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Big cats as a model system for the study of the evolution of intelligence
Behavioural Processes 141 (2017) 261–266
Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Big cats as a model system for the study of the evolution of intelligence Natalia Borrego a,b,∗ a b
Department of Life Sciences, University of Kwazulu-Natal, South Africa Lion Research Center, Department of Ecology, Evolution and Behavior, University of Minnesota, South Africa
a r t i c l e
i n f o
Article history: Received 15 October 2016 Received in revised form 11 February 2017 Accepted 15 March 2017 Available online 21 March 2017 Keywords: Panthera Social Intelligence Big cats Cognitive evolution Lions (Panthera Leo)
a b s t r a c t Currently, carnivores, and felids in particular, are vastly underrepresented in cognitive literature, despite being an ideal model system for tests of social and ecological intelligence hypotheses. Within Felidae, big cats (Panthera) are uniquely suited to studies investigating the evolutionary links between social, ecological, and cognitive complexity. Intelligence likely did not evolve in a unitary way but instead evolved as the result of mutually reinforcing feedback loops within the physical and social environments. The domain-specific social intelligence hypothesis proposes that social complexity drives only the evolution of cognitive abilities adapted only to social domains. The domain-general hypothesis proposes that the unique demands of social life serve as a bootstrap for the evolution of superior general cognition. Big cats are one of the few systems in which we can directly address conflicting predictions of the domain-general and domain-specific hypothesis by comparing cognition among closely related species that face roughly equivalent ecological complexity but vary considerably in social complexity © 2017 Elsevier B.V. All rights reserved.
Contents 1. 2.
3.
4.
5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261 Big cat biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262 2.1. The ecology and distribution of big cats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262 2.2. The evolution of sociality in lions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262 Cognition in the only social felid: lions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262 3.1. Cognitive demands of cooperative territorial and offspring defense; cognition and competition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262 3.2. Cognition and cooperative hunting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263 3.3. Social learning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263 Big cats as a comparative framework for the study of the evolution of intelligence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 4.1. Learning and memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 4.2. Innovative problem solving . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 265
1. Introduction Cognition can be broadly defined as, “all the ways in which animals take in information about the world through the senses, process, retain and decide to act on it” (Shettleworth 2001). Sev-
∗ Correspondence to: College of Life Sciences, University of Kwazulu-Natal, Westville Campus, Durban, 4041, South Africa. E-mail address: [email protected] http://dx.doi.org/10.1016/j.beproc.2017.03.010 0376-6357/© 2017 Elsevier B.V. All rights reserved.
eral hypotheses have been put forth to explain the evolution of complex cognition, i.e., intelligence. Ecological hypotheses propose that navigating physical/ecological environments selects for intelligence (reviewed by Dunbar 1998). Social intelligence and social brain hypotheses propose that intelligence evolves in response to the unique demands of navigating the complexities of social life (Byrne and Whiten, 1988; Dunbar, 1998; Humphrey, 1976; Jolly, 1966). Social and ecological intelligence hypotheses are not mutually exclusive; intelligence likely did not evolve in a unitary way but instead evolved as the result of mutually reinforcing feedback
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loops within the physical and social environments (Barrett et al., 2012; Barton, 2012). Disentangling the evolutionary connections among social, ecological, and cognitive complexity can be achieved through cognitive comparisons of ecologically diverse but socially similar taxa and comparisons of ecologically similar but socially diverse taxa. The genus Panthera (hereafter referred to as big cats) provides an ecologically equivalent but socially distinct comparative framework and is ideally suited to investigations of the link between social complexity and cognitive complexity. Currently, the literature is divided over the selective pressure sociality places on nonsocial cognition (e.g., cognitive abilities adapted to physical environments), resulting in disparate hypotheses. The domain-general social intelligence hypothesis proposes that sociality selects for overall cognitive complexity, including cognitive abilities adapted to nonsocial/physical environments and argues the unique selective pressures of social interactions serve as a bootstrap for the evolution of superior general cognition (Byrne and Whiten 1988). In contrast, the domain-specific social intelligence hypothesis proposes that sociality selects for only, or especially for, cognitive abilities adapted to social environments (Byrne and Whiten 1988). Proponents of this interpretation argue that, regardless of social complexity, species facing similar ecological complexity will not differ in cognition adapted to nonsocial realms. Big cats are one of the few systems in which we can directly address conflicting predictions by comparing cognition among closely related species that face roughly equivalent ecological complexity but vary considerably in social complexity. Yet, relative to other carnivores, big cats have been largely overlooked in comparative cognition research (Benson-Amram et al., 2016; Navarrete et al., 2016; Perez-Barberia et al., 2007). Here I review the relevant ecology and biology of big cats and the current literature on big cat cognition, with a focus on lions (Panthera leo), as lions are the most represented in the literature and our current understanding of big cat cognition is biased towards lions. I explore big cats’ suitability as a model system for comparisons aimed at gaining a more holistic understanding of the evolutionary mechanisms operating on cognition and resolving domain -specific and -general hypotheses.
2.2. The evolution of sociality in lions Big cats diverged from an asocial common ancestor roughly 6 MYA, and following the split, sociality evolved only in the lion lineage (Finarelli and Flynn 2009; Johnson et al., 2006; Nyakatura and Bininda-Emonds, 2012; Perez-Barberia et al., 2007). Originally, the evolution of sociality in lions was attributed to fitness payoffs associated with cooperative hunting. However, if the benefits of group hunting drove the evolution of sociality in lions, then compared to singletons, group-hunters should experience greater hunting success and higher food intake. Contrary to this prediction, lone lions perform as well as group hunters and hunting success does not vary with group size (Packer et al., 1990; Scheel and Packer 1991). Instead, the benefits of group territoriality (e.g., cooperative offspring defense and resource defense) appear to outweigh the benefits of group hunting, indicating sociality in lions is likely driven by the benefits of group territoriality (Mosser and Packer 2009; Mosser et al., 2015). Akin to primates, lions live in large fission-fusion societies consisting of a permanent pride of females (up to 21 individuals) and an associated coalition of males (Mosser and Packer 2009; Packer, 1986). Similar to other species with complex social systems, lion sociality is characterized by a high degree of cooperation: lions cooperatively hunt (Packer and Pusey, 1997), cooperate to defend their territory against intruders (McComb et al., 1994; Heinsohn and Packer, 1995; Heinsohn et al., 1996; Grinnell 2002; Mosser and Packer 2009), and communally nurse their young (Packer and Pusey, 1994). A recent analysis of lion social networks reveals a high degree of cohesiveness and provides additional support for the presence of socially complex associations (Dunston et al., 2016). In contrast, leopards, tigers, and jaguars are asocial and associate only during mating and with dependent offspring (Mazak 1981; Schaller 1972; Seymore 1989). Thus, cognition in leopards and tigers evolved in the absence of social complexity; cognitive abilities exhibited by lions but absent in asocial big cats represent abilities that evolved after their evolutionary split and under the selective pressures of sociality.
3. Cognition in the only social felid: lions
2. Big cat biology 2.1. The ecology and distribution of big cats The big cat genus is a monophyletic group comprised of lions, leopards (Panthera pardus), tigers (Panthera tigris), and jaguars (Panthera onca). All four species contend with patchily distributed resources, the difficulties of prey capture, broad diets that require flexible hunting strategies, and kill prey in a similar manner (i.e., throat hold)(Karanth and Sunquist 2000; Mazak 1981; Schaller 1972). Lions, leopards, and tigers are sympatric in areas of Africa and Asia, with some prey preference overlap (Hayward et al., 2006; Hayward and Kerley, 2005, 2008). Leopards are the most widely distributed of the big cats and their range extends from South Africa, through the Middle East and Southeast Asia (Stein and Hayssen 2013). Historically, tigers inhabited much of Asia, including regions in southeastern Russia and the Sunda islands, but in the past century their populations have drastically declined (Mazak 1981). Lions occur throughout most of Africa (Hass et al., 2005), and until the early 1900s, were distributed across the Indian subcontinent but today are confined to the Gir Sanctuary of western Indian (Hass et al., 2005). Given the similarities in lions’, leopards’, and tigers’ ecology and geographical distribution, sociality is the primary differentiating factor in these species evolutionary history.
3.1. Cognitive demands of cooperative territorial and offspring defense; cognition and competition In contrast to species that live alone or in loose aggregations, socially complex animals form permanent associations defined by regular interaction among group members. Group living requires individuals to anticipate and appropriately respond to each other’s behavior, but appropriate behavioral responses can change as relationships change and often vary according to individuals (Humphrey, 1976). This dynamic nature of social relationships places selective pressure on animals’ ability to recognize individual conspecifics and relationships among conspecifics. For example, social animals benefit from the ability to recognize territorial neighbors (‘dear enemies’), distinguish group members from non-group members, recognize individuals according to individual-specific traits, and recognize individuals’ ranks within a dominance hierarchy (Tibbetts and Dale, 2007; Wiley, 2013). Accordingly, dolphins (Tursiops truncates) demonstrate decades long social memory of individuals (Bruck, 2013), African elephants (Loxodonta africana) distinguish between familiar and unfamiliar individuals and recognize individuals (Byrne et al., 2009; McComb et al., 2000), spotted hyenas (Crocuta crocuta) distinguish kin from non-kin and may recognize the identities and ranks of their clan mates (Engh et al., 2005; Holekamp et al., 2015; Holekamp et al., 2007), and many primates recognize individuals, understand the ranks of third parties relative
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to each other, and distinguish kin relationships (Barrett and Henzi 2005; Byrne and Bates 2010). Although lions are egalitarian and therefore do not face challenges associated with navigating strict dominance hierarchies, cooperation among group members under the context of intergroup aggression is a powerful force in lion sociality (Packer et al., 1990). Lions display sexually selected infanticide and nomadic coalitions of males attempt to oust coalitions resident with a pride. Following a successful takeover, the new coalition kills all dependent offspring sired by the ousted residents (Bertram 1975; Packer and Pusey 1983). Prides of females likewise must defend against infanticidal intruders and compete against other prides to hold territory (Mosser and Packer, 2009; VanderWaal et al. 2009). Lions’ reproductive success thus relies on coalitions’ and prides’ ability to successfully defend against rivals, and individuals benefit from cognitive abilities that facilitate territory maintenance and offspring defense (e.g., distinguishing group members from rivals). As in other species with complex social systems, lions demonstrate both an ability to categorize conspecifics and the ability to distinguish individuals according to individual-specific characteristics. Male lions distinguish between the roars of males and females, are capable of discriminating one from many roaring lions, and differentiate coalition members from non-coalition members (Grinnell, 1994, 2002; Grinnell and McComb, 1996). Female lions discriminate between resident and unfamiliar males (Heinsohn and Packer, 1995; Mccomb et al., 1993). Furthermore, female lions show persistent individual differences in their response to interpride conflict, with certain individuals consistently lagging behind and other individuals consistently leading, and during simulated territorial incursions, these leaders and laggards exhibit conditional cooperation and ‘score keeping’ (Heinsohn and Packer, 1995). Thus, lions recognize, remember, and conditionally interact with pride or coalition members and assess the risks/benefits of cooperating with different group members (Grinnell, 2002; Heinsohn and Packer, 1995). Lions also possess cognitive abilities associated with assessing fitness during affiliative and agonistic social interactions. Male lions’ mane size and color are highly variable, and range from short to long and from light blond to black. Longer, darker manes indicate maturity, high levels of testosterone, and good nutrition, whereas short, light manes reflect poor fighting ability and shortterm health (West and Packer, 2002). Distinguishing between dark and light maned males likely confers fitness advantages to females, and in contests between males, is a high visibility signal of opponent’s fighting ability. Accordingly, females distinguish between dark and light maned males and preferentially mate with dark maned males (West and Packer, 2002). Conversely, when male lions are presented with models of light and dark maned intruders, they preferentially engage the shorter, lighter maned model (West and Packer, 2002). Male and female lions possess cognitive abilities associated with assessing mane length and darkness, enabling females to gain healthy and more aggressive mates and males to lower the potential costs of fighting. Finally, social species encountering frequent intergroup conflict benefit from cognition related to ‘assessing the odds’ of winning an aggressive encounter (Mason et al., 1991). Game theory models predict that when fighting is costly, animals should assess the strength and relative numbers of potential opponents and the value of the resource, and withdraw without escalation when the odds are not in their favor (Maynard Smith 1982). Accordingly, lions (McComb et al., 1994), akin to chimpanzees (Pan trogrlodytes; Wilson et al., 2001), spotted hyenas (Benson-Amram et al., 2011), and free ranging dogs (Bonanni et al., 2011), are capable of ‘numerically assessing’ the odds during aggressive encounters and only engage when the odds are favorable or the resource value is high.
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3.2. Cognition and cooperative hunting The group hunting strategies of social carnivores are often cited as evidence of cognitive complexity in the forms of coordination and collaboration (Boesch and Boesch, 1989; Creel and Creel, 1995; Gazda et al., 2005; Stander, 1992a). Boesch and Boesch (1989) describe four types of cooperative behavior at increasing levels of cognitive complexity: similarity (similar actions), synchrony (relate actions in time to other’s actions), coordination (relate actions in time and space to other’s actions), and collaboration (perform different complementary actions). The first two cooperative types are the simplest and can be achieved by simply ‘acting apart together’ (Noë, 2006). Coordination and collaboration are arguably more complex and require an individual to take into account, and in some instances anticipate, the behavior of its companion(s), e.g., attend to the need for a partner (Drea and Carter, 2009; Plotnik et al., 2011). Coordination and collaboration have been reported in lions, chimpanzees, wild dogs, bottlenose dolphins, and spotted hyenas (Boesch, 2002; Drea and Carter, 2009; Estes and Goddard, 1967; Gazda et al., 2005; Stander, 1992a). Lions demonstrate coordination and collaboration in the form of role specialization. Role specialization is often cited as evidence of coordination and is presumed to occur whenever individuals consistently occupy the same role, e.g., flush left (Anderson and Franks, 2001). Lions show distinct preferences for hunting positions, individuals consistently occupy the same unique but complimentary roles, may take account of hunting partners’ behavior by compensating for variations in each others’ roles, and adjust their tactics in response to the presence, absence, and position of other individuals (Stander, 1992a; b). For example, a ‘wing’ lion initiates attack far more frequently than a ‘center’ lion (Stander, 1992a). Historically, coordination and collaboration were assumed to be widespread in group hunting species. However, not all hunts require coordination. Recent research suggests the extent of complex cooperative strategies varies among populations and may only occur under a limited set of circumstances. For example, though African wild dogs in East Africa often show highly coordinated hunting strategies when pursuing a single wildebeest or gazelle in open habitat (Fanshaw and Fitzgibbon, 1993), wild dogs in Botswana do not display complex cooperation. Instead, pack members in Botswana only hunt simultaneously not cooperatively, with each individual pursuing a separate impala on its own (Creel and Creel, 1995; Fanshaw and Fitzgibbon, 1993). Similarly, the evidence for coordination and collaboration in lions is restricted to a single population in Etosha National Park that specializes in difficult prey (Stander, 1992a,b), whereas other populations show little sign of cooperating above the levels of similarity and synchrony (Kitchen and Packer, 1999; Scheel and Packer, 1991). Thus, the most complex types of cooperative hunting are only found under particular circumstances, and future research should focus efforts on describing the extent of complex cooperation in lion populations outside of Etosha and identifying factors predicting cooperative complexity (Hubel et al., 2016a,b). 3.3. Social learning Cooperative species, like lions, benefit from social mechanisms that aid the transfer of information between group members (Bailey et al., 2012), and these benefits likely selected for cognitive abilities that facilitate these social mechanisms, like social learning. Social learning is broadly defined as, “any process through which one individual (‘the demonstrator’) influences the behavior of another individual (‘the observer’) in a manner that increases the probability that the observer learns” (Heyes, 1994; Hoppitt and Laland, 2008). Social learning occurs in several forms: from simple ‘local enhancement’, where individuals are attracted to a location where
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conspecifics are present (Galef, 1976), to ‘social facilitation’, in which the presence of conspecifics draws an observer’s attention to and enhances their ability to learn about an object (Zajonc, 1965), to the highly complex and contentious ‘imitation’, where an individual learns to do an act by seeing it done (Thorndike, 1898). Apes and cetaceans show evidence of imitation (Abramson et al., 2013; Caldwell and Whiten, 2002), and spotted hyenas, elephants (Loxodonta africana), and capuchin monkeys (Cebus paella) demonstrate social facilitation (Greco et al., 2013; Benson-Amram et al., 2014; Dindo et al., 2009). Similarly, lions demonstrate the cognitive abilities requisite for social facilitation; on a non-social task, the observation of a model increased lions’ motivation and reduced neophobia, potentially increasing problem solving success (Borrego and Dowling, 2016). Although, a formal investigation of social learning has not yet been completed, the complexity of lions’ social system and reliance on cooperation suggest the presence of social learning in this species. 4. Big cats as a comparative framework for the study of the evolution of intelligence 4.1. Learning and memory Compared to their asocial counterparts, selective pressure on social animals memory and learning systems may be two-fold. In addition to ecological pressures, which often require remembering the location of recourses, how to acquire resources, and learning to extract food from novel or difficult matrices, social animals are also faced with navigating social relationships that require constant monitoring, accurate prediction, and appropriately timed behavior (Byrne 1997; Byrne and Bates, 2006; Byrne and Whiten, 1988). Thus, the selective force of sociality may also operate on nonsocial domains, acting as an additional evolutionary stimulus to nonsocial cognitive abilities, e.g., learning and memory. Lions face selective pressures stemming from the need to remember social relationships as well as remember the locations of resources. Unsurprisingly, lions demonstrate impressive longterm memory and remember the solution to a novel problem for at least seven months (Borrego and Dowling, 2016). Although direct comparisons of learning and memory between lions, leopards and tigers have not yet been performed, comparisons between spotted hyenas (hierarchical social structure) and leopards (solitary) reveal that, in accordance with the domain general hypothesis, spotted hyenas outperform leopards on a task requiring learning and memory (Balme et al. unpublished data). In this study, we compared the behavioral responses of wild leopards and hyenas to foot snares and found that the rate of capture for hyenas significantly decreased, whereas leopard capture rates remained constant (Balme et al. unpublished data). Notably, leopards were always alone at snares, while the majority of hyenas appeared in groups. 4.2. Innovative problem solving Currently, the only direct comparison of cognition among big cats is an investigation of lions’, tigers’, and leopards’ ability to solve an innovative, novel problem, a puzzle-box (Borrego and Gaines, 2016). Puzzle-boxes are a standard method for testing cognition and are an effective means of testing innovation and other cognitive processes associated with problem-solving (reviewed by Griffin and Guez, 2014). Innovation can be defined as “a solution to a novel problem or a novel solution to an old problem”(Kummer and Goodall, 1985). Innovation is associated with cognitive complexity, and in primates, innovation is positively correlated with relative brain size (Lefebvre et al., 2004; Manrique et al., 2013; Sol et al., 2005). Innovation applies to non-social contexts and enables
animals to exploit novel resources, use existing resources more efficiently, expand their niche, and adapt to changing environments (Day et al., 2003; Huebner and Fichtel 2015; Lefebvre et al., 2004; Reader and Laland 2001). In accordance with the domain-general hypothesis, lions significantly outperformed their asocial counterparts (leopards and tigers) on the nonsocial task, indicating that sociality operates on the evolution of general cognition and not just cognition adapted to social domains.
5. Conclusions The evolution of cognitive complexity is itself complex and not attributable to a single selective force. Rather, complex cognition is likely driven by the interplay of social and ecological forces. Currently, carnivores, and big cats in particular, are vastly underrepresented in cognitive literature, despite being an ideal model system for tests of social and ecological intelligence hypotheses. The few comparative studies of carnivore cognition rely on broad-scale comparisons and indicate that cognition is not solely bolstered by sociality. For example, two studies that included several species of carnivores found social complexity was not associated with performance on tasks that required nonsocial cognitive abilities, i.e., problem solving and self control (Benson-Amram et al., 2016; Maclean et al., 2014). Further support for ecological complexity as a powerful force in cognitive evolution comes from studies evidencing advanced cognition in black bears (Ursus americanus), a species that faces complex ecological challenges but lacks social complexity (Vonk and Beran, 2012; Vonk et al., 2012; Zamisch and Vonk, 2012). Although these studies support ecological complexity as an equally powerful force in cognitive evolution, they do not address whether sociality operates on general or domain-specific cognition. Interestingly, when the scale of comparison is narrowed and restricted to closely related species that differ primarily in social complexity, social species outperform their asocial relatives on tasks that require nonsocial cognition. Lions outperform leopards and tigers on solving a puzzle-box task (Borrego and Gaines, 2016), spotted hyenas significantly outperform their solitary counter parts (Striped hyenas [Hyaena hyaena]) on the same puzzle-box task used in the study comparing 39 carnivores (Holekamp et al., 2015), and spotted hyenas outperform solitary leopards in a natural experiment requiring learned avoidance of an aversive stimulus (Balme et al. unpublished data). Thus, the sparse research that does exist supports a domain-general view of cognitive evolution. Social intelligence hypotheses were originally proposed to explain the remarkably advanced cognitive abilities of primates, focusing early efforts on an exclusively social taxon. Although, the past decade has seen a proliferation of research investigating cognition in social non-primates, studies maintain a narrow focus on exclusively social taxa or rely on proximate measures of cognition (de Waal and Ferrari, 2010; Vonk, 2016). It is only within the past few years that research has expanded to include experimental comparisons of cognition among socially diverse taxa (BensonAmram et al., 2016; Borrego and Gaines, 2016; Maclean et al., 2014). Most notably, the emergence of cognitive comparisons in the socially diverse but grossly understudied family: Carnivora. However, within Carnivora, cats remain an understudied system; many cat species have not been studied at all with regard to cognitive capacities, but see Vitale Shreve and Udell’s (2015) review of domestic cat (Felis catus) cognition. A comparison of lion, leopard, cheetah (Acinonyx jubatus), and cougar (Puma concolor) brain volume showed female lion anterior cerebrums (the area containing the frontal cortex) were larger than the other felid species and also larger than males of their own species, which further highlights the value of comparing cognition within Felidae, as these comparisons
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may reveal variations not detected on broader scales (Sakai et al., 2016). Continuing cognitive comparisons of big cats and including currently unrepresented felid species will enable research aimed directly at disentangling the role of social complexity from the role of ecological complexity in the evolution of intelligence.
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Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Big cats as a model system for the study of the evolution of intelligence Natalia Borrego a,b,∗ a b
Department of Life Sciences, University of Kwazulu-Natal, South Africa Lion Research Center, Department of Ecology, Evolution and Behavior, University of Minnesota, South Africa
a r t i c l e
i n f o
Article history: Received 15 October 2016 Received in revised form 11 February 2017 Accepted 15 March 2017 Available online 21 March 2017 Keywords: Panthera Social Intelligence Big cats Cognitive evolution Lions (Panthera Leo)
a b s t r a c t Currently, carnivores, and felids in particular, are vastly underrepresented in cognitive literature, despite being an ideal model system for tests of social and ecological intelligence hypotheses. Within Felidae, big cats (Panthera) are uniquely suited to studies investigating the evolutionary links between social, ecological, and cognitive complexity. Intelligence likely did not evolve in a unitary way but instead evolved as the result of mutually reinforcing feedback loops within the physical and social environments. The domain-specific social intelligence hypothesis proposes that social complexity drives only the evolution of cognitive abilities adapted only to social domains. The domain-general hypothesis proposes that the unique demands of social life serve as a bootstrap for the evolution of superior general cognition. Big cats are one of the few systems in which we can directly address conflicting predictions of the domain-general and domain-specific hypothesis by comparing cognition among closely related species that face roughly equivalent ecological complexity but vary considerably in social complexity © 2017 Elsevier B.V. All rights reserved.
Contents 1. 2.
3.
4.
5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261 Big cat biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262 2.1. The ecology and distribution of big cats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262 2.2. The evolution of sociality in lions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262 Cognition in the only social felid: lions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262 3.1. Cognitive demands of cooperative territorial and offspring defense; cognition and competition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262 3.2. Cognition and cooperative hunting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263 3.3. Social learning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263 Big cats as a comparative framework for the study of the evolution of intelligence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 4.1. Learning and memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 4.2. Innovative problem solving . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 265
1. Introduction Cognition can be broadly defined as, “all the ways in which animals take in information about the world through the senses, process, retain and decide to act on it” (Shettleworth 2001). Sev-
∗ Correspondence to: College of Life Sciences, University of Kwazulu-Natal, Westville Campus, Durban, 4041, South Africa. E-mail address: [email protected] http://dx.doi.org/10.1016/j.beproc.2017.03.010 0376-6357/© 2017 Elsevier B.V. All rights reserved.
eral hypotheses have been put forth to explain the evolution of complex cognition, i.e., intelligence. Ecological hypotheses propose that navigating physical/ecological environments selects for intelligence (reviewed by Dunbar 1998). Social intelligence and social brain hypotheses propose that intelligence evolves in response to the unique demands of navigating the complexities of social life (Byrne and Whiten, 1988; Dunbar, 1998; Humphrey, 1976; Jolly, 1966). Social and ecological intelligence hypotheses are not mutually exclusive; intelligence likely did not evolve in a unitary way but instead evolved as the result of mutually reinforcing feedback
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loops within the physical and social environments (Barrett et al., 2012; Barton, 2012). Disentangling the evolutionary connections among social, ecological, and cognitive complexity can be achieved through cognitive comparisons of ecologically diverse but socially similar taxa and comparisons of ecologically similar but socially diverse taxa. The genus Panthera (hereafter referred to as big cats) provides an ecologically equivalent but socially distinct comparative framework and is ideally suited to investigations of the link between social complexity and cognitive complexity. Currently, the literature is divided over the selective pressure sociality places on nonsocial cognition (e.g., cognitive abilities adapted to physical environments), resulting in disparate hypotheses. The domain-general social intelligence hypothesis proposes that sociality selects for overall cognitive complexity, including cognitive abilities adapted to nonsocial/physical environments and argues the unique selective pressures of social interactions serve as a bootstrap for the evolution of superior general cognition (Byrne and Whiten 1988). In contrast, the domain-specific social intelligence hypothesis proposes that sociality selects for only, or especially for, cognitive abilities adapted to social environments (Byrne and Whiten 1988). Proponents of this interpretation argue that, regardless of social complexity, species facing similar ecological complexity will not differ in cognition adapted to nonsocial realms. Big cats are one of the few systems in which we can directly address conflicting predictions by comparing cognition among closely related species that face roughly equivalent ecological complexity but vary considerably in social complexity. Yet, relative to other carnivores, big cats have been largely overlooked in comparative cognition research (Benson-Amram et al., 2016; Navarrete et al., 2016; Perez-Barberia et al., 2007). Here I review the relevant ecology and biology of big cats and the current literature on big cat cognition, with a focus on lions (Panthera leo), as lions are the most represented in the literature and our current understanding of big cat cognition is biased towards lions. I explore big cats’ suitability as a model system for comparisons aimed at gaining a more holistic understanding of the evolutionary mechanisms operating on cognition and resolving domain -specific and -general hypotheses.
2.2. The evolution of sociality in lions Big cats diverged from an asocial common ancestor roughly 6 MYA, and following the split, sociality evolved only in the lion lineage (Finarelli and Flynn 2009; Johnson et al., 2006; Nyakatura and Bininda-Emonds, 2012; Perez-Barberia et al., 2007). Originally, the evolution of sociality in lions was attributed to fitness payoffs associated with cooperative hunting. However, if the benefits of group hunting drove the evolution of sociality in lions, then compared to singletons, group-hunters should experience greater hunting success and higher food intake. Contrary to this prediction, lone lions perform as well as group hunters and hunting success does not vary with group size (Packer et al., 1990; Scheel and Packer 1991). Instead, the benefits of group territoriality (e.g., cooperative offspring defense and resource defense) appear to outweigh the benefits of group hunting, indicating sociality in lions is likely driven by the benefits of group territoriality (Mosser and Packer 2009; Mosser et al., 2015). Akin to primates, lions live in large fission-fusion societies consisting of a permanent pride of females (up to 21 individuals) and an associated coalition of males (Mosser and Packer 2009; Packer, 1986). Similar to other species with complex social systems, lion sociality is characterized by a high degree of cooperation: lions cooperatively hunt (Packer and Pusey, 1997), cooperate to defend their territory against intruders (McComb et al., 1994; Heinsohn and Packer, 1995; Heinsohn et al., 1996; Grinnell 2002; Mosser and Packer 2009), and communally nurse their young (Packer and Pusey, 1994). A recent analysis of lion social networks reveals a high degree of cohesiveness and provides additional support for the presence of socially complex associations (Dunston et al., 2016). In contrast, leopards, tigers, and jaguars are asocial and associate only during mating and with dependent offspring (Mazak 1981; Schaller 1972; Seymore 1989). Thus, cognition in leopards and tigers evolved in the absence of social complexity; cognitive abilities exhibited by lions but absent in asocial big cats represent abilities that evolved after their evolutionary split and under the selective pressures of sociality.
3. Cognition in the only social felid: lions
2. Big cat biology 2.1. The ecology and distribution of big cats The big cat genus is a monophyletic group comprised of lions, leopards (Panthera pardus), tigers (Panthera tigris), and jaguars (Panthera onca). All four species contend with patchily distributed resources, the difficulties of prey capture, broad diets that require flexible hunting strategies, and kill prey in a similar manner (i.e., throat hold)(Karanth and Sunquist 2000; Mazak 1981; Schaller 1972). Lions, leopards, and tigers are sympatric in areas of Africa and Asia, with some prey preference overlap (Hayward et al., 2006; Hayward and Kerley, 2005, 2008). Leopards are the most widely distributed of the big cats and their range extends from South Africa, through the Middle East and Southeast Asia (Stein and Hayssen 2013). Historically, tigers inhabited much of Asia, including regions in southeastern Russia and the Sunda islands, but in the past century their populations have drastically declined (Mazak 1981). Lions occur throughout most of Africa (Hass et al., 2005), and until the early 1900s, were distributed across the Indian subcontinent but today are confined to the Gir Sanctuary of western Indian (Hass et al., 2005). Given the similarities in lions’, leopards’, and tigers’ ecology and geographical distribution, sociality is the primary differentiating factor in these species evolutionary history.
3.1. Cognitive demands of cooperative territorial and offspring defense; cognition and competition In contrast to species that live alone or in loose aggregations, socially complex animals form permanent associations defined by regular interaction among group members. Group living requires individuals to anticipate and appropriately respond to each other’s behavior, but appropriate behavioral responses can change as relationships change and often vary according to individuals (Humphrey, 1976). This dynamic nature of social relationships places selective pressure on animals’ ability to recognize individual conspecifics and relationships among conspecifics. For example, social animals benefit from the ability to recognize territorial neighbors (‘dear enemies’), distinguish group members from non-group members, recognize individuals according to individual-specific traits, and recognize individuals’ ranks within a dominance hierarchy (Tibbetts and Dale, 2007; Wiley, 2013). Accordingly, dolphins (Tursiops truncates) demonstrate decades long social memory of individuals (Bruck, 2013), African elephants (Loxodonta africana) distinguish between familiar and unfamiliar individuals and recognize individuals (Byrne et al., 2009; McComb et al., 2000), spotted hyenas (Crocuta crocuta) distinguish kin from non-kin and may recognize the identities and ranks of their clan mates (Engh et al., 2005; Holekamp et al., 2015; Holekamp et al., 2007), and many primates recognize individuals, understand the ranks of third parties relative
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to each other, and distinguish kin relationships (Barrett and Henzi 2005; Byrne and Bates 2010). Although lions are egalitarian and therefore do not face challenges associated with navigating strict dominance hierarchies, cooperation among group members under the context of intergroup aggression is a powerful force in lion sociality (Packer et al., 1990). Lions display sexually selected infanticide and nomadic coalitions of males attempt to oust coalitions resident with a pride. Following a successful takeover, the new coalition kills all dependent offspring sired by the ousted residents (Bertram 1975; Packer and Pusey 1983). Prides of females likewise must defend against infanticidal intruders and compete against other prides to hold territory (Mosser and Packer, 2009; VanderWaal et al. 2009). Lions’ reproductive success thus relies on coalitions’ and prides’ ability to successfully defend against rivals, and individuals benefit from cognitive abilities that facilitate territory maintenance and offspring defense (e.g., distinguishing group members from rivals). As in other species with complex social systems, lions demonstrate both an ability to categorize conspecifics and the ability to distinguish individuals according to individual-specific characteristics. Male lions distinguish between the roars of males and females, are capable of discriminating one from many roaring lions, and differentiate coalition members from non-coalition members (Grinnell, 1994, 2002; Grinnell and McComb, 1996). Female lions discriminate between resident and unfamiliar males (Heinsohn and Packer, 1995; Mccomb et al., 1993). Furthermore, female lions show persistent individual differences in their response to interpride conflict, with certain individuals consistently lagging behind and other individuals consistently leading, and during simulated territorial incursions, these leaders and laggards exhibit conditional cooperation and ‘score keeping’ (Heinsohn and Packer, 1995). Thus, lions recognize, remember, and conditionally interact with pride or coalition members and assess the risks/benefits of cooperating with different group members (Grinnell, 2002; Heinsohn and Packer, 1995). Lions also possess cognitive abilities associated with assessing fitness during affiliative and agonistic social interactions. Male lions’ mane size and color are highly variable, and range from short to long and from light blond to black. Longer, darker manes indicate maturity, high levels of testosterone, and good nutrition, whereas short, light manes reflect poor fighting ability and shortterm health (West and Packer, 2002). Distinguishing between dark and light maned males likely confers fitness advantages to females, and in contests between males, is a high visibility signal of opponent’s fighting ability. Accordingly, females distinguish between dark and light maned males and preferentially mate with dark maned males (West and Packer, 2002). Conversely, when male lions are presented with models of light and dark maned intruders, they preferentially engage the shorter, lighter maned model (West and Packer, 2002). Male and female lions possess cognitive abilities associated with assessing mane length and darkness, enabling females to gain healthy and more aggressive mates and males to lower the potential costs of fighting. Finally, social species encountering frequent intergroup conflict benefit from cognition related to ‘assessing the odds’ of winning an aggressive encounter (Mason et al., 1991). Game theory models predict that when fighting is costly, animals should assess the strength and relative numbers of potential opponents and the value of the resource, and withdraw without escalation when the odds are not in their favor (Maynard Smith 1982). Accordingly, lions (McComb et al., 1994), akin to chimpanzees (Pan trogrlodytes; Wilson et al., 2001), spotted hyenas (Benson-Amram et al., 2011), and free ranging dogs (Bonanni et al., 2011), are capable of ‘numerically assessing’ the odds during aggressive encounters and only engage when the odds are favorable or the resource value is high.
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3.2. Cognition and cooperative hunting The group hunting strategies of social carnivores are often cited as evidence of cognitive complexity in the forms of coordination and collaboration (Boesch and Boesch, 1989; Creel and Creel, 1995; Gazda et al., 2005; Stander, 1992a). Boesch and Boesch (1989) describe four types of cooperative behavior at increasing levels of cognitive complexity: similarity (similar actions), synchrony (relate actions in time to other’s actions), coordination (relate actions in time and space to other’s actions), and collaboration (perform different complementary actions). The first two cooperative types are the simplest and can be achieved by simply ‘acting apart together’ (Noë, 2006). Coordination and collaboration are arguably more complex and require an individual to take into account, and in some instances anticipate, the behavior of its companion(s), e.g., attend to the need for a partner (Drea and Carter, 2009; Plotnik et al., 2011). Coordination and collaboration have been reported in lions, chimpanzees, wild dogs, bottlenose dolphins, and spotted hyenas (Boesch, 2002; Drea and Carter, 2009; Estes and Goddard, 1967; Gazda et al., 2005; Stander, 1992a). Lions demonstrate coordination and collaboration in the form of role specialization. Role specialization is often cited as evidence of coordination and is presumed to occur whenever individuals consistently occupy the same role, e.g., flush left (Anderson and Franks, 2001). Lions show distinct preferences for hunting positions, individuals consistently occupy the same unique but complimentary roles, may take account of hunting partners’ behavior by compensating for variations in each others’ roles, and adjust their tactics in response to the presence, absence, and position of other individuals (Stander, 1992a; b). For example, a ‘wing’ lion initiates attack far more frequently than a ‘center’ lion (Stander, 1992a). Historically, coordination and collaboration were assumed to be widespread in group hunting species. However, not all hunts require coordination. Recent research suggests the extent of complex cooperative strategies varies among populations and may only occur under a limited set of circumstances. For example, though African wild dogs in East Africa often show highly coordinated hunting strategies when pursuing a single wildebeest or gazelle in open habitat (Fanshaw and Fitzgibbon, 1993), wild dogs in Botswana do not display complex cooperation. Instead, pack members in Botswana only hunt simultaneously not cooperatively, with each individual pursuing a separate impala on its own (Creel and Creel, 1995; Fanshaw and Fitzgibbon, 1993). Similarly, the evidence for coordination and collaboration in lions is restricted to a single population in Etosha National Park that specializes in difficult prey (Stander, 1992a,b), whereas other populations show little sign of cooperating above the levels of similarity and synchrony (Kitchen and Packer, 1999; Scheel and Packer, 1991). Thus, the most complex types of cooperative hunting are only found under particular circumstances, and future research should focus efforts on describing the extent of complex cooperation in lion populations outside of Etosha and identifying factors predicting cooperative complexity (Hubel et al., 2016a,b). 3.3. Social learning Cooperative species, like lions, benefit from social mechanisms that aid the transfer of information between group members (Bailey et al., 2012), and these benefits likely selected for cognitive abilities that facilitate these social mechanisms, like social learning. Social learning is broadly defined as, “any process through which one individual (‘the demonstrator’) influences the behavior of another individual (‘the observer’) in a manner that increases the probability that the observer learns” (Heyes, 1994; Hoppitt and Laland, 2008). Social learning occurs in several forms: from simple ‘local enhancement’, where individuals are attracted to a location where
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conspecifics are present (Galef, 1976), to ‘social facilitation’, in which the presence of conspecifics draws an observer’s attention to and enhances their ability to learn about an object (Zajonc, 1965), to the highly complex and contentious ‘imitation’, where an individual learns to do an act by seeing it done (Thorndike, 1898). Apes and cetaceans show evidence of imitation (Abramson et al., 2013; Caldwell and Whiten, 2002), and spotted hyenas, elephants (Loxodonta africana), and capuchin monkeys (Cebus paella) demonstrate social facilitation (Greco et al., 2013; Benson-Amram et al., 2014; Dindo et al., 2009). Similarly, lions demonstrate the cognitive abilities requisite for social facilitation; on a non-social task, the observation of a model increased lions’ motivation and reduced neophobia, potentially increasing problem solving success (Borrego and Dowling, 2016). Although, a formal investigation of social learning has not yet been completed, the complexity of lions’ social system and reliance on cooperation suggest the presence of social learning in this species. 4. Big cats as a comparative framework for the study of the evolution of intelligence 4.1. Learning and memory Compared to their asocial counterparts, selective pressure on social animals memory and learning systems may be two-fold. In addition to ecological pressures, which often require remembering the location of recourses, how to acquire resources, and learning to extract food from novel or difficult matrices, social animals are also faced with navigating social relationships that require constant monitoring, accurate prediction, and appropriately timed behavior (Byrne 1997; Byrne and Bates, 2006; Byrne and Whiten, 1988). Thus, the selective force of sociality may also operate on nonsocial domains, acting as an additional evolutionary stimulus to nonsocial cognitive abilities, e.g., learning and memory. Lions face selective pressures stemming from the need to remember social relationships as well as remember the locations of resources. Unsurprisingly, lions demonstrate impressive longterm memory and remember the solution to a novel problem for at least seven months (Borrego and Dowling, 2016). Although direct comparisons of learning and memory between lions, leopards and tigers have not yet been performed, comparisons between spotted hyenas (hierarchical social structure) and leopards (solitary) reveal that, in accordance with the domain general hypothesis, spotted hyenas outperform leopards on a task requiring learning and memory (Balme et al. unpublished data). In this study, we compared the behavioral responses of wild leopards and hyenas to foot snares and found that the rate of capture for hyenas significantly decreased, whereas leopard capture rates remained constant (Balme et al. unpublished data). Notably, leopards were always alone at snares, while the majority of hyenas appeared in groups. 4.2. Innovative problem solving Currently, the only direct comparison of cognition among big cats is an investigation of lions’, tigers’, and leopards’ ability to solve an innovative, novel problem, a puzzle-box (Borrego and Gaines, 2016). Puzzle-boxes are a standard method for testing cognition and are an effective means of testing innovation and other cognitive processes associated with problem-solving (reviewed by Griffin and Guez, 2014). Innovation can be defined as “a solution to a novel problem or a novel solution to an old problem”(Kummer and Goodall, 1985). Innovation is associated with cognitive complexity, and in primates, innovation is positively correlated with relative brain size (Lefebvre et al., 2004; Manrique et al., 2013; Sol et al., 2005). Innovation applies to non-social contexts and enables
animals to exploit novel resources, use existing resources more efficiently, expand their niche, and adapt to changing environments (Day et al., 2003; Huebner and Fichtel 2015; Lefebvre et al., 2004; Reader and Laland 2001). In accordance with the domain-general hypothesis, lions significantly outperformed their asocial counterparts (leopards and tigers) on the nonsocial task, indicating that sociality operates on the evolution of general cognition and not just cognition adapted to social domains.
5. Conclusions The evolution of cognitive complexity is itself complex and not attributable to a single selective force. Rather, complex cognition is likely driven by the interplay of social and ecological forces. Currently, carnivores, and big cats in particular, are vastly underrepresented in cognitive literature, despite being an ideal model system for tests of social and ecological intelligence hypotheses. The few comparative studies of carnivore cognition rely on broad-scale comparisons and indicate that cognition is not solely bolstered by sociality. For example, two studies that included several species of carnivores found social complexity was not associated with performance on tasks that required nonsocial cognitive abilities, i.e., problem solving and self control (Benson-Amram et al., 2016; Maclean et al., 2014). Further support for ecological complexity as a powerful force in cognitive evolution comes from studies evidencing advanced cognition in black bears (Ursus americanus), a species that faces complex ecological challenges but lacks social complexity (Vonk and Beran, 2012; Vonk et al., 2012; Zamisch and Vonk, 2012). Although these studies support ecological complexity as an equally powerful force in cognitive evolution, they do not address whether sociality operates on general or domain-specific cognition. Interestingly, when the scale of comparison is narrowed and restricted to closely related species that differ primarily in social complexity, social species outperform their asocial relatives on tasks that require nonsocial cognition. Lions outperform leopards and tigers on solving a puzzle-box task (Borrego and Gaines, 2016), spotted hyenas significantly outperform their solitary counter parts (Striped hyenas [Hyaena hyaena]) on the same puzzle-box task used in the study comparing 39 carnivores (Holekamp et al., 2015), and spotted hyenas outperform solitary leopards in a natural experiment requiring learned avoidance of an aversive stimulus (Balme et al. unpublished data). Thus, the sparse research that does exist supports a domain-general view of cognitive evolution. Social intelligence hypotheses were originally proposed to explain the remarkably advanced cognitive abilities of primates, focusing early efforts on an exclusively social taxon. Although, the past decade has seen a proliferation of research investigating cognition in social non-primates, studies maintain a narrow focus on exclusively social taxa or rely on proximate measures of cognition (de Waal and Ferrari, 2010; Vonk, 2016). It is only within the past few years that research has expanded to include experimental comparisons of cognition among socially diverse taxa (BensonAmram et al., 2016; Borrego and Gaines, 2016; Maclean et al., 2014). Most notably, the emergence of cognitive comparisons in the socially diverse but grossly understudied family: Carnivora. However, within Carnivora, cats remain an understudied system; many cat species have not been studied at all with regard to cognitive capacities, but see Vitale Shreve and Udell’s (2015) review of domestic cat (Felis catus) cognition. A comparison of lion, leopard, cheetah (Acinonyx jubatus), and cougar (Puma concolor) brain volume showed female lion anterior cerebrums (the area containing the frontal cortex) were larger than the other felid species and also larger than males of their own species, which further highlights the value of comparing cognition within Felidae, as these comparisons
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may reveal variations not detected on broader scales (Sakai et al., 2016). Continuing cognitive comparisons of big cats and including currently unrepresented felid species will enable research aimed directly at disentangling the role of social complexity from the role of ecological complexity in the evolution of intelligence.
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