The evolution of matrilineal social systems in fissiped carnivores

Abstract

We review matrilineal relationships in the societies of fissiped mammalian carnivores, focusing on how the most complex of these may have evolved from simpler systems. Although competition for food is very intense at the trophic level occupied by most carnivores, and although most species of extant fissiped carnivores therefore lead solitary lives, some species show at least rudimentary clustering of maternal kin and matrilineal resource-sharing or transmission of critical resources between generations. The resources shared or transmitted range from individual food items and territories to entire networks of potential allies. The greatest elaboration of matrilineal relationships has occurred in two large carnivores, lions and spotted hyenas, which occur sympatrically throughout much of Africa. The societies of both these species apparently evolved in response to a shared suite of ecological conditions. The highly matrilineal societies of spotted hyenas are unique among carnivores and closely resemble the societies of many cercopithecine primates. The conditions favouring the evolution of matrilineal societies in carnivores include male-biased dispersal, female philopatry, the need for assistance in protecting or provisioning offspring, reliance on large or abundant prey, particularly in open habitat, high population density and kin-structured cooperative interactions that have strong positive effects on fitness.

This article is part of the theme issue ‘The evolution of female-biased kinship in humans and other mammals’.

1. Introduction

Only 10–15% of all species in the mammalian order Carnivora aggregate during some period outside of the breeding season [1]. Because competition for food is very intense at the high trophic levels occupied by most carnivores, the vast majority of extant mammalian carnivores lead solitary lives. Mammalian carnivores represent an extreme case in which the negative effects of resource competition might be expected to outweigh the positive effects of living and cooperating with close kin. In light of the negative effects of intensive resource competition within this order of mammals, it may seem surprising that any matrilineal societies at all occur within the Carnivora, so it is worth exploring how such societies might have evolved. Our review reveals that some tolerance of proximity of close female kin and temporary group formation by close female kin occur even among various solitary carnivores. In these solitary species, we also find some of the rudimentary building blocks of more complex matrilineal societies, such as resource-sharing among close female kin or transmission of critical resources from one generation of females to the next. Furthermore, some species in multiple carnivore families are somewhat to highly gregarious, and several of these species show clustering of maternal kin in space, as well as matrilineal resource-sharing. Elaborate matrilineal societies characterized by a high frequency of nepotistic interactions have evolved in two highly gregarious carnivore species, the lion (Panthera leo) and the spotted hyena (Crocuta crocuta). In both these species, the positive effects on fitness of nepotistic and cooperative behaviour among female kin have been well-documented. Therefore, even in the extreme case of mammalian carnivores, which compete so intensively for food and spatial resources, the benefits of living and cooperating with female kin can favour the evolution of matrilineal societies.

Here we review the literature on matrilineal social systems in fissiped carnivores. ‘Fissiped’ literally means carnivores having toes separated to the base; these include all the extant mammalian carnivores except seals, sea lions and the walruses, all of which have toes joined by webbing to transform their feet into paddles (the ‘pinnipeds’). Although most fissiped carnivores are terrestrial, this group also includes otters, which are members of the same family (Mustelidae) that contains badgers and weasels. Various fissiped carnivores show at least rudimentary clustering of maternal kin and matrilineal resource-sharing or transmission of critical resources between generations. We first summarize long-standing ideas about how complex matrilineal social systems most likely evolved from simpler ones in carnivores. We then review the fissiped carnivore species in which rudimentary or complex forms of matrilineal social systems occur, as well as the specific traits and socio-ecological conditions that tend to favour the evolution of matrilineal social systems. We emphasize that many gaps currently exist in our knowledge about the social interactions of many carnivores, especially solitary, forest-dwelling species in the carnivore families Viverridae, Nandiniidae, Mephiditae and Ailuridae. Finally, we conclude by reviewing the ways in which nepotistic and cooperative behaviour among female kin can enhance fitness. In this final section, we focus largely on long-term studies of lions and spotted hyenas in Africa.

2. The evolution of matrilineal societies in carnivores

John Eisenberg [2,3] reviewed evidence suggesting that early carnivores existed in the Eocene at low densities and that they competed for both food and space. Each individual male and female most likely occupied its own home range and defended that space against incursions by all conspecifics. Each female reared her young alone, and the family split up during or shortly after weaning, as the maturing littermates began to compete for food with the mother and with one another. Moreover, within-litter aggression probably appeared early in the evolutionary history of carnivores and promoted the dispersal of family members [2]. An elaboration of this strictly solitary and territorial condition may have occurred when the home ranges of one or more females began to be encompassed by the home range of a single male. Under these conditions, an adult male could impregnate more than one female by excluding other males from his home range. In such solitary species, affiliative behaviour would only be seen during the mating season and during the offspring rearing phase; affiliative interactions would otherwise occur infrequently, if at all [4].

Eisenberg [2] argued that various forms of complex sociality in carnivores and other mammals can evolve from one of three types of temporary social units that form during specific phases of the reproductive cycle in solitary mammals. First, male and female conspecifics unite to mate when the female is in oestrus. When selection favours this male–female relationship to endure past fertilization, bonds evolve between mates, and this in turn may lead to long-term monogamous partnerships and shared responsibilities during the rearing of young. The parental family structure is characterized in its extreme form, particularly when dispersal opportunities are limited for subadult offspring, by a bonded pair of adults and their immature descendants. Such protracted monogamous relationships are common among extant canids and social mongooses, many of which engage in cooperative breeding [5–7].

Second, after the birth of a litter to a solitary female carnivore, the littermate offspring form a temporary social unit that persists until they disperse away from their mother. However, selection may act on this social unit to favour littermates who associate closely with one another even after they leave their mother to accomplish goals any solitary individual could not achieve on its own. Examples of this include sibling coalitions that may last for many years among male cheetahs (Acinonyx jubatus), male banded mongooses and male lions, which would be unable to acquire or defend important resources on their own; such key resources might include a territory or a group of females [8–11].

Finally, in solitary mammals, the relationship between a mother and the members of her litter endures only until that litter is weaned, after which offspring disperse and the mother resumes her solitary existence. However, selection may act to favour mothers and their offspring who remain together after weaning. This is particularly true for mothers and their daughters, because mammalian dispersal is often strongly male-biased. Mothers, daughters and sisters may then come to tolerate one another and maintain their close associations long after weaning, and in fact throughout their lives, to cooperatively acquire or defend key resources. Eisenberg and colleagues [2,4,5] referred to the temporary social unit composed of a mother and her dependent offspring as a ‘mother–family’, and it is from this unit that the most elaborate matrilineal social systems have evolved in mammalian carnivores, as they have in other orders of mammals, including primates [4]. The fact that carnivores and primates last shared a common ancestor roughly 90 Ma [12] suggests that selection on the mother–family to persist beyond weaning has a long history in mammals when ecological conditions favour its persistence.

3. The occurrence of matrilineal social systems in fissiped carnivores

The families of fissiped carnivores in which some form of matrilineal social systems occurs include Ursidae, Mustelidae, Procyonidae, Canidae, Felidae, Herpestidae, Eupleridae and Hyaenidae (table 1).

Table 1.

Summary of the literature on matrilinear characteristics in carnivores.

family	species	female social structure	intergenerational resource transmission	spatial clustering of female kin	cooperation among female kin	fitness benefits of matrilineal associations	references
Ursidae	American black bear	solitary	Y	Y	N	Y	[13]
	Asiatic black bear	solitary	Y	Y	N	Y	[14]
	brown bear	solitary	Y	Y	N	Y	[15]
	polar bear	solitary	N	Y	N	?	[16]
Mustelidae	European badger	flexible	Y	Y	Y (low)	?	[17–20]
	giant otter	group living	Y	Y	Y	Y	[21–23]
	river otter	solitary	?	?	N	?	[24]
Procyonidae	coati	group living	?	Y	Y	Y	[25–30]
	raccoon	solitary	?	Y	N	?	[31,32]
Canidae	swift fox	group living	Y	Y	Y	Y	[33,34]
Herpestidae	banded mongoose	group living	Y	Y	Y	Y	[35–37]
	dwarf mongoose	group living	Y	Y	Y	Y	[35,38–40]
	meerkat	group living	Y	Y	Y	Y	[35,41–43]
	white-tailed mongoose	solitary	?	Y	N	?	[35,44]
	yellow mongoose	flexible	?	Y	Y	?	[35,45]
Eupleridae	narrow-striped mongoose	group living	Y	Y	?	?	[35,46,47]
Felidae	leopard	solitary	Y	Y	N	Y	[48,49]
	lion	group living	Y	Y	Y	Y	[10,50,51]
Hyaenidae	brown hyena	group living	Y	Y	Y	Y	[52–56]
	spotted hyena	group living	Y	Y	Y	Y	[52,57–69]
	striped hyena	flexible	?	Y	Y	?

4. Ursidae

As with other carnivore families, the common ancestor of modern ursids was almost certainly solitary [70,71]. Extant ursids have remained solitary except during the mating season, and when females rear dependent cubs [71]. Despite the largely solitary habits of bears on their individual home ranges, kin-based spatial structures have been found among females in American black bears (Ursus americanus), Asiatic black bears (Ursus thibetanus), grizzly bears (Ursus arctos) and polar bears (Ursus maritimus). Most of these species show a matriline-based spatial distribution in which daughters establish ranges near or overlapping those of their mothers, resulting in spatial clustering of female kin [13–15,72]. Dispersal is male-biased. For example, on average, mother–son grizzly bear pairs are found three times farther apart in space than are mother–daughter pairs [72]. Similarly, genetic relatedness within adult female dyads of polar bears declines significantly with increasing geographical distance [16]). Female polar bears show den area fidelity and a stronger kin structure than males [16,73]. Black bear mothers allow their daughters to occupy portions of their territory, or share a territory with them [13].

5. Mustelidae

Most mustelids are solitary [1] except during mating and when females rear dependent young. Diet and resource distribution play important roles in shaping this solitary behaviour, and the biochemical mechanisms associated with delayed implantation may also contribute [1,74]. However, river otters (Lutra canadensis) show some rudimentary forms of matrilineal sociality. For instance, multiparous females sometimes allow their elder daughter(s) to return to live with them when they start to wean their current pups [24]. Yearling females either return to live with their mother, or they are aggressively expelled permanently from the mother's home range by an older sister. After being accepted back by her mother, an elder daughter becomes a full-time, cohabiting member of the family and a regular companion to the young pups [24].

Giant otters (Pteronura brasiliensis) live in highly cooperative groups led by an alpha pair [21]. Protracted allo-parental care is critical for pup survival in this species [22]. As in ursids, genetic relatedness declines significantly with increasing geographical distance within dyads of adult female, but not male, giant otters [21]. When the dominant female dies, a related female subordinate typically acquires her position and inherits the group and the territory [21,22].

European badgers (Meles meles) are highly flexible and facultatively social. In prime habitat and at high densities, they form groups characterized by both male and female philopatry [17], in which conspecifics that den together in communal burrow systems, called ‘setts’, share a common range [75]; within-group relatedness in setts is high [18]. Other forms of cooperation are rare in this species, but allo-parenting may occur among females [19]. In some habitats, females may disperse in coalitionary groups to form new setts (e.g. [20]).

6. Procyonidae

Coatis are the most gregarious Procyonid, living in bands composed of multiple adult females and their offspring. Male coatis disperse after puberty and live either solitarily or temporarily in multi-male groups [25–27]. Males are often excluded from bands except during the mating season, apparently because they may opportunistically prey upon juveniles [28]. The coati diet consists mainly of fruits and invertebrates; bands fission into smaller subgroups to forage on fruit. Pairs of females within bands preferentially groom one another and also support one another during infrequent aggression that occurs [29]. Bands split when groups exceed three to five females, with fission occurring along previously established lines of affiliation. In some populations, closely related adult females frequently direct aggression together toward unrelated group-mates in defence of concentrated resources used by their offspring and other kin [30]. Thus, kinship drives cooperative behaviour in these populations, although non-kin may also cooperate elsewhere [25,29].

Throughout their range, raccoons (Procyon lotor) show a high degree of flexibility in their socio-spatial organization. As adults, females may live partially on or close to their natal range, and greater overlap of home ranges is positively correlated with higher relatedness [31]. As in ursids and mustelids, genetic relatedness declines significantly with increasing geographical distance within dyads of female, but not male, raccoons [32]. Similarly, kinkajous (Potos flavus) are generally solitary but are sometimes found in groups composed of a mother–daughter pair plus one or two unrelated males [76].

7. Canidae

Most canids exhibit an enduring bond between mates, in which the male helps the female to rear young. Care of young usually includes provisioning of the female and her litter by the male and other group members [1]. In fact, provisioning the female and young by the male occurs even in those species that do not form packs, such as the arctic fox (Vulpes lagopus) and red fox (Vulpes vulpes). The social organization found in pack-hunting canids (wolves, Canis lupus, Cape hunting dogs Lycaon pictus, dohles, Cuon alpinus and bush dogs, Speothos venaticus) probably evolved through continued interaction between the bonded parents and their offspring after weaning [2,5,77,78]. Both provisioning and pair-bonding are probably phylogenetically old traits within the Canidae; both contribute to the successful rearing of the large litters generally borne by female canids. Selection for the formation of larger social groupings appears to have acted to enhance the association between the male–female pair and their offspring.

Because of the importance of food provisioning and territorial defence by males, the social structure in most canids is shared or even dominated by males. However, small, insectivorous canids show little paternal care, and they also show a bias toward female philopatry. For example, in contrast to most other canids, the social organization of the swift fox (Vulpes velox) is based on female territories, which are maintained even in the absence of males [33]. Neighbouring swift foxes are more closely related than non-neighbours, and female clusters are more extensive than male clusters [34]. Relatedness between female holders of adjacent territories is correlated with the degree to which they tolerate home range overlap [34], and neighbours sometimes even share dens. Relatedness also influences the likelihood that an individual will inherit a newly vacated home range [34]. The tolerance shown to neighbouring related swift foxes indicates that these animals can identify their kin and that they maintain long-term relationships with them. This unusual canid social system may have evolved because the importance of food provisioning and territorial defence by males is reduced in swift foxes owing to their reliance on insect food resources [33].

8. Herpestidae

At least 19 species of herpestids are known to be gregarious [35], and at least some indication of matrilineal social structure has been documented in five species: dwarf mongooses (Helogale parvula), banded mongooses (Mungus mungo), meerkats (Suricata suricatta), yellow mongooses (Cynictis penicillate) and white-tailed mongooses (Ichneumia albicauda). As in canids, group living in mongooses appears to be an elaboration of the relationship between a male–female pair and their offspring [79]. Dwarf mongoose and meerkat groups are characterized by male-biased dispersal, female dominance, an alpha pair that controls most reproduction [35] and high levels of intragroup relatedness among females and their descendants [38,41]. Among adult female banded mongooses, intragroup relatedness is often high, particularly in newly founded groups, such as those occurring when individuals disperse together [11,36,80]. In the cooperatively breeding mongooses, allo-care of pups is essential for their survival and may include nursing, guarding, carrying and feeding of young [35]. Helpers are subordinate individuals of both sexes that are often, but not always, related to the latest litter [35,39,81,82]. Both male and female banded mongooses can inherit breeding positions in their natal group, and reproductive skew in both sexes tends to be low in this species [37]. However, in dwarf mongooses [40] and meerkats [42], only female offspring can inherit the alpha breeding position, territory and subordinate helpers from their maternal kin. Reproductive skew in these species tends to be considerably greater than in banded mongooses.

At high densities, the facultatively social yellow mongoose may form groups containing multiple breeding females, which tend to be closely related, though allo-parental care is provided by both kin and non-kin [45]. Similarly, although white-tailed mongooses are typically solitary, at high densities they show range overlap among related adult females and their offspring [35]. Females of this species forage and den alone, but recognize and tolerate one another and act aggressively towards non-group members [44].

9. Eupleridae

This family contains five species of carnivores native only to Madagascar [12], all of which are severely understudied. As in herpestids, group living in euplerids has antipredator and resource defence benefits [46]. Female narrow-striped mongooses (Mungotictis decemlineata) live in small, philopatric groups of related females and their offspring [47]. Group members den together but do not provide allo-parental care [47]. Their social organization is matrilineal, with neighbouring groups sharing the same haplotypes [47].

10. Felidae

The efficiency of hunting and feeding characteristic of felids has facilitated the evolution of more-or-less exclusive home range use and a solitary lifestyle in most species in this family. The primary social grouping in most felids consists of the mother and her offspring. After weaning, the young usually leave voluntarily or are driven away by the mother [83]. However, specific evolutionary precursors to matrilineal societies appear even in solitary felids. For example, as population density increases among wild leopards (Panthera pardus), female home range size decreases, their home ranges show increasing overlap and females show a greater tendency to form matrilineal kin clusters [48].

The lion is the only felid living in mixed-sex groups that habitually hunt, feed and rest together [84,85]. A lion pride consists of several related females and their young; adult female pride-mates nurse one another's cubs. Most females remain in the natal pride for life, retaining close associations with 1–20 female relatives, such that female pride members are seldom more distantly related than cousins, sharing on average at least 12.5% of their genes [10]. By contrast, the males that associate with pride females are generally unrelated to them. Females often have close relatives in neighbouring prides, but very few relatives in prides with territories not abutting their own [86]. Relatedness among female lions declines sharply with geographical distance, and mean relatedness is greater in small than large prides [86]. Females occasionally leave their pride to avoid having their cubs killed by new males during pride takeovers. The formation of new prides involves emigration of a group of related females into an area within, or adjacent to, the territory of the natal pride [10]. Females cooperate in group hunts [87] and support one another in aggressive interactions with new cohorts of immigrant males in an effort to prevent infanticide by the males; females may be wounded or even killed in these fights. Cooperative defence of cubs appears to be an important aspect of communal rearing among female lions [88].

Given the rare appearance of enduring pair bonds between male and female parents in the family Felidae, complex social organizations could not have derived from a pair and their offspring, as occurred in canids. Instead, the basic social unit of the lion pride emerged from enhanced tolerance among females, based on the continued association of a lioness with her maturing daughters [85,89]. In contrast to canids, male felids do not provision their young, so this falls entirely to the mother and her female kin. The complex social structure in extant lions appears to have been shaped by selection acting on the mother–family as the original temporary social unit [5].

11. Hyaenidae

Two extant hyaenid species show simple forms of matrilineal social organization. Brown hyenas (Parahyaena brunnea) live in small groups, called clans, ranging in size from a single female and her cubs to approximately 14 animals [52]. Clan members share a common territory and den [53,54]. Larger clans consist of extended families that include a female, her adult offspring of both sexes and an immigrant male. Both males and females may provision den-dwelling cubs [52]. Brown hyenas forage solitarily to feed on carrion, fruit and small prey, resources that tend to be rare and widely dispersed, such that they provide food for only a single individual [52–54]. Females often spend their entire lives in their natal clans, and some males stay with their natal clans into adulthood, but dispersal is nevertheless strongly male-biased [52]. Females within clans are more closely related than females between clans and are more closely related than are males with female clan-mates [55].

Like brown hyenas, striped hyenas (Hyaena hyaena) feed mainly on carrion. These animals were long believed to be strictly solitary (e.g. [90]), but recent work has revealed that they sometimes form small aggregations (e.g. [66–69]). Although striped hyenas forage alone, closely related females sometimes share dens in habitats where resource abundance permits [68,69]. Mothers carry food back to the den for their cubs [90–92], and other kin of both sexes have also been observed provisioning den-dwelling cubs [68]. Thus, the social system of striped hyenas appears to be flexible; in resource-rich habitats, their groups closely resemble those of brown hyenas, although groups of brown hyenas tend to be larger than do striped hyena groups.

The spotted hyena exhibits by far the most complex matrilineal society found within the order Carnivora. Spotted hyenas live in large clans that typically contain multiple groups of matrilineal kin, as well as one to several immigrant males. Clans, which may contain more than 120 individuals [93], are structured by linear rank relationships [94–96]. Female kin generally occupy adjacent rank positions in the clan's hierarchy, so entire matrilines can be ranked as well as individual hyenas [57]. In contrast to brown and striped hyenas, spotted hyenas are very good hunters, killing up to 95% of their own prey; they prey mainly on medium- and large-bodied herbivores [97]. A group of hungry hyenas can reduce a 150 kg antelope to a skull and vertebrae in as little as 13 min, so feeding competition is extremely intense among clan-mates, and an individual's social rank determines its priority of access to carcasses [94,98]. Importantly, food intake limits the rate of reproduction among females [99].

All clan-mates know one another individually, rear their cubs together at a communal den and defend a common territory [58]. Litters, which usually contain only one or two cubs, are smaller in spotted hyenas than in other hyaenids. Maternal kinship is an extremely important determinant of interaction patterns in the societies of spotted hyenas. Females are philopatric whereas males disperse, so females spend their lives associating closely with their female kin [94,100], and they show extensive affiliative and cooperative behaviour toward them (e.g. [56,59,60]). Aggression among wild hyenas is more frequent between than within matrilines [94], although relatedness does not protect females from aggression; this and other costs associated with competition between relatives can outweigh the kin-selected benefits of altruism toward relatives in carnivores and other animals [61,101]. Female allies are critical in maintaining access to resources in spotted hyenas [102]. During early ontogeny, young spotted hyenas learn to acquire social ranks immediately below those of their mothers [96,103]. Emergence of a matrilineal social system occurs in both wild and captive spotted hyenas [104]. Matrilineal rank acquisition in both wild and captive environments appears to result from relationships generated between mother–offspring units and other group members (e.g. [105]).

As with lions, it has been hypothesized that spotted hyenas live in groups because cooperative hunting allows these animals to capture larger prey animals or enhance their hunting success, as occurs in pack-hunting canids (e.g. [77]). However, although cooperative hunting does increase the probability of success and allows spotted hyenas to capture larger prey animals, 75% of successful hunts are conducted by lone hyenas [62], and only the largest and most challenging of prey species require more than one hyena for a successful hunt [62,95]. This suggests that cooperative hunting was likely not paramount in the evolution of matrilineal societies in spotted hyenas, although assistance during hunts clearly represents a beneficial side-effect of group living. Instead, the need to defend spatial and food resources from competitors most likely favoured gregariousness among female hyenas. Moreover, the herbivores killed by spotted hyenas represent an abundant and readily renewable food resource that allows these hyenas to reach high population densities. Spotted hyenas often live and hunt in open habitat where competitors, such as lions and members of neighbouring hyena clans, can easily detect kills, which are typically too large to be monopolized by a single individual. These conditions appear to have favoured grouping by females to protect carcasses and also to protect group territories in areas of high population density.

12. Socio-ecological conditions facilitating the evolution of matrilineal societies in carnivores

Although many gaps still exist in our knowledge, particularly about social interactions among small-bodied solitary carnivores, field studies have taught us a great deal about the socio-ecological conditions favouring the evolution of matrilineal social systems in carnivores. These include male-biased dispersal, female philopatry, reliance on large or abundant prey, particularly in open habitat, the need for assistance either in protecting or provisioning offspring or in acquiring and protecting key resources. As in other orders of mammals, natal dispersal in most mammalian carnivores tends to be sexually dimorphic [106,107], with males typically dispersing farther or more frequently than females. In solitary carnivores, both sexes disperse away from the mother's territory, although female offspring tend to settle closer to their mothers than do their brothers. The spatial proximity between mothers and daughters sets the stage for the emergence of nepotistic behaviour among females. For example, as they get older, female leopards and bears relinquish portions of their home ranges to philopatric daughters [13,49].

Patterns of hunting and feeding in terrestrial carnivores, and the resultant tendencies towards clustering of female kin, are strongly influenced by both prey density and density of conspecifics. Both abundant food resources and high conspecific densities encourage reduced dispersal and increased aggregation of female kin in many carnivore families. For example, although dispersal distances are longer among female than male striped hyenas in areas with scarce resources [66], where resource abundance is high striped hyenas exhibit male-biased dispersal, home range overlap and den-sharing among female kin (e.g. [68,69]). Similarly, in both European badgers and giant otters, aggregations of females and inheritance of territorial resources by younger females occur in response to high population density, abundant food resources and the lack of available territories for dispersing offspring [17,21,22,108,109]. The spatial distributions among extant bears appear to be largely due to the patchy distribution of vital resources. However, bears and other solitary carnivores are known to aggregate during periods of, or at places characterized by, abundant food resources (e.g. polar bears [70], raccoons [110], leopards [48]). This may also occur in the other families of solitary carnivores, including Viverridae, Nandiniidae, Mephiditae and Ailuridae, but to our knowledge, it has not yet been described in the literature.

In most carnivores, other than canids and social mongooses, the reproductive roles of adult females, but not males, are dominated by infant care. Females obliged to care for infants on their own tend to have smaller litters than do females in carnivore species in which mates or kin help with offspring care [111]. During the early phases of development in the former species, the mother is solely responsible for protecting and feeding infants; when an infant enters the juvenile stages, the mother also plays an important role in its socialization. Protecting infants from infanticidal male conspecifics represents a challenge for female carnivores, who are often considerably smaller than males. In both bears and lions, this need appears to have favoured spatial clustering and resource-sharing by maternal kin. To reduce the risk of infanticide, female bears with young may avoid areas inhabited by adult males [103]. Infanticide has been observed in many carnivores, including American black bears, Asiatic black bears [14], brown bears, polar bears [103] and lions [88].

Variation in social structure among canid species appears to be strongly influenced by the importance to pup survival of food provisioning and territorial defence by males [33]. In pack-hunting canids (wolf, dhole, Cape hunting dog), both group living and cooperative hunting have evolved as adaptive responses to the presence of large prey that cannot be brought down by a single individual (e.g. [77]). Similar adaptations to feeding upon medium and large-bodied ungulates occurred within the Felidae and Hyaenidae, culminating in the evolution of large stable social groups in lions and spotted hyenas. However, whereas in canids, this occurred via the elaboration of the bond between a mated pair and their offspring, in felids and hyaenids, it occurred via the elaboration of the mother–family. More rudimentary forms of the extended mother–family appear in the mustelids, procyonids, euplerids and ursids.

The most elaborate matrilineal societies found in mammalian carnivores are those of lions and spotted hyenas. The widespread African grasslands and abundant herbivores present during the late Pliocene and Pleistocene probably created an environment favouring matrilineal kin aggregations in both these species. The lion evolved between 1 million and 800 000 Ma in Africa [112]; similarly, modern spotted hyenas first appear in the fossil record in Africa between 900 000 and 250 000 Ma [113]. Spotted hyenas and lions occur sympatrically throughout much of sub-Saharan Africa, so these two matrilineal societies presumably evolved in response to the same ecological conditions, the most important of which were abundant large-bodied prey, open grassland habitat and considerably higher population densities than is typical of other felids or hyaenids [50]. In open habitats, kills can be detected by competitors over long distances, so the defence of both kills and territorial boundaries demands cooperative action [63]. The spotted hyena is the only extant hyaenid adapted for the hunting of prey, as brown and striped hyenas feed mainly on carrion. Felids other than lions either prefer smaller-bodied prey or live in habitats characterized by denser vegetation than African savannahs [50]. Although it was long believed that the selection pressure favouring the evolution of matrilineal groups among lions was the need for help in capturing large prey, instead the evidence supports the hypothesis that selection favoured female lion kin who helped one another defend young, carcasses and territories [50,88].

Lions compete for carcasses directly with spotted hyenas and, because lions are much larger than hyenas, lions also represent a leading mortality source for hyenas [52,95,114]. Individual hyenas cannot effectively compete with lions for possession of a carcass, or defend themselves from predation by lions, without aid from conspecifics. However, when spotted hyenas join forces with group-mates, they can not only defend their own kills from lions, but they can also sometimes usurp kills made by lions [115]. Under conditions of high population density, effective maintenance of group territories also requires individual females from multiple hyena matrilines to cooperate to defend clan resources against neighbouring hyena clans [116]. Loss of a clan war can result in a substantial reduction of a clan's territory [95] and repeated losses can result in an overall loss of the territory to a neighbouring clan. Cooperative defence of territories appears to offer a similarly important advantage during intraspecific between-group conflicts in many other carnivores, including dwarf mongooses, meerkats, banded mongooses and Ethiopian wolves (Canis simensis, [117]), with the larger of two groups typically winning these disputes (e.g. [118,119]).

13. Fitness consequences of enduring association with maternal kin

Patterns of spatial proximity influence the frequency and outcomes of competitive and cooperative interactions among mammalian carnivores, and this can have profound effects on survival and reproduction, as can enhanced social tolerance among female kin. Inclusive fitness modulates intraspecific competition for resources in carnivores when female relatives are spatially aggregated and likely to interact cooperatively [120]. For instance, the matriarchal spatial distributions characteristic of many bears confer inclusive fitness benefits, because daughters can more easily establish and hold territories without risking dispersal [70]. Dispersal is particularly risky for small carnivores like herpestids [69]. Females need knowledge of local, ephemeral resources including den sites and food sources; this knowledge can protect them against both starvation and infanticide [70,88]. Thus, inheriting the dominant position in a natal group can be particularly beneficial for daughters. In meerkats, females gain a higher fitness benefit than do males from acquiring dominant breeding status, and this may explain why traits enhancing competitive ability are more highly developed in females than males [42]. Similarly, inheriting a territory and a breeding position obviates risky dispersal for female giant otters and European badgers [21–23].

Long-term studies of carnivore groups have revealed that the fitness benefits of allo-parental care by females other than the mother range from nil to substantial. Whereas increasing the number of allo-parental females per group correlates negatively with offspring fitness in European badgers [19], they correlate highly positively in meerkats [43] and lions [10,51,121]. Long-term studies have also shown that kin-structured cooperative interactions have strong positive effects on fitness in both lions and spotted hyenas.

The grouping patterns of female lions result from multiple factors, in particular, the demands of protecting young and maintaining a territory [10]. Successful breeding appears to be impossible without a territory in this species. Females compete aggressively against neighbouring prides and the larger pride usually wins between-group encounters [121]. Competition for territories directly affects the fitness of female lions, and larger prides gain and maintain access to the highest-quality habitat. Neighbours have a significant negative effect on female reproductive success and survival, and larger prides are also more likely to maintain control of disputed areas and to improve the quality of their territories [51]. Adult female lions are significantly less likely to be alone when a pride has more neighbours, suggesting sensitivity to the risk of encounter. Interestingly, prides that have recently split, and therefore contain related lions, seldom engage in intergroup territorial competition [51].

Whereas female lions seldom fight with related pride-mates over access to carcasses, female spotted hyenas frequently compete for food resources with their close kin. Kinship fails to protect spotted hyenas from attack when resources are at stake [61]. Some of the most intense competition observed in spotted hyenas occurs between full- and half-sibling littermates as they compete as infants for access to the mother's two teats [122]. Upon the death of an alpha female hyena, her youngest adult daughters may fight viciously with one another to fill the vacant alpha position. Nevertheless, closely related spotted hyenas exhibit strong nepotism and cooperation, both of which yield substantial fitness benefits. Not only do young females inherit their mother's social rank, but they also inherit her entire social network of associates [123]. Maternal kin associate more closely than do non-kin, they are more affiliative toward one another than are non-kin, they hunt together more than do non-kin, and they tolerate one another more readily than non-kin while feeding at kills [52,56,59,60,64]. Close maternal kin are usually the most common partners in coalitionary attacks on unrelated hyenas [61,124]. Furthermore, these animals recognize and respond to distress vocalizations emitted by close maternal kin far more vigorously than they respond to the distress vocalizations of non-kin [125]. In addition to generating these short-term benefits, close associations and coalition-formation among female kin also appear to play a central role in maintaining long periods of stability in the adult female dominance hierarchy [102]; they also cause the occasional coup d’état in the hierarchy that overthrows a higher-ranking lineage and thereby improves resource access for an entire matriline [52,65].

14. Conclusion

Evidence of matrilineal social systems is found in many mammalian carnivores, albeit only in rudimentary form in more solitary species. Regardless, it is straightforward to envision how the elaborate matrilineal societies of lions and spotted hyenas evolved from social systems characterized only by such rudimentary building blocks as the temporary mother–family described by Eisenberg [2]. We still know very little about matrilineal kin relationships in many rare or solitary carnivores, particularly small-bodied species occurring in habitats with dense vegetative cover, so this represents an important area for future research. The limits of nepotism in mammalian carnivores should also be explored in future work. The evolution of matrilineal social systems in carnivores has been favoured by high population density, reliance on large or abundant prey, small litter size, male-biased dispersal and the need for assistance in protecting or provisioning offspring or key resources. Once selection has favoured enhanced gregariousness, then the stage is set for the evolution of nepotistic behaviour and kin-structured cooperative interactions among female carnivores, and these in turn can have strong positive effects on fitness.

Data accessibility

This article has no additional data.

Authors' contributions

Each author reviewed the literature on four families and drafted the appropriate sections.

Competing interests

We declare we have no competing interests.

Funding

This work was supported by NSF grant nos DEB 1353110, OISE1556407, OISE1853934 and IOS1755089 to K.E.H., and by a Graduate Research Fellowship from NSF to M.A.S.