397:, and in mongooses), and one genus of primates (Callitrichidae). Cooperative breeding in mammals is not limited to these stated lineages, rather they are significant evolutionary events that provide the framework for understanding the origins and evolutionary pressures of cooperative breeding. All of these evolutionary transitions have occurred in lineages that had a socially monogamous or solitary breeding system, suggesting that strong kinship ties are an essential factor in the evolutionary history of cooperative breeding. Additionally, polytocy, or the birth of multiple offspring per birthing episode, is a highly correlated evolutionary determinant of cooperative breeding in mammals. These two factors, social monogamy and polytocy, are not evolutionary associated, suggesting that they are independent mechanisms leading to the evolution of cooperative breeding in mammals. The global distribution of mammals with cooperative breeding systems is widespread across various climatic regions, but evidence shows that the initial transitions to cooperative breeding are associated to species in regions of high aridity.
336:), in which studies found that the offspring's cell-mediated immune response was positively correlated with increase in the number of helpers at the nest. Studies on cooperative breeding in birds have also shown that high levels of cooperative breeding are strongly associated with low annual adult mortality and small clutch sizes, though it remains unclear whether cooperative breeding is a cause or consequence. It was originally suggested that cooperative breeding developed among bird species with low mortality rates as a consequence of βovercrowdingβ and thus fewer opportunities to claim territory and breed. However, many observers today believe cooperative breeding arose because of the need for helpers to rear young in the extremely infertile and unpredictable environments of
136:. Mutualism is a form of symbiosis that is beneficial to both involved organisms. Mutualism has many forms and can occur when the benefits are immediate or deferred, when individuals exchange beneficial behaviors in turn, or when a group of individuals contribute to a common good, where it may be advantageous for all group members to help raise young. When a group raises young together, it may be advantageous because it maintains or increases the size of the group. The greatest amount of research has been invested in reciprocal exchanges of beneficial behavior through the
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need for helpers to maintain the high reproductive costs, thus leading to cooperative breeding. Lukas et al. suggests polytocy may have encouraged the evolution of cooperative breeding. Their proposed model suggests the transition from monotocy to polytocy is favorable. Additionally, they found the transition from polytocy without cooperative breeding to polytocy with cooperative breeding is highly favorable. This suggests cooperative breeding evolved from noncooperative breeding monotocy to cooperative breeding polytocy.
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is the delegation of offspring holding, which allows the mother to forage without the added costs of holding her offspring. Additionally, in primate species with cooperative breeding systems, females have shorter interbirth intervals. Female grey mouse lemurs (Microcebus murinus) form social groups and cooperatively breed with closely related female kin. The females benefit from sharing limited nesting spaces and increased nest defense but do not exhibit food provisioning behaviors as they are solitary foragers.
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225:) have exhibited male territory defense strategies, where male helpers will fend off intruding males to prevent such intruders from mating with subordinates or dominant females. Additionally, subordinate female pregnant helpers are sometimes exiled from the group by a dominant female. This eviction causes the subordinate female to have an abortion, which frees up resources such as lactation and energy that can be used to help the dominant female and her pups.
490:. Cooperative breeding in humans is theorized as the optimal solution to high energetic costs of survival due to nature of human diet, which involved high-quality foods often in need of processing and cooking. Additionally, food provisioning in cooperate breeding societies may explain the relatively short period of weaning in humans, typically two to three years, when compared to non-human apes who wean their offspring for upwards of six years.
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provides passive benefits for helpers in addition to inclusive fitness. By group augmenting, each individual member reduces their chances of becoming a victim of predation. Additionally, an increase in members reduces each helper's duration as a sentinel (standing upon a high surface to survey for predators) or babysitting (guarding the offspring and den). The reduction in these guarding behaviors enables helpers to forage for longer periods.
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exponential scale depending upon the duration of the activity. Other activities, such as sentinel behavior and bipedal surveillance, cause helpers to have reduced foraging intervals inhibiting their weight gains. The reduced foraging behavior and increased weight loss reduces their chance to breed successfully, but increases their inclusive fitness by increasing the survival of related offspring.
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previously thought that a meerkat's contribution to a pup's diet depended on the degree of relatedness, it has been found that helpers vary in the number of food items they give to pups. This variation in food offering is due to variation in foraging success, sex, and age. Research has additionally found that the level of help is not correlated to the kinship of the litters they are rearing.
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reproductive suppression at the benefit of a single, dominant breeding mother. Instead, cooperative breeding is highly prevalent among grandparents, and juveniles, who are generally not competing for mating opportunities. This intergenerational flow of resources supports the theory of mutualism as an evolutionary pathway to cooperative breeding in humans.
61:
direct fitness is defined as the amount of fitness gained through producing offspring. Indirect fitness is defined as the amount of fitness gained through aiding the offspring of related individuals, that is, relatives are able to indirectly pass on their genes through increasing the fitness of related offspring. This is also called kin selection.
208:) juvenile male helpers contribute far less than females. This is due to a difference in the age of sexual maturity. Female banded mongooses reach sexual maturity at one year of age, but males reach sexual maturity at two years of age. The difference in age causes the prolonged energy allocation to be detrimental to a specific sex.
49:) and helpers that are the adult offspring of some but not all of the breeders in the group, to groups in which helpers sometimes achieve co-breeding status by producing their own offspring as part of the group's brood. Cooperative breeding occurs across taxonomic groups including birds, mammals, fish, and insects.
501:, and instead Portmann proposes they are "secondarily altricial" at birth due to the underdevelopment of neurological and cognitive capabilities. Therefore, human offspring are highly dependent on caregiver investment, a necessity that serves as the precursor for theories on the development of pair-bonding,
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believes that cooperative breeding is an ancestral trait in humans, a controversial proposition. In most non-human primates, the reproductive success and survival of offspring is highly dependent to the mother's ability to produce food resources. Therefore, one component of cooperative breeding
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may reduce helping behaviors until sexual maturity is reached. Similarly, if there is a lack of food due to environmental conditions, such as reduced rainfall, the degree of helper input may be reduced greatly within juveniles. Adults may maintain their full activity because they are sexually mature.
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Dominant males and females exhibit suppressive behaviors towards subordinates to maintain their breeding status. These suppressive acts are dependent upon the sex ratio of helpers. Therefore, the costs will be altered depending upon the helpers. For example, if there are more male helpers as compared
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Environmental conditions govern whether offspring disperse from their natal group or remain as helpers. Food or territory availability can encourage individuals to disperse and establish new breeding territories, but unfavorable conditions promote offspring to remain at the natal territory and become
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Lukas et al. proposed an evolutionary model for cooperative breeding, which linked the coevolution of polytocy, production of multiple offspring, and monotocy, production of single offspring, with the evolution of cooperative breeding. The model is based on the evolution of larger litters forcing the
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Helpers may also benefit from group interactions, such as huddling for thermodynamic benefits. These interactions provide necessary elements to survive. They may also benefit from the increased group interaction on the level of cognitive concern for one another increasing their overall life span and
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defense, offspring guarding and an increased cost of growth. Benefits for helpers include a reduced chance of predation, increased foraging time, territory inheritance, increased environmental conditions and an inclusive fitness. Inclusive fitness is the sum of all direct and indirect fitness, where
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presents a second hypothesis towards the evolution of cooperative breeding. This hypothesis suggests that increasing the size of the group through the addition of helpers aids in individual survival and may increase the helper's future breeding success. Group augmentation is favored if the grouping
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Helpers primarily benefit from an inclusive fitness. Helpers maintain an inclusive fitness while aiding related breeders and offspring. This type of kinship may lead to inheritance of quality foraging and breeding territories, which will increase the future fitness of helpers. Additional, helpers
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of cooperative breeding. The concept behind cooperative breeding is the forfeiting of an individual's reproductive fitness to aid the reproductive success of others. This concept is hard to understand and the evolution of cooperative breeding is important, but difficult to explain. Most hypotheses
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births; altricial is the production of young which are dependent upon adult aid to survive. This enables the breeding female to retain energy to be used within a new breeding attempt. Overall, the addition of helpers to a breeding pair encourages multiple reproductions per year, and increases the
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Cooperative breeding reduces the costs of many maternal investments for breeding members. Helpers aid the breeding females with provisioning, lactation stress, guarding of offspring and prenatal investment. Increasing the number of helpers enables a breeding female or male to maintain a healthier
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is the evolutionary strategy of aiding the reproductive success of related organisms, even at a cost to the own individual's direct fitness. Hamilton's rule (rBβC>0) explains that kin selection will exist if the genetic relatedness (r) of the aided recipient to the aiding individual, times the
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The cost to helpers varies depending upon presence or absence of related offspring. The presence of offspring has been found to increase the helper's cost by the helper contributing to guard behaviors. Guarding behaviors, such as babysitting, can cause individuals to experience weight loss on an
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A final factor influencing cooperative breeding is sexual dispersal. Sexual dispersal is the movement of one sex, male or female, from the natal territory to establish new breeding grounds. This is highly regulated by the reproductive costs in producing a male versus a female offspring. Maternal
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Male breeders can benefit directly from reproducing with subordinate females and aiding in raising the young. This allows the male to obtain a βrepayment investmentβ within these subordinate offspring. These offspring have a higher chance to become helpers once sexual maturity is reached. Thus,
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Female helpers can aid in lactation, but all helpers, male or female, can aid in food provisioning. Helper food provisioning reduces the need for the dominant breeding pair to return to the den, thus allowing them to forage for longer periods. The dominant female and male will adjust their care
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were produced at a higher rate under unfavorable conditions. Males were found to remain at the natal territory and become helpers. Thus, if environmental conditions favor the dispersal of a specific sex it is considered the dispersal sex. If environmental conditions are unfavorable females may
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pair that reserves the right to mate and will usually kill any young that is not their own. While the alpha female is away from the group, females that have never reproduced lactate and hunt in order to feed the pups, as well as watch, protect, and defend them from predators. Although it was
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Breeder costs consist of prenatal care, postnatal care and maintenance of breeding status. Prenatal care is the amount of maternal investment during fetus gestation and postnatal care is the investment following birth. Examples of prenatal care are fetal, placentae, uterus and mammary tissue
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Human mothers tend to have overlapping, dependent offspring due to shorter interbirth intervals, high fertility rates, and low infant mortality rates, thus imposing high energetic costs. Unlike other species with cooperative breeding systems, human female "helpers" do not incur the cost of
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Across all mammalian species, less than 1% exhibit cooperative breeding strategies. Phylogenetic analysis shows evidence of fourteen discrete evolutionary transitions to cooperative breeding within the class
Mammalia. These lineages are nine genera of rodents
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of the group is held within a select few breeding members and helpers have little to no reproductive fitness. With this system, breeders gain an increased reproductive fitness, while helpers gain an increased inclusive fitness.
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Cooperative breeding entails one or more individuals, usually females, acting as "helpers" to one or a few dominant female breeders, usually helpers' kin. This sociosexual system is rare in primates, so far demonstrated among
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Helpers contribute depending upon the cost. The act of helping requires an allocation of energy towards actually performing the behavior. Prolonged allocation of energy may greatly impact a helper's growth. In banded mongoose
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especially in food acquisition. Additionally, pro-social behaviors in cooperative breeding in humans had a by-product effect of enhancing cognitive capabilities, especially in social tasks involving coordination.
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to females, then the dominant male will suppress subordinate males and experience a higher cost. The opposite is true for females. Breeders will even suppress subordinates from mating with other subordinates.
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investment within female offspring may be considerably higher than male offspring for one species, or vice versa for another. During unfavorable conditions the cheaper sex will be produced at higher ratios.
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and suppression of subordinate mating. Breeders receive benefits as reductions in offspring care and territory maintenance. Their primary benefit is an increased reproductive rate and survival.
41:: offspring receive care not only from their parents, but also from additional group members, often called helpers. Cooperative breeding encompasses a wide variety of group structures, from a
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Additionally, the costs of being a helper can be more detrimental to one sex. For example, territorial defense costs are generally male dependent and lactation is female dependent. Meerkats (
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Nichols, H. J.; Amos, W.; Cant; Bell, M. B. V.; Hodge, S. J. (2010). "Top males gain high reproductive success by guarding more successful females in a cooperatively breeding mongoose".
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Clutton-Brock, T.H.; Brotherton, P.N.M.; O'Riain, M.J.; Griffin, A.S.; Gaynor, D.; Kansky, R.; Sharpe, L.; McIlrath, G.M. (2000). "Contributions to cooperative rearing in meerkats".
1989:
Valencia, Juliana; Elena Solis; Gabrielle Sorci; Carlos de la Cruz (2006). "Positive correlation between helpers at nest and nestling immune response in cooperative breeding bird".
1796:
Sorato, E.; Gullett, P. R.; Griffith, S. C.; Russell, A. F. (2012). "Effects of predation risk on foraging behaviour and group size: adaptations in a social cooperative species".
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helpers to obtain an inclusive fitness. Additionally, remaining at the natal territory enables offspring to possibly inherit the breeding role and/or territory of their parents.
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Mitchell, J. S.; Jutzeler, E.; Heg, D.; Taborsky, M. (2009). "Gender
Differences in the Costs that Subordinate Group Members Impose on Dominant Males in a Cooperative Breeder".
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Finally, helpers may derive inclusive fitness benefits from influencing the extra-pair behaviour of their parents. For example, by preventing their mothers from engaging in
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Rarely, a female helper or breeder will defend the territory while males are present. This suggests specific helping costs, such as territory defense, is rooted to one sex.
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paying into their care will increase the dominant male's overall fitness in the future. This act ensures the dominant male subordinate helpers for future reproduction.
108:) has been found to have high rates of kin selection. Helpers are predominantly found aiding closely related broods over nonrelated broods. Additional species such as
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Canestrari, D.; Vila, M.; Marcos, J. M.; Baglione, V. (2012). "Cooperatively breeding carrion crows adjust offspring sex ratio according to group composition".
278:, they can help their biological fathers protect their paternity and so increase their relatedness to future members of the cooperatively breeding group.
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Eberle, Manfred; Kappeler, Peter M. (2006-08-01). "Family insurance: kin selection and cooperative breeding in a solitary primate (Microcebus murinus)".
2443:
Tardif, Suzette D. (1994). "Relative energetic cost of infant care in small-bodied neotropical primates and its relation to infant-care patterns".
634:
Haydock, J.; Koenig, W. D.; Stanback, M. T. (2001-06-01). "Shared parentage and incest avoidance in the cooperatively breeding acorn woodpecker".
140:. In this model, two partners can either cooperate and exchange beneficial behavior or they can defect and refuse to help the other individual.
1286:
Marino, J.; Sillero-Zubiri, C.; Johnson, P. J.; Macdonald, D. W. (2012). "Ecological bases of philopatry and cooperation in
Ethiopian wolves".
469:. Cooperative breeding requires "repression" of helpers' reproduction, by pheromones emitted by a breeder, by coercion, or by self-restraint.
2607:
156:
A second factor affecting the sexual dispersal is the difference in ability of each sex to establish a new breeding territory. Carrion crow (
818:
Wong, Marian; Balshine, Sigal (2011-05-01). "The evolution of cooperative breeding in the
African cichlid fish, Neolamprologus pulcher".
869:
Bourke, Andrew F. G.; Heinze, Jurgen (1994-09-30). "The
Ecology of Communal Breeding: The Case of Multiple-Queen Leptothoracine Ants".
2073:
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Santema, P.; Clutton-brock, T. (2013). "Meerkat helpers increase sentinel behaviour and bipedal vigilance in the presence of pups".
2395:"The physiology of cooperative breeding in a rare social canid; sex, suppression and pseudopregnancy in female Ethiopian wolves"
1585:
Hodge, S. J. (2007). "Counting the costs: the evolution of male-biased care in the cooperatively breeding banded mongoose".
137:
1620:
Pauw, A (2000). "Parental care in a polygynous group of bat-eared foxes, Otocyon megalotis ( Carnivora : Canidae )".
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The presence of helpers allows the breeding female to reduce her prenatal investment in the offspring, which may lead to
171:
produce the philopatric sex, therefore generating more helpers and increasing the occurrence of cooperative breeding.
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Nichols, H. J.; et al. (2012). "Food availability shapes patterns of helping effort in a cooperative mongoose".
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become reproductively active at one year of age and can have up to four litters per year. However, usually it is the
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Approximately eight percent of bird species are known to regularly engage in cooperative breeding, mainly among the
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2505:
Kramer, Karen L. (2010-10-21). "Cooperative
Breeding and its Significance to the Demographic Success of Humans".
1372:
Sharp, S. P.; English, S.; Clutton-Brock, T. H. (2012). "Maternal investment during pregnancy in wild meerkats".
710:
2353:"Social Behaviour and Cooperative Breeding in Arctic Foxes, Alopex lagopus (L.), in a Semi-natural Environment"
1832:
101:
992:
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1081:"Individual contributions to territory defence in a cooperative breeder: weighing up the benefits and costs"
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with helpers that are offspring from a previous season, to groups with multiple breeding males and females (
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Dunsworth, Holly M.; Warrener, Anna G.; Deacon, Terrence; Ellison, Peter T.; Pontzer, Herman (2012-09-18).
993:"Reproductive skew, costs, and benefits of cooperative breeding in female wood mice (Apodemus sylvaticus)"
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species also promoted other pro-social behaviors such as social learning, increased social tolerance, and
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Today, there is growing support for the theory that cooperative breeding evolved by means of some form of
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benefit to the aid recipient (B) is greater than the cost to the aiding individual (C). For example, the
1232:
Clutton-Brock, Tim (2002). "Breeding
Together: Kin Selection and Mutualism in Cooperative Vertebrates".
510:
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aim to determine the reason helpers selectively reduce their fitness and take on an alloparental role.
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1977:
1027:"Kin selection, not group augmentation, predicts helping in an obligate cooperatively breeding bird"
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Kramer, Karen L. (2014). "Why What
Juveniles Do Matters in the Evolution of Cooperative Breeding".
2320:"Direct fitness benefits of delayed dispersal in the cooperatively breeding red wolf (Canis rufus)"
914:
Nicholas B. Davies, John R. Krebs, S. A. W. An
Introduction to Behavioural Ecology.pdf. 522 (2012).
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Cooperative breeding increases the rate of reproduction in females and decreases the litter size.
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Cockburn, Andrew (1998-01-01). "Evolution of
Helping Behavior in Cooperatively Breeding Birds".
695:"Direct benefits and the evolution of female-biased cooperative breeding in seychelles warblers"
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have been found to establish successful breeding territories at a higher rate than males. Male
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The benefits of cooperative breeding in birds have been well-documented. One example is the
162:) were found to produce more female offspring in favorable environmental conditions. Female
2804:
316:
203:
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2693:
2371:
2109:
1945:
1930:"Environmental Uncertainty and the Global Biogeography of Cooperative Breeding in Birds"
1878:"Mother guarding: how offspring may influence the extra-pair behaviour of their parents"
1458:
1245:
1186:
Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences
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882:
647:
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Direct expression of cooperative breeding includes facultative parental care, including
2720:
2677:
2590:(eds.), "Mind the Gap: Cooperative Breeding and the Evolution of Our Unique Features",
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2221:"Individual Contributions to babysitting in a cooperative mongoose, Suricata suricatta"
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Browning, L. E.; Patrick, S. C.; Rollins, L. A; Griffith, S. C.; Russell, A F. (2012).
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development. Postnatal examples are lactation, food provisions and guarding behavior.
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1182:"The evolution of cooperative breeding in birds: kinship, dispersal and life history"
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have shown that kin selection is a dominant driving force for cooperative breeding.
2010:
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of all sexually mature adults to be skewed towards one mating pair. This means the
46:
17:
2413:
2026:"Cooperative breeding in birds: a comparative test of the life history hypothesis"
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1668:
1598:
1504:
1341:
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486:, and extended post-menopausal lifespan in females, which forms the basis of the
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input, or food provisioning, depending on the degree of activity of the helpers.
1253:
871:
Philosophical Transactions of the Royal Society of London B: Biological Sciences
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2002:
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experience an increased chance of being helped if they were once a helper.
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847:
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671:
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505:, and cooperative breeding. The evolution of cooperative breeding in early
2066:
Global Runoff: Continental Comparisons of Annual Flows and Peak Discharges
1697:"First evidence for heritable variation in cooperative breeding behaviour"
1564:
1529:
Brotherton, P. N. M.; Riain, J. M. O.; Manser, M.; Skinner, J. D. (2013).
493:
Human offspring do not fall neatly into the dichotomous categorization of
693:
Richardson, David S.; Burke, Terry; Komdeur, Jan; Dunn, P. (2002-11-01).
466:
320:
2306:
Cooperative breeding, reproductive suppression, and body mass in canids.
2117:
593:
Dickinson, Janis L.; Koenig, Walter D.; Pitelka, Frank A. (1996-06-20).
413:
220:
769:
2745:"Allomaternal care, life history and brain size evolution in mammals"
2586:
van Schaik, Carel P.; Burkart, Judith M. (2010), Kappeler, Peter M.;
546:"Life histories and the evolution of cooperative breeding in mammals"
1851:
1531:"Costs of Cooperative Behaviour in Suricatas (Suricata Suricatta)"
1130:"The evolution of cooperative breeding through group augmentation"
595:"Fitness consequences of helping behavior in the western bluebird"
430:
404:
2094:"Climate and the distribution of cooperative breeding in mammals"
783:
Jennions, M (1994-01-01). "Cooperative breeding in mammals".
409:
An older female watches over pups while alpha female is away.
242:
physique, higher fitness, increased lifespan and brood size.
1746:"When should cuckolded males care for extra-pair offspring?"
1695:
Charmantier, A.; Keyser, A. J.; Promislow, D. E. L. (2007).
2304:
Moehlman, Patricia D., and H. E. R. I. B. E. R. T. Hofer. "
711:
10.1554/0014-3820(2002)056[2313:DBATEO]2.0.CO;2
2164:"Cooperative breeding and monogamy in mammalian societies"
1978:"Prevalence of different modes of parental care in birds"
1227:
1225:
2168:
Proceedings of the Royal Society B: Biological Sciences
1882:
Proceedings of the Royal Society B: Biological Sciences
1134:
Proceedings of the Royal Society B: Biological Sciences
1031:
Proceedings of the Royal Society B: Biological Sciences
550:
Proceedings of the Royal Society B: Biological Sciences
1079:
Mares, R.; Young, A. J.; Clutton-Brock, T. H. (2012).
325:
cooperative and cannot fledge young without helpers.
429:Cooperative breeding has been described in several
307:. Only a small fraction of these, for instance the
88:Many hypotheses have been presented to explain the
2024:Arnold, Kathryn E.; Ian P. F. Owens (7 May 1998).
1833:"How Our Ancestors Broke through the Gray Ceiling"
991:Gerlach, Gabriele; Bartmann, Susann (2002-05-01).
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1524:
1522:
2594:, Springer Berlin Heidelberg, pp. 477β496,
2162:Lukas, Dieter; Clutton-Brock, Tim (2012-06-07).
2682:Proceedings of the National Academy of Sciences
1323:
1321:
1319:
1317:
64:For the breeding pair, costs include increased
2351:Kullberg, Cecilia; AngerbjΓΆrn, Anders (1992).
1923:
1921:
1690:
1688:
1686:
2678:"Metabolic hypothesis for human altriciality"
8:
1928:Jetz, Walter; Rubinstein, Dustin R. (2011).
1871:
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2743:Isler, Karin; van Schaik, Carel P. (2012).
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984:
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980:
929:"Evolutionary explanations for cooperation"
2092:Lukas, Dieter; Clutton-Brock, Tim (2017).
1486:
1484:
2719:
2701:
2393:van Kesteren, Freya; et al. (2013).
2335:
2318:Sparkman, Amanda M.; et al. (2010).
2244:
2195:
2133:
2049:
1953:
1901:
1791:
1789:
1769:
1720:
1554:
1281:
1279:
1205:
1153:
1104:
1050:
952:
610:
569:
1580:
1578:
1576:
1574:
1367:
1365:
1363:
1361:
1359:
1074:
1072:
1070:
910:
908:
750:Annual Review of Ecology and Systematics
1405:
1403:
527:
344:under the rare favourable conditions.
2620:
2618:
2581:
2579:
2500:
2498:
2496:
2494:
2492:
2490:
2157:
2155:
2153:
2087:
2085:
2083:
2081:
1876:Welbergen, J. A.; Quadar, S. (2006).
1831:Isler, K.; Van Schaik, C. P. (2012).
922:
920:
544:Lukas, D.; Clutton-Brock, T. (2012).
7:
2519:10.1146/annurev.anthro.012809.105054
2064:See McMahon T.A. and Finlayson, B.;
1128:Kokko, H.; Johnstone, R. A. (2001).
2542:Behavioral Ecology and Sociobiology
1991:Behavioral Ecology and Sociobiology
1412:Behavioral Ecology and Sociobiology
1288:Behavioral Ecology and Sociobiology
2380:10.1111/j.1439-0310.1992.tb00843.x
1744:Liedtke, J.; Fromhage, L. (2012).
25:
785:Trends in Ecology & Evolution
254:rate of successful reproduction.
2225:Proceedings. Biological Sciences
2030:Proceedings: Biological Sciences
1750:Proceedings: Biological Sciences
1701:Proceedings: Biological Sciences
1467:10.1111/j.1439-0310.2009.01705.x
1085:Proceedings: Biological Sciences
832:10.1111/j.1469-185X.2010.00158.x
762:10.1146/annurev.ecolsys.29.1.141
656:10.1046/j.1365-294X.2001.01286.x
71:Cooperative breeding causes the
2445:American Journal of Primatology
1634:10.1080/15627020.2000.11407200
1:
2507:Annual Review of Anthropology
2414:10.1016/j.physbeh.2013.08.016
1810:10.1016/j.anbehav.2012.07.003
1669:10.1016/j.anbehav.2010.06.025
1599:10.1016/j.anbehav.2006.09.024
1505:10.1016/j.anbehav.2012.12.029
1342:10.1016/j.anbehav.2012.03.005
385:), four genera in Carnivora (
2764:10.1016/j.jhevol.2012.03.009
2600:10.1007/978-3-642-02725-3_22
797:10.1016/0169-5347(94)90202-x
52:Costs for helpers include a
2219:Clutton-Brock, T.H (2000).
1254:10.1126/science.296.5565.69
138:iterated prisoner's dilemma
2821:
2752:Journal of Human Evolution
2098:Royal Society Open Science
2639:10.1007/s12110-013-9189-5
2554:10.1007/s00265-006-0203-3
2402:Physiology & Behavior
2003:10.1007/s00265-006-0179-z
1955:10.1016/j.cub.2010.11.075
1424:10.1007/s00265-012-1375-7
1386:10.1007/s10682-012-9615-x
1300:10.1007/s00265-012-1348-x
1180:Hatchwell, B. J. (2009).
954:10.1016/j.cub.2007.06.004
319:, are however absolutely
459:Neotropical callitricids
313:Australo-Papuan babblers
144:Environmental conditions
102:chestnut-crowned babbler
2703:10.1073/pnas.1205282109
1009:10.1093/beheco/13.3.408
2457:10.1002/ajp.1350340205
2284:10.1006/anbe.2000.1631
2237:10.1098/rspb.2000.1000
2180:10.1098/rspb.2011.2468
2042:10.1098/rspb.1998.0355
1976:See Cockburn, Andrew;
1894:10.1098/rspb.2006.3591
1762:10.1098/rspb.2011.2691
1713:10.1098/rspb.2007.0012
1547:10.1098/rspb.1998.0281
1198:10.1098/rstb.2009.0109
1146:10.1098/rspb.2000.1349
1097:10.1098/rspb.2012.1071
1043:10.1098/rspb.2012.1080
891:10.1098/rstb.1994.0115
612:10.1093/beheco/7.2.168
562:10.1098/rspb.2012.1433
488:Grandmother Hypothesis
410:
111:Neolamprologus pulcher
2337:10.1093/beheco/arq194
927:West, Stuart (2007).
511:shared intentionality
408:
309:Australian mudnesters
106:Pomatostomus ruficeps
56:reduction, increased
1840:Current Anthropology
1374:Evolutionary Ecology
77:reproductive fitness
73:reproductive success
31:Cooperative breeding
2694:2012PNAS..10915212D
2688:(38): 15212β15216.
2372:1992Ethol..90..321K
2174:(1736): 2151β2156.
2118:10.1098/rsos.160897
2110:2017RSOS....460897L
1946:2011CBio...21...72J
1888:(1599): 2363β2368.
1459:2009Ethol.115.1162M
1246:2002Sci...296...69C
945:2007CBio...17.R661W
883:1994RSPTB.345..359B
648:2001MolEc..10.1515H
330:azure-winged magpie
282:Biological examples
18:Collective breeding
2324:Behavioral Ecology
997:Behavioral Ecology
820:Biological Reviews
599:Behavioral Ecology
471:Sarah Blaffer Hrdy
433:species including
411:
342:sub-Saharan Africa
276:extra-pair matings
222:Suricata suricatta
118:Group augmentation
2609:978-3-642-02724-6
2036:(1398): 739β745.
1756:(1739): 2877β82.
1707:(1619): 1757β61.
1541:(1392): 185β190.
1453:(12): 1162β1174.
1192:(1533): 3217β27.
1140:(1463): 187β196.
1091:(1744): 3989β95.
939:(16): R661βR672.
877:(1314): 359β372.
705:(11): 2313β2321.
636:Molecular Ecology
556:(1744): 4065β70.
39:alloparental care
37:characterized by
16:(Redirected from
2812:
2784:
2783:
2749:
2740:
2734:
2733:
2723:
2705:
2673:
2667:
2666:
2622:
2613:
2612:
2583:
2574:
2573:
2537:
2531:
2530:
2502:
2485:
2484:
2440:
2434:
2433:
2399:
2390:
2384:
2383:
2357:
2348:
2342:
2341:
2339:
2315:
2309:
2302:
2296:
2295:
2271:Animal Behaviour
2265:
2259:
2258:
2248:
2216:
2210:
2209:
2199:
2159:
2148:
2147:
2137:
2089:
2076:
2062:
2056:
2055:
2053:
2021:
2015:
2014:
1986:
1980:
1974:
1968:
1967:
1957:
1925:
1916:
1915:
1905:
1873:
1864:
1863:
1837:
1828:
1822:
1821:
1798:Animal Behaviour
1793:
1784:
1783:
1773:
1741:
1735:
1734:
1724:
1692:
1681:
1680:
1657:Animal Behaviour
1652:
1646:
1645:
1617:
1611:
1610:
1587:Animal Behaviour
1582:
1569:
1568:
1558:
1526:
1517:
1516:
1493:Animal Behaviour
1488:
1479:
1478:
1442:
1436:
1435:
1418:(9): 1225β1235.
1407:
1398:
1397:
1380:(5): 1033β1044.
1369:
1354:
1353:
1336:(6): 1377β1385.
1330:Animal Behaviour
1325:
1312:
1311:
1294:(7): 1005β1015.
1283:
1274:
1273:
1229:
1220:
1219:
1209:
1177:
1168:
1167:
1157:
1125:
1119:
1118:
1108:
1076:
1065:
1064:
1054:
1037:(1743): 3861β9.
1022:
1013:
1012:
988:
975:
974:
956:
924:
915:
912:
903:
902:
866:
860:
859:
815:
809:
808:
780:
774:
773:
745:
739:
738:
690:
684:
683:
642:(6): 1515β1525.
631:
625:
624:
614:
590:
584:
583:
573:
541:
443:Ethiopian wolves
334:Cyanopica cyanus
317:ground hornbills
21:
2820:
2819:
2815:
2814:
2813:
2811:
2810:
2809:
2790:
2789:
2788:
2787:
2747:
2742:
2741:
2737:
2675:
2674:
2670:
2624:
2623:
2616:
2610:
2585:
2584:
2577:
2539:
2538:
2534:
2504:
2503:
2488:
2442:
2441:
2437:
2397:
2392:
2391:
2387:
2355:
2350:
2349:
2345:
2317:
2316:
2312:
2303:
2299:
2267:
2266:
2262:
2231:(1440): 301β5.
2218:
2217:
2213:
2161:
2160:
2151:
2091:
2090:
2079:
2063:
2059:
2023:
2022:
2018:
1988:
1987:
1983:
1975:
1971:
1934:Current Biology
1927:
1926:
1919:
1875:
1874:
1867:
1835:
1830:
1829:
1825:
1795:
1794:
1787:
1743:
1742:
1738:
1694:
1693:
1684:
1654:
1653:
1649:
1622:African Zoology
1619:
1618:
1614:
1584:
1583:
1572:
1528:
1527:
1520:
1490:
1489:
1482:
1444:
1443:
1439:
1409:
1408:
1401:
1371:
1370:
1357:
1327:
1326:
1315:
1285:
1284:
1277:
1240:(5565): 69β72.
1231:
1230:
1223:
1179:
1178:
1171:
1127:
1126:
1122:
1078:
1077:
1068:
1024:
1023:
1016:
990:
989:
978:
933:Current Biology
926:
925:
918:
913:
906:
868:
867:
863:
817:
816:
812:
782:
781:
777:
747:
746:
742:
692:
691:
687:
633:
632:
628:
592:
591:
587:
543:
542:
529:
524:
480:
454:
427:
403:
350:
289:
284:
264:
239:
234:
195:
182:
177:
146:
86:
28:
23:
22:
15:
12:
11:
5:
2818:
2816:
2808:
2807:
2802:
2800:Social systems
2792:
2791:
2786:
2785:
2735:
2668:
2614:
2608:
2575:
2548:(4): 582β588.
2532:
2513:(1): 417β436.
2486:
2451:(2): 133β143.
2435:
2385:
2366:(4): 321β335.
2343:
2330:(1): 199β205.
2310:
2297:
2278:(4): 705β710.
2260:
2211:
2149:
2077:
2057:
2016:
1997:(3): 399β404.
1981:
1969:
1917:
1865:
1852:10.1086/667623
1823:
1804:(4): 823β834.
1785:
1736:
1682:
1663:(4): 649β657.
1647:
1612:
1593:(4): 911β919.
1570:
1518:
1499:(3): 655β661.
1480:
1437:
1399:
1355:
1313:
1275:
1221:
1169:
1120:
1066:
1014:
1003:(3): 408β418.
976:
916:
904:
861:
826:(2): 511β530.
810:
775:
740:
685:
626:
605:(2): 168β177.
585:
526:
525:
523:
520:
479:
476:
453:
450:
426:
423:
402:
399:
359:Heterocephalus
349:
346:
288:
285:
283:
280:
263:
260:
238:
235:
233:
230:
211:Male juvenile
194:
191:
181:
178:
176:
173:
145:
142:
85:
82:
26:
24:
14:
13:
10:
9:
6:
4:
3:
2:
2817:
2806:
2803:
2801:
2798:
2797:
2795:
2781:
2777:
2773:
2769:
2765:
2761:
2757:
2753:
2746:
2739:
2736:
2731:
2727:
2722:
2717:
2713:
2709:
2704:
2699:
2695:
2691:
2687:
2683:
2679:
2672:
2669:
2664:
2660:
2656:
2652:
2648:
2644:
2640:
2636:
2632:
2628:
2621:
2619:
2615:
2611:
2605:
2601:
2597:
2593:
2589:
2582:
2580:
2576:
2571:
2567:
2563:
2559:
2555:
2551:
2547:
2543:
2536:
2533:
2528:
2524:
2520:
2516:
2512:
2508:
2501:
2499:
2497:
2495:
2493:
2491:
2487:
2482:
2478:
2474:
2470:
2466:
2462:
2458:
2454:
2450:
2446:
2439:
2436:
2431:
2427:
2423:
2419:
2415:
2411:
2407:
2403:
2396:
2389:
2386:
2381:
2377:
2373:
2369:
2365:
2361:
2354:
2347:
2344:
2338:
2333:
2329:
2325:
2321:
2314:
2311:
2307:
2301:
2298:
2293:
2289:
2285:
2281:
2277:
2273:
2272:
2264:
2261:
2256:
2252:
2247:
2242:
2238:
2234:
2230:
2226:
2222:
2215:
2212:
2207:
2203:
2198:
2193:
2189:
2185:
2181:
2177:
2173:
2169:
2165:
2158:
2156:
2154:
2150:
2145:
2141:
2136:
2131:
2127:
2123:
2119:
2115:
2111:
2107:
2104:(1): 160897.
2103:
2099:
2095:
2088:
2086:
2084:
2082:
2078:
2075:
2074:3-923381-27-1
2071:
2067:
2061:
2058:
2052:
2047:
2043:
2039:
2035:
2031:
2027:
2020:
2017:
2012:
2008:
2004:
2000:
1996:
1992:
1985:
1982:
1979:
1973:
1970:
1965:
1961:
1956:
1951:
1947:
1943:
1939:
1935:
1931:
1924:
1922:
1918:
1913:
1909:
1904:
1899:
1895:
1891:
1887:
1883:
1879:
1872:
1870:
1866:
1861:
1857:
1853:
1849:
1846:: S453βS465.
1845:
1841:
1834:
1827:
1824:
1819:
1815:
1811:
1807:
1803:
1799:
1792:
1790:
1786:
1781:
1777:
1772:
1767:
1763:
1759:
1755:
1751:
1747:
1740:
1737:
1732:
1728:
1723:
1718:
1714:
1710:
1706:
1702:
1698:
1691:
1689:
1687:
1683:
1678:
1674:
1670:
1666:
1662:
1658:
1651:
1648:
1643:
1639:
1635:
1631:
1627:
1623:
1616:
1613:
1608:
1604:
1600:
1596:
1592:
1588:
1581:
1579:
1577:
1575:
1571:
1566:
1562:
1557:
1552:
1548:
1544:
1540:
1536:
1535:Proc Biol Sci
1532:
1525:
1523:
1519:
1514:
1510:
1506:
1502:
1498:
1494:
1487:
1485:
1481:
1476:
1472:
1468:
1464:
1460:
1456:
1452:
1448:
1441:
1438:
1433:
1429:
1425:
1421:
1417:
1413:
1406:
1404:
1400:
1395:
1391:
1387:
1383:
1379:
1375:
1368:
1366:
1364:
1362:
1360:
1356:
1351:
1347:
1343:
1339:
1335:
1331:
1324:
1322:
1320:
1318:
1314:
1309:
1305:
1301:
1297:
1293:
1289:
1282:
1280:
1276:
1271:
1267:
1263:
1259:
1255:
1251:
1247:
1243:
1239:
1235:
1228:
1226:
1222:
1217:
1213:
1208:
1203:
1199:
1195:
1191:
1187:
1183:
1176:
1174:
1170:
1165:
1161:
1156:
1151:
1147:
1143:
1139:
1135:
1131:
1124:
1121:
1116:
1112:
1107:
1102:
1098:
1094:
1090:
1086:
1082:
1075:
1073:
1071:
1067:
1062:
1058:
1053:
1048:
1044:
1040:
1036:
1032:
1028:
1021:
1019:
1015:
1010:
1006:
1002:
998:
994:
987:
985:
983:
981:
977:
972:
968:
964:
960:
955:
950:
946:
942:
938:
934:
930:
923:
921:
917:
911:
909:
905:
900:
896:
892:
888:
884:
880:
876:
872:
865:
862:
857:
853:
849:
845:
841:
837:
833:
829:
825:
821:
814:
811:
806:
802:
798:
794:
790:
786:
779:
776:
771:
767:
763:
759:
755:
751:
744:
741:
736:
732:
728:
724:
720:
716:
712:
708:
704:
700:
696:
689:
686:
681:
677:
673:
669:
665:
661:
657:
653:
649:
645:
641:
637:
630:
627:
622:
618:
613:
608:
604:
600:
596:
589:
586:
581:
577:
572:
567:
563:
559:
555:
551:
547:
540:
538:
536:
534:
532:
528:
521:
519:
515:
512:
508:
504:
503:alloparenting
500:
496:
491:
489:
485:
484:alloparenting
477:
475:
472:
468:
464:
460:
451:
449:
446:
444:
440:
436:
432:
424:
422:
419:
415:
407:
400:
398:
396:
392:
388:
384:
380:
376:
372:
368:
364:
360:
356:
347:
345:
343:
339:
335:
331:
326:
324:
323:
318:
314:
310:
306:
302:
298:
294:
293:Coraciiformes
286:
281:
279:
277:
272:
268:
261:
259:
255:
252:
247:
243:
236:
231:
229:
226:
224:
223:
217:
214:
209:
207:
206:
199:
192:
190:
186:
179:
174:
172:
169:
168:Corvus corone
165:
164:Corvus corone
161:
160:
159:Corvus corone
154:
150:
143:
141:
139:
135:
131:
126:
122:
119:
115:
113:
112:
107:
103:
98:
97:Kin selection
94:
91:
83:
81:
78:
74:
69:
67:
66:mate guarding
62:
59:
55:
50:
48:
44:
43:breeding pair
40:
36:
35:social system
32:
27:Social system
19:
2758:(1): 52β63.
2755:
2751:
2738:
2685:
2681:
2671:
2633:(1): 49β65.
2630:
2627:Human Nature
2626:
2592:Mind the Gap
2591:
2545:
2541:
2535:
2510:
2506:
2448:
2444:
2438:
2405:
2401:
2388:
2363:
2359:
2346:
2327:
2323:
2313:
2300:
2275:
2269:
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2228:
2224:
2214:
2171:
2167:
2101:
2097:
2065:
2060:
2033:
2029:
2019:
1994:
1990:
1984:
1972:
1937:
1933:
1885:
1881:
1843:
1839:
1826:
1801:
1797:
1753:
1749:
1739:
1704:
1700:
1660:
1656:
1650:
1625:
1621:
1615:
1590:
1586:
1538:
1534:
1496:
1492:
1450:
1446:
1440:
1415:
1411:
1377:
1373:
1333:
1329:
1291:
1287:
1237:
1233:
1189:
1185:
1137:
1133:
1123:
1088:
1084:
1034:
1030:
1000:
996:
936:
932:
874:
870:
864:
823:
819:
813:
791:(3): 89β93.
788:
784:
778:
753:
749:
743:
702:
698:
688:
639:
635:
629:
602:
598:
588:
553:
549:
516:
506:
492:
481:
461:, including
455:
447:
439:Arctic foxes
428:
412:
394:
390:
386:
382:
378:
374:
370:
366:
362:
358:
354:
351:
333:
327:
321:
290:
273:
269:
265:
256:
248:
244:
240:
227:
221:
218:
213:Mungos mungo
212:
210:
205:Mungos mungo
204:
200:
196:
187:
183:
167:
163:
158:
155:
151:
147:
127:
123:
116:
109:
105:
95:
87:
70:
63:
51:
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30:
29:
1940:(1): 72β8.
1628:: 139β145.
756:: 141β177.
381:and two in
134:reciprocity
2794:Categories
2588:Silk, Joan
522:References
435:red wolves
383:Peromyscus
322:obligately
305:Sylvioidea
297:Piciformes
271:survival.
2712:0027-8424
2647:1045-6767
2562:1432-0762
2527:0084-6570
2465:1098-2345
2408:: 39β45.
2188:0962-8452
2126:2054-5703
899:0962-8436
840:1469-185X
735:198157808
719:0014-3820
699:Evolution
664:1365-294X
621:1045-2249
499:altricial
495:precocial
463:marmosets
379:Atherurus
371:Rhabdomys
355:Cryptomys
338:Australia
251:altricial
130:mutualism
90:evolution
84:Evolution
58:territory
2780:40160308
2772:22578648
2730:22932870
2663:23028482
2655:24430798
2570:22186719
2481:55324849
2473:31936968
2430:46671897
2422:23994497
2360:Ethology
2292:53181036
2255:10714885
2206:22279167
2144:28280589
1964:21185192
1912:16928639
1860:83106627
1818:53155823
1780:22438493
1731:17490945
1677:53148678
1642:85572501
1607:53152204
1513:53171632
1475:10968991
1447:Ethology
1432:14646037
1394:15575678
1350:53146761
1308:17233754
1270:12254536
1262:11935014
1216:19805429
1164:11209890
1115:22810429
1061:22787025
971:14869430
963:17714660
856:39910620
848:20849492
805:21236784
727:12487360
680:21904045
672:11412372
580:22874752
467:tamarins
452:Primates
414:Meerkats
401:Meerkats
367:Meriones
363:Microtus
299:, basal
237:Breeders
232:Benefits
180:Breeders
2721:3458333
2690:Bibcode
2368:Bibcode
2246:1690529
2197:3321711
2135:5319355
2106:Bibcode
2051:1689041
2011:1898846
1942:Bibcode
1903:1636085
1771:3367774
1722:2493572
1565:9493405
1556:1688874
1455:Bibcode
1242:Bibcode
1234:Science
1207:2781872
1155:1088590
1106:3427572
1052:3415917
941:Bibcode
879:Bibcode
644:Bibcode
571:3427589
497:versus
348:Mammals
301:Passeri
262:Helpers
193:Helpers
54:fitness
2805:Mating
2778:
2770:
2728:
2718:
2710:
2661:
2653:
2645:
2606:
2568:
2560:
2525:
2479:
2471:
2463:
2428:
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2253:
2243:
2204:
2194:
2186:
2142:
2132:
2124:
2072:
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1962:
1910:
1900:
1858:
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1778:
1768:
1729:
1719:
1675:
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1553:
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1430:
1392:
1348:
1306:
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1260:
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1162:
1152:
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1059:
1049:
969:
961:
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846:
838:
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770:221705
768:
733:
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717:
678:
670:
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568:
478:Humans
425:Canids
395:Lycaon
387:Alopex
375:Castor
2776:S2CID
2748:(PDF)
2659:S2CID
2566:S2CID
2477:S2CID
2426:S2CID
2398:(PDF)
2356:(PDF)
2288:S2CID
2007:S2CID
1856:S2CID
1836:(PDF)
1814:S2CID
1673:S2CID
1638:S2CID
1603:S2CID
1509:S2CID
1471:S2CID
1428:S2CID
1390:S2CID
1346:S2CID
1304:S2CID
1266:S2CID
967:S2CID
852:S2CID
766:JSTOR
731:S2CID
676:S2CID
431:canid
418:alpha
391:Canis
287:Birds
175:Costs
33:is a
2768:PMID
2726:PMID
2708:ISSN
2651:PMID
2643:ISSN
2604:ISBN
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1960:PMID
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1727:PMID
1561:PMID
1258:PMID
1212:PMID
1160:PMID
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1057:PMID
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340:and
315:and
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1190:364
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