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Integrating molecular techniques with field methods in studies of social behavior: a revolution results.

INTRODUCTION

When social behavior is defined as encompassing interactions between individuals, in the sense of Tinbergen (1953), then the purview of this topic is wide. It includes mating behavior as well as family and group interactions, cooperation, competition, and the evolution of societies. Molecular methods have the potential to enrich studies over this entire spectrum, but their application so far has been limited to particular taxa and questions. Most studies are of birds, mammals, and Hymenoptera (ants, bees, and wasps), and address either parentage or genetic relatedness. If the results of such studies were mere confirmation and refinement of what observations would predict, then we might expect a relatively short list of publications with titles similar to a recent one: "Behavior predicts genetic structure in a wild primate group" (Altmann et al. 1996). This is not the case, however. The application of molecular methods has yielded startling revelations about mating systems and social groups.

In this review I give an overview of recent publications, emphasizing work that has challenged accepted theory and suggested new avenues for research. I first consider how molecular methods have affected the study of mating systems in species for which mating associations are prolonged. Molecular methods have enlivened the study of monogamy by showing that individuals may mate outside of their pair bond. I also describe how molecular methods have so changed our understanding of other mating systems that underlying theory must be reevaluated. Second, I consider how molecular methods have enriched the study of sociality by detailing how reproductive success is partitioned among individuals in groups. Finally, I describe how molecular methods have been applied to eusocial insects to estimate genetic relatedness among colony members and to identify mechanisms generating variance in relatedness such as number of mates per queen.

MATING SYSTEMS AND GENETIC MATING SYSTEMS

The study of mating systems focuses on ways individuals obtain mates, the number of individuals with which they mate, how long mates stay together, and allocation of parental care (although many would argue that this last feature is a separate question). These behaviors are often analyzed in the context of how they affect lifetime reproductive success (e.g., Emlen and Oring 1977, Davies 1991). Mating patterns often correlate with ecological factors; for example, monogamy and biparental care may be responses to food limitation so severe that a single parent could not succeed. Mating systems have often been described from behavioral data alone, but molecular techniques can reveal unexpected patterns of gene transmission (pedigree connection) resulting from the diverse behavioral tactics that individuals employ. The "genetic mating system" is a description of which individuals are reproducing and with whom, as distinct from the "social mating system" based on observable associations between individuals (these social mating systems are used as subheadings below). Accurate parentage assignment permits determination of the genetic payoff for observed behavioral strategies, and lifetime reproductive success.

Monogamy

Monogamy is the nearly exclusive association of one male with one female for one or more breeding attempts; it is characteristic of birds, but rare in other taxa (Mock and Fujioka 1990). The recent explosion in use of molecular markers has shown that this apparently simple mating system frequently involves more than just a single pair of birds. In monogamous species, observations have been frequently documented of pair-bonded individuals copulating with individuals other than their mates (see reviews in Birkhead 1987, Westneat et al. 1990), but the genetic consequence of these "extra-pair copulations" (EPCs) were little known before the widespread use of molecular methods. Earlier work, using estimates of heritability, experimental manipulation, plumage markers, and allozymes had shown that extra-pair copulations could lead to extra-pair fertilizations (EPFs) (Westneat et al. 1990). Two important consequences of EPFs are that males often invest parental care in chicks to which they are unrelated and that they can achieve reproductive success outside of the pair bond.

Molecular markers are the easiest and most accurate way to assess the consequences of matings observed between nonpair mates because behavioral observations can dramatically underestimate or overestimate the frequency of EPFs. For example, in Indigo Buntings, Passerina cyanea, only 3.3% of observed copulations were EPCs, yet 27-42% of young resulted from EPFs (Westneat 1987a, b). In other cases, the frequency of EPCs overestimates the frequency of EPFs. In a study of Willow Warblers, Phylloscopus trochilus, 13% of copulations were EPCs, but none of 120 offspring were determined to have resulted from EPFs using DNA fingerprints (Gyllensten et al. 1990). In yet other studies of avian populations, EPCs accurately predict EPFs, such as in the Shag, Phalacrocorax aristotelis (Graves et al. 1991).

When the frequency of EPFs is high, the role of long-term bonds in maximizing individual reproductive success is called into question. In some species, the frequency of EPFs is extremely high: 55% in Reed Bunting chicks, Emberiza schoeniclus (Dixon et al. 1994), and 41-57% in Tree Swallows, Tachycineta bicolor (Dunn et al. 1994). Particularly in such cases, though also in species where frequency of EPFs is lower, monogamy can no longer be viewed as a simple strategy; both males and females achieve reproductive success through a mixed strategy of intra-pair and extra-pair reproductive effort. Further, if males that sire extra-pair young do not lose paternity to a similar degree on their own territories, then variance in male reproductive success is increased over that of females; this establishes a precondition for the operation of sexual selection in these "monogamous" species (Gibbs et al. 1990, Yezerinac et al. 1995).

Molecular methods have confirmed that some socially monogamous species are genetically monogamous, though these are the minority. In Dunnocks, Prunella modularis, none of 37 chicks from 15 monogamous pairs resulted from EPFs (Burke et al. 1989). Likewise, in Willow Warblers, Phylloscopus trochilus, none of 120 chicks from 19 families resulted from EPFs (Gyllensten et al. 1990). Merlins, Falco columbaris, are apparently monogamous (Warkentin et al. 1994) as are Black Vultures, Coragyps atratus (Decker et al. 1993), Fulmars, Fulmarus glacialis (Hunter et al. 1992), Leach's Storm Petrels, Oceanodroma leucorhoa (Mauck et al. 1995), and Cory's Shearwaters, Calonectris diomedea (Swatschek et al. 1994). Cory's Shearwaters display the epitome of bird monogamy: very long-term mate fidelity is matched by a very low frequency of EPCs even though they nest colonially; coloniality is normally associated with an increased frequency of EPCs (Moller and Birkhead 1993). In contrast, a recent review listed [greater than]20 studies of socially monogamous species that revealed EPFs (Moller and Birkhead 1993).

Social monogamy is rare in mammals, though it is typical of canids. As in birds, socially monogamous mammals have been observed mating outside their pair bonds, and microsatellite data revealed that in the Ethiopian wolf, Canis simensis, litters may have multiple sires (Sillero-Zubiri et al. 1996). In contrast, DNA fingerprinting has been used to make the first convincing demonstration of monogamy in a rodent, Peromyscus californicus (Ribble 1991). It has also been used to reject monogamy as an explanation of observed behavior, as in the case of hooded seals, Cistophora cristata, which have a prolonged association between a female, a pup, and a male during the course of the breeding season. DNA fingerprinting of these trios definitively excluded the male consort as father, demonstrating that this is not a case of long-term pair bonding and monogamy (McRae and Kovacs 1994). In contrast, behavioral observations led to the classification of the mating system of the gray seal, Halichoerus grypus, as polygynous, but a combination of DNA fingerprinting and microsatellite analysis showed that there were many full siblings in the population, suggesting high mate fidelity across years (Amos et al. 1995).

Success in extra-pair matings, as well as susceptibility to their effects, may be related to age. In Purple Martins, Progne subis, and Bobolinks, Dolichonyx oryzivorus, the frequency at which males lose paternity in their own nests has been shown to decline with age (Morton et al. 1990, Bollinger and Gavin 1991). There are no demonstrations of age-specific effects of EPFs on female fitness, but it is intriguing that older female Bobolinks chose extra-pair males more often than did younger females (Bollinger and Gavin 1991). A thorough understanding of how mating strategies influence lifetime reproductive success must consider these age-related changes.

The frequency of extra-pair fertilization may also affect the pattern of parental investment, as males should not invest in offspring other than their own if they have a means of detecting unrelated young. On the other hand, if a male gave less care to a brood in which he had lower confidence of paternity, he may jeopardize the survival of any offspring in the brood of which he actually is the father. In such circumstances, females should weigh the benefits of mating with extra-pair males against lost assistance in raising offspring. The most convincing demonstration of this phenomenon comes from a study of Reed Buntings, in which male assistance changed according to the change in paternity from one brood to the next, in the same year, with the same mate (Dixon et al. 1994). Males fed a second brood more than they fed their first brood when they had higher paternity in the second brood. Conversely, they fed second broods less when they had lower paternity. This male response to loss of paternity may be widespread; there is evidence for it in Dunnocks (Burke et al. 1989) and Barn Swallows, Hirundo rustica (Moller 1988, 1991). However, in studies of other species there was no relationship between male parentage and the parental care they provide, such as in Indigo Buntings (Westneat 1988), Yellow Warblers (Yezerinac et al. 1996), and Galapagos Hawks (DeLay et al. 1996).

Females may avoid inbreeding or outbreeding depression by seeking EPFs. In the Splendid Fairy Wren, Malurus splendens, described behaviorally as having monogamous pairs living in groups with helpers, an extraordinary proportion of offspring are sired by extra-pair, apparently extra-group males. Allozyme data showed that [greater than]65% (and perhaps 100%) of offspring resulted from EPFs (Brooker et al. 1990, Rowley and Russel 1990). In this case, females may be seeking unrelated males because the sedentary nature of the birds makes it likely that within-group mates are close relatives. In contrast, in Pied Flycatchers, genetically similar pairs had fewer extra-pair young than less closely related mates (Ratti et al. 1995). This result is consistent with females seeking an optimal degree of outbreeding. Where other species fall along this continuum will be readily tested by analysis of existing data sets.

Polygyny

Classic polygyny refers to the prolonged association of one male with more than one female. The "polygyny threshold model" hypothesizes that this mating system arises when males control access to resources in such a way that some females benefit more by breeding with an already mated male than by breeding with an unmated male (Emlen and Oring 1977). However, this reasoning must be modified in light of the molecular evidence on paternity. Parentage assignment in Red-winged Blackbirds, Agelaius phoeniceus, showed that 28% of chicks are not offspring of their social father (Gibbs et al. 1990). An average of 21% of male reproductive success derived from fertilization of females other than those nesting within their territories. Between 0 and 67% of individual males' success was realized with out-of-territory females. Furthermore, residents that were more successful at fertilizing females nesting within their territories were also more successful in achieving EPFs. These results suggest that a female's choice of mate is partly independent of her choice of where to nest, which may explain the lack of support for models of the evolution of polygyny outlined above (Lightbody and Weatherhead 1988, Davies 1989). In light of such findings, new models for the evolution of polygyny should hypothesize how females choose the optimal available combination of high-quality territory and high-quality mate.

Parentage in polygynous mammals should provide a good proving ground for these models. Naturally occurring spatial variation in resource abundance is correlated with the mating system of Gunnison's prairie dogs, Cynomys gunnisoni, determined from DNA fingerprinting (Travis et al. 1995a). As predicted by the polygyny threshold model, uniform resource distribution was associated with monogamy, while polygyny and polygynandry (the association of several males with several females) occurred with increasing resource patchiness. In a population showing harem polygyny, 61% of progeny were sired by extra-territorial males (Travis et al. 1995b). Further, there was variation in female strategies, which ranged from producing offspring sired exclusively by the territorial male, to producing offspring sired exclusively by one or more extra-territorial males. This variation may be explicable in terms of female choice of resources and mates.

Leks

In some animals, males form groups called leks at particular arenas where they display to attract females. After females visit these male aggregations and mate, they leave to raise their offspring alone. Behavioral data show that certain males are chosen more often by females and achieve the majority of copulations. Molecular methods have the potential to assess the relative reproductive successes of lekking males. In Long-tailed Manakins, Chiroxiphia linearis, a lek has at its core two males that perform a Cooperative display at a particular site over several years (McDonald 1989). Apparently, only the alpha male mates at any appreciable frequency, raising the possibility that behavior of beta males is shaped by kin selection. Microsatellite genotype data refuted this hypothesis, however, by showing that cooperating males were not related (McDonald and Potts 1994). Instead, beta males may benefit from eventually ascending to alpha status, from female fidelity to active, orderly leks (no fighting for dominance status), and perhaps from occasional copulations. Whether selection favors males remaining in beta positions because they receive delayed benefits through ascending to alpha status or direct benefits through fertilizations could be determined by parentage assignment of offspring in future studies.

Lekking behavior in manakins, Pipridae, has also been approached from a phylogenetic perspective using both molecular and morphological phylogenies (though mostly the latter; Prum 1994). Prum (1994) mapped lek-related behavioral traits onto a phylogeny to determine the evolutionary paths taken. This analysis showed that there is a strong phylogenetic component to lekking behavior in this family: species that form leks are descended from ancestral lekking species. Originally this clade seems to have derived from an ancestral species with a "dispersed" lek consisting of large male territories and few males per lek. Smaller, more concentrated leks have evolved in several branches. Similarly, a highly coordinated display has arisen several times. In one species, lekking has secondarily been lost and males defend territories in which females nest. Further work may show which environmental shifts are associated with changes in lekking behavior. Molecular data can be used in the creation of such phylogenetic hypotheses against which hypotheses for the evolution of behavior can be tested. This is critical to evaluating current hypotheses about the evolution of this intriguing mating system, as well as in more proximate studies of lek dynamics. For example, relatedness of displaying males could be assayed for more species in this clade, and the actual distribution of reproductive success among males in a lek could be determined.

Polyandry

Polyandry is the long-term association of a female with more than one male. Recent molecular work with a classic example of polyandry, the Tasmanian Native Hen, Tribonyx mortieri, suggests that the species is characterized by genetic monogamy, though polyandry did occur in one of six groups (Gibbs et al. 1994). In other studies, molecular methods have confirmed polyandrous mating; examples include the Dunnock (Burke et al. 1989), and the Galapagos Hawk, Buteo galapagoensis (Faaborg et al. 1995). Groups of male Galapagos Hawks have long-term stable membership; the data showed that group members were not close relatives and had approximately equal chances of siring young. In Brown Skuas, Catharacta lonnbergi, males within groups were also unrelated, but had highly variable probabilities of siring young (Millar et al. 1994). The authors emphasize, however, that parentage studies based on data from a single year should be interpreted with caution, as reproductive success may vary widely between years.

An alternative form of polyandry is sequential polyandry, in which a female lays clutches for two or more males in quick succession, leaving each male in turn to raise a brood. A study of sequentially polyandrous Spotted Sandpipers, Actitis macularia, showed that early-pairing males had higher than expected reproductive success because sperm storage by females allowed these males to father offspring in later broods (Oring et al. 1992).

In some species the mating system includes more than one of the patterns described above. In the Dunnock, a small European passerine, the mating system embraces monogamy, polygyny, polyandry, and polygynandry (Davies 1985). Burke et al. (1989) used DNA fingerprinting to resolve parentage, and showed that patterns of paternity provided reasonable explanations for behavioral observations of paternal care and intrasexual aggression. Males fed broods according to their access to females during the mating period, which was a good predictor of their paternity. Alpha males attempted to drive off beta males, apparently because they did not gain sufficient benefits from the cooperation of a second male to make up for the loss of paternity they suffered.

Which individuals are responsible for extra-pair young?

When molecular markers are sufficiently polymorphic and the population adequately characterized, parentage assignments can be made. Under these circumstances, factors influencing choice of extra-pair mates can be determined. In Red-winged Blackbirds, extra-pair fathers were generally (20 of 26 cases) neighboring males (Gibbs et al. 1990). Similarly, in Yellow Warblers, Dendroica petechia, 89% of extra-pair young were sired by a neighbor or next-to-neighbor (Yezerinac et al. 1995). And in Great Reed Warblers, Acrocephalus arundinaceus, nests closest to neighboring males had a greater chance of containing young sired by EPF (Hasselquist et al. 1995). Old males were disproportionately represented as EPF sires in Purple Martins (Morton et al. 1990, Wagner et al. 1996), while in Blue Tits (Kempenaers et al. 1992), and Red-winged Blackbirds (Weatherhead and Boag 1995) large males achieved more EPFs. In Tree Swallows, no physical or behavioral correlates of extra-pair fathers could be found, but only 21% of extra-pair young could be assigned to a known father, so the test was not strong (Dunn et al. 1994). Apparently, female Tree Swallows copulated with males nesting elsewhere or with unmated "floaters."

The schedule of age-specific reproduction is partly determined by developmental changes in the rate at which members of both sexes employ alternative mating tactics. Young female Purple Martins mated to young males choose older males as EPFs partners, perhaps because age is an index for fitness (Morton et al. 1990, Wagner et al. 1996). In Bobolinks, too, young males suffered more losses to EPFs than old males, though young females had fewer EPFs offspring than old females (Bollinger and Gavin 1991). No age specific effects were found in Tree Swallows (Dunn et al. 1994). It will be interesting to see how age-related changes in EPFs affect lifetime reproductive success.

What predicts the frequency of extra-pair young?

Molecular techniques have made it clear that individuals may achieve a large fraction of their reproductive success through extra-pair mating. One obvious next step is to understand what factors determine general patterns in extra-pair mating. One factor that has been extensively investigated is males' guarding of mates during females' fertile periods (e.g., Moller and Birkhead 1993). If mate guarding has evolved because it increases paternity, then EPFs and mate guarding are predicted to be negatively correlated, and polygynously mated males are predicted to suffer more EPFs than monogamously mated males. Analyses have provided mixed support for these two predictions.

The frequency of mate guarding bears no simple relationship to paternity determined from molecular data. Contrary to expectation in Eastern Bluebirds and Great Reed Warblers, the frequency of mate guarding is positively correlated with frequency of EPFs (Gowaty and Bridges 1991a, Hasselquist et al. 1995). However, in Red-winged Blackbirds, there is strong experimental evidence that guarding increases males' paternity (Westneat 1994). Males that were supplemented with food spent less time foraging, guarded more, and had higher paternity (0.88 of chicks raised on their territories) than unsupplemented males (0.69). The food supplements also reduced female forays away from the territory, but the effect was much smaller than on male behavior, so it is reasonable to conclude that the increase in the primary mate's paternity was due largely to the effect of mate guarding.

Similarly, polygynously mated males do not necessarily suffer lower paternity in their own nests. In neither the Pied Flycatcher, Ficedula hypoleuca (Lifjeld et al. 1991), nor Great Reed Warblers (Hasselquist et al. 1995), did polygynous males suffer greater loss of paternity to EPFs than monogamous males. Within polygynous male bobolinks' territories, primary females had more EPF offspring than secondary females, and monogamously mated females had an intermediate number (Bollinger and Gavin 1991). A comparison of two congeners, in the same environment, showed that there were no EPFs in either polygynous Wood Warblers or monogamous Willow Warblers (Gyllensten et al. 1990).

These results provide weak support for the explanatory framework based on male tactics for increasing fertilization rate and reproductive success. A fruitful new line of research focuses on development of a parallel set of expectations based on the female perspective (e.g., Stutchbury et al. 1994, Stutchbury and Morton 1995). In birds, recent evidence suggests that the resolution of reproductive conflicts of interests between males and females favors female interests. Patterns of paternity suggest females control paternity in Red-winged Blackbirds (Gray 1996), Alpine Accentors and Dunnocks (Davies et al. 1996), and Purple Martins (Wagner et al. 1996). In Purple Martins it was additionally shown that the balance shifted toward males' interests in pairs where males were significantly larger than their mates.

Population density is expected to influence the frequency of EPFs by controlling the opportunity to mate with others. In Red-winged Blackbirds, high population density was significantly associated with increased extra-pair paternity (Gibbs et al. 1990). In addition to EPFs, proximity of conspecifics may lead to the possibility of conspecific brood parasitism (CBP, females laying eggs in other females' nests, see next section), as in Eastern Bluebirds (Gowaty and Bridges 1991a, b). However, there was no effect of population density on mating tactics in Tree Swallows (Dunn et al. 1994) or Bobolinks (Bollinger and Gavin 1991).

Breeding synchrony may be another constraint on male and female strategies. In a review of published studies, Stutchbury and Morton (1995) showed a positive correlation between rate of EPFs and breeding synchrony. This is consistent with the conclusions above that females control the frequency of EPFs and that females seek high-quality males as extra-pair mates. Breeding synchrony causes all males to compete and display at the same time, enabling females to choose among the widest possible selection. EPFs should be more advantageous under those conditions because females will be better able to assess which males are high quality.

While little has been done in other taxa, the few results available suggest that much remains to be learned about mating systems. For example, in dense populations of bluegill sunfish, Lepomis macrochirus, males that made and defended nests often lost paternity to transient individuals (Philipp and Gross 1994). Thus, the idea that male-only parental care has evolved in such species because external fertilization gives males higher confidence of paternity must be reexamined, especially with regard to natural variation in population density. And, in garter snakes, Thamnophis sirtalis, there is frequently multiple paternity within broods of offspring, showing that the copulatory plug is at best only partly effective in preventing later males from fertilizing eggs (Schwartz et al. 1989).

Conspecific brood parasitism

Estimating reproductive success in birds is further complicated when females lay eggs in other females' nests, behavior called conspecific brood parasitism (CBP; reviewed in Rohwer and Freeman 1989). Prior to the application of molecular techniques, this behavior was identified through deviations in the normal laying pattern of eggs, and this is still a useful technique (e.g., Bjorn and Erikstad 1994). CBP is also readily detected when molecular data exclude the social mother as a parent. It is less common for females to lay eggs in a conspecific's nest than for females to seek extrapair copulations (Gowaty and Bridges 1991b, MacWhirter 1991). For example, in Eastern Bluebirds, Sialia sialis, in South Carolina, allozyme electrophoresis and behavioral data showed that 0.5-4% of offspring resulted from CBP, while 10-30% of offspring result from EPFs (Gowaty and Karlin 1984). In the same species in Ontario, DNA fingerprinting showed that 2.4% of offspring resulted from CBP, while 8.4% resulted from EPFs (Meek et al. 1994). The frequency of CBP may rise as high as 10.9% (Zebra Finches; Birkhead et al. 1990), but most molecular studies have shown negligible levels of CBP. Detailed molecular analysis of CBP in Moorhens, Gallinula chloropus, showed that hosts accept parasitic eggs (McRae and Burke 1996). The authors suggest that such tolerance may be facilitated by the high average relatedness among neighbors which results from natal philopatry. More maternity assignment studies will be needed to determine general trends in the costs and benefits of CBP, and future research will concentrate on defining the ecological and demographic correlates of this behavior.

Living in social groups

In the species discussed below, social behavior goes beyond mating relationships and parental behavior. Mating may occur among some but not all group members, or the group may form for reasons unrelated to reproduction. Of the species included above, the polyandrous species would fit equally well below. They are labeled by their presumed mating system, but except for serially polyandrous examples, they live in stable groups similar to those of the cooperatively breeding birds below.

Family groups

A useful distinction can be made between animal groups that form when offspring remain with parents, and when "peers" come together in a group that may or may not consist of relatives. Most interest has centered on species in which offspring stay in their natal group and become helpers to the reproducing individuals.

When an individual remains in its natal group, or joins relatives, it has an opportunity to help its kin. For this reason, studies of social behavior have often been framed in Hamilton's logic (Hamilton 1964a, b). Hamilton's work introduced the idea of inclusive fitness, the sum of direct fitness (results from an individual's own reproductive efforts) and indirect fitness (enhancements in reproduction of kin caused by the focal individual's assistance, with each increment multiplied by the degree of relatedness between the focal individual and the reproductive). Molecular markers provide a way to determine the values of two critical variables for studies of social groups, genetic relatedness and exact distribution of reproduction among members of groups. Previously these were inferred from demographic and behavioral data.

Group formation by retention of offspring has been strongly linked to population density and habitat quality (Pruett-Jones and Lewis 1990, Koenig et al. 1992, Emlen 1994). Individuals are predicted to delay dispersal when this offers higher inclusive fitness than the alternatives of dispersing to become either an independent reproducer or a nonterritorial "floater." It is hard to evaluate the lifetime reproductive success for the three options because any particular individual can choose only one at a particular time in its life, but observations of group-living species support the reasoning. Seychelles Warblers, Acrocephalus sechellensis, changed dispersal patterns over time following their introduction onto an unoccupied island. At low-population density, all juveniles dispersed shortly after fledging. As population density increased, offspring began to remain on natal territories and cooperate with their parents in raising further broods (Komdeur 1992). This situation, called cooperative breeding, coincided with habitat saturation, and first occurred on high-quality territories. While lack of suitable breeding territories has often been implicated in delayed dispersal, male Superb Blue Wrens apparently delay dispersal primarily due to the lack of mates, and only secondarily due to the lack of suitable territories (Pruett-Jones and Lewis 1990).

Groups of cooperatively breeding birds are often described as having a monogamous pair assisted by helpers, which are offspring from previous years. Red-cockaded Woodpeckers, Picoides borealis, are such a species (Haig et al. 1994). DNA fingerprinting identified only one of 32 progeny as a product of an EPFs, and it was apparently sired by a nongroup mate. Similarly, in Scrub Jays, Aphelocoma coerulescens, the dominants thought to be the breeding pair were confirmed by DNA fingerprinting to be parents of all offspring raised by the group (G. Woolfenden, cited in Birkhead and Moller 1992). Thus, in these species, helpers apparently do not reproduce directly.

In other species, molecular methods have revealed that helpers do sometimes reproduce directly. In Stripebacked Wrens, Campylorhynchus nuchalis, a breeding pair may be aided by male and female offspring from previous years. Delayed dispersal was previously thought to be maintained by indirect reproductive success and delayed direct benefits in the form of production of future helpers and inheriting the position of breeding male in the group (Rabenold 1985). However, DNA fingerprinting showed that when the breeding female (their mother) dies and is replaced by an immigrant (unrelated female), auxiliary males may sire some of the new female's offspring (9% of all offspring produced fell in this category; Rabenold et al. 1990). In the sympatric population of Bicolored Wrens, C. griseus, auxiliary males sire just 2.3% of offspring; again, they only reproduce when they are unrelated to the breeding female (Haydock et al. 1996). In these two species, breeding females only occasionally mate with a male outside their group (1% in C. nuchalis and 2.3% in C. griseus). Thus, the Bicolored Wren genetic mating system approaches monogamy. Allozymes show that auxiliary males reproduce within groups of Acorn Woodpeckers, Melanerpes formicivorous, too (Joste et al. 1985), though the rate may be quite low (Mumme et al. 1985). Indeed, socially monogamous Acorn Woodpeckers are nearly (98%) genetically monogamous, too (Dickinson et al. 1995). However, when Acorn Woodpecker groups contain a behaviorally identifiable breeding pair, it is clear that the benefits of natal philopatry and helping behavior are a more complicated blend of direct and indirect effects than we had previously imagined. More complete data sets must be examined, from a larger number of cooperatively breeding species before we understand the diversity of routes through which this social system has evolved and been maintained.

In long-term studies of individually marked vertebrates, kinship can be estimated from inferred pedigree connections, and molecular methods can be integrated with long-term observations to confirm relationships and resolve unknown pedigree connections. This approach has allowed a thorough examination of the choice that individual dwarf mongooses, Helogale parvula, make as to whether to disperse or remain in their natal pack (Creel and Waser 1994, Keane et al. 1994). The analysis correctly predicted that males should be more likely to disperse than females. Genotyping of chimpanzees, Pan troglodytes, from Gombe allowed the assignment of paternity for offspring of females that mated with multiple males during their fertile period (Morin et al. 1994b). The data were used to confirm relatedness among cooperative males, and therefore a potential role for kin selection in the evolution of their behavior (Morin et al. 1994a). Morin's work shows how microsatellite markers are peculiarly appropriate for such studies; they can be obtained from tiny DNA samples, collected with minimal intrusion (shed hairs from chimp nests in this case; Morin and Woodruff 1992), and yet they yield a large quantity of high-quality information.

Dominance hierarchies are conspicuous features of many animal social groups. Individuals are presumed to contend for high dominance rank because it confers access to mates or breeding status. Parentage assignment using molecular markers has confirmed this presumption in some species, but in other species there is no clear relationship. Dominance status and male access to females inferred from behavioral observations of savannah baboons, Papio cyanocephalus, accurately predicted genetic relationships identified through DNA fingerprinting (Altmann et al. 1996). Behavioral observation overestimated reproductive success of dominant grey seals, Halichoerus gryphus, consistent with furtive behavior of subordinates (Amos et al. 1993b). Alpha male rhesus macaques, M. mulatta, were able to monopolize reproduction, too, at least in small groups (Melnick et al. 1984, Melnick 1987), but three other studies suggest caution in assuming that high dominance rank automatically confers high reproductive success. Under controlled conditions, alpha-male poeciliids, Limia perugiae, dominated reproduction in small groups but failed to reproduce in large groups (Schartl et al. 1993). In a study of three social groups of Pukekos, Porphyrio porphyrio melanotus, no relationship was found between dominance status and reproduction. Indeed, in one group, the alpha male fathered none of the 14 chicks hatched over three seasons (Lambert et al. 1994). In Barbary macaques, Macaca sylvanus, there was little reproductive dominance by the "alpha" male, and most males in a group sired offspring (von Segesser et al. 1995). The caution sounded by Millar et al. (1994) and Altmann et al. (1996) about interpretation of studies based on a limited part of the reproductive lifetime are particularly pertinent here; more work is required before abandoning the theory that animals fight for high dominance rank because it confers higher fitness. The data indicate that the size of the group in which an individual lives may be especially important in the dynamic relationship between its dominance status and its reproductive success.

Identification of group structure

In other social animals, individual identification and close behavioral observation are so difficult that molecular methods represent the only feasible approach to understanding their behavior. One of the first such studies was the investigation of the huge nursery colonies of Mexican free-tailed bats, Tadarida brasiliensis (McCracken 1984). McCracken used allozymes to show that females find and nurse their own pups most of the time, contrary to previous statements about indiscriminate nursing. This has been confirmed in other species of bats using DNA fingerprinting (Bishop et al. 1992, Watt and Fenton 1995). In lions, Panthera leo, long lifespan and low population density make it difficult to study a large sample of individuals over their lifetimes, let alone a sample of prides over the lives of all lions in those groups. DNA fingerprinting readily confirmed kinship among females within prides and revealed details of relatedness among males that form coalitions. Large coalitions of males are much more likely to consist of relatives than small coalitions (Packer et al. 1991). Though larger coalitions are more successful in taking over prides, it becomes increasingly unlikely, as size of coalition increases, that each individual male will mate following a takeover. Related males in larger coalitions will still benefit indirectly through reproduction of their male relatives. Naked mole-rats, Heterocephalus glaber, are African rodents that attract attention by being the only eusocial mammals, but defy study by their entirely fossorial life style (Jarvis et al 1994). DNA fingerprinting of individuals caught from wild colonies revealed intense inbreeding within colonies and high genetic similarity among colonies. These results are consistent with near-zero dispersal and colony formation by fission (Reeve et al. 1990). Whales are, perhaps, the epitome of difficult study subjects; Amos and colleagues have taken advantage of the opportunity presented by Faroese whale hunts where whole pods of long-finned pilot whales, Globicephala melas, are slaughtered. DNA fingerprinting using tissue samples from individuals and fetuses showed that female pod members were closely related, and that offspring were probably sired by males from other pods (Amos et al. 1991). Using microsatellite loci, the authors showed that males neither dispersed from, nor bred in, their natal pod (Amos et al. 1993a). So it seems likely that mating occurs when pods meet and temporarily fuse.

Two DNA fingerprinting studies of long-lived and highly mobile birds reveal different degrees of kinship among group members. Adult Black Vultures that shared communal roosts were shown to associate preferentially with relatives (Parker et al. 1995). This suggests that kin selection could promote the evolution of social behavior in such groups, including enhancement of communal roosts as "information centers." In contrast, Ravens, Corvus corax, which form feeding aggregations at carcasses, were shown to be generally unrelated to other members of foraging groups (Parker et al. 1994).

Social insects

Within groups of many social insects, individuals exhibit the most extreme form of altruism: they completely forgo reproduction to help raise another's offspring. In social Hymenoptera, molecular methods have been used extensively to yield data that allow estimation of relatedness among colony members. Coefficients of relatedness in a social insect colony containing a queen and her progeny reveal asymmetries that result from the haplodiploid sex determination system of Hymenopterans. Males develop from unfertilized eggs; they have one-half of their mother's genome, do not have a father, and produce genetically identical sperm. Females develop from fertilized eggs. Thus, female progeny of a single, once-mated, queen share all the paternal component of their genome and, on average, one-half of their mother's contribution. So females share 75% of their genes with their sisters but only 50% with their own offspring. Thus, adaptations for production of more sisters should be favored over adaptations for production of offspring. For this reason, the extraordinarily high relatedness among full sisters has been identified as a driving force in the repeated evolution of sociality in this family (Hamilton 1972). But pedigrees are rarely so simple and estimation of relatedness must rely on molecular techniques. Methods of analysis are sufficiently advanced (Pamilo 1984, Queller and Goodnight 1989) that estimating average relatedness is fairly easy in comparison to measuring the fitness decrement to altruists and fitness increments to kin (the cost and benefit terms of Hamilton's rule). While this approach leaves cost and benefit terms to future studies, estimating relatedness does show what the cost-benefit relationship must be for sociality to be favored.

Relatedness can be estimated from DNA fingerprints or their equivalent (Reeve et al. 1992), but most work has used single-locus markers, primarily allozymes. The estimate of average relatedness within a colony is a summary value. It reflects the number of queens, relative egg laying by queens, number of mates per queen, relative use of sperm from different mates, and relatedness within and between queens and their mates (Ross 1990, Queller 1993). The future application of single-locus markers, especially microsatellites (Choudhary et al. 1993, Hughes and Queller 1993), holds the promise of estimating relatedness values among subgroups within colonies, even between interacting pairs (Queller and Goodnight 1989). There are reasons to expect, however, that getting reliable evidence for pairwise relatedness values more distant than first-order requires genotype data from an enormous number of loci (Brookfield and Parkin 1993).

A wide variety of average relatedness values has been reported for Hymenoptera. In the best studied genus of wasps, Polistes, relatedness among females ranges from the value expected for full sisters, 0.75, down to 0.3 (Strassmann et al. 1989, Tsuchida 1994). In tropical wasps, which live in more complex colonies, there is also a range of relatedness among females from fairly high levels (r = 0.49) among females in some nests of Protopolybia exigua, to very low levels (r = 0.11) in Parachartergus colobopterus (Queller et al. 1988, 1993).

The wide range of relatedness values, especially the low values, provide many avenues for further work. Low relatedness indicates that individuals are presented an array of close to distant relatives with which they may cooperate or compete. In an investigation of whether Polistes annularis females choose to help close rather than distant relatives, allozyme data showed that cooperating groups were not closely related subsets of the group of all possible cooperators (Queller et al. 1990). The maintenance of sociality in the face of low relatedness implies a high benefit to cost ratio for sociality. Such a high ratio may be provided by demographic advantages. For example, when an individual emerges as an adult, it could choose to help raise related larvae and pupae already present in the nest. This yields a reproductive "headstart" over an individual that chooses to start her own nest (Queller 1989). Queller's work shows that the array of such demographic advantages can favor sociality even when relatedness is very low.

In ants, an even wider range of relatedness values has been reported. For example, in colonies with many queens, especially when those queens are mobile between colonies as in Iridomyrmex humilis, relatedness is close to zero, and intra-colony mating does not lead to appreciable inbreeding (Kaufmann et al. 1992). In other species, for example the slave-making ant Harpagoxenus sublaevis, relatedness among female nest mates is 0.75, confirming the presence of a single, once-mated queen (Bourke et al. 1988 and other examples in Page and Metcalf 1982). For Camponotus ants, multiple maternity within colonies has been revealed (Gertsch et al. 1995).

The primitively social bees are of particular interest for studies of the evolution of sociality in insects, since they have members which are solitary, grading through various levels of complexity to eusociality. Here, eusociality is defined as the presence within a colony of overlapping generations of adults that cooperate in caring for a brood produced by a subset of colony members. Social bees offer an opportunity to investigate factors that lead to sociality, and that lead from primitive sociality to the most complex expression of sociality, including presence of sterile castes. As in ants and wasps, relatedness values among female nestmates range from zero to fairly high (reviewed in Kukuk and Sage 1994). A strong test of how relatedness is involved in evolutionary pathways toward sociality and eusociality requires that demographic characters associated with sociality be evaluated in a clade that contains solitary, primitive, and advanced social species. This approach has recently been started in the genus Halictus by creating phylogenies based on allozyme data and then mapping social characters onto the cladogram (Packer 1991, Richards 1994). In the taxa studied, sociality is ancestral, but the analysis does show that reversals to solitary living have occurred. This approach has great potential for revealing the ecological conditions under which sociality evolves; the reversals to solitary life provide an opportunity to test the necessity of these ecological correlates for its maintenance.

Mating behavior is difficult to observe in many social insects and molecular methods are the only feasible way of measuring individual differences in reproductive success. In the ant Leptothorax acervorum, allozyme data were used to infer several aspects of reproductive biology (Stille et al. 1991): high relatedness among queens suggested that daughters were recruited back into the nest as additional queens, that colonies with a single queen had previously been multiqueen, and that colonies did not reproduce by budding. The finding of multiple mtDNA haplotypes within ant colonies suggests that matrilines may be traceable, at least when queen associations are unrelated individuals (Stille and Stille 1992). Application of microsatellite loci can even reveal how many males have contributed to a queen's store of sperm; amplification of loci from sperm extracted from the spermatheca of a tropical wasp showed that queens mate once (Goodnight et al. 1996). In bumble bees, four species have been found to have singly mated queens, while females of a fifth species mate multiply (Estoup et al. 1995).

Relatedness coefficients in social insect colonies have profound implications for how colonies produce sexual offspring (Trivets and Hare 1976). "Split sex ratio theory" predicts that colonies with higher than average female relatedness should specialize in producing female reproductives that are sisters of the workers, while colonies with lower than average relatedness should produce male reproductives that are the workers' own sons. For this to occur, three conditions must be met: mean within-colony relatedness varies among colonies, workers can assess relatedness, and workers control colony-level investment in male and female reproductive offspring (Boomsma 1990, Boomsma and Grafen 1991). Microsatellite markers were used to determine not only that male offspring are produced by workers in Myrmica ants (Evans 1993), but also that in Myrmica tahoensis, female sexuals are produced by colonies with high relatedness among females, and males in colonies with lower relatedness (Evans 1995). Further, workers seem to assess relatedness itself, not an index such as queen number, in making sex allocation decisions. Relatedness has been shown to change over time within colonies of social wasps, and consistent with predictions, female reproductives were produced when colonies had high relatedness, and males when relatedness was lower (Queller et al. 1993, Strassmann et al. 1997). Strong support for split sex ratio theory will require resolution of exceptions such as the primitively social bee Halictus ligatus. Here, relatedness values estimated from allozyme data suggest that the expected pattern is reversed (Richards et al. 1995). The authors' re-interpretation of sex investment models to give consideration to the timing of reproduction may resolve the conflict.

Genetic diversity in social insect colonies has recently been suggested to be important in its own right (rather than as a way of estimating relatedness). Four hypotheses suggest advantages to queens that mate multiply and risk internecine conflict and the possibility of reduced colony productivity. The enhanced genetic diversity that results from multiple mating may: (1) allow more complete expression of caste diversity; (2) expand the range of environmental variation that a colony can tolerate; (3) reduce the number of sterile diploid males produced (which develop from zygotes homozygous at the sex determining locus); and/or (4) increase colonywide immunity to parasites and diseases (Page and Metcalf 1982, Page 1986, Sherman et al. 1988). These hypotheses may explain the extraordinary number of mates in honey bees; allozyme and DNA fingerprinting data revealed that naturally mated queen honey bees use the sperm from several males (as many as 11-12 per queen; Page and Metcalf 1982, Blanchetot 1991, Haberl and Moritz 1994). An experiment in which queen honey bees, Apis mellifera, were artificially inseminated showed that colonies with queens inseminated with sperm from several males were sometimes more productive, and sometimes less productive, than colonies where the queen was singly inseminated (Oldroyd et al. 1992). Consistent with hypothesis 1, genetic subgroups of colonies appear to differ in the frequency with which they perform tasks (Page et al. 1992, O'Donnell 1996). Despite hypothesized benefits to multiple mating, data have also shown that queens in many species mate only once. Single-mating species are often those with multiple queens per colony, which is an alternative mechanism by which genetic diversity is increased (reviewed in Goodnight et al. 1996).

The relationship between social structure and genetic population structure

A small number of studies have used molecular methods to address the relationship between social structure and larger scale genetic population structure. For example, tight social grouping may lead to genetic divergence among groups (Chesser 1991a, b) and eventually to local adaptation and speciation (Baker and Marler 1980). Using protein electrophoresis, Melnick was able to determine the relationship between behavior and population structure of rhesus macaques (Melnick et al. 1984, Melnick 1987). Groups were not as genetically differentiated as had been presumed on the basis of behavior alone; high gene flow is mediated by male dispersal, which also leads groups to be outbred. A similar pattern was found in Barbary macaques (Melnick 1987, Scheffrahn et al. 1993). In ants, allozyme data showed that two closely related species, Myrmica ruginodis and M. rubra, differed significantly in the level of genetic differentiation between sites within localities, and between localities (Seppa and Pamilo 1995). This is likely a reflection of the tendency of M. rubra to form new colonies by fission. It leads to the expectation that neighboring colonies will be related, and predicts that inter-colony behavior will differ substantially between the species. Field voles, Microtus ochrogaster, have been shown to have greater home range overlap with relatives than nonrelatives, suggesting a role for relatedness in aspects of space use and population structure (Sera and Gaines 1994).

Limited dispersal is often correlated with greater levels of inbreeding, as seen in social vs. nonsocial spiders. In web-building social spiders, allozyme electrophoresis revealed significant population structure; apparently, the lack of movement of social species that need to construct a large web leads to considerable inbreeding (reviewed by Reichert and Roeloffs 1993). In contrast, a large, social, hunting spider from Australia, Delena cancerides, showed no inbreeding and high heterozygosity, suggesting a large panmictic population (Rowell and Aviles 1995).

Living in nonfamily groups

When group members are unrelated, kin selection cannot explain social behavior, and alternative models based on reciprocity, mutualism, and ecological advantages associated with group living need to be evaluated (reviewed by Connor 1995, Mesterton-Gibbons and Dugatkin 1992). Formation of groups by unrelated individuals may result when animals live in groups to gain access to a limited resource, to reduce predation, and/or to enable individuals to take advantage of a food resource too rarely available to solitary animals (Alexander 1974). However, group living involves costs, particularly increased disease and parasite transmission (e.g., Cote and Poulin 1994) and increased competition for resources, including mates. Competition for mates can potentially be assessed through the use of molecular markers to determine whether there is a high probability of extra-pair matings. Certainly there is a behaviorally demonstrated relationship between EPCs and sociality (Moller and Birkhead 1993). There are also demonstrations that this is not an automatic cost; DNA fingerprinting failed to detect any extra-pair young in colonial Cory's Shearwaters (Swatschek et al. 1994), Fulmars (Hunter et al. 1992), or Leach's Storm Petrels (Mauck et al. 1995).

Reciprocity and mutualism are not alternatives to kin selection as explanations of social behavior; all may operate simultaneously. For example, vampire bats, Desmodus rotundus, roost together in stable female associations. The main selective advantage for maintaining cohesive female groups is food sharing between associates (Wilkinson 1985a). Allozyme electrophoresis allowed Wilkinson to determine that relatedness was low among females within groups, despite the fact that some daughters were recruited into groups (Wilkinson 1985b). In this species, both relatedness and reciprocity independently and approximately equally predict performance of an altruistic behavior, the donation of blood to an individual that failed to obtain a blood meal and would probably starve to death without the donation (Wilkinson 1984).

THE EVOLUTION OF SOCIAL BEHAVIOR

Models of reproductive skew within social groups attempt to put social behavior in vertebrates and social insects into a single framework. Reproductive skew is the degree to which dominant animals monopolize the reproductive output of groups (Vehrencamp 1983, Reeve 1991, Reeve and Nonacs 1992, Reeve and Ratnieks 1993, Reeve and Keller 1995). The logic of reproductive skew theory is that a dominant animal must allow subordinates limited reproduction as an inducement to stay or to be peaceful. All else being equal, when the group consists of relatives, the dominant animal is predicted to allow less subordinate reproduction than when the group consists of nonrelatives because subordinate relatives gain indirect fitness benefits, raising the threshold at which leaving the group offers higher inclusive fitness. While the specifics of tests of predictions such as these are debated (e.g., Strassmann 1993), the data from social insects and vertebrates are consistent with the hypotheses (Packer et al. 1991, Reeve and Keller 1995). Future studies in this field will undoubtedly make extensive use of molecular methods for assessing both relatedness among individuals and accurately quantifying reproduction of dominants and subordinates.

The comparative approach to social behavior

Rigorous use of the comparative method can offer insights into the adaptive value of social behavior that are unobtainable in any other way (Ligon 1993). One prerequisite for such an analysis is a well-resolved phylogeny (Harvey and Pagel 1991). Pioneering analyses using phylogenies based on morphology include McKitrick's (1992) analysis of parental care, Prum's (1994) analysis of manakin social behavior, and Carpenter's (1989, 1991) work on the evolution of eusociality in Hymenoptera. DNA sequence data are now the data of choice for generating phylogenies, but other molecular techniques have also been used, as mentioned earlier. The phylogeny of birds based on DNA-DNA hybridization data (Sibley et al. 1988, Sibley and Ahlquist 1990) has provided the foundation for several comparative studies of avian social behavior. Transitions from monogamy to polygamy have been shown to be more common than reversals and are concentrated in certain monophyletic groups having precocial young (Temrin and Sillen-Tullberg 1994). Precocial development is also associated with transitions to shorter periods of pair bonding, and to polyandry but not polygyny (Temrin and Sillen-Tullberg 1995). These character-state changes largely occur within families, often in terminal taxa, providing opportunities for future comparative analyses to examine both the origin and maintenance of such mating systems.

Cooperative breeding in birds has a strong phylogenetic component (Edwards and Naeem 1993). By examining taxa in which cooperative and noncooperative breeding were both present, Edwards and Naeem (1993) concluded that origins of cooperative breeding are often ancient, preceding diversification of the groups. As Prum (1994) points out, the ecological factors associated with a character-state change will be most evident when such a change has occurred in a terminal lineage. Otherwise, the passage of time and phylogenetic inertia may obscure the relationship, as perhaps with cooperative breeding. Ideally, a phylogeny will include enough species and enough recent character-state changes to give confidence in the relationship to ecological change.

Eusociality in Hymenoptera also has a strong phylogenetic component. A "total evidence" approach to the evolution of social bees, using morphological and DNA sequence data in combination, supports a single, presumably ancient, origin of sociality (Chavarria and Carpenter 1994). This emphasizes the need to study taxa in which the social behavior of interest is variable among the terminal taxa. Questions about the evolutionary origin of sociality in the Hymenoptera seem most likely to be answered by studies like Packer's phylogenetically explicit analyses of the solitary and primitively social bees (Packer 1991, Richards 1994).

SUMMARY

The integration of molecular techniques into behavioral and demographic approaches to the study of social systems has not led to simply a refinement of details, but rather to challenges of existing paradigms and new hypotheses. I expect that the number of such studies will continue to burgeon until the field of social biology viewed by Tinbergen (1953) is as influenced by application of molecular techniques as developmental biology has been by molecular genetics over the same time period.

Molecular studies of mating systems have revealed much greater variation within and among populations than previously recognized. Monogamy in birds has been shown to subsume a wide range of genetic mating systems. The high frequency at which females may choose to mate with extra-pair males requires that the original hypotheses for the evolution of polygyny be revised to explicitly consider that the choice of mate is not determined solely by the territory upon which a female nests. Discussion of polyandry has been shown to be premature in some species because only one male mates with a female. We are currently in a period of large-scale data gathering to examine the mating systems of many populations and species inhabiting a range of habitats. Only then can a more complete view of genetic mating systems emerge.

Inevitably, one lasting impact of widespread application of molecular techniques in studies of mating systems will be abandonment of simplicity. A term such as monogamy will not conjure up an image of an enduring exclusive mating relationship between socially bonded male and female. The social bond must be assessed independently of mating relationships. The strategies by which females and males may maximize their reproductive success, constraints on their expression, conflicts between them, and the mechanisms by which conflicts are resolved, will all affect the mating relationship.

Molecular methods have provided data for estimating two of the crucial values for understanding the evolution of social behavior (beyond mating systems), genetic relatedness, and direct reproduction, especially by subordinates. Ready estimation of relatedness turns attention back to costs and benefits of social behavior that are determined by ecological parameters such as predation and resource abundance. These remain difficult to estimate. The methods have also permitted estimates of previously unknowable variables, such as the effects of sperm storage and relatedness among very long-lived animals. In social insects, the role of relatedness in determining the sex ratio of progeny has been established, but there is still no clear answer to the big question of what role relatedness played in the initial stages of social evolution of Hymenoptera.

There are new areas of research that would not have been developed but for the early data from molecular methods. These include investigation of whether animals are making sophisticated genetic assessments of other individuals; do birds seek mates that are optimally unrelated to them to avoid both inbreeding and outbreeding depression (Pusey and Wolf 1996)? Similarly, do social insects alter their behavior according to changes in genetic relatedness? What is the role of genetic diversity in social insect colonies, and the relative importance of hypothesized advantages for lower relatedness?

So far, molecular methods have contributed to sociobiology primarily by revealing pedigree connections, or their average, among individuals within a population. However, these techniques also have the power to estimate relatedness among populations, species, and higher taxa (Avise 1994), and these applications are likely to be emphasized in future work. For example, DNA sequence data will be used to generate phylogenies that permit rigorous use of the comparative method to infer the ecological circumstances favoring origin of social traits. Phylogenies of populations could be used to investigate the influence of ecological variables on social characters such as EPFs or cooperative breeding.

Future applications will also broaden the spectrum of questions addressed both taxonomically and conceptually. In social insects, for example, a major avenue for future work will be to look at even more fine-scale questions such as cooperation and conflict at the level of patrilines and matrilines, and specialization in task performance. Moving in the other direction, now that we have accurate descriptions of the genetic and social dynamics within populations, studies examining the consequences of those patterns for population structure and local adaptation should become more common.

To date, applications of molecular techniques to studies of social behavior have made every attempt to use neutral markers; those genomic regions that are most useful for identifying individuals within populations are those that are highly variable and are under no functional constraints (they are not under selection). In contrast, most techniques outlined in molecular biology reference volumes are aimed at elucidating the functional roles of particular loci. New levels of understanding of social behavior will be reached when loci influencing behavior are identified, and when control of expression of such loci is understood.

ACKNOWLEDGMENTS

I wish to thank NDEPSCoR and NSF through grant DEB94 24625 for support while working on this review. I am grateful to Patty Parker and Allison Snow for their many helpful comments on earlier versions of the manuscript. I also wish to thank the external reviewer who put so much effort into improving the paper.

LITERATURE CITED

Alexander, R. D. 1974. The evolution of social behavior. Annual Review of Ecology and Systematics 5:325-383.

Altmann, J., S. Alberts, and S. A. Haines. 1996. Behavior predicts genetic structure in a wild primate group. Proceedings of the National Academy of Sciences (USA) 93: 5797-5801.

Amos, B., J. Barrett, and G. A. Dover. 1991. Breeding behaviour of pilot whales revealed by DNA fingerprinting. Heredity 67:49-55.

Amos, B., C. Schlotterer, and D. Tautz. 1993a. Social structure of pilot whales revealed by analytical DNA profiling. Science 260:670-672.

Amos, W., S. Twiss, P. P. Pomeroy, and S. S. Anderson. 1993b. Male mating success and paternity in the grey seal, Halichoerus gryphus: a study using DNA fingerprinting. Proceedings of the Royal Society of London, Series B, 252: 199-207.

Amos, B., S. Twiss, P. Pomeroy, and S. Anderson. 1995. Evidence for mate fidelity in the gray seal. Science 268: 1897-1899.

Avise, J. C. 1994. Molecular markers, natural history and evolution. Chapman and Hall, New York, New York, USA.

Baker, M., and P. Marler. 1980. Behavioral adaptations that constrain the gene pool in vertebrates. Pages 59-80 in H. Markl, editor. Evolution of social behavior, hypotheses and empirical tests. Verlag Chemic, Weinheim, Germany.

Birkhead, T. 1987. Sperm competition in birds. Trends in Ecology and Evolution 2:268-272.

Birkhead, T. R., T. Burke, R. Zann, F. M. Hunter, and A. P. Krupa. 1990. Extra-pair paternity and intraspecific brood parasitism in wild zebra finches Taeniopygia guttata, revealed by DNA fingerprinting. Behavioral Ecology and Sociobiology 27:315-324.

Birkhead, T. R., and A. P. Moller. 1992. Sperm competition in birds. Academic Press, London, UK.

Bishop, C. M., G. Jones, C. M. Lazarus, and P. A. Racey. 1992. Discriminate suckling in pipistrelle bats is supported by DNA fingerprinting. Molecular Ecology 1:255-258.

Bjorn, T. H., and K. E. Erikstad. 1994. Patterns of intraspecific nest parasitism in the high Arctic Common Eider (Somateria mollissima borealis). Canadian Journal of Zoology 72:1027-1034.

Blanchetot, A. 1991. Genetic relatedness in honeybees as established by DNA fingerprinting. Journal of Heredity 82: 391-396.

Bollinger, E. K., and T. A. Gavin. 1991. Patterns of extra-pair fertilizations in bobolinks. Behavioral Ecology and Sociobiology 29:1-7.

Boomsma, J. J. 1990. Intraspecific variation in ant sex ratios and the Trivers-Hare hypothesis. Evolution 44:1026-1034.

Boomsma, J. J., and A. Grafen. 1991. Colony-level sex ratio selection in the eusocial Hymenoptera. Journal of Evolutionary Biology 3:383-407.

Bourke, A. F. G., T. M. van der Have, and N. R. Franks. 1988. Sex ratio determination and worker reproduction in the slave-making ant Harpagoxenus sublaevis. Behavioral Ecology and Sociobiology 23:233-245.

Brooker, M. G., I. Rowley, M. Adams, and P. R. Baverstock. 1990. Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species. Behavioral Ecology and Sociobiology 26:191-199.

Brookfield, J. F. Y., and D. T. Parkin. 1993. The use of single-locus DNA probes in the establishment of relatedness in wild populations. Heredity 70:660-663.

Burke, T., N. B. Davies, M. W. Bruford, and B. J. Hatchwell. 1989. Parental care and mating behavior of polyandrous dunnocks Prunella modularis related to paternity by DNA fingerprinting. Nature 338:249-251.

Carpenter, J. M. 1989. Testing scenarios: wasp social behavior. Cladistics 5:131-144.

-----. 1991. Phylogenetic relationships and the origin of social behavior in the Vespidae. Pages 7-32 in K. Ross and R. Matthews, editors. The social biology of wasps. Cornell University Press, Ithaca, New York, USA.

Chavarria, G., and J. M. Carpenter. 1994. "Total evidence" and the evolution of highly social bees. Cladistics 10:229-258.

Chesser, R. K. 1991a. Influence of gene flow and breeding tactics on gene diversity within populations. Genetics 129: 573-584

-----. 1991b. Gene diversity and female philopatry. Genetics 127:437-448.

Choudhary, M., J. E. Strassman, C. R. Solis, and D. C. Queller. 1993. Microsatellite variation in a social insect. Biochemical Genetics 31:87-96.

Connor, R. C. 1995. Altruism among non-relatives: alternatives to the 'Prisoner's Dilemma'. Trends in Ecology and Evolution 10:84-86.

Cote, I. M., and R. Poulin. 1994. Parasitism and group size in social animals: a meta-analysis. Behavioral Ecology 6: 159-165.

Creel, S. R., and P.M. Waser. 1994. Inclusive fitness and reproductive strategies in dwarf mongooses. Behavioral Ecology 5:339-348.

Davies, N. B. 1985. Cooperation and conflict among Dunnocks, Prunella modularis, in a variable mating system. Animal Behaviour 33:628-648.

-----. 1989. Sexual conflict and the polygamy threshold. Animal Behaviour 38:226-234.

-----. 1991. Mating systems. Pages 263-294 in J. R. Krebs and N. B. Davies, editors. Behavioural ecology, an evolutionary approach, Third edition. Blackwell, London, UK.

Davies, N. B., I. R. Hartley, B. J. Hatchwell, and N. E. Langmore. 1996. Female control of copulations to maximize male help: a comparison of polygynandrous alpine accentors, Prunella collaris, and dunnocks, P. modularis. Animal Behaviour 51:27-47.

Decker, M. D., P. G. Parker, D. J. Minchella, and K. N. Rabenold. 1993. Monogamy in black vultures: genetic evidence from DNA fingerprinting. Behavioral Ecology 4:29-35.

DeLay, L. S., J. Faaborg, J. Naranjo, S. M. Paz, T. DeVries, and P. G. Parker. 1996. Paternal care in the cooperatively polyandrous Galapagos hawk. Condor 98:300-311.

Dickinson J., J. Haydock J., W. Koenig, M. Stanback, and F. Pitelka. 1995. Genetic monogamy in single-male groups of acorn woodpeckers, Melanerpes formicivorous. Molecular Ecology 4:765-769.

Dixon, A., D. Ross, S. L. C. O'Malley, and T. Burke. 1994. Paternal investment inversely related to degree of extra-pair paternity in the Reed Bunting. Nature 371:698-700.

Dunn, P. O., R. J. Robertson, D. Michaud-Freeman, and P. T. Boag. 1994. Extra-pair paternity in Tree Swallows: why do females mate with more than one male? Behavioral Ecology and Sociobiology 35:273-281.

Edwards, S. V., and S. Naeem. 1993. The phylogenetic component of cooperative breeding in perching birds. American Naturalist 141:754-789.

Emlen, S. T. 1994. Benefits, constraints and the evolution of the family. Trends in Ecology and Evolution 9:282-285.

Emlen, S. T., and L. W. Oring. 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197: 215-223.

Estoup, A., A. Scholl, A. Pouvreau, and M. Solignac. 1995. Monoandry and polyandry in bumble bees (Hymenoptera; Bombinae) as evidenced by highly variable microsatellites. Molecular Ecology 4:89-93.

Evans, J. D. 1993. Parentage analyses in ant colonies using simple sequence repeat loci. Molecular Ecology 2:393-397.

-----. 1995. Relatedness threshold for the production of female sexuals in colonies of a polygynous ant, Myrmica tahoensis, as revealed by microsatellite DNA analysis. Proceedings of the National Academy of Sciences (USA) 92: 6514-6517.

Faaborg, J., P. G. Parker, L. DeLay, T. de Vries, J. C. Bednarz, S. Maria Paz, J. Naranjo, and T. A. Waite. 1995. Confirmation of cooperative polyandry in the Galapagos Hawk (Buteo galapagoensis). Behavioral Ecology and Sociobiology 36:83-90.

Gertsch, P., P. Pamilo, and S.-L. Varvio. 1995. Microsatellites reveal high genetic diversity within colonies of Camponotus ants. Molecular Ecology 4:257-260.

Gibbs, H. L., A. W. Goldizen, C. Bullough, and A. R. Goldizen. 1994. Parentage analysis of multi-male social groups of Tasmanian Native Hens (Tribonyx mortierii): genetic evidence for monogamy and polyandry. Behavioral Ecology and Sociobiology 35:363-371.

Gibbs, H. L., P. J. Weatherhead, P. T. Boag, B. N. White, L. M. Tabak, and D. J. Hoysak. 1990. Realized reproductive success of polygynous red-winged blackbirds revealed by DNA markers. Science 250:1394-1397.

Goodnight, K. F., J. E. Strassmann, C. J. Klingler, and D.C. Queller. 1996. Single mating and its implications for kinship structure in a multiple-queen wasp, Parachartergus colobopterus. Ethology, Ecology and Evolution 8:191-198.

Gowaty, P. A., and W. C. Bridges. 1991a. Behavioral, demographic and environmental correlates of extra-pair fertilizations in eastern blue birds. Behavioral Ecology 2:339-350.

Gowaty, P. A., and W. C. Bridges. 1991b. Nestbox availability affects extra-pair fertilizations and conspecific nest parasitism in eastern bluebirds, Sialia sialis. Animal Behaviour 41:661-675.

Gowaty, P. A., and A. A. Karlin. 1984. Multiple maternity and paternity in single broods of apparently monogamous eastern bluebirds (Sialia sialis). Behavioral Ecology and Sociobiology 15:91-95.

Graves, J., R. T. Hay, M. Scallan, and S. Rowe. 1991. Extra-pair paternity in the shag, Phalacrocorax aristotelis, as determined by DNA fingerprinting. Journal of Zoology, London 226:399-408.

Gray, E. M. 1996. Female control of offspring paternity in a western population of red-winged blackbirds (Agelaius phoeniceus). Behavioral Ecology and Sociobiology 38: 267-278.

Gyllensten, U. B., S. Jakobsson, and H. Temrin. 1990. No evidence for illegitimate young in monogamous and polygynous warblers. Nature 343:168-170.

Haberl, M., and R. F. A. Moritz. 1994. Estimation of intracolonial worker relationship in a honey bee colony (Apis mellifera L.) using DNA fingerprinting. Insectes Sociaux 41:263-272.

Haig, S. M., J. R. Walters, and J. H. Plissner. 1994. Genetic evidence for monogamy in the cooperatively breeding Red-Cockaded Woodpecker. Behavioral Ecology and Sociobiology 34:295-303.

Hamilton, W. D. 1964a. The genetical evolution of social behaviour. I. Journal of Theoretical Biology 7:1-16.

-----. 1964b. The genetical evolution of social behaviour. II. Journal of Theoretical Biology 7:17-52.

-----. 1972. Altruism and related phenomena, mainly in the social insects. Annual Review of Ecology and Systematics 3:193-232.

Harvey, P. H., and M.D. Pagel. 1991. The comparative method in evolutionary biology. In R. M. May and P. H. Harvey, editors. Oxford Series in Ecology and Evolution. Oxford University Press, Oxford, UK.

Hasselquist, D., S. Bensch, and T. von Schantz. 1995. Low frequency of extrapair paternity in the polygynous Great Reed Warbler, Acrocephalus arundinaceus. Behavioral Ecology 6:27-38.

Haydock, J., P. G. Parker, and K. N. Rabenold. 1996. Extrapair paternity uncommon in the cooperatively breeding bicolored wren, Campylorhynchus griseus. Behavioral Ecology and Sociobiology 38:1-16.

Hughes, C. R., and D. C. Queller. 1993. Detection of highly polymorphic microsatellite loci in a species with little allozyme polymorphism. Molecular Ecology 2:131-137.

Hunter, F. M., T. Burke, and S. E. Watts. 1992. Frequent copulation as a method of paternity assurance in the northern fulmar. Animal Behavior 44:149-156.

Jarvis, J. U. M., J. O'Riain, N. C. Bennet, and P. W. Sherman. 1994. Mammalian eusociality: a family affair. Trends in Ecology and Evolution 9:47-51.

Joste, N., D. Ligon, and P. B. Stacey. 1985. Shared paternity in the acorn woodpecker (Melanerpes formicivorus). Behavioral Ecology and Sociobiology 17:39-41.

Kaufmann, B., J. J. Boomsma, L. Passera, and K. N. Peterson. 1992. Relatedness and inbreeding in a French population of the unicolonial ant Iridomyrmex humilis (Mayr). Insectes Sociaux 39:195-213.

Keane, B., P. M. Waser, S. R. Creel, N.M. Creel, L. F. Elliot, and D. J. Minchella. 1994. Subordinate reproduction in dwarf mongooses. Animal Behaviour 47:65-75.

Kempenaers, B., G. R. Verheyen, M. Van Den Broeck, T. Burke, C. Van Broeckhoven, and A. A. Dhondt. 1992. Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357:494-496.

Koenig, W. D., F. A. Pitelka, W. J. Carmen, R. L. Mumme, and M. T. Stanback. 1992. The evolution of delayed dispersal in cooperative breeders. Quarterly Review of Biology 67:111-150.

Komdeur, J. 1992. Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler. Nature 358:493-495.

Kukuk, P. F., and G. K. Sage. 1994. Reproductivity and relatedness in a communal halictine bee Lasioglossum (Chilalictus) hemichalceum. Insectes Sociaux 41:443-455.

Lambert, D. M., C. D. Millar, K. Jack, S. Anderson, and J. L. Craig. 1994. Single- and multilocus DNA fingerprinting of communally breeding Pukeko: do copulations or dominance ensure reproductive success? Proceedings of the National Academy of Sciences, (U S A) 91:9641-9645.

Lifjeld, J. T., T. Slagsvold, and H. M. Lampe. 1991. Low frequency of extra-pair paternity in pied flycatchers revealed by DNA fingerprinting. Behavioral Ecology and Sociobiology 29:95-101.

Lightbody, J. P., and P. J. Weatherhead. 1988. Female settling patterns and polygyny: tests of a neutral-mate-choice hypothesis. American Naturalist 132:20-33.

Ligon, J. D. 1993. The role of phylogenetic history in the evolution of contemporary mating and parental care systems. Pages 1-46 in D. M. Power, editor. Current Ornithology. Volume 10. Plenum, New York, New York, USA.

MacWhirter, R. B. 1991. On the rarity of intraspecific brood parasitism. Condor 91:485-492.

Mauck, R. A., T. A. Waite, and P. G. Parker. 1995. Monogamy in Leach's storm petrel: DNA fingerprinting evidence. Auk 112:473-482.

McCracken, G. F. 1984. Communal nursing in mexican free-tailed bat maternity colonies. Science 223:1090-1091.

McDonald, D. B. 1989. Cooperation under sexual selection: age-graded changes in a lekking bird. American Naturalist 134:709-730.

McDonald, D. B., and W. K. Potts. 1994. Cooperative display and relatedness among males in a lek-mating bird. Science 266:1030-1032.

McKitrick, M. C. 1992. Phylogenetic analysis of avian parental care. Auk 109:828-846.

McRae, S. B., and T. Burke. 1996. Intraspecific brood parasitism in the moorhen: parentage and parasite-host relationships determined by DNA fingerprinting. Behavioral Ecology and Sociobiology 38:115-129.

McRae, S. B., and K. M. Kovacs. 1994. Paternity exclusion by DNA fingerprinting, and mate guarding in the hooded seal Cystophora cristata. Molecular Ecology 3:101-107.

Meek, S. B., R. J. Robertson, and P. T. Boag. 1994. Extrapair paternity and intraspecific brood parastism in Eastern Bluebirds revealed by DNA fingerprinting. Auk 111:739-744.

Melnick, D. J. 1987. The genetic consequences of primate social organization: a review of macaques, baboons and vervet monkeys. Genetica 73:117-135.

Melnick, D. J., C. J. Jolly, and K. K. Kidd. 1984. The genetics of a wild population of rhesus monkeys (Macaca mulatta). I. Genetic variability within and between social groups. American Journal of Physical Anthropology 63: 341-360.

Mesterton-Gibbons, M., and L. A. Dugatkin. 1992. Cooperation among unrelated individuals: evolutionary factors. Quarterly Review of Biology 67:267-281.

Millar, C. D., I. Anthony, D. M. Lambert, P. M. Stapleton, C. C. Bergmann, A. R. Bellamy, and E. C. Young. 1994. Patterns of reproductive success determined by DNA fingerprinting in a communally breeding oceanic bird. Biological Journal of the Linnean Society 52:31-48.

Mock, D. W., and M. Fujioka. 1990. Monogamy and long-term pair bonding in vertebrates Trends in Ecology and Evolution 5:39-43.

Moller, A. P. 1988. Paternity and paternal care in the swallow, Hirundo rustica Animal Behaviour 36:996-1005.

-----. 1991. Defence of offspring by male swallows, Hirundo rustica, in relation to participation in extra-pair copulations by their mates. Animal Behaviour 42:261-268.

Moller, A. P., and T. R. Birkhead. 1993. Cuckoldry and sociality: a comparative study of birds. American Naturalist 142:118-140.

Morin, P. A., J. J. Moore, R. Chakraborty, J. Li, J. Goodall, and D. S. Woodruff. 1994a. Kin selection, social structure, gene flow and the evolution of chimpanzees. Science 265: 1193-1201.

Morin, P. A., J. Wallis, J. J. Moore, and D. S. Woodruff. 1994b. Paternity exclusion in a community of wild chimpanzees using hypervariable simple sequence repeats. Molecular Ecology 3:469-478.

Morin, P., and D. S. Woodruff. 1992. Paternity exclusion using multiple hypervariable microsatellite loci amplified from nuclear DNA of hair cells. Pages 63-81 in R. D. Martin, A. F. Dixson, and E. J. Wickings, editors. Paternity in primates: genetic tests and theories. Implications of human DNA fingerprinting. Karger, Basel, Switzerland.

Morton, E. S., L. Forman, and M. Braun. 1990. Extrapair fertilizations and the evolution of colonial breeding in purple martins. Auk 107:275-283.

Mumme, R. L., W. D. Koenig, R. M. Zink, and J. A. Marten. 1985. Genetic variation and parentage in a California population of acorn woodpeckers. Auk 102:305-312.

O'Donnell, S. 1996. RAPD markers suggest genotypic effects on forager specialization in a eusocial wasp. Behavioral Ecology and Sociobiology 38:83-88.

Oldroyd, B. P., T. E. Rinderer, J. R. Harbo, and S. M. Buco. 1992. Effects of intracolonial genetic diversity on the honey bee (Hymenoptera: Apidae) colony performance. Annals of the Entomological Society of America 85:335-343.

Oring, L. W., R. C. Fleischer, M. J. Reed, and K. E. Marsden. 1992. Cuckoldry through stored sperm in the sequentially polyandrous spotted sandpiper. Nature 359:631-633.

Packer, C., D. Gilbert, A. Pusey, and S. O'Brien. 1991. A molecular genetic analysis of kinship and cooperation in African lions. Nature 351:562-565.

Packer, L. 1991. The evolution of social behavior and nest architecture in the sweat bees of the sub-genus Evylaeus (Hymenoptera: Halictidae): a phylogenetic approach. Behavioral Ecology and Sociobiology 29:153-160.

Page, R. E. 1986. Sperm utilization in social insects. Annual Review of Entomology 31:297-320.

Page, R. E., and R. A. Metcalf. 1982. Multiple mating, sperm utilization and social evolution. American Naturalist 119: 263-281.

Page, R., G. Robinson, D. Britton, and M. K. Fondrk. 1992. Genotypic variability for rates of behavioral development in worker honeybees (Apis mellifera L.). Behavioral Ecology 3:173-180.

Pamilo, P. 1984. Genetic relatedness and evolution of insect sociality. Behavioral Ecology and Sociobiology 15:241-248.

Parker, P. G., T. A. Waite, and M. D. Decker. 1995. Kinship and association in communally roosting black vultures. Animal Behaviour 49:395-401.

Parker, P. G., T. A. Waite, B. Heinrich, and J. M. Marzluff. 1994. Do common ravens share ephemeral food resources with kin? DNA fingerprinting evidence. Animal Behaviour 48:1085-1093.

Philipp, D. P., and M. R. Gross. 1994. Genetic evidence for cuckoldry in bluegill Lepomis macrochirus. Molecular Ecology 3:563-569.

Pruett-Jones, S. G., and M. J. Lewis. 1990. Sex ratio and habitat limitation promote delayed dispersal in Superb Fairy-wrens. Nature 348:541-542.

Prum, R. O. 1994. Phylogenetic analysis of the evolution of alternative social behavior in the Manakins (Aves: Pipridae). Evolution 48:1657-1675.

Pusey, A., and M. Wolf. 1996. Inbreeding avoidance in animals. Trends in Ecology and Evolution 11:201-206.

Queller, D. C. 1989. The evolution of eusociality: reproductive headstarts of workers. Proceedings of the National Academy of Sciences (USA) 86:3224-3226.

-----. 1993. Genetic relatedness and its components in polygynous colonies of social insects. Pages 132-152 in L. Keller, editor. Queen number and sociality in insects. Oxford University Press, Oxford, UK.

Queller, D. C., and K. F. Goodnight. 1989. Estimating relatedness using genetic markers. Evolution 43:258-275.

Queller, D. C., C. R. Hughes, and J. E. Strassmann. 1990. Wasps fail to make distinctions. Nature 344:6265.

Queller, D. C., J. E. Strassmann, and C. R. Hughes. 1988. Genetic relatedness in colonies of tropical wasps with multiple queens. Science 242:1155-1157.

Queller, D. C., J. E. Strassmann, C. R. Solis, C. R. Hughes, and D. M. DeLoach. 1993. A selfish strategy of social insect workers that promotes social cohesion. Nature 365: 639-641.

Rabenold, K. N. 1985. Cooperation in breeding by nonreproductive wrens: kinship, reciprocity and demography. Behavioral Ecology and Sociobiology 17:1-17.

Rabenold, P. P., K. N. Rabenold, W. H. Piper, J. Haydock, and S. W. Zack. 1990. Shared paternity revealed by genetic analysis in cooperatively breeding tropical wrens. Nature 348:538-540.

Ratti, O., M. Hovi, A. Lundberg, H. Tegelstrom, and R. V. Alatalo. 1995. Extra-pair paternity and male characteristics in the pied flycatcher. Behavioral Ecology and Sociobiology 37:419-425.

Reeve, H. K. 1991. Polistes. Pages 99-148 in K. Ross and R. Matthews, editors. The social biology of wasps. Cornell University Press, Ithaca, New York, NY.

Reeve, H. K., and L. Keller. 1995. Partitioning of reproduction in mother-daughter versus sibling associations: a test of optimal skew theory. American Naturalist 145:119-132.

Reeve, H. K., and P. Nonacs. 1992. Social contracts in wasp societies. Nature 359:823-825.

Reeve, H. K., and F. L. W. Ratnieks. 1993. Queen-queen conflicts in polygynous societies: mutual tolerance and reproductive skew. Pages 45-85 in L. Keller, editor. Queen number and sociality in insects. Oxford University Press, Oxford, UK.

Reeve, H. K., D. F. Westneat, W. A. Noon, P. W. Sherman, and C. F. Aquadro. 1990. DNA "fingerprinting" reveals high levels of inbreeding in colonies of the eusocial naked mole rat. Proceedings of the National Academy of Sciences (USA) 87:2496-2500.

Reeve, H. K., D. F. Westneat, and D.C. Queller. 1992. Estimating average within-group relatedness from DNA fingerprints. Molecular Ecology 1:223-232.

Reichert, S. E., and R. M. Roeloffs. 1993. Evidence for and consequences of inbreeding in the cooperative spiders. Pages 283-303 in N. Thornhill, editor. The natural history of inbreeding and outbreeding. University of Chicago Press, Chicago, Illinois, USA.

Ribble, D. O. 1991. The monogamous mating system of Peromyscus californicus as revealed by DNA fingerprinting. Behavioral Ecology and Sociobiology 29:161-166.

Richards, M. H. 1994. Social evolution in the genus Halictus: a phylogenetic approach. Insectes Sociaux 41:315-325.

Richards, M. H., L. Packer, and J. Seger. 1995. Unexpected patterns of parentage and relatedness in a primitively eusocial bee. Nature 373:239-241.

Rohwer, F. C., and S. Freeman. 1989. The distribution of conspecific nest parasitism in birds. Canadian Journal of Zoology 67:239-253.

Ross, K. G. 1990. Breeding systems and kin selection in social Hymenoptera. Pages 347-348 in G. K. Veeresh, B. Mallik, and C. A. Viraktamath, editors. Social insects and the environment. Oxford University Press, New Delhi, India.

Rowell, D. M., and L. Aviles. 1995. Sociality in a bark-dwelling huntsman spider from Australia, Delena cancerides Walckenaer (Areneae: Sparassidae). Insectes Sociaux 42:287-302.

Rowley, I., and E. M. Russell. 1990. Philandering - a mixed mating strategy in the splendid fairy wren Malurus splendens. Behavioral Ecology and Sociobiology 27:431-437

Schartl, M., C. Erbelding-Denk, S. Holter, I. Nanda, M. Schmid, J. H. Schroder, and J. T. Epplen. 1993. Reproductive failure of dominant males in the poeciliid fish Limia perugiae determined by DNA fingerprinting. Proceedings of the National Academy of Sciences (USA) 90:7064-7068.

Scheffrahn, W., N. Menard, D. Vallet, and B. Gaci. 1993. Ecology, demography, and population genetics of barbary macaques in Algeria. Primates 34:381-394.

Schwartz, J. M., G. F. McCracken, and G. M. Burghardt. 1989. Multiple paternity in wild populations of the garter snake, Thamnophilus sirtalis. Behavioral Ecology and Sociobiology 25:269-273.

Seppa, P., and P. Pamilo. 1995. Gene flow and population viscosity in Myrmica ants. Heredity 74:200-209.

Sera, W. E., and M. S. Gaines. 1994. The effect of relatedness on spacing behavior and fitness of female prairie voles. Ecology 75:1560-1566.

Sherman, P. W., T. D. Seeley, and H. K. Reeve. 1988. Parasites, pathogens, and polyandry in social Hymenoptera. American Naturalist 131:602-610.

Sibley, C. G., and J. E. Ahlquist. 1990. Phylogeny and classification of birds. Yale University Press, New Haven, Connecticut, USA.

Sibley, C. G., J. E. Ahlquist, and B. L. Monroe, Jr. 1988. A classification of the living birds of the world based on DNA-DNA hybridization studies. Auk 105:409-423.

Sillero-Zubiri, C., D. Gottelli, and D. W. Macdonald. 1996. Male philopatry, extra-pack copulations and inbreeding avoidance in Ethiopian wolves (Canis simensis). Behavioral Ecology and Sociobiology 38:331-340.

Stille, M., and B. Stille. 1992. Intra- and inter-nest variation in mitochondrial DNA in the polygynous ant Leptothorax acervorum (Hymenoptera; Formicidae). Insectes Sociaux 39:335-340.

Stille, M., B. Stille, and P. Douwes. 1991. Polygyny, relatedness and nestfounding in the polygynous myrmicine ant Leptothorax acervorum (Hymenoptera: Formicidae). Behavioral Ecology and Sociobiology 28:91-96.

Strassmann, J. E. 1993. Weak queen or social contract? Nature 363:502-503.

Strassmann, J. E., C. R. Hughes, D. C. Queller, S. Turillazzi, R. Cervo, S. K. Davis, and K. F. Goodnight. 1989. Genetic relatedness in primitively eusocial wasps. Nature 342:268-270.

Strassmann, J. E., C. R. Solis, C. R. Hughes, K. F. Goodnight, and D. C. Queller. 1997. Colony life history and demography of a swarm founding wasp. Behavioral Ecology and Sociobiology 40:71-78.

Stutchbury, B. J., and E. S. Morton. 1995. The effect of breeding synchrony on extra-pair mating systems in songbirds. Behaviour 132:675-690.

Stutchbury, B. J., J. M. Rhymer and E. S. Morton. 1994. Extra-pair paternity in hooded warblers. Behavioral Ecology 5:384-392.

Swatschek, I., D. Ristow, and M. Wink. 1994. Mate fidelity and parentage in cory's shearwater Calonectris diomedea - field studies and DNA fingerprinting. Molecular Ecology 3:259-262.

Temrin, H., and B. Sillen-Tullberg. 1994. The evolution of avian mating systems: a phylogenetic analysis of male and female polygamy and length of pair bond. Biological Journal of the Linnean Society 52:121-149.

Temrin, H., and B. Sillen-Tullberg. 1995. A phylogenetic analysis of the evolution of avian mating systems in relation to altricial and precocial development. Behavioral Ecology 6:296-307.

Tinbergen, N. 1953. Social behaviour in animals. In M. Abercrombie, editor. Methuen's monographs on biological subjects. Methuen, London, UK.

Travis, S. E., C. N. Slobodchikoff, and P. Keim. 1995a. Ecological and demographic effects on intraspecific variation in the social system of prairie dogs. Ecology 76:1794-1803.

Travis, S. E., C. N. Slobodchikoff, and P. Keim. 1995b. Social assemblages and mating relationships in prairie dogs: a DNA fingerprint analysis. Behavorial Ecology 7:95-100.

Trivers, R. L., and H. Hare. 1976. Haplodiploidy and the evolution of the social insects. Science 191:249-263.

Tsuchida, K. 1994. Genetic relatedness and the breeding structure of the Japanese paper wasp, Polistes jadwigae. Ethology Ecology and Evolution 6:237-242.

Vehrencamp, S. L. 1983. A model for the evolution of despotic versus egalitarian societies. Animal Behaviour 31: 667-682.

von Segesser, F., W. Scheffrahn, and R. D. Martin. 1995. Parentage analysis within a semi-free-ranging group of Barbary macaques, Macaca sylvanus. Molecular Ecology 5: 115-120.

Wagner, R. H., M. D. Schug, and E. S. Morton. 1996. Condition-dependent control of paternity by female purple martins: implications for coloniality. Behavioral Ecology Sociobiology 38:379-389.

Wagner, R. H., M. D. Schug, and E. S. Morton. In press. Sexual selection and colony formation: relative control of extra-pair fertilizations by female purple martins. Behavioral Ecology and Sociobiology.

Warkentin, I. G., A. D. Curzon, R. E. Carter, J. H. Wetton, P. C. James, L. W. Oliphants, and D. T. Parkin. 1994. No evidence for extrapair fertilizations in the merlin revealed by DNA fingerprinting. Molecular Ecology 3:229-234.

Watt, E. M., and M. B. Fenton. 1995. DNA fingerprinting provides evidence of discriminative suckling and non-random mating in little brown bats Myotis lucifugus. Molecular Ecology 4:261-264.

Weatherhead, P. J., and P. T. Boag. 1995. Pair and extra-pair mating success relative to male quality in red-winged blackbirds. Behavioral Ecology and Sociobiology 37:81-91.

Westneat, D. 1987a. Extra-pair fertilizations in a predominantly monogamous birds: genetic evidence. Animal Behavior 35:877-886.

-----. 1987b. Extra-pair copulations in a predominantly monogamous bird: observations of behaviour. Animal Behavior 35:865-876.

-----. 1988. Male parental care and extrapair copulations in the indigo bunting. Auk 105:149-160.

-----. 1994. To guard mates or go forage: conflicting demands affect the paternity of male Red-Winged Blackbirds. American Naturalist 144:343-354.

Westneat, D. F., P. W. Sherman, and M. L. Morton. 1990. The ecology and evolution of extra-pair copulations in birds. Volume 7. Current ornithology. Plenum, New York, New York, USA.

Wilkinson, G. S. 1984, Reciprocal food sharing in the vampire bat. Nature 308:181-184.

-----. 1985a. The social organization of the common vampire bat. I. Pattern and cause of association. Behavioral Ecology and Sociobiology 17:111-121.

-----. 1985b. The social organization of the common vampire bat. II. Mating system, genetic structure, and relatedness. Behavioral Ecology and Sociobiology 17:123-134.

Yezerinac, S. M., P. J. Weatherhead, and P. T. Boag. 1995. Extra-pair paternity and the opportunity for sexual selection in a socially monogamous bird (Dendroica petechia). Behavioral Ecology and Sociobiology 37:179-188.

Yezerinac, S. M., P. J. Weatherhead, and P. T. Boag. 1996. Cuckoldry and lack of parentage dependent paternal care in yellow warblers: a cost benefit approach. Animal Behaviour 52:821-132.
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