I assume in Chaps. 3, 4, and 5 that types “decide” to join or to leave groups or that they are expelled from groups as a function of their l* values and that these values reflect different viabilities under different thermal regimes (Chap. 2). Reaction norms can be partitioned into causes comprising traits covarying with fitness (egg to adult viability: Ketola et al. 2013), and, for students of mammals, we are fundamentally interested in the performance of traits in fluctuating regimes (Fig. 2.2; Jones 2009). In addition to reviewing factors inducing group structures in mammals, the present brief concerns the varieties of mechanisms employed by group-living mammals to manage competition (Table. 1.1, 2.1) and to gain a reproductive advantage over conspecifics, seeking to minimize l*within and/or l*between. Throughout this and the following section’s discussion of mammalian population architectures, it is useful to ask: How might social actions function to minimize both of the latter functions, and what condition-dependent reproductive costs, benefits, and tradeoffs attend each fitness-maximizing act (Fig. 2.2)? The statement by Eisenberg (1981) quoted at the beginning of this chapter informs the reader that marsupials may be employed as a control group for questions related to mammalian evolution. In effect, the previous author’s view is that marsupial morphology is a relatively invariant constant against which traits characterizing other mammalian taxa may be compared. Though marsupials are an evolutionarily primitive mammalian group (Metatheria), they occupy a broad range of environmental regimes, exhibiting many types of population structure found in the class as well as several examples of “fast” life-history trajectories (Stearns and Koella 1986), similar to most small mammals (Eisenberg 1981). As a result of Eisenberg’s (1981) influence, marsupials, in particular, macropods, are treated relative to eutherians herein. A “toolkit” is proposed (Table 3.1, Fig. 3.1) whereby proteins associated with tolerant or facilitating phenotypes are available to connect and reconnect like ©Lego pieces, differently colored pieces comparable to different proteins in the toolkit. Mammals, also, are characterized by relatively large brains controlling and coordinating action patterns embodying noteworthy abilities for opportunistic, facultative “decision making.”

Fig. 3.1
figure 1

A prehistoric dog, Hesperocyon gregarius (Canidae, Hesperocyoninae), endemic to North America, 37–31 mya. These “fox-like,” carnivores were probably communal, “stalking and pouncing” small animals. Their relatives, the hypercarnivorous, possibly omnivorous, Borophaginae, gave rise to extant wolves, foxes, coyotes, jackals, and dogs. (©Victoria Wheeler)

Full size image
Table 3.1 Table summarizing social traits in “prehistoric” social mammals. (Table and inferences based on Kielan-Jaworowska et al. 2004; Turner 2004; Kermack and Kermack 1984; Eisenberg 1981; Chapman and Feldhamer 1982; Brook and Bowman 2002; Morales and Giannini 2013; Rakotoarisoa et al. 2013; Wilson et al. 2012; Packer 1986; KD Angielczyk, personal communication)
Full size table

Information is presented taxonomically, not, chronologically. Synthesis of Table 3.1 suggests that aggregations (e.g., during opportunistic foraging or hunting) and social tendencies or sociality among “prehistoric” mammals are associated (1) with herbivory and/or carnivory; (2) with spatiotemporal dispersion of limiting resources, particularly, food, water, and breeding sites; (3) with predation pressures and other associates of competition; (4) with indicators of sexual selection; (5) with variations in geochemical events (e.g., climate); and, (6) with morphological design (“phylogeny”). These and other early mammalian features may have constituted a “toolkit” of genetically correlated traits that, when combined and recombined, were favorable to social evolution. Patterns of events detected in the table also suggest that costs associated with detection, search, acquisition, or allocation of limiting resources were correlated with dangerous, difficult, rare, or risky conditions. Information summarized in this table indicates that large body size and, probably, a generalized phenotype, disfavored the expression of quasi-social or social traits, partially explaining why sociality is restricted in most orders of class Mammalia.

3.1 The Evolution of Thermal Niches and the Evolution of Mammalian Sociality

Intra- and inter-type effects via differential thermal niches within and between local regimes determine population structure . “The factors that influence space use in female mammals ultimately determine social organization” (Fisher and Owens 2000; also see Jarmon and Southwell 1986) “because females ultimately limit male reproductive success” (Emlen and Oring 1977; Trivers 1972). Mammalian “social” organization varies by subclass, with eutherians more sensitive to dispersion of resources, while macropods are more sensitive to climate (Fisher and Owens 2000). Perhaps for the latter reason, the “body plan” and population architectures of macropods and other marsupials has remained conserved and stable over time, reflecting adaptation to “moving target” environments that cannot be tracked by types (Roughgarden 1979) within the constraints of generation time (Jones 2012). For similar reasons, rodents are a model system for eutherians as a whole.

Among mammals, larger home range sizes correlate with larger group sizes, and larger groups are usually “social” (Fisher and Owens 2000), although cooperatively breeding mammals and the long lived, eusocial mole rats (Bathyergidae) are small taxa in small groups. The latter observations imply that more than one “route” to sociality may have influenced mammalian social evolution (Chap. 1). The evolution of large groups may be opposed by “kin selection” since, according to Hamilton (1964), “decisions” by type in a group to reproduce indirectly rather than directly will favor small group size. The latter effect may lead to conflicting reproductive optima between the sexes since mammalian females, even in “solitary” species, are more likely to be social (e.g., exhibiting helping, hygienic or stress-decreasing grooming, or allomothering: see Chap. 8). This apparent trade-off between the benefits of kin selection and the benefits of living in large groups highlights a physiological dilemma (foraging efficiency) that may explain: (1) the relative infrequency of sociality in mammals as well as (2) the apparent correlation between division-of-labor and stability of limiting resources, particularly, food and refugia (Crespi 2007; Alexander et al. 1991) .

Higher grades of sociality , particularly, division of labor, appear to demand a significant dedication to specialist strategies, particularly, foraging strategies and feeding selectivity, although selectivity of plant species choice and of plant parts is characteristic of large mammalian herbivores, as well. In macropods and eutherians, small taxa are more “selective foragers” than large taxa, and many group-living mammalian herbivores demonstrate a significant degree of specialization (“discriminative feeding”: see Sedio and Ostling 2013; Owen-Smith and Chafota 2012) in their feeding habits (reviewed in Fisher and Owens 2000; also see Bodmer 1990; Milligan and Koricheva 2013; Di Stefano et al. 2011; Owen-Smith and Chafota 2013; Matsuda et al. 2013; Kermack and Kermack 1984, p. 12). “Selective feeding” may place limits on the evolution of traits associated with l*within and l*between. Seemingly paradoxical, the transition to sociality in mammals has, also, been constrained by flexible physiological and behavioral characters in mammals, decreasing benefits of and opportunities for division-of-labor since in these, often large, species, totipotency reigns (single types perform many different tasks).

Finally, most large mammals are iteroparous breeders and most eusocial taxa, including, social insects and eusocial Bathyergids, exhibit very high reproductive rates relative to body size (see macropods for interesting cases as per Eisenberg 1981), further suggesting that cooperation in large mammals and sociality in small mammals are products of different “routes” that may be differentially energy-efficient relative to (thermal) conditions. Possibly supporting the latter view is Lacey’s (2000) finding that social Bathyergids have evolved in arid habitats providing abundant, evenly distributed, subterranean supplies of food. On the other hand, Stahler et al. (2013), studying reproductive female wolves (Canis lupus), concluded that: “Large body size and sociality [promote] individual fitness in stochastic and competitive environments,” regimes characteristic of those in which most eutherian mammals evolved (see Jones 2009). A mammalian “toolkit” (Table 3.1), then, might have permitted more than one “route” (Chap. 1) to sociality, but only if shared reproductive interests were obtained (Chap. 2) .

3.2 Abiotic and Biotic “Drivers” of Body Sizes and Home-Range Sizes in Mammals

Following Fisher and Owens (2000), in both macropods and eutherians, “variation in body size was related to variation in home-range size.” Habitat productivity measured by rainfall, however, was the primary effect for home-range size across macropods (negative correlation), ecological factors (e.g., food dispersion, “patchy” distribution of limiting resources), for most eutherian groups. Interspecific differences in macropod home-range size, however, were “attributed to diet,” and it is important to know whether this effect is a general R* function (Chap. 2) where different species compete for limiting resources. Among both macropods and eutherians, large animals (e.g., eutherian grazers: Bodmer 1990) are “much less selective foragers than small species” (but see Kermack and Kermack 1984), and “mean group size [of both taxa] is [positively] correlated with body size.” The aforementioned associations highlight the primary drivers of “sociality” in the class; however, Fisher and Owens (2000) review additional trends. Based on the aforementioned associations, in general, abiotic factors are more robust predictors of “sociality” for macropods, possibly, consistent with the findings of Jetz and Rubenstein (2011) for birds. Importantly, however, the latter authors point out that climate variability may be used as a proxy for heterogeneity of food resources, a testable hypothesis for mammals and other vertebrates.

Continuing to highlight the macropod paper, Fisher and Owens (2000), also, reported that “variation in body size was related to variation in home range size,” a finding consistent with findings for eutherians. Data on body size relative to abiotic and biotic factors are of particular note because body size reflects first principles of ecology (e.g., energy acquisition, consumption, and allocation). Based upon phylogenetically independent contrasts, variation in macropod home ranges was more strongly associated with habitat productivity than for eutherians, with rainforest species exhibiting small home ranges, “arid zone” taxa, the largest home ranges. The latter findings for macropods conform to findings for eutherians. Importantly, home-range size, relative to group size, reflects energy requirements and, possibly, energy reserves, thus providing opportunities to test numerous hypotheses theoretically and empirically (e.g., Smith et al. 2010), and in ecological context. There do appear to be outliers, however. For example, consistent with Bodmer’s (1990) analysis, fungi-eating Bettongia spp. (bettongs) do not appear to follow classical patterns as per home-range metrics (see also fungus-eating Primates: Callitrichidae, Fig. 5.1).

The discussion of foraging by Fisher and Owens (2000) exemplifies the “toolkit” paradigm, advanced in the present document, as well as the characteristic flexibility of mammalian behavior and population structures. In addition, despite caveats pertaining to spatiotemporal models of ecology (Chap. 6), the previous authors demonstrated the explanatory power of resource, particularly, food, dispersion (distribution, abundance, and type) for edifying variations in population structure. For example, across mammals, “foraging habitat of small herbivores is patchy because they feed on more clumped and sparsely distributed food” (Fisher and Owens 2000; also, see Lee and Cockburn 1985). On the other hand, “food for larger herbivorous mammals is more patchy, because habitat is more heterogeneous at larger scales” (Fisher and Owens 2000; also, see Bodmer 1990). Thus, when assessing patterning of mammals in space and time, body size relative to resources must be considered, and these variables might vary by local conditions and by habitat, including, abiotic (e.g., soil) and biotic (e.g., tree line) gradients. Fisher and Owens (2000) highlight several extreme features of Australia’s “extreme” environments that might account for the differences between macropods and eutherians, including wide variation in climate, low productivity of forests, “small range of body sizes relative to the strong climate gradient” (n.b., scale), and stasis in one or more mammalian characters (see Eisenberg 1981).

Continuing with macropod: eutherian comparisons, Fisher and Owens (2000) noted that, in both taxa, mean group size and body size are correlated. Group size and group living are associated positively in macropods and eutherians, and a predictor of variations in population organization might be the relationship between “patch” or habitat or population density and body size and/or group size. On the other hand, the highest grades of sociality are associated with genetic homogeneity caused by philopatry and/or recruitment of kin, conditions favored by “kin selection” according to the latter authors. Consistent with the aforementioned findings, variations in density were negatively correlated with female home-range size. Thus, higher densities are associated with body sizes and home range sizes in a manner that should reflect female dispersions and subsequent “mapping” of male dispersions onto those of females (Chap. 6).

3.3 What Roles Do Mammalian Males Play in Determining Population Structure? Interactions Between Intrasexual Selection, Sexual Dimorphism in Home Range Sizes, and the Potential for Male Monopolization of Females

In both macropods and eutherians, male home ranges are largest whereas females are found on small home ranges or territories (Fisher and Owens 2000), a condition likely to induce sexually segregated and polygynous population architectures, the most common population structures in mammals . An inference from the previous authors’ review is that territorial males whose ranges overlap those of females appear to represent an intermediate architecture. Deductions from the literature reviewed in the paper on macropods await quantitative testing, particularly, given the theoretical treatment by Rodrigues and Gardner (2013) showing that group-size effects are not straightforward and that temporal factors (e.g., climate) may have stronger effects than spatial factors (e.g., food dispersion) in many regimes (cf. macropods: Eisenberg 1981; cavies, Caviidae: Adrian and Sachser 2011).

The patterns specified by Rodrigues and Gardner (2013) have important implications for apparent differences between macropods and eutherians whose population parameters may be more affected by rainfall and ecological variables, respectively. Finally, the importance of variations in group size must be weighed by mammalian social biologists since small group size is ubiquitously assumed to correlate with higher grades of sociality in mammals and many other taxa (e.g., birds; Sect. 5.4; Synopsis). Rodrigues and Gardner’s (2013) analysis questioned the latter assumption. However, their conclusions depended upon the relative viscosity (variations in dispersal distance) within populations, suggesting that some patterns of mammalian population structure may be a function of variations in dispersal rate (see Johnson and Gaines 1990; Waser et al. 2013).

Other caveats do obtain, however, since males’ energetic requirements and intrasexual selection (“male–male competition”; this brief, Sect. 8.5) may yield male dispersions that are theoretically suboptimal for male reproductive benefits. In macropods, monogamy is associated with small, exclusive, female territories (Fisher and Owens 2000; also see Hennessy et al. 2012). Monogamy may also occur where female dispersion may be unpredictable or sparse, decreasing benefits or increasing costs of polygyny, in this case, male ranges overlapping the ranges of > 1 female. Variations in the factors associated with the aforementioned conditions may yield insights into differences in social organization between monogamous mammals (e.g., Potorous longipes, and polygynous, P. tridactylus). Monogamy is rare in the primitive group, cavies (Table 3.2), suggesting that this sociosexual structure is highly derived (see Adrian and Sachser 2011) .

Table 3.2 Variations in spatiotemporal architecture of populations of caviomorph rodents (family Caviidae) relative to variations in environmental factors. (Based on Adrian and Sachser 2011)
Full size table

In the mammalian literature, terminology for mating systems is often not differentiated from terminology for social systems. As well, use of terminology is sometimes inconsistent. Terminology in mammalian social biology is strongly influenced by terminology found in the literature on birds with an emphasis on mating systems (“polyandry,” “leks,” “monogamy,” “polygyny,” “polygynandry”). Perhaps, the best example is use of the word, “polygyny” (see cavies, Cavia aperea: Rémy et al. 2013; Asher et al. 2004), a type of population architecture whereby (1) a single male’s home range or territory overlaps that of 1 or > 1 female home range or territory, or (2) a single male in residence with 1 or > 1 female on a home range or territory. “Polyandry,” also, is in need of clarification (cf. Andersson 1994: “classical” polyandry and multiple mating by females). Despite “fuzziness” and lack of scientific consensus about terminology, the defining feature of mammalian population structure is spatial dispersion rather than patterns of mating per se. The prior perspective strongly suggests that spatial, or spatiotemporal, dispersion “drives” coevolution between sexual and social systems (Crespi 2007: Sect. 1.1), and that aggregations, tolerance, and, possibly, group life are prior (see polygynous bank voles, Myodes glareolus: Rémy et al. 2013).

Fisher and Owens (2000) provided a convincing analysis of the relationship between “mating systems and sex differences in home range size,” and their schemas correspond well with reviews and empirical reports on other terrestrial mammals (e.g., platypus, Ornithorhynchus anatinus: Grant and Temple-Smith 1998; shrews, Soricidae: Churchfield 1990; tree-shrews, Tupai: Emmons 2000; humans, Homo sapiens: Lee and DeVore 1976; Meggitt 1965; short-tailed opossum, Monodelphis domestica: Caramaschi et al. 2011; brown bears, Ursus arctos: Steyært et al. 2013; ruminants, Conradt 1998, c.f.; Metatheria: Lee and Cockburn 1985). Despite the apparent generalities of the schemas presented by Fisher and Owens (2000), anomalies remain (e.g., red acouchies, Myoprocta exilis: Dubost 1988; dasyurids, Antechinus: Lee and Cockburn 1985; pentail tree-shrews, Ptilocercus: Emmons 2000). A possible consideration is that temporal factors may be particularly constraining for these and other anomalous taxa, whereas, as reviewed above and below, spatial factors appear to explain many variations in mammalian population dispersions. Temporal and spatial factors need to be decomposed quantitatively, including, experimentally, projects that would reveal both strengths and weaknesses of spatiotemporal analyses (Chap. 6).

3.4 “Promiscuous” Associations with Overlapping Home Ranges Without Male Monopolization: A Mammalian “Toolkit”

Most eutherians demonstrate one or another type of “polygyny” (Eisenberg 1966, 1981; Wilson 1975), but macropod “social” organization is conserved and relatively invariant, with nonterritorial, “promiscuous” structures being most common (Fisher and Owens 2000; see Cornwallis et al. 2010 for a general model). In particular, the home ranges of male and female macropods overlap one another, with little evidence of either sex monopolizing the other. Supporting Eisenberg’s (1981) proposition, it seems reasonable to suggest that the “promiscuous” dispersion is an evolved template providing a flexible “toolkit” for the elaboration of population structure in response to spatial and temporal, abiotic and biotic , including, intraspecific (l*between, l*within), effects. It follows from the discussion so far that short-term and long-term variations in “patch” and “population” density are expected to have been critical determinants of the differential reproductive costs and benefits to individuals of exhibiting mechanisms to manage competition . Although the present monograph is not intended to “unpack” the phylogenetic progression of mammalian social evolution, it seems likely that the “promiscuous” arrangements described for macropods constitute the primitive structures in the class, dependent upon tolerance possibly imposed environmentally by high population densities or, simply, by chance encounters of conspecifics during movements in “patches” and habitats (e.g., for mate search). Tolerance might have been particularly beneficial during dispersal or migration as well as any activity requiring search strategies.

By manipulating variables hypothesized to determine female home range or territory sizes, it seems to require uncomplicated evolutionary trajectories (“fast” or “slow”: see Selman et al. 2012) from “promiscuous” population structure to any other of the social structures described for mammals. In addition to the critical factors and correlations already discussed in this chapter, it is useful to begin with the assumption that “female mammals are expected to minimize home ranges enabling them to forage widely enough to find sufficient food with minimum risk and energy expenditure” (Fisher and Owens 2000; McNab 1980). Depending, then, upon the condition-dependent “potential” for females to “maximize” reproductive success (via direct and/or indirect reproduction) , males, time-minimizers, are expected to “maximize” the number of females monopolizeable. It is apparent that in mammals, males generally avoid coresidence with females. Of course, types, ultimately, do the best they can (Waser et al. 2013; Austad 1984), and, sometimes, males will do best by minimizing competition via tolerating or facilitating other reproductive males and/or females, such as, by forming multimale groups in association with females, a social structure that is relatively common in primates and a few other mammalian taxa (Fig. 2.1, Chap. 4, Sect. 8.5), virtually absent in Aves.

The flexibility of the “promiscuous” template echoes Lee’s (1976) terminology for human social evolution, accordion-like “concentration and dispersion,” a useful paradigm for mammals in general. Cavies, as noted, would make a good model system for investigations of the evolution of a range of grouping structures (this brief Table 3.2; see Rood 1972), consistent with the principles reviewed above as well as with spatiotemporal theories of group formation and group maintenance (Chap. 6). The reviews of marsupials by Lee and Cockburn (1985) and of cavies by Adrian and Sachser (2011) are consistent with the rules of population assembly reviewed by Fisher and Owens (Fisher and Owens 2000; see Andersson 2005 for a compatible analysis based on the “operational sex ratio”). It is clear from Lee and Cockburn’s paper (2000) how the evolution of greater flexibility in social organization might be advantageous in heterogeneous regimes, as well as, how the evolution of monogamy (also see “temporary monogamy” in coyotes, Canis latrans: Gilbert-Norton et al. 2013) in habitats with an even food distribution is a good “fit” to the dispersion of animals when food is sparsely distributed.

An interesting aside is that most mammalian taxa demonstrate relative flexibility of population structure, even when the same basic architecture is retained across species in a family, such as, tree shrew (Tupaiidae) territoriality combined with solitary foraging differentially responsive to variations in population density (compare Tupaia glis and T. longipes: Emmons 2000). Cavies have become a model taxon for the flexibility and variability of mammalian grouping patterns (Table 3.2), deserving targeted programs of investigation from biochemical to higher levels of organization (Adrian and Sachser 2011; Asher et al. 2004; Meserve et al. 1984), particularly, in combination with their Old World relatives (e.g., Bathyergidae). Fleming et al. (1987) concluded that neotropical forests demonstrated less heterogeneity than Paleotropical forests, two dynamic states that might have predictive value when comparing and contrasting grouping patterns between the two regions.

Fisher and Owens’ (2000, pp 1090–1091) discussion of the roles that males play in determining population architecture leads one to the conclusion that the intensity of male–male competition or the spatiotemporal unpredictability of females may stress males’ time budgets (Sect. 8.6), leading them to adopt strategies that are not, theoretically, optimal (e.g., “monogamy,” leks). Indeed, lekking, whereby males gather on an exclusive breeding ground visited by females who “choose” one or more displaying males, is rare in mammals compared to birds; although a few taxa exhibit elements of the social structure whereby females float (?) or search (?) male home ranges or territories during a breeding season or as a matter of course (e.g., some pinnipeds, sea otters, some ungulates). Importantly, lek and some other systems (Hemelrijk 1999; polygynandrous mantled howler monkeys, Alouatta palliata: Jones and Cortés-Ortiz 1998) exhibit “female emancipation” (Andersson 2005; Emlen and Oring 1977), and, as suggested above, some male strategies may have evolved in response to costs incurred from multiple mating by females (in the previous cases, male–male tolerance at stationary breeding areas; multiple male coresidence in bisexual groups on home ranges whereby males may exhibit tolerance or various types of sociality such as group defense or coalition formation), and male tolerance of multiple mating by females (Chap. 8). Each of these strategies may be expected to reduce costs of male–male competition, favoring superior males within (l*within) or between (l*between) groups via reductions in thermal stress and increased energetic efficiency (see Gittleman and Thompson 1988).

3.5 “Solitary” Mammals and Sexual Segregation Grade to Polygyny

What are the “drivers” of “solitary” (“sexually segregated”) population structures in mammals? Factors intrinsic and extrinsic to populations are deterministic, particularly, the potential for males to monopolize females and the dispersion of resources required by females to reproduce. Table 3.2, for example, displays the fundamental relationship between promiscuity and sexual segregation in C. magna , a transition probably dependent upon variations in population density whereby the ancestral, promiscuous state, responds to increasing density and increased competition among males for access to variably dispersed females (see Steyært et al. 2013). Let us assume that mammal populations are inherently responsive to environmental perturbations because of their evolution in heterogeneous regimes favoring traits characteristic of invasive taxa designed for rapid expansion into new regimes. An integral element of mammalian flexibility would be the ability to adjust responses to abiotic (e.g., soil gradients, breeding sites) and biotic (e.g., food dispersion, nutrient gradients, predation) changes across space (e.g., across patches or habitats) and time (e.g., across seasons), and factors opposing the evolution of sociality in the class (Jones 2009).

Compare C. magna and G. musteloides in Table 3.2 whereby, hypothetically, in the latter species, some threshold level of population increase induced deleterious effects on male reproductive success, increasing benefits of male–male tolerance (multimale–multifemale groups) and facilitation of females (“female dominance”) in some regimes. In these cases, components of a “promiscuous” spatiotemporal structure without male monopolization of females and with overlapping male and female home ranges acts as a multipurpose ©Lego kit bounded by the environmental potential to accommodate reproductive tactics and strategies of types. Reviewing the literature on cavies, Adrian and Sachser (2011) stated: “Female behavior is obviously a decisive factor that prevents monopolization by males.” Importantly, the latter authors’ treatment highlights sexual conflict between mammalian males and females (Aloise King et al. 2013), as well as the coevolution of tactics and strategies, leading to the conclusion that population structure in cavies, and possibly other mammals, is an ultimate function of the dispersion and sizes of female home ranges relative to male thermal zones.