her Emlen, Jr., a pioneer in modem studies of bee-eaters, dominant breeders preferen- eldest mature son over her retention, vs. animal behavior. The manuscript benefitted tially disrupt the breedings of their closest his assumption, ofbreeder status. Mothers from comments by N. J. Demong, L. Keller, kin (64, 67), often inducing the latter to will often lose their breeding positions to 0. F. Linares, L. W. Oring, H. K Reeve, and become helpers at their nests. their dominant sons at these times. M. J. West-Eberhard. I thank N. J. Demong for In families of Dwarf mongooses, the The arrival of a replacement breeder is editorial assistance and help compiling Table 1. dominant male and female typically sup- predicted to cause further disruptions. For various financial support, I thank the John press the reproduction of subordinates. In There will be reduced incentive for current Simon Guggenheim Foundation, the Center for keeping with Predictions 13 and 15, those offspring to remain at home or for step- Advanced Study in the Behavioral Sciences, the subordinates that do reproduce are the parents to invest heavily in these offspring. William Puibright Scholar Program of the oldest and those least closely related to the Step-families thus are forecasted to be less Council for International Exchange ofScholars, dominant breeders (69, 70). stable than biologically intact families. the National Geographic Society, and espe- Qnly three other cases of egalitarian Delayed dispersal, coupled with the shar- cially, the National Science Foundation. have been of direct dominants breeding reported among ing reproduction by 1. Wilson, E. 0. (1975) Sociobiology: The New highly social cooperatively breeding ver- with subordinates, gives rise to a diversity of Synthesis (Belknap, Harvard Univ., Cambridge, tebrates (66, 68, 107). In each, the multiple extended, as opposed to simple family struc- MA). breeders have proven to be nonrelatives. tures. The final four predictions describe 2. Maynard-Smith, J. (1982) Evolution and the Although the predictions for reproduc- conditions under which extended families TheoryofGames (Cambridge Univ. Press, Cam- within kin are univar- are to and which bridge, U.K). tive sharing groups expected form, specify 3. Parker, G. A. (1989) Ethol. Ecol. Evol. 1, 195- iate, the four parameters of reproductive family members will become cobreeders. 211. skew theory interact with each other. The Prediction 15 offers the counterintuitive ar- 4. Dawkins, R. (1982) The Extended Phenotype full value of the theory can only be tested gument that dominants will be most likely to (Freeman, Oxford). Downloaded by guest on September 29, 2021 Review: Emlen Proc. Natl. Acad. Sci. USA 92 (1995) 8099

5. Dunbar, R. I. M. (1984) Reproductive Decisions: 40. Clarke, M. F. (1984) Behav. Ecol. Sociobiol. 14, 73. Farber, B. (1964) Family: Organization and In- An Economic Analysis of Gelada Baboon Social 137-146. teraction (Chandler, San Francisco). Strategies (Princeton Univ. Press, Princeton). 41. Clarke, M. F. (1989) Ethology 80, 292-306. 74. Nock, S. L. (1992) Sociology ofthe Family (Pren- 6. Trivers, R. L. (1974) Am. Zool. 14, 249-264. 42. P6ldmaa, T. (1995) Behav. Ecol. Sociobiol., in tice-Hall, Englewood Cliffs, NJ). 7. Trivers, R. L. & Willard, D. E. (1973) Science press. 75. Fox, R. (1967) Kinship and Marriage (Penguin, 179, 90-92. 43. Curry, R. L. (1988) Behav. Ecol. Sociobiol. 22, Harmondsworth, Middlesex, U.K.). 8. Alexander, R. D. (1979) Darwinism and Human 141-152. 76. van den Berghe, P. L. (1979) Human Family Affairs (Univ. Washington Press, Seattle). 44. Marzluff, J. M. & Balda, R. P. (1990) in Coop- Systems: An Evolutionary View (Elsevier, New 9. Daly, M. & Wilson, M. I. (1985) Ethol. Socio- erative Breeding in Birds: Long-Tern Studies of York). biol. 6, 197-210. Ecology and Behavior, eds. Stacey, P. B. & Koe- 77. Stacey, P. & Ligon, J. D. (1987) Am. Nat. 130, 10. Daly, M. & Wilson, M. I. (1988) Homicide (de nig, W. D. (Cambridge Univ. Press, Cambridge, 654-676. Gruyter, New York). U.K.), pp. 197-237. 78. Zack, S. (1990) Ethology 86, 265-286. 11. Koenig, W. D. & Pitelka, F. A. (1981) in Natural 45. Owen, D. D. & Owen, M. J. (1984) Nature 79. Zack, S. & Stutchbury, B. (1993) Behaviour 123, Selection and Social Behavior: Recent Research (London) 308, 843-846. 194-219. and New Theory, eds. Alexander, R. D. & Tin- 46. Creel, S. R., Monfort, S. L., Wildt, D. E. & Waser, 80. Mumme, R. L. (1992) Trends Ecol. Evol. 7, kle, D. W. (Chiron, Newton, MA), pp. 261-280. P. M. (1991) Nature (London) 351, 660-662. 330-331. 12. Emlen, S. T. (1982) Am. Nat. 119, 29-39. 47. Pusey, A. E. & Packer, C. (1994) Behav. Ecol. 5, 81. MacDonald, D. W. & Moehlman, P. D. (1982) 13. Brown, J. L. (1987)Helpingand Communal Breed- 362-374. Perspect. Ethol. 5, 433-469. ing in Birds: Ecology and Evolution (Princeton 48. Koenig, W. D. (1990) Behav. Ecol. 1, 55-61. 82. Stacey, P. B. & Koenig, W. B., eds. (1990) Coop- Univ. Press, Princeton). 49. Walters, J. R. (1990) in Cooperative Breeding in erative Breeding in Birds: Long-Term Studies of 14. Emlen, S. T. (1991) in Behavioral Ecology: An Ecology and Behavior (Cambridge Univ. Press, eds. & Birds: Long-Tern Studies ofEcology andBehavior, EvolutionaryApproach, Krebs, J. Davies, eds. Stacey, P. B. & Koenig, W. D. (Cambridge Cambridge, U.K.). N. B. (Blackwell Scientific, Oxford), pp. 301- 83. Solomon, N. G. & French, J. A., eds. (1995) 337. Univ. Press, Cambridge, U.K), pp. 67-102. 50. Brown, R. J. & Brown, M. N. (1980) Emu 80,89. Cooperative Breeding in Mammals (Cambridge 15. Koenig, W. D., Pitelka, F. A., Carmen, W. J., Univ. Press, Cambridge, U.K.), in press. Mumme, R. L. & Stanback, M. T. (1992) Q. 51. Zahavi, A. (1990) in Cooperative Breeding in Birds: Long-Term Studies ofEcology and Behav- 84. Wilson, E. 0. (1971) The Insect Societies Rev. Biol. 67, 111-150. (Belknap, Harvard Univ., Cambridge, MA). 16. Emlen, S. T. (1994) Trends Ecol. Evol. 9, 282- ior, eds. Stacey, P. B. & Koenig, W. D. (Cam- bridge Univ. Press, Cambridge, U.K.), pp. 103- 85. Brockmann, H. J. (1984) in Behavioural Ecology: 285. An Evolutionary Approach, eds. Krebs, J. R. & 17. Hamilton, W. D. (1964) J. Theor. Biol. 7, 1-52. 130. 52. Mumme, R. L., Koenig, W. D. & Pitelka, F. A. Davies, N. B. (Blackwell Scientific, Oxford), 2nd 18. Alexander, R. D. (1974) Annu. Rev. Ecol. Syst. Ed., pp. 340-361. 5, 325-383. (1983) Anim. Behav. 31, 1094-1106. 53. Piper, W. H. & Slater, G. (1993) Behaviour 124, 86. Kullmann, E. (1972) Am. Zool. 12, 419-426. 19. Emlen, S. T. (1982) Am. Nat. 119, 40-53. 87. Buskirk, R. E. (1981) in Social Insects, ed. Her- 20. Vehrencamp, S. L. (1983) Anim. Behav. 31, 227-247. 54. Stacey, P. B. (1979) Behav. Ecol. Sociobiol. 6, mann, H. R. (Academic, New York), pp. 281-367. 667-682. 88. K., Ballou, J. D. & A. 21. Vehrencamp, S. L. (1983) Am. Zool. 23, 327- 53-66. Ralls, Templeton, (1988) 55. Stacey, P. B. & Edwards, T. C. (1983) Auk 100, Conserv. Biol. 2, 185-193. 335. D. & A. 22. Emlen, S. T. & Vehrencamp, S. L. (1983) in 731-733. 89. Ralls, K., Ballou, J. Templeton, (1988) Perspectives in Ornithology, eds. Brush, A. H. & 56. Curry, R. L. & Grant, P. R. (1990) in Cooper- Conserv. Biol. 2, 185-193. Clark, J. G. A. (Cambridge University Press, ative Breeding in Birds: Long-Term Studies of 90. Thornhill, N. W. (1993) The Natural History of Cambridge, U.K.), pp. 93-133. Ecology and Behavior, eds. Stacey, P. B. & Koe- Inbreeding and Outbreeding: Theoretical and 23. Reeve, H. K. & Ratnieks, F. L. W. (1993) in nig, W. D. (Cambridge Univ. Press, Cambridge, Empirical Perspectives (Univ. Chicago Press, Queen Number and Sociality in Insects, ed. U.K.), pp. 291-331. Chicago). Keller, L. (Oxford Univ. Press, Oxford), pp. 57. Hrdy, S. B. (1977) Am. Sci. 65, 40-49. 91. Jiminez, J. A., Hughes, K. A., Alaks, G., Gra- 45-85. 58. Hausfater, G. & Hrdy, S. B., eds. (1984) Infan- ham, L. & Lacy, R. C. (1994) Science 266, 24. Keller, L. & Reeve, H. K. (1994) Trends Ecol. ticide: Comparative and Evolutionary Perspec- 271-273. Evol. 9, 98-102. 92. Keller, L. F., Arcese, P., Smith, J. N. M., tives (Aldine, New York). Hochachka, W. M. & Stearns, S. C. Na- 25. Emlen, S. T. (1984) in Behavioral Ecology: An 59. Mumme, R. L. (1992) Behav. Ecol. Sociobiol. (1994) EvolutionaryApproach, eds. Krebs, J. & Davies, ture (London) 372, 356-357. 31, 319-328. 93. Craig, J. L. & Jamieson, I. G. (1988) Am. Nat. N. (Blackwell Scientific, Oxford), 2nd Ed., pp. 60. Komdeur, J. (1994) Proc. R Soc. London B 256, 305-335. 131, 58-70. 47-52. 94. Reeve, H. K., Westneat, D. F., Noon, W. A., 26. Walters, J. R., Copeyon, C. K. & Carter, I. J. H. 61. Rowley, I., Russell, E. M., Payne, R. B. & Payne, (1992) Auk 109, 90-97. Sherman, P. W. & Aquadro, C. F. (1990) Proc. L. L. (1989) Ethology 83, 229-247. Natl. Acad. Sci. USA 87, 2496-2500. 27. duPlessis, M. (1992) Oecologia 90, 205-211. 62. Curry, R. L. (1988) Anim. Behav. 36, 1708- 28. Pruett-Jones, S. G. & Lewis, M. J. (1990) Na- 95. Bengtsson, B. 0. (1978) J. Theor. Biol. 73, 439- 1728. 444. ture (London) 348, 541-542. 63. Koenig, W. D. & Mumme, R. L. (1987) Popu- 29. Woolfenden, G. & Fitzpatrick, J. (1984) The 96. Waser, P. M., Austad, S. N. & Keane, B. (1986) lation Ecology ofthe Cooperative BreedingAcorn Am. Nat. 128, 529-537. Florida Scrub Jay: Demography ofa Cooperative Woodpecker (Princeton Univ. Press, Princeton). Breeding Bird (Princeton Univ. Press, Prince- 97. Trivers, R. L. (1972) in Sexual Selection and the 64. Emlen, S. T. & Wrege, P. H. (1992) Nature Descent ofMan, ed. Campbell, B. (Aldine, New ton). (London) 356, 331-333. 30. Curry, R. L. (1989) Behav. Ecol. Sociobiol. 25, York), pp. 136-179. 65. Jamieson, I., Quinn, J. S., Rose, P. A. & White, 98. Westneat, D. F. & Sherman, P. W. (1993) Be- 147-160. B. 31. Komdeur, J. (1992) Nature (London) 358, 493- N. (1994) Proc. R. Soc. London B 257, 271- hav. Ecol. 4, 66-77. 495. 277. 99. Mock, D. W. (1984) in Infanticide: Comparative 32. Wolff, J. 0. (1992) Nature (London) 359, 409- 66. Faaborg, J., Parker, P. G., DeLay, L., deVries, and Evolutionary Perspectives, eds. Hausfater, 410. T. J., Bednarz, J. C., Pax, S. M., Naranjo, J. & G. & Hrdy, S. B. (Aldine, New York), pp. 3-30. 33. Jones, W. T., Waser, P. M., Elliott, L. F., Link, Waite, T. A. (1995) Behav. Ecol. Sociobiol. 36, 100. Rohwer, S. (1986) Curr. Ornithol. 3, 253-336. N. E. & Bush, B. B. (1988) Ecology 69, 1466- 83-90. 101. Emlen, S. T., Demong, N. J. & Emlen, D. 1473. 67. Emlen, S. T. & Wrege, P. H. (1992) Nature (1989) Auk 105, 1-7. 34. Hannon, S. J., Mumme, R. L., Koenig, W. D. & (London) 359, 24. 102. Rabenold, K. N. (1985) Behav. Ecol. Sociobiol. Pitelka, F. A. (1985) Behav. Ecol. Sociobiol. 17, 68. Koford, R. R., Bowen, B. S. & Vehrencamp, 17, 1-17. 303-312. S. L. (1990) in Cooperative Breeding in Birds: 103. Rowley, I. & Russell, E. (1990) in Cooperative 35. Stacey, P. & Ligon, J. D. (1991) Am. Nat. 137, Long-Term Studies ofEcology and Behavior, eds. Breeding in Birds: Long-Term Studies ofEcology 831-846. Stacey, P. B. & Koenig, W. D. (Cambridge and Behavior, eds. Stacey, P. B. & Koenig, 36. Brown, J. L. & Brown, E. R. (1990) in Cooper- Univ. Press, Cambridge, U.K.), pp. 335-355. W. D. (Cambridge Univ. Press, Cambridge, ative Breeding in Birds: Long-Term Studies of 69. Creel, S. R. & Waser, P. M. (1991) Behav. Ecol. U.K.), pp. 1-30. Ecology and Behavior, eds. Stacey, P. B. & Koe- 2, 7-15. 104. Balcombe, J. P. (1989) Evol. Ecol. 3, 77-79. nig, W. D. (Cambridge Univ. Press, Cambridge, 70. Keane, B., Waser, P. M., Creel, S. R., Creel, 105. Reeve, H. K. & Keller, L. (1995) Am. Nat. 145, U.K.), pp. 267-288. N. M., Elliott, L. F. & Minchella, D. J. (1994) 119-132. 37. Woolfenden, G. E. & Fitzpatrick, J. W. (1978) Anim. Behav. 47, 65-75. 106. Sherman, P. W. (1988) Anim. Behav. 36, 616- BioScience 28, 104-108. 71. Packer, C., Gilberg, D. A., Pusey, A. E. & 619. 38. Zack, S. & Rabenold, K. (1989) Anim. Behav. O'Brien, S. J. (1992) Nature (London) 351, 562- 107. Davies, N. B. (1992) Dunnock Behaviour and 38, 235-247. 565. Social Evolution (Oxford Univ. Press, Oxford). 39. Emlen, S. T. & Wrege, P. H. (1988)Behav. Ecol. 72. Goode, W. J. (1964) The Family (Prentice-Hall, 108. Tinbergen, N. (1963) Z. Tierpsychol. 20, 410- Sociobiol. 23, 305-315. Englewood Cliffs, NJ), 2nd Ed. 433. Downloaded by guest on September 29, 2021