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A framework for studying social complexity

A framework for studying social complexity Social complexity has been one of the recent emerging topics in the study of animal and human societies, but the concept remains both poorly defined and understood. In this paper, I critically review definitions and studies of social complexity in invertebrate and vertebrate societies, arguing that the concept is being used inconsistently in studies of vertebrate sociality. Group size and cohesion define one cornerstone of social complexity, but the nature and patterning of social interactions contribute more to interspecific variation in social complexity in species with individual recognition and repeated interactions. Humans provide the only example where many other unique criteria are used, and they are the only species for which intraspecific variation in social complexity has been studied in detail. While there is agreement that complex patterns emerge at the group level as a result of simple interactions and as a result of cognitive abilities, there is consensus neither on their relative importance nor on the role of specific cognitive abilities in different lineages. Moreover, aspects of reproduction and parental care have also been invoked to characterize levels of social complexity, so that no single comprehensive measure is readily available. Because even fundamental components of social complexity are difficult to compare across studies and species because of inconsistent definitions and operationalization of key social traits, I define and characterize social organization, social structure, mating system, and care system as distinct components of a social system. Based on this framework, I outline how different aspects of the evolution of social complexity are being studied and suggest questions for future research. Significance statement Animal and human societies differ in social complexity, i.e., the number and association patterns of group members as well as the nature and patterning of their social relationships, but the dimensions of social complexity, the processes that generate it, the selective forces that engender different levels of social complexity, and the evolutionary consequences of this variation remain to be comprehensively understood. Here, I offer a conceptual framework for the systematic and comparative studies of social complexity by defining its main components as well as their proximate and ultimate relationships. . . . . . Keywords Social complexity Animal societies Social organization Social structure Behavior Evolution Introduction The systematic comparative study of animal societies over the last century (Espinas 1878; Deegener 1918; Allee 1927; Communicated by D. Lukas Wheeler 1928;Scott 1956;Crook 1970; Wilson 1971, 1975; This article is a contribution to the Topical Collection Social complexity: Smuts et al. 1987;Lee 1994; Clutton-Brock 2016; see also patterns, processes, and evolution - Guest Editors: Peter Kappeler, Rubenstein and Abbot 2017a) has revealed stunning interspe- Susanne Shultz, Tim Clutton-Brock, and Dieter Lukas cific diversity in the size, composition, and cohesion of social units, as well as in the patterning of reproductive skew, coop- * Peter M. Kappeler eration, and competition among their members. This diversity pkappel@gwdg.de has historically been perceived as reflecting a natural gradient Behavioral Ecology & Sociobiology Unit, German Primate Center, that has been expressed as either categorical or continuous Gottingen, Germany variation in social complexity (see below and Dew et al. Wissenschaftskolleg zu Berlin, Berlin, Germany 2016; Rubenstein et al. 2016). Even though understanding 13 Page 2 of 14 Behav Ecol Sociobiol (2019) 73:13 the causes and consequences of variation in social complexity forms. This terminology continues to be widely used by stu- is central to understanding the diversity and evolution of ani- dents of invertebrate societies, and it has recently been refined mal societies, social complexity remains both poorly charac- by recognizing the existence of casteless species, i.e., those terized and incompletely understood, however, and it has without lifetime commitment to queen-like or worker-like therefore been recently identified as one of the remaining roles despite the existence of skew in reproduction or frontiers in the study of animal behavior (Bradbury and alloparental care (Dew et al. 2016). Vehrencamp 2014). Among vertebrates, some obligate cooperative breeders, In this paper, I argue that inconsistent definitions of the which share the three defining traits with eusocial invertebrates features of social systems contributing to social complexity, (Sherman et al. 1995), have also been depicted as “highly so- a lack of relevant operational definitions applicable to a wide cial” (e.g., Bateman et al. 2012)oras representing “the highest range of species, variation in conceptual and methodological level of social complexity” (e.g., Fischer et al. 2017a), but it approaches used in the study of social insect and vertebrate remains unclear whether the presence or absence of cooperative societies, and lack of a general consensus on its key determi- breeding represents the only or only one important criterion for nants and consequences have hampered progress towards a this assessment. As a result, the distinction among cooperative better understanding of social complexity. Therefore, I offer breeding, eusociality, and social complexity has always been a conceptual framework for the systematic and comparative somewhat blurred. While one can see why some authors study- study of social complexity by defining its main components as ing vertebrates also emphasize cooperative breeding as a key well as their proximate and ultimate relationships. criterion for assessing the degree of social complexity to high- light similarities with social insects, different non-cooperative breeders have also been characterized as “highly social” (e.g., Patterns of social complexity and their Kelly and Goodson 2015; Markham et al. 2015; Reisinger et al. underlying processes 2017), often without an explanation for this classification. Only “communal breeding,” as originally defined for invertebrates Anyone staring at a busy ant colony, witnessing the versatile (Michener 1969), has been consistently used to classify verte- flight maneuvers of a flock of starlings or observing the man- brate societies (with respect to the number of co-breeding fe- ifold interactions among the members of a primate group, males: Brown 1978; Doody et al. 2009; Clutton-Brock 2016). must be impressed by the level of behavioral complexity ex- Last but not least, vertebrate social complexity has often been hibited by these and many other animal species. It is therefore operationalized as variation in group size (e.g., Dunbar and not surprising that the current literature on the study of animal Shultz 2007; Freeberg et al. 2012), whereas group size variation societies has increasingly included reference to their social has played a smaller role in studying insect social complexity complexity. However, researchers studying different taxa have (but see, e.g., Bourke 1999; Ferguson-Gow et al. 2014; been using different criteria and technical terms to define Feinerman and Traniello 2016). levels of social complexity (Rubenstein and Abbot 2017b), We therefore lack both a general concept of which features with a pronounced divide between studies of invertebrate of a social system contribute to social complexity, whether and and vertebrate societies (Rubenstein and Abbot 2017a). how they can be ranked in any meaningful way, and whether a Presumably, going back to the notion of a natural progres- single framework can accommodate studies of both inverte- sion of societies from simple to more complex ones first pro- brates and vertebrates. Additional interesting questions in this posed by Spencer (1895), classification of the social systems context address the processes, correlates, consequences, and of social insects has always invoked a gradient of increasing evolution of social complexity. I will address each of these social complexity (Wheeler 1910, 1928) based on the aspects below after outlining a general concept of social presence/absence of three key features. Species with overlap- complexity. ping generations, cooperative brood care, and reproductive division of labor, which not only are widespread among hy- Defining social complexity menoptera and termites but also found in beetles, aphids, thrips, and shrimp, have been defined as “eusocial” (Batra Very generally speaking, complexity is the opposite of sim- 1966) and are widely considered to represent the highest level plicity. A system is said to be complex if its parts are neither of sociality or social complexity. Species exhibiting various arranged completely randomly nor completely ordered. combinations of permutations of only one or two of these According to a very general definition, which also applies to traits have been classified as solitary, subsocial, communal, phenomena in physics or molecular biology, for example, quasi-, or semisocial, respectively (Michener 1969; Wilson “complex systems are made up of multiple parts that interact 1971; Crespi and Yanega 1995;reviewedinDew et al. in multiple ways, generating non-linear emergent effects that 2016; see also Costa and Fitzgerald 2005) and therefore as are greater than the sum of its parts” (wikipedia.org). These representing less socially complex or somehow less social aspects are also evident in a recent definition of social Behav Ecol Sociobiol (2019) 73:13 Page 3 of 14 13 complexity: “Complex social systems are those in which complexity that is independent of the emergent properties individuals frequently interact in many different contexts due to variation in group size alone (Dunbar and Shultz with many different individuals, and often repeatedly 2010). However, the complexity of social interactions is not interact with many of the same individuals over time” completely independent of group size because the number of (Freeberg et al. 2012). Thus, the number of individuals and individuals an animal can interact with increases linearly with their interactions represent two key components of social group size and because the number of all potential dyads complexity, so that a pair-living species with virtually no so- among group members increases exponentially with group cial interactions represents a baseline of social complexity size. When the same individuals interact repeatedly, the emer- (Dröscher and Kappeler 2013). gent properties of these repeated interactions can be described Because species in which adult individuals lead solitary as social relationships (Hinde 1976), which, in turn, can differ lives are typically not in the focus of studies of social com- in at least seven dimensions (frequency, diversity, symmetry, plexity, the “number of individuals aspect” usually refers to tenor, tension, predictability, and stability; Silk et al. 2013). the size of groups or other social units. Variation in group size Social complexity is also enhanced by interactions that in- is a key determinant of social complexity because it can affect volve more than two individuals simultaneously, creating, group cohesion, group composition (especially the adult sex for example, opportunities for audience effects (Zuberbühler ratio), association patterns, and reproductive skew, all of 2008), eavesdropping (Valone 2007) and coalitionary inter- which arguably contribute to social complexity. Specifically, vention (Harcourt and de Waal 1992). with increasing group size, there is more potential for a de- Social interactions and relationships contribute to more social crease in spatio-temporal cohesion, and thus an increasing complexity when interactions take multiple forms and occur in potential for fission-fusion dynamics (Aureli et al. 2008; different contexts, when individuals recognize each other, mem- Couzin and Laidre 2009), because more individuals have orize past interactions, have many opportunities to interact with more options for distributing themselves in space and time. the same individuals again in the future, and if they modify their Moreover, larger groups also have a greater potential for behavior in response to previous interactions (de Waal and multi-level structuring, i.e., the presence of multiple functional Tyack 2003). Variation in these aspects of social interactions subunits (Grueter et al. 2012) and patterns of spatial assort- depends foremost on the type of group, i.e., whether they are ment (Farine et al. 2017), whereas the potential for larger transient aggregations or permanent societies, as well as on changes in the adult sex ratio decreases with increasing group lineage-specific life history traits, especially longevity. These size (Kappeler 2017). Furthermore, larger groups in eusocial factors broadly explain, for example, why dolphins and ravens species are characterized by a reduction in workers’ reproduc- have richer and more diverse social interactions than herring or tive potential, the degree of caste determination, and the in- termites. Importantly, the patterning and nature of social inter- tensity of reproductive conflict (Bourke 1999). actions are functionally relevant because fitness of individuals in In terms of processes contributing to social complexity, group-living species depends in part on the outcome of their there is much interspecific variation in whether individuals interactions with other group members (Silk 2012), which is form groups or not, in the optimal size of groups, in how highly unpredictable because conspecifics differ in multiple in- stable and permanent groups are in space and time, in ternal and external states as well as in their social competence whether social units contain members of different (Taborsky and Oliveira 2012). Thus, variation not only in group generations, in whether males and females are permanently size but also in behavioral traits contributing to social complex- associated, and in the adult sex ratio of group members. ity has fitness consequences. Intraspecific variation in these traits has remained Whereas there is a broad consensus about the contribution understudied even though Lott (1991) highlighted its preva- of social interactions and relationships to social complexity, lence and significance decades ago. The various ultimate costs there is some controversy about the relative importance of and benefits modulating corresponding variation among spe- processes of self-organization in this context. This discussion cies have been relatively well studied by behavioral ecologists has two components. One is concerned with the question (Pulliam and Caraco 1984; van Schaik and Kappeler 1997; whether and to what extent processes of self-organization con- Conradt and Roper 2000; Krause and Ruxton 2002;Székely tribute to observed patterns of complexity in social structure. et al. 2014), however, and the proximate behavioral mecha- Self-organization is now recognized as an important determi- nisms generating this variation are largely studied as demo- nant of highly structured collective behavior not only in social graphic and life history variables, such as births, deaths, mat- insects (Bonabeau et al. 1997;Fewell 2015) but also in verte- uration, and dispersal events (Greenwood 1980;Geffenetal. brates on the move (Couzin and Krause 2003; Farine et al. 1996;Ancona etal. 2017). 2017), foraging behavior (Farine et al. 2014;Heet al. 2019), Even though quantity can have a quality all its own, it has dominance hierarchies, and other differentiated relationships long been recognized that the nature and patterning of social (Hemelrijk et al. 2008, 2017; Franz et al. 2015). Thus, simple interactions contributes a qualitative component to social 13 Page 4 of 14 Behav Ecol Sociobiol (2019) 73:13 behaviors at the individual or dyadic level can give rise to based on a given number of individuals and a given type of complex patterns at the group level. behavioral variable (Krause et al. 2007; Farine and Whitehead The more controversial component has to do with the pu- 2015; Kurvers et al. 2014; Weiss et al. 2019), but in most tative required cognitive underpinnings. The rich diversity of studies, only one behavioral variable has been included at a complex social relationships, particularly in primates and oth- time and, more importantly, the resulting network metrics er mammals, has been attributed to, or at least associated with, cannot easily be compared between groups of the same spe- enhanced brain size and special cognitive abilities, such as the cies, let alone across species. Dynamic (Farine 2018)and attribution of mental states to others (Seyfarth and Cheney multi-layer social networks (Boccaletti et al. 2014) may pro- 2015), according to some authors (e.g., de Waal and Tyack vide a promising future option for generating more compre- 2003;Sewall 2015; Platt et al. 2016), whereas others empha- hensive objective measures of social complexity, however. size the fact that complex patterns can be reproduced with Thus, at the moment, there is no single comprehensive mea- relatively simple models and, hence, without any special cog- sure or index of animal social complexity that can be used for nitive abilities (e.g., Barrett et al. 2007; Hemelrijk et al. 2017; meaningful interspecific comparisons or rankings. Kershenbaum and Blumstein 2017). This apparent controver- Humans provide an interesting exception in this context, sy might be resolved by more detailed and careful analysis of however, because they exhibit massive intraspecific variation which specific behavior patterns require which specific cog- in social complexity that has additionally also changed over nitive abilities. time. In the past, scholars in history, archeology, sociology, anthropology, and other related disciplines have used very Quantifying social complexity different and mostly single measures of social complexity (population size: Marquet et al. 2012; Vaesen et al. 2016; If it is interesting or meaningful for a specific question to group size: Derex et al. 2013; warfare: Turchin et al. 2013; compare levels of social complexity across species, we require connectedness of populations: Muthukrishna et al. 2013;age a scale that ideally integrates measures of both group size and structure: Lienard 2016). A recent multi-disciplinary collabo- relationship diversity. Most previous studies have focused on rative project that also included evolutionary biologists used a either one of these measures, however. Blumstein and list of 51 variables that reflect the size and hierarchical com- Armitage (1998) proposed an index of social complexity that plexity of social units along with some human-specific fea- integrated information on interspecific variation in the repre- tures, such as the information and monetary system (Turchin sentation of different age and sex classes. This index therefore et al. 2018). Surprisingly, a single principal component cap- included more information than group size alone, but it did not tured 77% of the variance among more than 400 societies account for social interactions. Avilés and Harwood (2012) from 30 regions around the world, indicating not only inter- esting functional relationships among these variables, but also proposed a continuous index of sociality based upon measures of philopatry, grouping tendencies, and the tendency of indi- that it should be possible to develop reliable measures of so- viduals to contribute to reproductive altruism. This index, cial complexity for animal societies with similar procedures as however, is only applicable to cooperative breeders because well. of its third component, which requires intraspecific variation in sociality (proportion of nest or colonies consisting of soli- Acentury of “social’ism” tary and multiple adult individuals). This sort of variation is rare or poorly documented in most animal lineages, and this Given these practical difficulties with developing a compre- index ignores sex differences in philopatry, which are hensive quantitative index of overall social complexity, a sys- common among vertebrates. tematic qualitative inventory of social and life history vari- Other measures of social complexity focused on social re- ables may provide a basis for a meaningful ranking and for lationships. Bergman and Beehner (2015) recommended that identifying key factors in different taxa. Most such existing social complexity should be measured as the number of dif- comparisons focused on particular lineages (e.g., Wilson ferentiated relationships that individuals have, where “differ- 1971; Smuts et al. 1987; Connor et al. 1998; de Waal and entiated relationships are those that can be distinguished by an Tyack 2003; Wolff and Sherman 2007), which has the advan- observer.” This proposal does not acknowledge variation in tage of controlling for variation in fundamental life history group size, however, and it may generate data that are difficult traits. Thus, comparisons of levels or categories of social com- to compare across taxa because of the unspecific nature of the plexity among mammals or among carnivores might be both operational recommendation, however. Fischer et al. (2017b) easier and more meaningful than comparisons across all ver- proposed a more specific procedure to quantify the diversity tebrates or animals. Only one recent research program offered of differentiated relationships among group members, but it a broad comparative perspective covering all main social lin- did not incorporate information on group size either. Finally, eages (Rubenstein and Abbot 2017c). Apart from many new social network analyses can generate a number of metrics insights about social evolution (Rubenstein and Abbot Behav Ecol Sociobiol (2019) 73:13 Page 5 of 14 13 2017b), this broad comparison also highlighted a key problem kin ties and reproduction. Espinas not only had a surprisingly of comparative studies: inconsistent definitions and profound modern understanding of animal societies given the operationalization of key social traits across studies hamper available information at the time, but he also distinguished both general and quantitative comparisons. between temporary and permanent groups, and, in discussing The arbitrary use of “social” in combination with various interspecific variation in their size and composition, consis- nouns lies at the heart of this problem. Social behavior, social tently used the term “organization” (e.g., on p. 491). He also structure, social organization, social system, social roles, so- noted variation among societies in their “complexité cial strategies, and several other similar terms have been and organique” and considered the social organization of mam- are being used to refer to both the same and very different mals to be “a little bit higher.” Paul Deegener (1918) also aspects of sociality in different studies. In particular, the two emphasized the difference between “accidental” and “essen- main components of social complexity—group size and com- tial” societies, but his complete classification scheme pro- position as well as patterns of social relationships—have both posed 92 categories of social organization (he only used the been referred to as social organization and social structure, term “Gesellschaften,” i.e., “societies”) expressed in unwieldy making it impossible to infer from the title of a study alone Greek terminology. which aspect was examined. Sometimes, these terms are even In the twentieth century, Wheeler (1910) provided the first used synonymously in the same paper (see, e.g., Nandini et al. comprehensive description of the “social habit” of ants and 2017 for a recent example) or to define each other (see, e.g., other insects, a term adopted by Allee (1927), who also McFarland 2014). This rampant “social’ism” creates at least discussed the evolutionary origins of “more advanced forms three fundamental problems. of social life.” Allee was mainly concerned with group size First, in contrast to say physicists, neurobiologists, or im- and composition and compared levels of complexity (“the munologists, which study clearly defined nuclear particles, highest type of social organization, such as occurs in ants brain regions, or molecular processes, respectively, as students and termites, ….”), but he also used “social structure” to refer of social behavior, we jeopardize our scientific reputation in to the same traits, in both cases without defining either term. In both the scientific community and the public at large because a later paper, Allee (1942) discussed data on dominance in we can apparently not agree on even the most fundamental birds and mice and used “group organization,”“social orga- definitions of our study objects. Second, the lack of a gener- nization,” and social structure to refer to the observed hierar- ally agreed upon vocabulary also hampers conceptual prog- chies. Similarly, Scott (1956) referred to the description of ress within our own discipline, where various formal and ver- basic patterns of social behavior and their organization into bal models (e.g., Nonacs and Hager 2011; Clutton-Brock and social relationships as the study of social organization. Janson 2012) have played important roles in guiding research, Influential early papers in behavioral ecology (e.g., Crook but different scholars use different terms for the same model 1970) also used social structure and social organization to components. Finally, a lack of consensus on how to label and refer to group size and composition as well as to define different features of a social system comes with the risk interindividual relations. It was not until Peter Jarman (1974) that variables with the same label (e.g., “monogamy”)may consistently referred to group size and composition as social contain different measures (in this example pair-living, pair- organization, and Robert Hinde (1976) provided a clear defi- bonding, genetic monogamy and solitary breeding; Kappeler nition of social structure, which he used consistently to refer to 2014; Tecot et al. 2016), leading to an enhanced risk for com- the emergent patterning of dyadic social relationships, that parative studies to reach different conclusions even though social terminology was used more carefully, however. they are based on the same primary studies (see, e.g., Lukas and Clutton-Brock 2013;Opieet al. 2013). I therefore think The components of social systems that there is an urgent need to agree upon commonly used definitions in the study of animal sociality. As in taxonomy, Based on the historical precedency of key terms discussed where different names were often proposed for the same spe- above, I advocate the consistent use of the following terms to cies by different authors, the principle of priority should also describe and study the components of the Social system of a provide objective guidance on the proper use of existing syn- species (see Fig. 1 and also Kappeler and Schaik 2002). Social onyms in the study of animal sociality. organization refers to the size and composition of a social unit. So, who introduced and defined the key terms characteriz- These are two demographic features that can simply be deter- ing a social system? The first comparative discussion and mined (assuming different age/sex classes are easily distinguish- classification of animal societies were conducted by Alfred able) without knowing or assuming anything about how these Espinas (1878), who distinguished between “accidental” and individuals interact with each other. In describing patterns of “normal” societies, of which he recognized two types (primi- social organization, it is necessary to identify these species- tive and advanced), and contrasted both of these with groups specific social units, such as solitary individuals, pairs, aggrega- (“peuplades”), which are, according to him, held together by tions, colonies, groups, or societies. A fundamental distinction 13 Page 6 of 14 Behav Ecol Sociobiol (2019) 73:13 Social system Care system Social organizaon Social structure Mang system Group size Social interacons Who mates? Group composion Who cares? Communicaon Who reproduces? Kinship paern Solitary Social relaonships Mang paern Parental care Pair living Social bonding Reproducve skew Allo-parental care Group living Singular vs. plural breeding Spaal variaon Dominance hierarchy Alternave reproducve Cooperave breeding Temporal variaon Communicave taccs Helper dynamics Sexual segregaon complexity Reproducve division of Caste polymorphism Adult sex rao Between-group relaons labor Fig. 1 A framework for the study of social systems and social that provide a general characterization of a given species. The bottom row complexity. The first row indicates the four core components of a social lists more specific aspects that contribute to social complexity. The system. The second row lists the main variables or questions addressed by differentiation between rows 2 and 3 is somewhat arbitrary, whereas the each component. The third row contains key features of a social system separation into different columns is not. See text for detailed explanation exists between solitary individuals and those that spend the ma- coalitions or redirected aggression, and agonistic interactions can jority of their activity period in association with at least one other be followed by post-conflict interactions, such as reconciliation adult conspecific. Non-solitary social units can be operationally or consolation, that enhance social complexity (Aureli et al. defined as “a set of animals that interact regularly and more so 2012). Because acts of intraspecific communication also repre- with each other than with members of other such groups” sent forms of social interaction, I consider communicative com- (Struhsaker 1969), where interaction in this context should refer plexity to constitute a core aspect of social structure (see also to association. Variation in spatial cohesion or temporal persis- Wilson 1971), rather than a separate entity being driven by social tence may make this task operationally challenging in some taxa, complexity (see below). An often neglected aspect of social however (e.g., Whitehead 2008; Schneider and Kappeler 2016). structure concerns relationships between neighboring social The smallest group size equals 2; the largest animal groups can units, which can vary massively in mutual tolerance (Willems include millions of individuals (Parrish and Edelstein-Keshet and van Schaik 2015). Matings and other sexual interactions are 1999). Group composition will typically refer to the sex and excluded from the set of social interactions as they define a age of group members, which are also often strong predictors distinct functional component of the social system. Social net- of kin relations. Additional aspects of the genetic structure of a work analyses and other methods provide modern quantitative social unit can be inferred from behavioral data (who disperses? measures of different dimensions of social structure, including Which sex is philopatric?), whereas more fine-grained descrip- their temporal dynamics (Krause et al. 2007; Neumann et al. tion of kinship patterns requires genetic analyses. 2011;Farine 2018) and the relative importance of direct and Social structure is defined by the content, quality, and pattern- indirect social relationships (Brent 2015). ing of social relationships emerging from repeated interactions Because mating interactions have direct fitness conse- between pairs of individuals belonging to the same social unit. In quences, and because there is no 1:1 relation between social species where individuals interact little, often in very similar organization and mating patterns (Kappeler and Schaik 2002; forms and in the same contexts, it is not possible to identify Rubenstein and Abbot 2017a), the Mating system represents a differentiated relationships because these species also typically distinct component of every social system. Studies of mating lack individual recognition. Social bonds represent a subset of systems can yield information on the identity and average differentiated relationships with particular characteristics (high number of mates of males and females. These data based on affiliation and low agonism) and often have functional impor- behavioral observations can be complemented with genetic tance (Silk 2012; Silk et al. 2013; Seyfarth and Cheney 2015). data to reveal who actually reproduced (i.e., who fertilized Dominance relationships develop as a result of repeated agonis- the eggs). The resulting emergent patterns at the level of the tic interactions and represent a functionally important aspect of social unit allow classification of species as monogamous, social structure because they regulate access to resources and polygynous, polyandrous, or polygynandrous (i.e., promiscu- mates in many species. In some species, dominance relationships ous), adjectives that should not be used to refer to types of social organization to acknowledge their conceptual may be established or stabilized by polyadic interactions, such as Behav Ecol Sociobiol (2019) 73:13 Page 7 of 14 13 separation. For most species, it will be easy to determine criterion, e.g., > 50, 67, or 75%, seems indicated to character- whether a single or multiple females breed and/or whether ize the modal social organization, mating, or care system. there is a reproductive division of labor. However, interindi- Species in which otherwise solitary individuals occur only vidual variation in mating and reproductive success often re- temporarily in association (Psorakis et al. 2015), individuals quire more detailed studies to determine patterns of male and associate during their period of inactivity and are solitary dur- female reproductive skew, Bateman gradients or the existence ing their period of activity or vice versa (Kappeler 2012), of alternative reproductive tactics. social organization changes seasonally (breeding pairs vs. Finally, because the categories of social systems defined by winter flocks in some songbirds, Aplin et al. 2015), or were specialists studying different taxa regularly also include as- males and females are segregated into different types of social pects of parental care (Rubenstein and Abbot 2017b), I pro- organization for most of the year (Ruckstuhl and Neuhaus pose the Care system as the fourth component of a social 2002; Wearmouth and Sims 2008) pose additional challenges system. By detailing who cares for dependent young, infor- for social taxonomy that still require a general consensus. The mation on either the absence of parental care or on maternal, framework outlined above may be useful for identifying and paternal, bi-parental, or allo-parental care can be provided. defining generally agreed upon criteria. This component will also specify the presence of cooperative breeding as well as caste polymorphism in species where they play a role. Together, these four components define the cor- The evolution of social complexity nerstones of a social system and provide a basis for the sys- tematic study of social complexity. Evolutionary questions about social complexity can be A final comment on practical difficulties with studying any grouped into at least four categories. The selective factors that or all components of a social system is indicated. These diffi- give rise to variation in traits that contribute to social complex- culties arise from the fact that any empirical study including ity have always been in the focus of behavioral ecologists. several social units is bound to find variation among them. More recently, a new line of research has begun to explore Thus, a key problem for making general statements about the genetic and other proximate mechanisms facilitating or “the social system of species x” as well as for extracting data accompanying evolutionary changes in social complexity. from primary studies for quantitative comparative studies is Another distinct set of questions deals with evolutionary tran- how to deal with intraspecific variation (see, e.g., Lukas and sitions in traits characterizing social complexity and their co- Clutton-Brock 2017; Schradin 2017). This variation exists evolution. Finally, a large body of literature has examined among neighboring social units, within social units over time, consequences and correlates of variation in social complexity and sometimes among different populations of a given spe- for other traits, especially brain size. cies. In cases where such variation is measured on a continu- ous scale, such as group size or grooming rates, the appropri- Variation in social systems ate descriptive statistic such as the median or the (weighted) mean can be reported and used, respectively. Repeated mea- First, the selective factors and evolutionary mechanisms giv- sures of the same social units over time, which are increasing- ing rise to variation in the core components of social systems ly available from long-term studies, require a justified criteri- have constituted areas of intensive research in behavioral ecol- on for non-independence so that data on group size, adult sex ogy from the beginning (Winn 1958; Klopfer 1962; Crook ratio, or the number of helpers, for example, can be used for 1964; Krebs and Davies 1981). Apart from general principles, determining the appropriate central tendencies. It will largely this line of research also revealed and emphasized taxon- depend on the species’ life history whether such repeated specific factors that influence the balance of the factors that measures will be statistically independent after a week, month, impact variation in the size, composition and spatio-temporal year, or even longer periods. stability of social units. The list of factors that determine In cases where intraspecific variation occurs on a categor- whether individuals of a given species live in groups or pairs, ical scale, classification can be more challenging. In classify- or not, is today basic textbook knowledge in behavioral ecol- ing a species as either group or pair living, for example, spe- ogy and does not require repetition here (Krause and Ruxton cies that switch between these two states from year to year 2002;Davies et al. 2012). Moreover, interspecific variation in (e.g., striped mice: Schradin 2013), have adjacent groups with social structure has been mainly studied in primates and other either social organization (callitrichids: Garber et al. 2016), or mammals, where the nature of food competition as well as exhibit other patterns of intraspecific variation (Lott 1991)are phylogenetic similarity have been identified as the most im- difficult to classify. A similar problem is often encountered in portant ultimate determinants of variation in social structure nominally pair-living species where a certain proportion of (Sterck et al. 1997; Clutton-Brock and Janson 2012). social units includes an additional adult male or female (e.g., Furthermore, the evolution of mating systems has also been Kappeler and Fichtel 2016). In those cases, a majority a classic topic for behavioral ecologists, who identified the 13 Page 8 of 14 Behav Ecol Sociobiol (2019) 73:13 distribution of receptive females in space and time as funda- beginning to be addressed in both vertebrates and with respect mental determinants of interspecific variation in mating sys- to physiological mechanisms as well (Rubenstein and tems (Emlen and Oring 1977; Greenwood 1980; Thornhill Hofmann 2015; Taborsky and Taborsky 2015). and Alcock 1983; Clutton-Brock 1989; Shuker and Simmons 2014). Which sex, if any, provides parental care is Evolutionary transitions broadly predicted by particular life history constraints defin- ing higher taxa, such as internal vs. external fertilization, Third, how social complexity has been modified across time ovipary vs. vivipary, litter or clutch size, or lactation, but eco- and taxa can be studied by various comparative approaches logical factors, adult sex ratios, and kinship play additional and methods. A fundamental question in all comparative anal- roles (Clutton-Brock 1991; Reynolds et al. 2002;Hughes yses concerns the degree to which a social trait is correlated to et al. 2008; Kokko and Jennions 2008; Gilbert and Manica phylogeny. Traits with relatively weak phylogenetic signal are 2015). Finally, whether allo-parents contribute care for depen- free to vary more in response to ecological and social factors, dent young has also been explained by a combination of life whereas strongly phylogenetically constrained traits might be history traits and ecological traits (Rubenstein and Lovette less flexible and therefore less likely to increase social com- 2007;Hatchwell 2009; Wong and Balshine 2011; plexity (Kappeler et al. 2013). Compared to morphological Cornwallis et al. 2010; Lukas and Clutton-Brock 2012; Shen and physiological traits, behavioral and social traits tend to et al. 2017). Any modern textbook on animal behavior attest exhibit relatively weak phylogenetic signal, however to the enormous progress made towards a detailed understand- (Blombergetal. 2003; Kamilar and Cooper 2013;Strier ing of the many causes of variation in social systems and, et al. 2014). Moreover, reconstructing the presence/absence hence, social complexity across species. of an aspect of social complexity on the phylogeny of a given lineage can reveal the directionality of evolutionary transitions Proximate underpinnings and therefore disclose whether social complexity increased (more easily) through certain stepping stones or whether Second, because social complexity evolves in the sense that it changes in any direction are possible at every speciation event. varies systematically among species and higher taxa, its con- Such recent analyses revealed, for example, that the evolution stituent components must have a genetic basis. A fairly recent of family-living in birds was a pivotal precondition for the line of research has therefore begun to illuminate the genomics subsequent evolution of cooperative breeding (under particu- of social evolution by examining the molecular changes ac- lar ecological conditions) (Griesser et al. 2017) and that euso- companying evolutionary transitions among different types of cial and communally breeding snapping shrimp evolved inde- social organizations (Robinson et al. 2005; Kapheim 2016, pendently from pair-living ancestors (Chak et al. 2017). 2019). Because an increasing amount of genomic information It is also possible to reconstruct the co-evolution of an has become available for hymenoptera and termites, the geno- aspect of social complexity and a life history or ecological mic sources of phenotypic social novelty have primarily been trait to identify preconditions for major shifts in social com- studied by comparing closely related solitary and eusocial plexity, and theoretical models can predict certain contingen- insect species (Korb et al. 2015; Kapheim 2016). The key cies in social evolution (e.g., Quiñones and Pen 2017)that can question in this context is whether the evolution of social be tested with such comparative studies. For example, in squa- complexity (or new types of social behavior) relies on genes mate reptiles, vivipary has been a crucial precursor in the with new functions, changes in gene regulation, or both evolution of permanent groups containing both adults and (Robinson and Ben-Shahar 2002). Comparative studies across juveniles (Halliwell et al. 2017), and in stingless bees, a dif- several solitary and eusocial insect species indicated that key ferentiated soldier caste evolved in association with the ap- changes in gene regulation may have evolved independently pearance of parasitic robber bees (Grüter et al. 2017). In hy- in ants and (honey) bees, whereas changes in gene function menoptera inhabiting an ecological gradient of habitats, eco- may have allowed for subsequent taxon-specific social and logical constraints and developmental rates were found to pre- ecological adaptations (Simola et al. 2013), but across bees, dict predominant types of social system at different elevations for example, there is no single road map to eusociality, i.e., (Kocher et al. 2014), indicating that different factors promote independent evolutionary transitions in social organization are the emergence of different aspects of social complexity in based on different genetic mechanisms (Kapheim et al. 2015). independent lineages and that we are nowhere near to having Interestingly, in bee species with greater social complexity, a complete list of relevant factors. many important genes show evidence of neutral evolution, A better understanding of the evolution of social complex- indicating relaxed selection. Integration of proposed mecha- ity can also be achieved by studying the co-evolution of dif- nisms at the genetic, developmental, and behavioral level that ferent components of social systems (Elgar 2015). accompany changes in social organization is now an exciting Correlations between group size and the size of a species’ vocal repertoire or other communication signals represent task for future research (Rehan and Toth 2015) and one that is Behav Ecol Sociobiol (2019) 73:13 Page 9 of 14 13 the most commonly studied research question in this context. indicates the existence of multiple mutual contingencies that For example, comparative analyses revealed that among deserve additional study in the future. halictid bees, eusocial species have more elaborate sensorial machinery linked to chemical communication than solitary species (Wittwer et al. 2017). There is also evidence suggest- So what? ing that odor profiles and other aspects of signal complexity may also be more elaborate in eusocial compared to solitary Finally, whereas social complexity poses many questions that species (Leonhardt et al. 2016; Wenseleers and Zweden make its study interesting in its own right, the question about 2017). Similar positive relationships between measures of so- its consequences addresses an important conceptual point, cial and communicative complexity have been reported for namely “Do species differences in social complexity actually birds(Kramsetal. 2012; Leighton 2017) and mammals matter?” Does the fact that we can rank species according to (Pollard and Blumstein 2012; Bouchet et al. 2013) and have different levels of social complexity explain or predict any- recently been reviewed elsewhere (Pollard and Blumstein thing interesting, or does it simply reflect a human tendency to 2012; Peckre et al. 2019, topical collection on Social classify, group and rank natural entities? A more cynical in- complexity; see also Pika 2017). terpretation holds that referring prominently to higher levels of sociality or social complexity may simply be part of a strategy to publish in high-profile journals. Co-evolution of social systems Two interesting consequences of social complexity have been proposed. First, relatively little attention has been given Other relationships between different components of a social to the notion that “the relationships that result from complex system are expected, suggesting they also co-evolve together social groups are thought to make possible pro-social behavior (see also Rubenstein 2012). For example, a given social orga- like cooperation and reciprocity” (Freeberg and Krams 2015). nization will predict the mating system to some extent—a This hypothesis assumes that communicative complexity in- baboon species living in bisexual groups of 50 individuals is creases with social complexity as well as cognitive processing unlikely to be monogamous, for example—and the reproduc- ability in the social domain, including contexts that require or tive consequences of living in single-male or multi-male facilitate cooperation. The specific examples presented in favor groups (Davies 2000) or in colonies of single or multiple of this hypothesis so far (Krams et al. 2012) refer to situations in queens (Keller 1995) have been studied in detail. However, which the recipient of a particular call can benefit from this because matings outside the social unit are widespread signal emitted by a group or flock member. More formal com- (Westneat and Stewart 2003; Cohas and Allainé 2009), intra- parative tests of this hypothesis might reveal whether the spec- specific variation in either or both components is common in ified links are robust in other taxa and modalities, potentially some lineages (Schradin 2013), and, because some species providing another example of how different components of so- change their social organization during the breeding season cial systems, in this case two components of social structure as (Wearmouth and Sims 2008), the two components should be defined and argued above, co-evolve. conceptually and terminologically separated. Furthermore, the Second, the most-studied correlate of social complexity to social organization may also predict the care system in some date is brain size. There are at least five hypotheses that link cases—pair-living species are more likely to exhibit bi- brain size with some aspect of sociality (Dunbar and Shultz parental care—and the mating system, especially the degree 2017), and all of them assume that the cognitive demands for of reproductive skew, may even predicate the type of parental managing and monitoring social relationships have selected for care, particularly the presence of paternal care (Kokko and an increase in the size of the brain or a particular part thereof. Jennions 2008), but there is no fixed 1:1 relationship between While most empirical studies testing these hypotheses have been these two components of a social system (e.g., paternal care is conducted with birds or mammals (Dunbar and Shultz 2007; absent in some pair-living species and present in some group- Isler and van Schaik 2009; Fox et al. 2017), similar relationships living species; e.g., Tecot et al. 2016). Moreover, interesting have now also been studied in some invertebrates, where results relationships between social structure and components of the have been inconsistent (Feinerman and Traniello 2016;Kamhi mating and care systems have been identified that correspond et al. 2016). These types of comparative studies have been crit- to variation in average levels of kinship among group mem- icized on a number of grounds, however (Healy and Rowe bers (Lukas and Clutton-Brock 2018). Finally, different com- 2007), and brain size variation has recently also been linked to ponents of one component of social systems, such as the dis- many other factors, including energy (Weisbecker et al. 2015), persal regime and grouping patterns, may also not vary inde- environmental change (Holekamp and Benson-Amram 2017), pendently (e.g., Strier et al. 2014), but such contingencies and diet (DeCasien et al. 2017). Because many of these studies remain poorly studied. Thus, the fact that the components of used group size as the main or only measure of social complex- ity, future studies using more specific measures of behavioral a social system do not vary arbitrarily at different levels 13 Page 10 of 14 Behav Ecol Sociobiol (2019) 73:13 Evolution,” which took place in Göttingen in December 2017, Claudia complexity and cognitive demands may eventually resolve this Fichtel for many discussions and Louise Peckre, Ferenc Jordán, Dieter question. Lukas, Phyllis Lee, and Dan Blumstein for excellent comments. I was a Thus, variation in social complexity matters for at least fellow at the Wissenschaftskolleg while this review was conceived. three reasons. First, it provides a framework for the compre- hensive and comparative study of sociality. The emergence of Compliance with ethical standards sociality represents one of the major transitions in evolution (Maynard Smith and Szathmary 1995), so that studying the Conflict of interest The author declares that he has no conflict of interest. evolution of social complexity allows identification of evolu- tionary principles and patterns, and by exploring the proxi- Open Access This article is distributed under the terms of the Creative mate underpinnings of social complexity, we can learn some- Commons Attribution 4.0 International License (http:// creativecommons.org/licenses/by/4.0/), which permits unrestricted use, thing about control and regulation of complex traits. Second, distribution, and reproduction in any medium, provided you give appro- understanding variation in brain size and the attendant cogni- priate credit to the original author(s) and the source, provide a link to the tive abilities are major questions in biology that cannot be Creative Commons license, and indicate if changes were made. answered by neuroscientists unfamiliar with the social context in which these traits function and evolve. Finally, species with greater social complexity are also ecologically more success- Publisher’sNote Springer Nature remains neutral with regard to juris- dictional claims in published maps and institutional affiliations. ful, as evidenced by termites, hymenoptera, and our own spe- cies, lending support to the notion that ecological and social adaptations are closely linked (see also Brooks et al. 2017; References Cornwallis et al. 2017). Allee WC (1927) Animal aggregations. 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Curr Biol 18:R189–R190 Evol 85:125–135 Weiss M, Franks DW, Croft DP, Whitehead H (2019) Measuring social complexity from association data using mixture models. Behav Ecol Sociobiol, https://doi.org/10.1007/s00265-018-2603-6 (this issue) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral Ecology and Sociobiology Springer Journals

A framework for studying social complexity

Behavioral Ecology and Sociobiology , Volume 73 (1) – Jan 19, 2019

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Springer Journals
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Copyright © 2019 by The Author(s)
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Life Sciences; Behavioral Sciences; Zoology; Animal Ecology
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0340-5443
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1432-0762
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10.1007/s00265-018-2601-8
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Abstract

Social complexity has been one of the recent emerging topics in the study of animal and human societies, but the concept remains both poorly defined and understood. In this paper, I critically review definitions and studies of social complexity in invertebrate and vertebrate societies, arguing that the concept is being used inconsistently in studies of vertebrate sociality. Group size and cohesion define one cornerstone of social complexity, but the nature and patterning of social interactions contribute more to interspecific variation in social complexity in species with individual recognition and repeated interactions. Humans provide the only example where many other unique criteria are used, and they are the only species for which intraspecific variation in social complexity has been studied in detail. While there is agreement that complex patterns emerge at the group level as a result of simple interactions and as a result of cognitive abilities, there is consensus neither on their relative importance nor on the role of specific cognitive abilities in different lineages. Moreover, aspects of reproduction and parental care have also been invoked to characterize levels of social complexity, so that no single comprehensive measure is readily available. Because even fundamental components of social complexity are difficult to compare across studies and species because of inconsistent definitions and operationalization of key social traits, I define and characterize social organization, social structure, mating system, and care system as distinct components of a social system. Based on this framework, I outline how different aspects of the evolution of social complexity are being studied and suggest questions for future research. Significance statement Animal and human societies differ in social complexity, i.e., the number and association patterns of group members as well as the nature and patterning of their social relationships, but the dimensions of social complexity, the processes that generate it, the selective forces that engender different levels of social complexity, and the evolutionary consequences of this variation remain to be comprehensively understood. Here, I offer a conceptual framework for the systematic and comparative studies of social complexity by defining its main components as well as their proximate and ultimate relationships. . . . . . Keywords Social complexity Animal societies Social organization Social structure Behavior Evolution Introduction The systematic comparative study of animal societies over the last century (Espinas 1878; Deegener 1918; Allee 1927; Communicated by D. Lukas Wheeler 1928;Scott 1956;Crook 1970; Wilson 1971, 1975; This article is a contribution to the Topical Collection Social complexity: Smuts et al. 1987;Lee 1994; Clutton-Brock 2016; see also patterns, processes, and evolution - Guest Editors: Peter Kappeler, Rubenstein and Abbot 2017a) has revealed stunning interspe- Susanne Shultz, Tim Clutton-Brock, and Dieter Lukas cific diversity in the size, composition, and cohesion of social units, as well as in the patterning of reproductive skew, coop- * Peter M. Kappeler eration, and competition among their members. This diversity pkappel@gwdg.de has historically been perceived as reflecting a natural gradient Behavioral Ecology & Sociobiology Unit, German Primate Center, that has been expressed as either categorical or continuous Gottingen, Germany variation in social complexity (see below and Dew et al. Wissenschaftskolleg zu Berlin, Berlin, Germany 2016; Rubenstein et al. 2016). Even though understanding 13 Page 2 of 14 Behav Ecol Sociobiol (2019) 73:13 the causes and consequences of variation in social complexity forms. This terminology continues to be widely used by stu- is central to understanding the diversity and evolution of ani- dents of invertebrate societies, and it has recently been refined mal societies, social complexity remains both poorly charac- by recognizing the existence of casteless species, i.e., those terized and incompletely understood, however, and it has without lifetime commitment to queen-like or worker-like therefore been recently identified as one of the remaining roles despite the existence of skew in reproduction or frontiers in the study of animal behavior (Bradbury and alloparental care (Dew et al. 2016). Vehrencamp 2014). Among vertebrates, some obligate cooperative breeders, In this paper, I argue that inconsistent definitions of the which share the three defining traits with eusocial invertebrates features of social systems contributing to social complexity, (Sherman et al. 1995), have also been depicted as “highly so- a lack of relevant operational definitions applicable to a wide cial” (e.g., Bateman et al. 2012)oras representing “the highest range of species, variation in conceptual and methodological level of social complexity” (e.g., Fischer et al. 2017a), but it approaches used in the study of social insect and vertebrate remains unclear whether the presence or absence of cooperative societies, and lack of a general consensus on its key determi- breeding represents the only or only one important criterion for nants and consequences have hampered progress towards a this assessment. As a result, the distinction among cooperative better understanding of social complexity. Therefore, I offer breeding, eusociality, and social complexity has always been a conceptual framework for the systematic and comparative somewhat blurred. While one can see why some authors study- study of social complexity by defining its main components as ing vertebrates also emphasize cooperative breeding as a key well as their proximate and ultimate relationships. criterion for assessing the degree of social complexity to high- light similarities with social insects, different non-cooperative breeders have also been characterized as “highly social” (e.g., Patterns of social complexity and their Kelly and Goodson 2015; Markham et al. 2015; Reisinger et al. underlying processes 2017), often without an explanation for this classification. Only “communal breeding,” as originally defined for invertebrates Anyone staring at a busy ant colony, witnessing the versatile (Michener 1969), has been consistently used to classify verte- flight maneuvers of a flock of starlings or observing the man- brate societies (with respect to the number of co-breeding fe- ifold interactions among the members of a primate group, males: Brown 1978; Doody et al. 2009; Clutton-Brock 2016). must be impressed by the level of behavioral complexity ex- Last but not least, vertebrate social complexity has often been hibited by these and many other animal species. It is therefore operationalized as variation in group size (e.g., Dunbar and not surprising that the current literature on the study of animal Shultz 2007; Freeberg et al. 2012), whereas group size variation societies has increasingly included reference to their social has played a smaller role in studying insect social complexity complexity. However, researchers studying different taxa have (but see, e.g., Bourke 1999; Ferguson-Gow et al. 2014; been using different criteria and technical terms to define Feinerman and Traniello 2016). levels of social complexity (Rubenstein and Abbot 2017b), We therefore lack both a general concept of which features with a pronounced divide between studies of invertebrate of a social system contribute to social complexity, whether and and vertebrate societies (Rubenstein and Abbot 2017a). how they can be ranked in any meaningful way, and whether a Presumably, going back to the notion of a natural progres- single framework can accommodate studies of both inverte- sion of societies from simple to more complex ones first pro- brates and vertebrates. Additional interesting questions in this posed by Spencer (1895), classification of the social systems context address the processes, correlates, consequences, and of social insects has always invoked a gradient of increasing evolution of social complexity. I will address each of these social complexity (Wheeler 1910, 1928) based on the aspects below after outlining a general concept of social presence/absence of three key features. Species with overlap- complexity. ping generations, cooperative brood care, and reproductive division of labor, which not only are widespread among hy- Defining social complexity menoptera and termites but also found in beetles, aphids, thrips, and shrimp, have been defined as “eusocial” (Batra Very generally speaking, complexity is the opposite of sim- 1966) and are widely considered to represent the highest level plicity. A system is said to be complex if its parts are neither of sociality or social complexity. Species exhibiting various arranged completely randomly nor completely ordered. combinations of permutations of only one or two of these According to a very general definition, which also applies to traits have been classified as solitary, subsocial, communal, phenomena in physics or molecular biology, for example, quasi-, or semisocial, respectively (Michener 1969; Wilson “complex systems are made up of multiple parts that interact 1971; Crespi and Yanega 1995;reviewedinDew et al. in multiple ways, generating non-linear emergent effects that 2016; see also Costa and Fitzgerald 2005) and therefore as are greater than the sum of its parts” (wikipedia.org). These representing less socially complex or somehow less social aspects are also evident in a recent definition of social Behav Ecol Sociobiol (2019) 73:13 Page 3 of 14 13 complexity: “Complex social systems are those in which complexity that is independent of the emergent properties individuals frequently interact in many different contexts due to variation in group size alone (Dunbar and Shultz with many different individuals, and often repeatedly 2010). However, the complexity of social interactions is not interact with many of the same individuals over time” completely independent of group size because the number of (Freeberg et al. 2012). Thus, the number of individuals and individuals an animal can interact with increases linearly with their interactions represent two key components of social group size and because the number of all potential dyads complexity, so that a pair-living species with virtually no so- among group members increases exponentially with group cial interactions represents a baseline of social complexity size. When the same individuals interact repeatedly, the emer- (Dröscher and Kappeler 2013). gent properties of these repeated interactions can be described Because species in which adult individuals lead solitary as social relationships (Hinde 1976), which, in turn, can differ lives are typically not in the focus of studies of social com- in at least seven dimensions (frequency, diversity, symmetry, plexity, the “number of individuals aspect” usually refers to tenor, tension, predictability, and stability; Silk et al. 2013). the size of groups or other social units. Variation in group size Social complexity is also enhanced by interactions that in- is a key determinant of social complexity because it can affect volve more than two individuals simultaneously, creating, group cohesion, group composition (especially the adult sex for example, opportunities for audience effects (Zuberbühler ratio), association patterns, and reproductive skew, all of 2008), eavesdropping (Valone 2007) and coalitionary inter- which arguably contribute to social complexity. Specifically, vention (Harcourt and de Waal 1992). with increasing group size, there is more potential for a de- Social interactions and relationships contribute to more social crease in spatio-temporal cohesion, and thus an increasing complexity when interactions take multiple forms and occur in potential for fission-fusion dynamics (Aureli et al. 2008; different contexts, when individuals recognize each other, mem- Couzin and Laidre 2009), because more individuals have orize past interactions, have many opportunities to interact with more options for distributing themselves in space and time. the same individuals again in the future, and if they modify their Moreover, larger groups also have a greater potential for behavior in response to previous interactions (de Waal and multi-level structuring, i.e., the presence of multiple functional Tyack 2003). Variation in these aspects of social interactions subunits (Grueter et al. 2012) and patterns of spatial assort- depends foremost on the type of group, i.e., whether they are ment (Farine et al. 2017), whereas the potential for larger transient aggregations or permanent societies, as well as on changes in the adult sex ratio decreases with increasing group lineage-specific life history traits, especially longevity. These size (Kappeler 2017). Furthermore, larger groups in eusocial factors broadly explain, for example, why dolphins and ravens species are characterized by a reduction in workers’ reproduc- have richer and more diverse social interactions than herring or tive potential, the degree of caste determination, and the in- termites. Importantly, the patterning and nature of social inter- tensity of reproductive conflict (Bourke 1999). actions are functionally relevant because fitness of individuals in In terms of processes contributing to social complexity, group-living species depends in part on the outcome of their there is much interspecific variation in whether individuals interactions with other group members (Silk 2012), which is form groups or not, in the optimal size of groups, in how highly unpredictable because conspecifics differ in multiple in- stable and permanent groups are in space and time, in ternal and external states as well as in their social competence whether social units contain members of different (Taborsky and Oliveira 2012). Thus, variation not only in group generations, in whether males and females are permanently size but also in behavioral traits contributing to social complex- associated, and in the adult sex ratio of group members. ity has fitness consequences. Intraspecific variation in these traits has remained Whereas there is a broad consensus about the contribution understudied even though Lott (1991) highlighted its preva- of social interactions and relationships to social complexity, lence and significance decades ago. The various ultimate costs there is some controversy about the relative importance of and benefits modulating corresponding variation among spe- processes of self-organization in this context. This discussion cies have been relatively well studied by behavioral ecologists has two components. One is concerned with the question (Pulliam and Caraco 1984; van Schaik and Kappeler 1997; whether and to what extent processes of self-organization con- Conradt and Roper 2000; Krause and Ruxton 2002;Székely tribute to observed patterns of complexity in social structure. et al. 2014), however, and the proximate behavioral mecha- Self-organization is now recognized as an important determi- nisms generating this variation are largely studied as demo- nant of highly structured collective behavior not only in social graphic and life history variables, such as births, deaths, mat- insects (Bonabeau et al. 1997;Fewell 2015) but also in verte- uration, and dispersal events (Greenwood 1980;Geffenetal. brates on the move (Couzin and Krause 2003; Farine et al. 1996;Ancona etal. 2017). 2017), foraging behavior (Farine et al. 2014;Heet al. 2019), Even though quantity can have a quality all its own, it has dominance hierarchies, and other differentiated relationships long been recognized that the nature and patterning of social (Hemelrijk et al. 2008, 2017; Franz et al. 2015). Thus, simple interactions contributes a qualitative component to social 13 Page 4 of 14 Behav Ecol Sociobiol (2019) 73:13 behaviors at the individual or dyadic level can give rise to based on a given number of individuals and a given type of complex patterns at the group level. behavioral variable (Krause et al. 2007; Farine and Whitehead The more controversial component has to do with the pu- 2015; Kurvers et al. 2014; Weiss et al. 2019), but in most tative required cognitive underpinnings. The rich diversity of studies, only one behavioral variable has been included at a complex social relationships, particularly in primates and oth- time and, more importantly, the resulting network metrics er mammals, has been attributed to, or at least associated with, cannot easily be compared between groups of the same spe- enhanced brain size and special cognitive abilities, such as the cies, let alone across species. Dynamic (Farine 2018)and attribution of mental states to others (Seyfarth and Cheney multi-layer social networks (Boccaletti et al. 2014) may pro- 2015), according to some authors (e.g., de Waal and Tyack vide a promising future option for generating more compre- 2003;Sewall 2015; Platt et al. 2016), whereas others empha- hensive objective measures of social complexity, however. size the fact that complex patterns can be reproduced with Thus, at the moment, there is no single comprehensive mea- relatively simple models and, hence, without any special cog- sure or index of animal social complexity that can be used for nitive abilities (e.g., Barrett et al. 2007; Hemelrijk et al. 2017; meaningful interspecific comparisons or rankings. Kershenbaum and Blumstein 2017). This apparent controver- Humans provide an interesting exception in this context, sy might be resolved by more detailed and careful analysis of however, because they exhibit massive intraspecific variation which specific behavior patterns require which specific cog- in social complexity that has additionally also changed over nitive abilities. time. In the past, scholars in history, archeology, sociology, anthropology, and other related disciplines have used very Quantifying social complexity different and mostly single measures of social complexity (population size: Marquet et al. 2012; Vaesen et al. 2016; If it is interesting or meaningful for a specific question to group size: Derex et al. 2013; warfare: Turchin et al. 2013; compare levels of social complexity across species, we require connectedness of populations: Muthukrishna et al. 2013;age a scale that ideally integrates measures of both group size and structure: Lienard 2016). A recent multi-disciplinary collabo- relationship diversity. Most previous studies have focused on rative project that also included evolutionary biologists used a either one of these measures, however. Blumstein and list of 51 variables that reflect the size and hierarchical com- Armitage (1998) proposed an index of social complexity that plexity of social units along with some human-specific fea- integrated information on interspecific variation in the repre- tures, such as the information and monetary system (Turchin sentation of different age and sex classes. This index therefore et al. 2018). Surprisingly, a single principal component cap- included more information than group size alone, but it did not tured 77% of the variance among more than 400 societies account for social interactions. Avilés and Harwood (2012) from 30 regions around the world, indicating not only inter- esting functional relationships among these variables, but also proposed a continuous index of sociality based upon measures of philopatry, grouping tendencies, and the tendency of indi- that it should be possible to develop reliable measures of so- viduals to contribute to reproductive altruism. This index, cial complexity for animal societies with similar procedures as however, is only applicable to cooperative breeders because well. of its third component, which requires intraspecific variation in sociality (proportion of nest or colonies consisting of soli- Acentury of “social’ism” tary and multiple adult individuals). This sort of variation is rare or poorly documented in most animal lineages, and this Given these practical difficulties with developing a compre- index ignores sex differences in philopatry, which are hensive quantitative index of overall social complexity, a sys- common among vertebrates. tematic qualitative inventory of social and life history vari- Other measures of social complexity focused on social re- ables may provide a basis for a meaningful ranking and for lationships. Bergman and Beehner (2015) recommended that identifying key factors in different taxa. Most such existing social complexity should be measured as the number of dif- comparisons focused on particular lineages (e.g., Wilson ferentiated relationships that individuals have, where “differ- 1971; Smuts et al. 1987; Connor et al. 1998; de Waal and entiated relationships are those that can be distinguished by an Tyack 2003; Wolff and Sherman 2007), which has the advan- observer.” This proposal does not acknowledge variation in tage of controlling for variation in fundamental life history group size, however, and it may generate data that are difficult traits. Thus, comparisons of levels or categories of social com- to compare across taxa because of the unspecific nature of the plexity among mammals or among carnivores might be both operational recommendation, however. Fischer et al. (2017b) easier and more meaningful than comparisons across all ver- proposed a more specific procedure to quantify the diversity tebrates or animals. Only one recent research program offered of differentiated relationships among group members, but it a broad comparative perspective covering all main social lin- did not incorporate information on group size either. Finally, eages (Rubenstein and Abbot 2017c). Apart from many new social network analyses can generate a number of metrics insights about social evolution (Rubenstein and Abbot Behav Ecol Sociobiol (2019) 73:13 Page 5 of 14 13 2017b), this broad comparison also highlighted a key problem kin ties and reproduction. Espinas not only had a surprisingly of comparative studies: inconsistent definitions and profound modern understanding of animal societies given the operationalization of key social traits across studies hamper available information at the time, but he also distinguished both general and quantitative comparisons. between temporary and permanent groups, and, in discussing The arbitrary use of “social” in combination with various interspecific variation in their size and composition, consis- nouns lies at the heart of this problem. Social behavior, social tently used the term “organization” (e.g., on p. 491). He also structure, social organization, social system, social roles, so- noted variation among societies in their “complexité cial strategies, and several other similar terms have been and organique” and considered the social organization of mam- are being used to refer to both the same and very different mals to be “a little bit higher.” Paul Deegener (1918) also aspects of sociality in different studies. In particular, the two emphasized the difference between “accidental” and “essen- main components of social complexity—group size and com- tial” societies, but his complete classification scheme pro- position as well as patterns of social relationships—have both posed 92 categories of social organization (he only used the been referred to as social organization and social structure, term “Gesellschaften,” i.e., “societies”) expressed in unwieldy making it impossible to infer from the title of a study alone Greek terminology. which aspect was examined. Sometimes, these terms are even In the twentieth century, Wheeler (1910) provided the first used synonymously in the same paper (see, e.g., Nandini et al. comprehensive description of the “social habit” of ants and 2017 for a recent example) or to define each other (see, e.g., other insects, a term adopted by Allee (1927), who also McFarland 2014). This rampant “social’ism” creates at least discussed the evolutionary origins of “more advanced forms three fundamental problems. of social life.” Allee was mainly concerned with group size First, in contrast to say physicists, neurobiologists, or im- and composition and compared levels of complexity (“the munologists, which study clearly defined nuclear particles, highest type of social organization, such as occurs in ants brain regions, or molecular processes, respectively, as students and termites, ….”), but he also used “social structure” to refer of social behavior, we jeopardize our scientific reputation in to the same traits, in both cases without defining either term. In both the scientific community and the public at large because a later paper, Allee (1942) discussed data on dominance in we can apparently not agree on even the most fundamental birds and mice and used “group organization,”“social orga- definitions of our study objects. Second, the lack of a gener- nization,” and social structure to refer to the observed hierar- ally agreed upon vocabulary also hampers conceptual prog- chies. Similarly, Scott (1956) referred to the description of ress within our own discipline, where various formal and ver- basic patterns of social behavior and their organization into bal models (e.g., Nonacs and Hager 2011; Clutton-Brock and social relationships as the study of social organization. Janson 2012) have played important roles in guiding research, Influential early papers in behavioral ecology (e.g., Crook but different scholars use different terms for the same model 1970) also used social structure and social organization to components. Finally, a lack of consensus on how to label and refer to group size and composition as well as to define different features of a social system comes with the risk interindividual relations. It was not until Peter Jarman (1974) that variables with the same label (e.g., “monogamy”)may consistently referred to group size and composition as social contain different measures (in this example pair-living, pair- organization, and Robert Hinde (1976) provided a clear defi- bonding, genetic monogamy and solitary breeding; Kappeler nition of social structure, which he used consistently to refer to 2014; Tecot et al. 2016), leading to an enhanced risk for com- the emergent patterning of dyadic social relationships, that parative studies to reach different conclusions even though social terminology was used more carefully, however. they are based on the same primary studies (see, e.g., Lukas and Clutton-Brock 2013;Opieet al. 2013). I therefore think The components of social systems that there is an urgent need to agree upon commonly used definitions in the study of animal sociality. As in taxonomy, Based on the historical precedency of key terms discussed where different names were often proposed for the same spe- above, I advocate the consistent use of the following terms to cies by different authors, the principle of priority should also describe and study the components of the Social system of a provide objective guidance on the proper use of existing syn- species (see Fig. 1 and also Kappeler and Schaik 2002). Social onyms in the study of animal sociality. organization refers to the size and composition of a social unit. So, who introduced and defined the key terms characteriz- These are two demographic features that can simply be deter- ing a social system? The first comparative discussion and mined (assuming different age/sex classes are easily distinguish- classification of animal societies were conducted by Alfred able) without knowing or assuming anything about how these Espinas (1878), who distinguished between “accidental” and individuals interact with each other. In describing patterns of “normal” societies, of which he recognized two types (primi- social organization, it is necessary to identify these species- tive and advanced), and contrasted both of these with groups specific social units, such as solitary individuals, pairs, aggrega- (“peuplades”), which are, according to him, held together by tions, colonies, groups, or societies. A fundamental distinction 13 Page 6 of 14 Behav Ecol Sociobiol (2019) 73:13 Social system Care system Social organizaon Social structure Mang system Group size Social interacons Who mates? Group composion Who cares? Communicaon Who reproduces? Kinship paern Solitary Social relaonships Mang paern Parental care Pair living Social bonding Reproducve skew Allo-parental care Group living Singular vs. plural breeding Spaal variaon Dominance hierarchy Alternave reproducve Cooperave breeding Temporal variaon Communicave taccs Helper dynamics Sexual segregaon complexity Reproducve division of Caste polymorphism Adult sex rao Between-group relaons labor Fig. 1 A framework for the study of social systems and social that provide a general characterization of a given species. The bottom row complexity. The first row indicates the four core components of a social lists more specific aspects that contribute to social complexity. The system. The second row lists the main variables or questions addressed by differentiation between rows 2 and 3 is somewhat arbitrary, whereas the each component. The third row contains key features of a social system separation into different columns is not. See text for detailed explanation exists between solitary individuals and those that spend the ma- coalitions or redirected aggression, and agonistic interactions can jority of their activity period in association with at least one other be followed by post-conflict interactions, such as reconciliation adult conspecific. Non-solitary social units can be operationally or consolation, that enhance social complexity (Aureli et al. defined as “a set of animals that interact regularly and more so 2012). Because acts of intraspecific communication also repre- with each other than with members of other such groups” sent forms of social interaction, I consider communicative com- (Struhsaker 1969), where interaction in this context should refer plexity to constitute a core aspect of social structure (see also to association. Variation in spatial cohesion or temporal persis- Wilson 1971), rather than a separate entity being driven by social tence may make this task operationally challenging in some taxa, complexity (see below). An often neglected aspect of social however (e.g., Whitehead 2008; Schneider and Kappeler 2016). structure concerns relationships between neighboring social The smallest group size equals 2; the largest animal groups can units, which can vary massively in mutual tolerance (Willems include millions of individuals (Parrish and Edelstein-Keshet and van Schaik 2015). Matings and other sexual interactions are 1999). Group composition will typically refer to the sex and excluded from the set of social interactions as they define a age of group members, which are also often strong predictors distinct functional component of the social system. Social net- of kin relations. Additional aspects of the genetic structure of a work analyses and other methods provide modern quantitative social unit can be inferred from behavioral data (who disperses? measures of different dimensions of social structure, including Which sex is philopatric?), whereas more fine-grained descrip- their temporal dynamics (Krause et al. 2007; Neumann et al. tion of kinship patterns requires genetic analyses. 2011;Farine 2018) and the relative importance of direct and Social structure is defined by the content, quality, and pattern- indirect social relationships (Brent 2015). ing of social relationships emerging from repeated interactions Because mating interactions have direct fitness conse- between pairs of individuals belonging to the same social unit. In quences, and because there is no 1:1 relation between social species where individuals interact little, often in very similar organization and mating patterns (Kappeler and Schaik 2002; forms and in the same contexts, it is not possible to identify Rubenstein and Abbot 2017a), the Mating system represents a differentiated relationships because these species also typically distinct component of every social system. Studies of mating lack individual recognition. Social bonds represent a subset of systems can yield information on the identity and average differentiated relationships with particular characteristics (high number of mates of males and females. These data based on affiliation and low agonism) and often have functional impor- behavioral observations can be complemented with genetic tance (Silk 2012; Silk et al. 2013; Seyfarth and Cheney 2015). data to reveal who actually reproduced (i.e., who fertilized Dominance relationships develop as a result of repeated agonis- the eggs). The resulting emergent patterns at the level of the tic interactions and represent a functionally important aspect of social unit allow classification of species as monogamous, social structure because they regulate access to resources and polygynous, polyandrous, or polygynandrous (i.e., promiscu- mates in many species. In some species, dominance relationships ous), adjectives that should not be used to refer to types of social organization to acknowledge their conceptual may be established or stabilized by polyadic interactions, such as Behav Ecol Sociobiol (2019) 73:13 Page 7 of 14 13 separation. For most species, it will be easy to determine criterion, e.g., > 50, 67, or 75%, seems indicated to character- whether a single or multiple females breed and/or whether ize the modal social organization, mating, or care system. there is a reproductive division of labor. However, interindi- Species in which otherwise solitary individuals occur only vidual variation in mating and reproductive success often re- temporarily in association (Psorakis et al. 2015), individuals quire more detailed studies to determine patterns of male and associate during their period of inactivity and are solitary dur- female reproductive skew, Bateman gradients or the existence ing their period of activity or vice versa (Kappeler 2012), of alternative reproductive tactics. social organization changes seasonally (breeding pairs vs. Finally, because the categories of social systems defined by winter flocks in some songbirds, Aplin et al. 2015), or were specialists studying different taxa regularly also include as- males and females are segregated into different types of social pects of parental care (Rubenstein and Abbot 2017b), I pro- organization for most of the year (Ruckstuhl and Neuhaus pose the Care system as the fourth component of a social 2002; Wearmouth and Sims 2008) pose additional challenges system. By detailing who cares for dependent young, infor- for social taxonomy that still require a general consensus. The mation on either the absence of parental care or on maternal, framework outlined above may be useful for identifying and paternal, bi-parental, or allo-parental care can be provided. defining generally agreed upon criteria. This component will also specify the presence of cooperative breeding as well as caste polymorphism in species where they play a role. Together, these four components define the cor- The evolution of social complexity nerstones of a social system and provide a basis for the sys- tematic study of social complexity. Evolutionary questions about social complexity can be A final comment on practical difficulties with studying any grouped into at least four categories. The selective factors that or all components of a social system is indicated. These diffi- give rise to variation in traits that contribute to social complex- culties arise from the fact that any empirical study including ity have always been in the focus of behavioral ecologists. several social units is bound to find variation among them. More recently, a new line of research has begun to explore Thus, a key problem for making general statements about the genetic and other proximate mechanisms facilitating or “the social system of species x” as well as for extracting data accompanying evolutionary changes in social complexity. from primary studies for quantitative comparative studies is Another distinct set of questions deals with evolutionary tran- how to deal with intraspecific variation (see, e.g., Lukas and sitions in traits characterizing social complexity and their co- Clutton-Brock 2017; Schradin 2017). This variation exists evolution. Finally, a large body of literature has examined among neighboring social units, within social units over time, consequences and correlates of variation in social complexity and sometimes among different populations of a given spe- for other traits, especially brain size. cies. In cases where such variation is measured on a continu- ous scale, such as group size or grooming rates, the appropri- Variation in social systems ate descriptive statistic such as the median or the (weighted) mean can be reported and used, respectively. Repeated mea- First, the selective factors and evolutionary mechanisms giv- sures of the same social units over time, which are increasing- ing rise to variation in the core components of social systems ly available from long-term studies, require a justified criteri- have constituted areas of intensive research in behavioral ecol- on for non-independence so that data on group size, adult sex ogy from the beginning (Winn 1958; Klopfer 1962; Crook ratio, or the number of helpers, for example, can be used for 1964; Krebs and Davies 1981). Apart from general principles, determining the appropriate central tendencies. It will largely this line of research also revealed and emphasized taxon- depend on the species’ life history whether such repeated specific factors that influence the balance of the factors that measures will be statistically independent after a week, month, impact variation in the size, composition and spatio-temporal year, or even longer periods. stability of social units. The list of factors that determine In cases where intraspecific variation occurs on a categor- whether individuals of a given species live in groups or pairs, ical scale, classification can be more challenging. In classify- or not, is today basic textbook knowledge in behavioral ecol- ing a species as either group or pair living, for example, spe- ogy and does not require repetition here (Krause and Ruxton cies that switch between these two states from year to year 2002;Davies et al. 2012). Moreover, interspecific variation in (e.g., striped mice: Schradin 2013), have adjacent groups with social structure has been mainly studied in primates and other either social organization (callitrichids: Garber et al. 2016), or mammals, where the nature of food competition as well as exhibit other patterns of intraspecific variation (Lott 1991)are phylogenetic similarity have been identified as the most im- difficult to classify. A similar problem is often encountered in portant ultimate determinants of variation in social structure nominally pair-living species where a certain proportion of (Sterck et al. 1997; Clutton-Brock and Janson 2012). social units includes an additional adult male or female (e.g., Furthermore, the evolution of mating systems has also been Kappeler and Fichtel 2016). In those cases, a majority a classic topic for behavioral ecologists, who identified the 13 Page 8 of 14 Behav Ecol Sociobiol (2019) 73:13 distribution of receptive females in space and time as funda- beginning to be addressed in both vertebrates and with respect mental determinants of interspecific variation in mating sys- to physiological mechanisms as well (Rubenstein and tems (Emlen and Oring 1977; Greenwood 1980; Thornhill Hofmann 2015; Taborsky and Taborsky 2015). and Alcock 1983; Clutton-Brock 1989; Shuker and Simmons 2014). Which sex, if any, provides parental care is Evolutionary transitions broadly predicted by particular life history constraints defin- ing higher taxa, such as internal vs. external fertilization, Third, how social complexity has been modified across time ovipary vs. vivipary, litter or clutch size, or lactation, but eco- and taxa can be studied by various comparative approaches logical factors, adult sex ratios, and kinship play additional and methods. A fundamental question in all comparative anal- roles (Clutton-Brock 1991; Reynolds et al. 2002;Hughes yses concerns the degree to which a social trait is correlated to et al. 2008; Kokko and Jennions 2008; Gilbert and Manica phylogeny. Traits with relatively weak phylogenetic signal are 2015). Finally, whether allo-parents contribute care for depen- free to vary more in response to ecological and social factors, dent young has also been explained by a combination of life whereas strongly phylogenetically constrained traits might be history traits and ecological traits (Rubenstein and Lovette less flexible and therefore less likely to increase social com- 2007;Hatchwell 2009; Wong and Balshine 2011; plexity (Kappeler et al. 2013). Compared to morphological Cornwallis et al. 2010; Lukas and Clutton-Brock 2012; Shen and physiological traits, behavioral and social traits tend to et al. 2017). Any modern textbook on animal behavior attest exhibit relatively weak phylogenetic signal, however to the enormous progress made towards a detailed understand- (Blombergetal. 2003; Kamilar and Cooper 2013;Strier ing of the many causes of variation in social systems and, et al. 2014). Moreover, reconstructing the presence/absence hence, social complexity across species. of an aspect of social complexity on the phylogeny of a given lineage can reveal the directionality of evolutionary transitions Proximate underpinnings and therefore disclose whether social complexity increased (more easily) through certain stepping stones or whether Second, because social complexity evolves in the sense that it changes in any direction are possible at every speciation event. varies systematically among species and higher taxa, its con- Such recent analyses revealed, for example, that the evolution stituent components must have a genetic basis. A fairly recent of family-living in birds was a pivotal precondition for the line of research has therefore begun to illuminate the genomics subsequent evolution of cooperative breeding (under particu- of social evolution by examining the molecular changes ac- lar ecological conditions) (Griesser et al. 2017) and that euso- companying evolutionary transitions among different types of cial and communally breeding snapping shrimp evolved inde- social organizations (Robinson et al. 2005; Kapheim 2016, pendently from pair-living ancestors (Chak et al. 2017). 2019). Because an increasing amount of genomic information It is also possible to reconstruct the co-evolution of an has become available for hymenoptera and termites, the geno- aspect of social complexity and a life history or ecological mic sources of phenotypic social novelty have primarily been trait to identify preconditions for major shifts in social com- studied by comparing closely related solitary and eusocial plexity, and theoretical models can predict certain contingen- insect species (Korb et al. 2015; Kapheim 2016). The key cies in social evolution (e.g., Quiñones and Pen 2017)that can question in this context is whether the evolution of social be tested with such comparative studies. For example, in squa- complexity (or new types of social behavior) relies on genes mate reptiles, vivipary has been a crucial precursor in the with new functions, changes in gene regulation, or both evolution of permanent groups containing both adults and (Robinson and Ben-Shahar 2002). Comparative studies across juveniles (Halliwell et al. 2017), and in stingless bees, a dif- several solitary and eusocial insect species indicated that key ferentiated soldier caste evolved in association with the ap- changes in gene regulation may have evolved independently pearance of parasitic robber bees (Grüter et al. 2017). In hy- in ants and (honey) bees, whereas changes in gene function menoptera inhabiting an ecological gradient of habitats, eco- may have allowed for subsequent taxon-specific social and logical constraints and developmental rates were found to pre- ecological adaptations (Simola et al. 2013), but across bees, dict predominant types of social system at different elevations for example, there is no single road map to eusociality, i.e., (Kocher et al. 2014), indicating that different factors promote independent evolutionary transitions in social organization are the emergence of different aspects of social complexity in based on different genetic mechanisms (Kapheim et al. 2015). independent lineages and that we are nowhere near to having Interestingly, in bee species with greater social complexity, a complete list of relevant factors. many important genes show evidence of neutral evolution, A better understanding of the evolution of social complex- indicating relaxed selection. Integration of proposed mecha- ity can also be achieved by studying the co-evolution of dif- nisms at the genetic, developmental, and behavioral level that ferent components of social systems (Elgar 2015). accompany changes in social organization is now an exciting Correlations between group size and the size of a species’ vocal repertoire or other communication signals represent task for future research (Rehan and Toth 2015) and one that is Behav Ecol Sociobiol (2019) 73:13 Page 9 of 14 13 the most commonly studied research question in this context. indicates the existence of multiple mutual contingencies that For example, comparative analyses revealed that among deserve additional study in the future. halictid bees, eusocial species have more elaborate sensorial machinery linked to chemical communication than solitary species (Wittwer et al. 2017). There is also evidence suggest- So what? ing that odor profiles and other aspects of signal complexity may also be more elaborate in eusocial compared to solitary Finally, whereas social complexity poses many questions that species (Leonhardt et al. 2016; Wenseleers and Zweden make its study interesting in its own right, the question about 2017). Similar positive relationships between measures of so- its consequences addresses an important conceptual point, cial and communicative complexity have been reported for namely “Do species differences in social complexity actually birds(Kramsetal. 2012; Leighton 2017) and mammals matter?” Does the fact that we can rank species according to (Pollard and Blumstein 2012; Bouchet et al. 2013) and have different levels of social complexity explain or predict any- recently been reviewed elsewhere (Pollard and Blumstein thing interesting, or does it simply reflect a human tendency to 2012; Peckre et al. 2019, topical collection on Social classify, group and rank natural entities? A more cynical in- complexity; see also Pika 2017). terpretation holds that referring prominently to higher levels of sociality or social complexity may simply be part of a strategy to publish in high-profile journals. Co-evolution of social systems Two interesting consequences of social complexity have been proposed. First, relatively little attention has been given Other relationships between different components of a social to the notion that “the relationships that result from complex system are expected, suggesting they also co-evolve together social groups are thought to make possible pro-social behavior (see also Rubenstein 2012). For example, a given social orga- like cooperation and reciprocity” (Freeberg and Krams 2015). nization will predict the mating system to some extent—a This hypothesis assumes that communicative complexity in- baboon species living in bisexual groups of 50 individuals is creases with social complexity as well as cognitive processing unlikely to be monogamous, for example—and the reproduc- ability in the social domain, including contexts that require or tive consequences of living in single-male or multi-male facilitate cooperation. The specific examples presented in favor groups (Davies 2000) or in colonies of single or multiple of this hypothesis so far (Krams et al. 2012) refer to situations in queens (Keller 1995) have been studied in detail. However, which the recipient of a particular call can benefit from this because matings outside the social unit are widespread signal emitted by a group or flock member. More formal com- (Westneat and Stewart 2003; Cohas and Allainé 2009), intra- parative tests of this hypothesis might reveal whether the spec- specific variation in either or both components is common in ified links are robust in other taxa and modalities, potentially some lineages (Schradin 2013), and, because some species providing another example of how different components of so- change their social organization during the breeding season cial systems, in this case two components of social structure as (Wearmouth and Sims 2008), the two components should be defined and argued above, co-evolve. conceptually and terminologically separated. Furthermore, the Second, the most-studied correlate of social complexity to social organization may also predict the care system in some date is brain size. There are at least five hypotheses that link cases—pair-living species are more likely to exhibit bi- brain size with some aspect of sociality (Dunbar and Shultz parental care—and the mating system, especially the degree 2017), and all of them assume that the cognitive demands for of reproductive skew, may even predicate the type of parental managing and monitoring social relationships have selected for care, particularly the presence of paternal care (Kokko and an increase in the size of the brain or a particular part thereof. Jennions 2008), but there is no fixed 1:1 relationship between While most empirical studies testing these hypotheses have been these two components of a social system (e.g., paternal care is conducted with birds or mammals (Dunbar and Shultz 2007; absent in some pair-living species and present in some group- Isler and van Schaik 2009; Fox et al. 2017), similar relationships living species; e.g., Tecot et al. 2016). Moreover, interesting have now also been studied in some invertebrates, where results relationships between social structure and components of the have been inconsistent (Feinerman and Traniello 2016;Kamhi mating and care systems have been identified that correspond et al. 2016). These types of comparative studies have been crit- to variation in average levels of kinship among group mem- icized on a number of grounds, however (Healy and Rowe bers (Lukas and Clutton-Brock 2018). Finally, different com- 2007), and brain size variation has recently also been linked to ponents of one component of social systems, such as the dis- many other factors, including energy (Weisbecker et al. 2015), persal regime and grouping patterns, may also not vary inde- environmental change (Holekamp and Benson-Amram 2017), pendently (e.g., Strier et al. 2014), but such contingencies and diet (DeCasien et al. 2017). Because many of these studies remain poorly studied. Thus, the fact that the components of used group size as the main or only measure of social complex- ity, future studies using more specific measures of behavioral a social system do not vary arbitrarily at different levels 13 Page 10 of 14 Behav Ecol Sociobiol (2019) 73:13 Evolution,” which took place in Göttingen in December 2017, Claudia complexity and cognitive demands may eventually resolve this Fichtel for many discussions and Louise Peckre, Ferenc Jordán, Dieter question. Lukas, Phyllis Lee, and Dan Blumstein for excellent comments. I was a Thus, variation in social complexity matters for at least fellow at the Wissenschaftskolleg while this review was conceived. three reasons. First, it provides a framework for the compre- hensive and comparative study of sociality. The emergence of Compliance with ethical standards sociality represents one of the major transitions in evolution (Maynard Smith and Szathmary 1995), so that studying the Conflict of interest The author declares that he has no conflict of interest. evolution of social complexity allows identification of evolu- tionary principles and patterns, and by exploring the proxi- Open Access This article is distributed under the terms of the Creative mate underpinnings of social complexity, we can learn some- Commons Attribution 4.0 International License (http:// creativecommons.org/licenses/by/4.0/), which permits unrestricted use, thing about control and regulation of complex traits. Second, distribution, and reproduction in any medium, provided you give appro- understanding variation in brain size and the attendant cogni- priate credit to the original author(s) and the source, provide a link to the tive abilities are major questions in biology that cannot be Creative Commons license, and indicate if changes were made. answered by neuroscientists unfamiliar with the social context in which these traits function and evolve. Finally, species with greater social complexity are also ecologically more success- Publisher’sNote Springer Nature remains neutral with regard to juris- dictional claims in published maps and institutional affiliations. ful, as evidenced by termites, hymenoptera, and our own spe- cies, lending support to the notion that ecological and social adaptations are closely linked (see also Brooks et al. 2017; References Cornwallis et al. 2017). Allee WC (1927) Animal aggregations. 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