American Journal of Primatology

REVIEW ARTICLE Why “Monogamy” Isn’t Good Enough STACEY R. TECOT1,2,3*, BRITT SINGLETARY1, AND ELIZABETH EADIE1,3 1 School of Anthropology, University of Arizona, Tucson, Arizona 2 Centre ValBio, BP 33, Ranomafana, Ifanadiana, Madagascar 3 Laboratory for the Evolutionary Endocrinology of Primates, University of Arizona, Tucson, Arizona

Rare in mammals but more common in primates, there remains a considerable controversy concerning whether primate species traditionally described as monogamous actually express this highly specialized breeding pattern. Unfortunately the definition of “monogamy” varies greatly, inhibiting our understanding of this trait and two related traits with which monogamy is often conflated: pairliving and pair-bonding. Strepsirrhine primates are useful models to study factors that select for pairliving, pair-bonding, and monogamy because this taxon exhibits high incidences of each trait, in addition to species that exhibit behaviors that reflect combinations of these traits. Several hypotheses have been articulated to help explain the evolution of “monogamy,” but again, these hypotheses often conflate pair-living, pair-bonding, and/or monogamy. In this review, we (1) propose clear, discrete, and logical definitions for each trait; (2) review variation in strepsirrhines with respect to these three traits; (3) clarify which of these traits can be explained by existing hypotheses; and (4) provide an example of the applicability of the Resource Defense Hypothesis (RDH) to understand two of these traits, pairliving and pair-bonding, in the red-bellied lemur (Eulemur rubriventer). Available data support the RDH for pair-living in red-bellied lemurs. They live in stable family groups with one adult pair. Both sexes actively codefend territories that overlap little with other pairs’ territories. Agonism is extremely rare within groups and intergroup and interspecific agonism varies with food availability. Available data also support the RDH for pair-bonding. Pair-bonds are cohesive year-round. Pairs coordinate behaviors to defend territories with auditory and olfactory signals. Cohesion increases with food abundance and both sexes reinforce bonds. We indicate where additional data will help to more rigorously test the RDH for each trait and encourage others to test alternative hypotheses. Am. J. Primatol. © 2015 Wiley Periodicals, Inc. Key words:

monogamy; pair-bonding; pair-living; resource defense hypothesis; lemur

INTRODUCTION Monogamous mating is expected to be rare because theoretically, under conditions in which males have access to several breeding females and offspring can survive without paternal care, a male mammal can increase his reproductive success by associating and mating with more than one female [e.g., Trivers, 1972]. Relative to birds, mammalian males who invest in mating rather than parenting carry a lower cost and higher potential benefit because only mothers can provide nourishment for nursing offspring [Orians, 1969; Weatherhead & Robertson, 1979]. In these ecological scenarios, a male mammal’s direct parental investment is, therefore, less beneficial to his offspring, or his lack of investment is less costly to offspring survivorship [Orians, 1969]. Indeed, only 9% of mammals are classified as “monogamous” [Lukas & Clutton-Brock, 2013]. Primates are unusual in that approximately 29% of species [Lukas & Clutton-Brock, 2013], including

© 2015 Wiley Periodicals, Inc.

roughly 17% of human cultures [Low, 2003; Marlowe, 2000], are considered “monogamous.” While

Contract grant sponsor: The National Science Foundation; contract grant number: BCS-0424234; contract grant sponsor: Primate Action Fund; contract grant sponsor: American Association of University Women; contract grant sponsor: American Society of Primatologists; contract grant sponsor: UT-Austin; contract grant sponsor: Primate Conservation, Inc.; contract grant sponsor: University of Arizona (UA) School of Anthropology Conflicts of interest: None 

Correspondence to: Stacey R. Tecot, School of Anthropology, University of Arizona, 1009 East South Campus Dr. PO Box 210030, Tucson, AZ 85721. E-mail: [email protected] Received 2 May 2014; revised 9 March 2015; revision accepted 10 March 2015 DOI: 10.1002/ajp.22412 Published online XX Month Year in Wiley Online Library (wileyonlinelibrary.com).

2 / Tecot et al.

estimates of the abundance of monogamy in primates can be problematic (e.g., Lukas and Clutton-Brock [2013] include all species of tamarins and marmosets as monogamous, in contrast with data from wild groups; see Garber et al. 2015, this volume), current calculations suggest that there has been particularly strong selective pressure for this system within the Primate Order. The term “monogamy,” however, has been used in the literature to refer to a type of social organization (pair-living), social relationship (close social bonding between two adults of opposite sex), and/or mating system (exclusive and consistent monogamous mating) [Fuentes, 1998; Reichard, 2003; Wickler & Seibt, 1983]. Though they are often associated, each is a separate component of a social system [Kappeler & van Schaik, 2002], and these components do not always covary. For example, pair-living species are commonly bonded [e.g., titi monkeys, Callicebus; Anzenberger et al., 1986], but bonding is not necessary for pair-living (e.g., red-tailed sportive lemurs, Lepilemur ruficaudatus; [Hilgartner et al., 2012]; fork-marked lemurs, Phaner furcifer; [Sch€ ulke, 2005]). Similarly, pair-living species commonly mate monogamously (e.g., Azara’s owl monkey, Aotus azarae; [Huck et al., 2014]), but monogamous mating is not required (e.g., fat-tailed dwarf lemur, Cheirogaleus medius; [Fietz et al., 2000]). As a result of using terminology inconsistently, our ability to understand the selective pressures leading to the evolution of these traits is limited. Hypotheses for the evolution of “social monogamy,” defined variably as a social organization, social relationship, or mating system, have been proposed to explain the presence of pair-living, pair-bonding, monogamous mating, or a combination of these traits while distinct ecological or social factors are likely to select for each trait (see below) [Reichard, 2003; van Schaik & Dunbar, 1990]. Although several hypotheses claim to explain some aspect of “monogamy,” many of these more appropriately explain a pairliving social organization than a mating system, making it difficult to construct comparative datasets based on similar measures across taxa. Finally, the scientific community is hindered in attempts to build upon earlier research, as a synthesis of work using different definitions is challenging. Previous work has highlighted the need to adopt consistent, discrete definitions [Fuentes, 1998; Fuentes, 2002; Reichard, 2003; Wickler & Seibt, 1983], yet these issues persist. This special issue on Primate Monogamy resulted from a symposium at the American Society of Primatologists conference in 2013 in which participants were asked to define their terms, in full recognition that we adapt our usage according to the systems that we study. In this review, we address this challenge, and first propose a set of discrete definitions that we hope will be used by future researchers addressing topics on the evolution

Am. J. Primatol.

of pair-living, pair-bonding, and monogamous mating. Using these terms consistently will allow us to continue our collaborative efforts, perhaps not under the umbrella of “monogamy,” but in a way that can lead to a deeper understanding of the evolution of these traits. Next, we review the distribution of pairliving, pair-bonding, and monogamous mating in Lemuroidea because lemurs exhibit nearly all combinations of these three traits. Lemurs, therefore, demonstrate the importance of addressing each trait individually, as well as the limitations of failing to do so. We review existing hypotheses for “monogamy” and clarify whether each hypothesis should be applied to pair-living, pair-bonding, monogamous mating, or a combination of these traits, with the goal of helping to identify appropriate hypotheses for future research, and the appropriate data needed to test them. Finally, as an example of how our proposed definitions may be used to examine these reframed hypotheses, we describe predictions of the Resource Defense Hypothesis (RHD), and review how existing data for one lemur species, Eulemur rubriventer, can help test these predictions. As these data are limited, we suggest areas in which additional research will be helpful. Defining Pair-living, Pair-bonding, and Monogamy For the reasons just described, it is important that researchers come to a consensus on the definitions for these commonly used terms. To that end, Figure 1 illustrates the interrelationships between each trait and presents a set of definitions that we believe are clear, logical, and discrete. Below we discuss these definitions in more detail so that they can be compared with previous work. Our definitions largely follow Fuentes [1998], except as noted below. We define pair-living as a demographic structure or social organization, in which two adults of opposite sex live together within a home range with their non-reproducing offspring [sensu Norscia & Borgognini-Tarli, 2008]. Fuentes [1998] referred to this category as a “two-adult group.” While several researchers use the qualifiers “social” and “sexual” to distinguish two types of monogamy, we use the term pair-living [cf Reichard, 2003] for three reasons: (1) it clearly conveys the distinction between monogamous mating and living in a pair, (2) the term monogamy technically refers to a mating system rather than a social organization [Kappeler & van Schaik, 2002], and (3) it makes no assumptions about the nature of the pair’s relationship or offspring parentage. We define pair-bonding as a long-term social relationship (i.e., extending beyond one breeding season), between two unrelated individuals of the opposite sex, that can be “assessed by rates of affiliative interaction, proximity scores, and a measure of reciprocity between two individuals” [Fuentes,

Pair-Living, Pair-Bonding, and Monogamy / 3

Fig. 1. Concept map defining the differences between pairliving, monogamous, and pair-bonded systems. Many of the possible combinations of these strategies are present in the strepsirrhine suborder, with different species falling in different areas of the map depending on which combination they exhibit. For example: Eulemur rubriventer and Indri indri occupy the center of the map where all three concepts overlap; Lepilemur ruficaudatus and Avahi laniger occupy the area of the map where monogamy and pair-living overlap; Cheirogaleous medius occupies the area of the map where pair-living and pairbonding overlap; and Phaner furcifer occupies only the pairliving area of the map.

2002; p 954]. Fuentes [2002] referred to this category as a “social pair-bond.” Categorizing a species as pairbonded can be difficult, as bonding is a continuous variable. Finally, we define monogamy as a mating and breeding system (see Garber et al., 2015, this volume) in which two individuals consistently mate exclusively, though we recognize that measuring consistency and exclusivity can be challenging [Dewsbury, 1988; Thornhill & Alcock, 1983]. Fuentes [2002] referred to this category as a “sexual pair-bond.” Categorizing a species as monogamous (as defined here) is complicated by the fact that there is no consensus on how long the monogamous pairing should last. For example, does exclusive mating with a different partner each year constitute monogamy, must the exclusive mating relationship persist until one partner dies, or is there another temporal benchmark that must be met [Wickler & Seibt, 1983]? In addition, it is important to consider what level of extra-pair copulations, if any, would still constitute a monogamous mating system. Pair-living, pair-bonding, and monogamy in Lemuroidea Recent phylogenetic reconstructions indicate that pair-living evolved independently several times in the Primate Order [Kappeler & van Schaik, 2002],

and it also appears to have evolved independently several times just within the Lemuroidea superfamily [Lukas & Clutton-Brock, 2013; Sch€ ulke, 2005; Shultz et al., 2011]. Lemuroidea demonstrate a great deal of variation in the degree to which pairs of one adult male and one adult female are bonded and mate exclusively. This taxon, therefore, highlights the importance of independently investigating the pressures that selected for each of these traits, and/or those that act to maintain them today. We build upon previous work by Fuentes [2002] in compiling a table of Lemuroidea species and their associated social organizations, social relationships, mating systems, and other traits of interest, such as the presence of allomaternal care, home range size, and diet (Table S1). Indri (Indri indri) is an example of a species that exhibits pair-living, pair-bonding, and monogamy. Pairs are cohesive, defend territories together through elaborate duetting, and extra-pair copulations have only been observed once [Bonadonna et al., 2014; Pollock, 1986; Powzyk, 1997; Torti et al., 2013]. While ring-tailed lemurs (Lemur catta) also form male–female bonds, they do not mate monogamously, and live in multi-male multi-female groups [Gould, 1996]. Some nocturnal, pair-living strepsirrhine species are cohesive (e.g., Western wooly lemur, Avahi occidentalis; [Thalmann, 2001]), yet several others are less cohesive, sleeping together during the day, and foraging alone at night (e.g. Phaner spp., Lepilemur spp.) [Sch€ ulke & Kappeler, 2003]. The term “dispersed pair-living” has been used for species, such as the red-tailed sportive lemur (L. ruficaudatus) [M€ uller & Thalmann, 2000], where a male and female share a home range, but based on evidence that they exhibit low cohesion, low encounter rates, and interactions that are mainly agonistic with no affiliation, they are not bonded [Hilgartner et al., 2012]. Physical contact only occurs during the mating season when the male, who defends the range against other males (but not females), maintains proximity [Hilgartner et al., 2012]. Some “dispersed pair-living” species are considered monogamous (e.g., redtailed sportive lemur, L. ruficaudatus; [Hilgartner et al., 2008]; Eastern wooly lemur, Avahi laniger; [Norscia & Borgognini-Tarli, 2008]; Milne-Edwards’ sportive lemur, Lepilemur edwardsi; [Thalmann 2001]), though genetic analyses to confirm monogamy have only been reported in red-tailed sportive lemurs (see [Hilgartner et al., 2008,2012]). In other dispersed pair-living species, extra-pair paternity can be quite high (e.g., P. furcifer’s rate of extra-pair paternity is 0.75, n ¼ 4 [Sch€ ulke et al., 2004]). However, extra-pair paternity can be high in pair-living, pairbonded species as well. Fat-tailed dwarf lemurs (C. medius) live in long-term (multi-year) cohesive pairs, and infant survival requires male help with babysitting and guarding; but 44% of offspring result from extra-pair copulations [Fietz et al., 2000]. A female

Am. J. Primatol.

4 / Tecot et al.

often has a social pair-mate with whom she lives and who helps care for offspring, and a sexual pairmate who donates sperm [Fietz, 1999; Fietz & Dausmann, 2003; Fietz et al., 2000]. Thus, pairliving, pair-bonding, and male care do not guarantee monogamy. Hypotheses Several hypotheses have been proposed that can explain the evolution and maintenance of “monogamy.” Here we describe five leading hypotheses, and attempt to clarify which predict a social organization (pair-living), social relationship (pair-bonding), and/ or mating strategy (monogamy) (Table I). We note when hypotheses best address the maintenance of traits, rather than their evolutionary origins, though this was not always possible given conflicting results regarding the sequence of when these traits and other traits of interest (e.g., allomaternal care and infanticide) evolved [Lukas & Clutton-Brock, 2013; Opie et al., 2013; Shultz et al., 2011]. It should be kept in mind that it is unlikely that there is a single unitary hypothesis that can explain the recurrent evolution of pair-living in primates, and that the following hypotheses are not mutually exclusive [Fuentes, 1998; Reichard, 2003; van Schaik & Dunbar, 1990]. More than one hypothesis might apply to a given species, as they may address different traits.

Optimal group size hypothesis This hypothesis proposes that group size is a result of the often-argued opposing factors of protection from predators and degree of food competition [Terborgh & Janson, 1986]. Pair-living may be an advantage over living in larger groups due to lower intragroup food competition, under conditions in which food is scarce and resources are small. It can also be an advantage over living solitarily because predation risk is expected to be lower and the pair is better able to defend resources against solitary individuals and other groups, assuming the other groups also contain only two adults. Under this hypothesis, pair-living is predicted to arise when the optimal adult group size is 2. This hypothesis applies directly to pair-living, and has indirect implications for pair-bonding and monogamy. These adults may or may not benefit from mating monogamously and/ or bonding socially. This hypothesis provides a potential explanation for the evolution of pair-living, and can also explain its maintenance in response to current predation and resource pressures. Infant care hypothesis This hypothesis proposes that pair-living, and perhaps secondarily monogamous mating, will evolve when a mother requires the care of a male (who is not also caring for other females’ offspring) to

Am. J. Primatol.

successfully rear offspring [Wittenberger & Tilson, 1980]. Theoretically, males should provide care when mating opportunities are rare and paternal care has a large effect on offspring survival and reproduction. Paternal care is predicted to enhances the pair’s overall reproductive success above what might be expected if the male did not provide care, by increasing the survival rate of offspring and/or allowing the female to produce larger litters or reduce the inter-birth interval [Clutton-Brock, 1989; Fietz & Dausmann, 2003; Lack, 1968; Wittenberger & Tilson, 1980; Wynne-Edwards, 1987]. The infant care hypothesis may explain the transition from solitary to pair-living in some species, and may also explain pair-bonding since coordinated care may be necessary to ensure that the female can nurse her infant [Kleiman, 1977; but see Komers & Brotherton, 1997]. Monogamy is not required, though the costs of parenting may begin to outweigh the benefits for a male if he sacrifices mating opportunities to raise the offspring of other males. Thus, increasing paternal investment costs may select for behaviors that reduce extra-pair copulations. Paternal care and pair-living are frequently associated across animal species, but species with paternal care may have very high rates of extra-pair copulations (e.g., fattailed dwarf lemurs, C. medius, [Fietz & Dausmann, 2003]), or species can be monogamous and lack paternal care completely [Kleiman & Malcolm, 1981; Lack, 1968; Smuts & Gubernick, 1992; Wittenberger & Tilson, 1980]. Based on phylogenetic reconstructions, it is generally accepted that paternal care evolved after pair-living in most lineages, within mammals [Huck et al., 2014; Komers & Brotherton, 1997; Lukas & Clutton-Brock, 2013], and within primates specifically [Opie et al., 2013; Komers & Brotherton, 1997].

Infanticide prevention hypothesis This hypothesis proposes that infant survival is higher when a male helps a female protect offspring from infanticidal intruders [Palombit, 2000; van Schaik & Dunbar, 1990; van Schaik & Kappeler, 1997; Wolff & Macdonald, 2004]. This strategy is expected when a female’s lactation length is longer than her gestation length, since lactational amenorrhea inhibits a male’s chances of fertilization [van Schaik & Kappeler, 1997]. Infanticide risk is less likely when species lack lactational amenorrhea, and when ovulation is entrained to external cues (e.g., photoperiod) and not responsive to the loss of an infant. It has been argued that a breeding male should remain in close proximity to a female for at least one inter-birth interval to reduce her infant’s vulnerability to infanticide [see Fuentes 2002]. This hypothesis may explain the transition from solitary living to pair-living in taxa, such as early lemurids. It also may explain pair-bonding in primates that form larger groups, such as saki monkeys [Thompson &

Resource defense

Mate defense

Infanticide

Infant care

Optimal group size

Proposes selective pressure for pairs to associate year-round. Within-group agonism and competition are low. Pair associations should not be restricted to the pre-breeding and breeding periods. Proposes selective pressure for solitary individuals to associate with adult of opposite sex during infant dependence. Other selective pressures may drive longer associations. Males help raise offspring. Proposes selective pressure for solitary female to associate with male during infant dependence, until infanticide no longer shortens time to ovulation. Other selective pressures may drive longer associations. Males defend infants. Pair avoids/ agonistic toward extra-pair males. Solitary individuals and potentially some pairs with infants experience infanticide. Proposes selective pressure for prebreeding and breeding associations; ranges shared throughout the year. Mate defense may drive short-term associations in seasonal breeders and longer associations in a seasonal breeders. Males maintain proximity. Females widely distributed in environment; male cannot defend more than one female. Males agonistic toward extra-pair males. Proposes selective pressure for pairs to associate and defend resources year-round. Pairs defend territories. Within-group agonism and competition are low. Solitary individuals do not maintain territories and lose inter-group contests. Pair associations not restricted to the pre-breeding and breeding periods.

Pair-living

Does not propose selective pressure for monogamy. Pairs may mate monogamously depending upon other selective pressures.

Proposes selective pressure for pairs to mate monogamously. Males defend access to females during the pre-breeding and breeding season.

Does not propose selective pressure for pairs to bond. Pairs may bond due to other pressures. Agonistic interactions during pre-breeding and breeding season possible due to conflicts between male and female interests.

Proposes selective pressures for pairs to bond to defend resources together. Bonding varies with food abundance. Either sex maintains bond. Bonding not restricted to breeding season or infant dependency period.

Proposes selective pressure for greater paternity certainty that may result in monogamous mating.

Proposes selective pressure for monogamous mating if parenting costs to the male are high.

Does not propose selective pressure for monogamy. Monogamy due to other selective pressures.

Monogamy

Proposes selective pressure for females to maintain bonds with males during the infant dependency period.

Proposes selective pressure for pairs to bond during the infant dependency period. Bonding may precede infant’s birth in preparation for care.

Does not propose selective pressure for pairs to bond. Pairs may or may not bond depending upon other selective pressures.

Pair-bonding

TABLE I. General Predictions for the Evolution of Pair-Living, Pair-Bonding, and Monogamy According to Five Leading Hypotheses. The Applicability of Each Hypothesis to a Particular Species or System Depends in Part on a Variety of Factors Including Ancestral State and Reproductive Seasonality

Pair-Living, Pair-Bonding, and Monogamy / 5

Am. J. Primatol.

6 / Tecot et al.

Norconk, 2011], but it likely does not explain pairbonding in species who live in pairs [Fuentes, 2002; Palombit, 1999]. Within groups consisting of more adults than a single pair, pair cohesion as infanticide avoidance is expected to be necessary for the early phases of infancy at a minimum, until theoretically it would no longer be beneficial for an outside male to kill the infant if she has already resumed ovulating, or if other adult group members act collectively to repel an invading male. Thus, if infanticide is a strong selective pressure, females should invest heavily in maintaining bonds with males [Palombit, 1999]. Monogamous mating among the pair-bond in gregarious groups is not required for infanticide prevention behaviors, under conditions in which a resident male or set of resident males acts aggressively to repel intruder males. Such defense can occur under conditions of high degrees of intrasexual intolerance between resident males and extragroup males, or if there is a greater than 0% chance of resident male paternity. This hypothesis suggests that infanticide may have selected for pair-living (as an advantage over living solitarily), pair-bonding (in larger groups), and/or monogamy as a male counterstrategy. Some interpret the absence of infanticide as potential evidence of having evolved successful counterstrategies and, alternatively, as evidence that infanticide has played no role in pair-living, pair-bonding, and/or monogamy.

Mate defense hypothesis This hypothesis proposes that when female dispersion is large and polygyny potential is low, a male will have the highest reproductive success if he defends mating access to a female from competing males, thus effectively mating monogamously [Clutton-Brock & Harvey, 1978; Emlen & Oring, 1977; Lukas & Clutton-Brock, 2013; Palombit, 2000]. Hypothetically, when mate defense is the only benefit of interactions between the pair, contact is expected to decrease as the length of the breeding season decreases. Thus, in species with tightly delimited breeding seasons, associations and contact between the pair may be extremely rare. This hypothesis attempts to explain the evolution of monogamous mating, but whether or not it can explain pair-living depends in part on the length and predictability of the breeding season. It does not propose a selective pressure that leads to pairbonding [contra Fuentes, 2002]. Mate defense also can explain the maintenance of monogamous mating and pair-living in response to current intrasexual contest competition. Resource defense hypothesis Similar to the Optimal Group Size Hypothesis, this hypothesis proposes that when resources are highly dispersed, low in quality, or rare, pair-living may represent the most stable strategy [Rutberg,

Am. J. Primatol.

1983; but see Fernandez-Duque, 2015, this volume for an alternative explanation]. However, unique to the RDH, pairs are predicted to work separately or together to defend resources in territories. Early versions of this hypothesis suggested that the male defends resources for a female, rather than with her [e.g., resource brokering, Gowaty, 1996; Wrangham, 1979], primarily to gain mating access. However, this hypothesis does not preclude female participation in territorial defense, and it is likely that males receive significant benefits from resource defense when resources are particularly scarce. Each sex may benefit from shared knowledge of food resource distribution, and females may prefer males that can better defend resources for the pair, based on this shared knowledge [Thalmann, 2001]. Therefore, we suggest that resource defense also may occur when a pair co-defends resources in a range that cannot support more than two adults [Fuentes, 2002]. Some variance in the trait may be expected where a species lives in a food abundant habitat and is released from the constraints of resource scarcity and the need to defend a territory, though their evolved suite of traits and community ecology may further constrain them from adopting a different strategy. This hypothesis applies directly to pair-living, and depending on additional factors may or may not apply to pairbonding and monogamy [Fuentes, 2002; Goldizen, 2003; van Schaik & Dunbar, 1990; Wittenberger & Tilson, 1980; Wright, 1990]. Bonding is expected when the likelihood of encountering competitors while feeding is high, and pair-mates may be more cohesive if they jointly defend resources throughout the year. The spatial distribution of individuals and the degree of bonding within pairs are likely to influence the probability of monogamy (as a secondary adaptation). This hypothesis provides a potential evolutionary explanation for pair-living and pairbonding. It can also explain the maintenance of these traits and monogamy in response to current pressures, particularly where resources are low in quality or scarce even during relatively abundant seasons, or where community ecology constrains the exploitation of resources large enough to accommodate larger groups. It may not be possible to satisfactorily test the above hypotheses against one another because they focus on different traits. Additionally, more than one hypothesis may explain the traits observed in a single species [Clutton-Brock & Janson, 2012]. Future research employing phylogenetic reconstructions can help determine the evolutionary sequence of these traits if they take care to categorize each species along these three axes. Reassessing the RDH in E. rubriventer We now test the RDH to explain pair-living and pair-bonding in red-bellied lemur (E. rubriventer).

Pair-Living, Pair-Bonding, and Monogamy / 7

We chose to explore this hypothesis because a review of the red-bellied lemur’s natural history (discussed below) reveals that this hypothesis seems to provide the most appropriate explanations for the aforementioned traits in this species. At the end of this section, we address the likelihood that the additional four hypotheses can explain pair-living, pair-bonding, and/or monogamy in this species. Little research has focused on the RDH in primates [but see Dr€oscher & Kappeler, 2014; Fernandez-Duque, this volume; Hilgartner et al., 2012; Overdorff & Tecot, 2006; van Schaik & Dunbar, 1990]. Van Schaik and Dunbar [1990] argued that the RDH was unconvincing in explaining “monogamy” (i.e., pair-living and pair-bonding) for primates because there is (1) a lack of interspecific territoriality, (2) frequent occurrence of range overlap, and (3) no evidence that resource defense is essential for reproduction. Since van Schaik and Dunbar [1990] formulated these criticisms, researchers have gathered more data on species, such as gibbons [Suwanvecho & Brockelman, 2012], suggesting that interspecific territoriality is common. Furthermore, while it is likely that access to any single resource may not impact reproduction, continuous encroachment by others into a territory may have a greater impact. Additionally, under conditions in which resources exhibit extreme temporal and spatial patchiness such as occurs in several different types of habitats (e.g., see [Bollen & Donati, 2006]) resource defense can be critical in times of food scarcity. Malagasy primates in particular are an ideal taxon to test the RDH. Madagascar’s rainfall and fruit availability are highly unpredictable [Dewar & Richard, 2007; Wright, 1999,2006]. Soil fertility is low and tree growth is slow, resulting in low tree crown productivity, poor quality fruit, and relatively prolonged periods of fruit scarcity (up to 6 months) [Bollen & Donati, 2005; Ganzhorn et al., 2009; Wright et al., 2005]. These environmental challenges can exacerbate the potential for contest competition within and between groups, and between species. Thus, the ecological pressures to live in small, bonded pair groups may be particularly strong in lemurs. Previous research investigated whether the RDH could explain “monogamy” in the redbellied lemur (E. rubriventer) [Overdorff & Tecot, 2006]. This species lives in pairs that are bonded and mate monogamously (i.e., the same male and female exhibit an exclusive mating relationship that lasts at least 6 years, and based on genetic evidence the male–female pair are the parents of the group’s offspring) [Merenlender, 1993; Overdorff, 1991; Overdorff & Tecot, 2006]. They live in the ecologically unpredictable eastern rainforests of Madagascar and are sensitive to environmental change [Tecot, 2008]. In Ranomafana National Park (RNP) Madagascar, fruit availability was the strongest predictor of fecal

cortisol (anti-stress hormone) levels (compared with behavior and climate), and significantly higher cortisol levels occurred during fruit scarcity [Tecot, 2008, 2013]. There also is strong selection on the timing of reproduction with fruit availability; 0% of infants born out of peak season (August through October) survived [Tecot, 2010]. Using unpublished and previously published results, we reassess the RDH as an explanation for the evolution of pair-living, and then as an explanation for pair-bonding (N.B. this hypothesis does not propose to explain the evolution of monogamous mating). This method allows us to focus on each trait individually and potentially identify support for or against resource defense needs as a driver of their evolution. Most data were collected in RNP during several different studies by various researchers. Methods for each study can be found within the cited material. When reporting unpublished data, associated methods are reported. Reviewing Support for Pair-Living Under the RDH

Prediction 1a Pairs of one adult male and one adult female are stable for at least 1 year and pairs persist through changes in resource availability and reproductive season (N.B. this prediction does not imply spatial cohesion). Based on 33 months of behavioral observations and an additional 5 years of censuses on eight social groups in RNP, it is clear that redbellied lemurs live in stable groups that are best described as an adult pair and their offspring [Merenlender, 1993; Overdorff, 1991; Overdorff & Tecot, 2006]. Solitary males and females have been observed rarely and are presumed to have been in a transitory state of dispersal from their natal groups, or searching for a new group due to the former group’s takeover or dissolution (resulting from an adult group member’s death) [Overdorff &, Tecot 2006]. Pair-groups persist through time, up to at least 6 years, and through demographic changes such as infant births, deaths, and the emigration of offspring at approximately 2.5–4.5 years of age [Merenlender, 1993; Overdorff & Tecot, 2006; Tecot, personal observation]. Prediction 2 Pairs work together to defend home ranges and territorial signaling varies with resource availability [Fuentes, 1998; Hilgartner et al., 2012; Sch€ ulke, 2005; Zinner et al., 2003]. The D index of defensibility [Mitani & Rodman, 1979] compares day range and home range size to determine whether or not a group can feasibly monitor and defend home range boundaries. Territorial primate species have D values above 1, though 0.98 was suggested to more clearly define the difference between territorial and non-

Am. J. Primatol.

8 / Tecot et al.

territorial species [Lowen & Dunbar 1994]. Based on published data on three study groups, red-bellied lemurs exhibit a D value of 0.9 (range 0.14–2.07), with a mean daily path length of 0.44 km (range 0.07–1.02 km) and a home range size of 0.19 km2 [Overdorff, 1991,1993a]. Thus, based solely on this index, red-bellied lemurs should not be considered able to defend their home range. Because this index does not account for detection of intruders via signals, such as olfaction or vision, it may underestimate territoriality. Although the D value for these groups calculated using the mean day range is less than 1, the D value calculated using the maximum day range is higher (D ¼ 2.07) and falls within the range of values expected for territorial species. On days when pairs travel 0.5 km or more (D ¼ 1.02), this index suggests that they can succeed in monitoring the boundaries of their territory on certain days or during certain periods of the year. We do not have data to determine whether or how the D value changes seasonally. Male–female pairs do maintain exclusive access to relatively small (19 ha) home ranges with only 8% overlap (n ¼ 2 groups, 19-ha home range in both groups) [Overdorff, 1993a]. They range evenly throughout their territories, moving through the center and visiting their borders via linear travel on a daily basis [Overdorff, 1991,1993a]. They demonstrate territorial behavior, actively defending their borders against adjacent groups [Overdorff, 1993a; Overdorff & Tecot, 2006]. Ranging activity does not vary seasonally, but is influenced by daily dietary choices [Overdorff, 1993a], which are likely impacted by the fruiting schedules of individual trees and competition from other groups and species. Pairs can use additional or alternative means of maintaining and defending resources in a territory, such as broadcast signals (e.g., duetting or conspicuous vocalizations, scent-marking, non-nutritive tree-gauging; [Geissmann & Mutschler 2006; Rasoloharijaona et al., 2010]). Red-bellied lemurs use scent-marking, and perhaps vocalizations, to demarcate feeding territories [Overdorff, 1988; Overdorff & Tecot, 2006; Tecot, personal observation]. Scent glands are located on the head in males [StangerHall, 1997] and in the anogenital region and the palms in males and females [Schilling, 1979]. The complexity of scent secretions [delBarco-Trillo et al., 2012] and the scent-marking repertoire of redbellied lemurs are most similar to that of pair-living, territorial mongoose lemurs (Eulemur mongoz), but differ in kind from other Eulemur species living in multi-male multi-female groups that are also less territorial [see Colquhoun, 2011]. Red-bellied lemurs use scent glands to mark other individuals (“affiliative scent-marking”) and substrates, and do so more than 34 times more frequently than non-territorial sympatric congeners (Eulemur rufifrons, red-fronted brown lemurs) living in multi-male multi-female

Am. J. Primatol.

groups [Overdorff, 1991; Singletary, 2013], earning them the moniker “Eulemur rubristinker.” Both males and females mark substrates, and males are always within 5 m of their pair-mate when doing so [Overdorff & Tecot, 2006]. Males triplemark home range borders, with a sequence of palmar marks followed by headmarks, followed by anogenital marks [Overdorff, 1991]. Females also mark the home range using anogenital scent-marks, often over-marking male marks on the borders [Overdorff, 1991]. Scent-marking varies with resource availability. Anogenital marking occurs more frequently during food abundance and on important feeding trees, with males marking significantly more than their pair-mates [Overdorff & Tecot, 2006], suggesting that these marks are for resource defense. The red-bellied lemur loud call has not been studied in detail, but Overdorff [1991] suggested that it may be used to defend or demarcate a territory when used by individuals living in pair groups. This call can be heard from a distance of at least 300 m and is used during territorial disputes and when an individual is lost or alone [Overdorff, 1991]. Sympatric, non-territorial red-fronted brown lemurs have very similar call repertoires, yet they lack this loud call [Overdorff, 1991]. It is unknown whether one sex produces this call more than the other, and whether the loud call varies with food resources.

Prediction 3 Within-group agonism between adults is low relative to between-group and between-species agonism; otherwise pair-living would be too costly relative to living solitarily [Overdorff & Tecot, 2006]. Within-group agonism is rare, with only 39 agonistic events (all “cuffing”: striking another individual with a cupped hand) out of approximately 6,300 hr of behavioral observation [1988–1989 study using instantaneous recording on focal animals: rate 0.01/hr, n ¼ 20 events, three social groups, Overdorff & Tecot, 2006; 2003–2005 study using continuous recording on focal animals: rate 0.0004/hr, n ¼ 19 events, five social groups, Tecot, 2008]. Only two of these events occurred between the adult male and female [Overdorff & Tecot, 2006], reflecting the absence of hierarchical relationships as previously reported for the species (contra results from a captive study by Marolf et al. [2007]) [Overdorff & Tecot, 2006]. This level of agonism is consistent with other pair-living species, such as gibbons, owl monkeys, and titi monkeys [Bartlett, 2003; Wright, 1986] and is extremely low compared with lemur species living in multi-male multi-female groups. For example, the mean rate of agonistic interactions in wild redfronted brown lemurs (E. rufifrons) is 0.25 events per individual/hour (Overdorff, unpublished data). Ringtailed lemur (L. catta) males and females are reported to have an annual mean rate of 1.14 agonistic events per individual/hour at the Duke

Pair-Living, Pair-Bonding, and Monogamy / 9

Lemur Center (DLC), Durham, NC [Digby & Kahlenberg, 2002; Pereira & Kappeler, 1997]. Though rates of agonism are generally higher among captive primate populations, agonistic interactions between males and females are reported to occur daily in the wild [see Gould, 1994]. Similarly, intersexual dominance interactions in black lemurs (Eulemur flavifrons) (excluding mating and birth seasons) occurred at a mean rate of 0.81 events per individual/hour at the DLC [Digby & Kahlenberg, 2002]. Rates of agonism in red-bellied lemurs are also low compared with dispersed pair-living lemurs. Wild red-tailed sportive lemurs lack any affiliation, and a mean of 47.3% of encounters between the adult male and female are agonistic [e.g., Hilgartner et al., 2012]. Rates of agonism are not available for this species, and it is difficult to calculate the percent of encounters between red-bellied lemur adult males and females that are agonistic, as they “encounter” each other nearly constantly. For comparison, a percentage of agonistic encounters would be well below 1% (Tecot, unpublished data). Relative to within-group agonism between adults, red-bellied lemurs engage in more between-group agonism (i.e., fights) with conspecifics (mean rate 0.01/hr).

Prediction 4 Between-group and between-species agonism vary with food availability. Between-group agonism rates during periods of food scarcity are ten times higher than during food abundance (mean rates of agonism 0.03/hr and 0.003/hr, respectively), when groups may be forced to come into contact (seasons defined based on phenological patterns at this site; see [Hemingway & Overdorff, 1999] and [Tecot, 2008]) [Overdorff & Tecot, 2006]. The vast majority of interactions with other groups occurred between or along territorial borders at feeding sources, and both males and females participated [Overdorff & Tecot, 2006]. Red-bellied lemurs also interact with other species including red-fronted brown lemurs (Eulemur rufifrons), black and white ruffed lemurs (Varecia variegata), and Milne-Edwards’ sifaka (Propithecus edwardsi) [Overdorff & Tecot, 2006]. Rates of interspecific agonism (mean rate 0.4/hr) are higher than within-group agonism, and they are twice as high during food abundance than food scarcity (mean rates 0.06/hr and 0.03/hr, respectively) [Overdorff & Tecot, 2006]. Red-bellied lemurs are able to exploit smaller trees during fruit scarcity than other primate species living in larger groups, such as red-fronted brown lemurs, effectively eliminating their competitors from their resources. However, during fruit abundance, red-bellied lemurs encounter other species more frequently because there is a greater overlap in core home ranges and diet [Overdorff, 1993a,b]. Several studies have found that inter-specific agonistic interactions occur most frequently with red-fronted brown lemurs, who have the greatest overlap in diet with

red-bellied lemurs compared with other sympatric species. Red-bellied lemurs in RNP lose 86% of interactions with red-fronted brown lemurs (N ¼ 16), and 88% of all inter-specific interactions (N ¼ 57) [de Winter, 2014; Overdorff, 1993a; Overdorff & Tecot, 2006; Wright et al., 2011]. Such interactions can have mortal effects. For example, an adult female red-bellied lemur was found dead 1 day after suffering an injury during an interaction with red-fronted brown lemurs [Tecot and Baden, unpublished data].

Reviewing Support for Pair-Bonding Under the RDH

Prediction 5a Pair members are spatially cohesive (i.e., coordinate behaviors) year-round, suggesting that pairliving is maintained outside of the mating season and infant dependence (in seasonal breeders), as it is important to defend resources throughout the year [Pollock, 1986]. Lemurs generally have one mating season per year, consisting of a very short estrus period (12–48 hr in most species) [e.g., Bogart et al., 1977; Jolly, 1966; Petter-Rousseaux, 1980]. Redbellied lemurs are highly seasonal breeders, with a birth peak between August and October [Tecot, 2010]. They maintain close proximity throughout the entire year, while at rest and traveling [Overdorff, 1988; Tecot & Romine, 2012]. They are within 5 m of another individual in the group (including offspring) over 90% of the time, and adult males and females are each other’s nearest neighbors (within 5 m) 42.9% of the time [Overdorff & Tecot, 2006]. In contrast, dispersed (unbonded) pairs of red-tailed sportive lemurs are within 10 m of each other 25.7% of the time on average, and only 8.8% of the time when excluding the mating season [Hilgartner et al., 2012]. Redbellied lemurs maintain affiliative physical contact quite often, and often rest in a “huddle,” where two or more individuals inactively sit in close or wholebody contact (often with tails wrapped around each other’s bodies) in a hunched or semi-hunched position (Fig. 2) [Pereira et al., 1988]. Singletary [2013] studied four non-reproductive pairs at the DLC. Each pair was housed individually in four connected indoor–outdoor cells, with a total ranging area of 30 m2 per pair. She found that males and females were in physical contact (as measured by huddling, resting in contact, mutual grooming, and allo-grooming) over 20% of the time despite having no possibility of reproducing due to being contracepted, neutered, or considered postreproductive by the DLC [Singletary, 2013]. In the wild, affiliative contact between pair-mates via alloand mutual grooming occurs frequently (0.05 bouts/ hr; this figure may be an underestimate due to the difficulty of observing who is involved in grooming behavior while animals are at rest high in trees) [Overdorff & Tecot, 2006].

Am. J. Primatol.

10 / Tecot et al.

Fig. 2. Red-bellied lemur (Eulemur rubriventer) male and female resting in a huddle. The male is grooming the female. Photo credit: VELONTSARA Jean Baptiste.

Prediction 5b Spatial cohesion of the pair-group varies with food availability [Overdorff & Tecot, 2006]. While resource defense is important throughout the year, constraints on access to resources differ during food abundance and food scarcity. For example, preferred foods may be rare during the scarce season, necessitating spatial cohesion to defend scarce resources; increased dietary overlap between groups and species when resources are abundant [Rehg, 2006] can result in a higher frequency of encounters between groups depending on how resources are distributed. Compared with when food is scarce, during food abundance, adult males and females are more affiliative and in physical contact more often (mutual groom: X2 ¼ 5.07, P < 0.04, df ¼ 1; allogroom: X2 ¼ 3.67, P < 0.05, df ¼ 1), and are more cohesive and spend less time alone (Mann–Whitney U-test male alone Z ¼ 2.85, P < 0.004; female alone Z ¼ 2.41, P < 0.02) [Overdorff & Tecot, 2006], suggesting that resource availability influences pairbond behavior. Prediction 6 Pair-bonds are actively maintained (e.g., via grooming) by both sexes due to their mutual interest in coordinated resource defense [Anzenberger, 1992; Fuentes, 2002; Kleiman, 1977; Palombit, 1996]. Individuals may be expected to weigh the costs and benefits of devoting substantial time and energy fostering relationships with others [Dunbar & Shultz, 2007]. Once individuals have committed to forming a pair-bond, they should invest energy in bond maintenance to decrease the likelihood of partner infidelity and/or desertion [Anzenberger, 1992; Kleiman, 1977]. Affiliative behavior, spatial proximity, and physical contact likely signal mutual willingness to invest in maintaining a bond, or coalition, between pair-mates [Zahavi, 1977; Zahavi, 1987]. Across pair-bonded primate species, observed

Am. J. Primatol.

patterns in who actively initiates bond maintenance are inconsistent across taxa, and may indicate different selective pressures for bonding [e.g., Anzenberger, 1992; Curtis & Zaramody, 1999; Fuentes, 2002; Kinzey & Wright, 1982; Wolovich et al., 2010]. It has been proposed that, where resource defense drives pair-living, females will maintain pairbonds because the costs of living a solitary lifestyle are greater for a female than for a male [Fuentes, 2002]. While we acknowledge that females should play a large role in bond maintenance, males are also expected to actively maintain bonds if they benefit from coordinated resource defense. Red-bellied lemur pair-bonds are actively maintained by both sexes. In RNP, all individuals in the group are equally likely to initiate mutual grooming bouts with each other, though females are less likely to initiate allo-grooming with the adult male [Overdorff & Tecot, 2006]. During travel, the male most often follows the female (70% vs. 30% of all adultled progressions), but in the rare instances when new group formation has been observed, females appear to seek out males [Overdorff & Tecot, 2006; Tecot & Romine, 2012]. Captive red-bellied lemurs housed at the DLC showed no significant differences in how often the male or female approached or initiated contact with their pair-mate [Singletary 2013]. In contrast, at the Parc Zoologique et Botanique in Mulhouse, France, reproductive females in two groups maintained spatial proximity more than males (as indicated by the Hinde-Index) [Marolf et al., 2007]. Further investigation of who maintains pair-bonds under different natural contexts (e.g., pair-bond formation, reproductive stages, food availability seasons) may help explain these conflicting results, though both sexes clearly contribute to pairbond maintenance. Summary of Support for Pair-Living and Pair-Bonding Under the RDH While these data are limited and more study is necessary to fully test the RDH in this species, multiple lines of evidence support the hypothesis that red-bellied lemurs live in pairs for resource defense, and that pair-bonding may function to secure resources as well. Red-bellied lemurs are highly frugivorous, with ripe fruits accounting for 85% of feeding time [Overdorff, 1996; Tecot, 2008]. In RNP, fruit availability can be very low (see [Tecot, 2008] for details), and there are times of the year when only a single tree species fruits, and all frugivores seek that source [RNP records; Tecot, personal observation]. While pair-living can support coordinated resource defense, strong, stable bonds with a high level of spatial cohesion among pairmates may be particularly important during resource scarcity (versus other red-bellied lemur groups) and perhaps resource abundance (versus

Pair-Living, Pair-Bonding, and Monogamy / 11

other species) in this environment. Red-bellied lemur pair-mates use multiple methods of territorial defense, often working together to mark and advertise the territory and participate in agonistic disputes with conspecifics and other species. And, although we have observed only one case in which a pair-mate was injured and died in over 17 years of behavioral observation, we argue that the potentially mortal effects of a such direct competition [Tecot and Baden, unpublished data] may place pressure on the pair to be cohesive, as solitary individuals are unable to maintain territories [see Overdorff & Tecot, 2006]. Research on solitary red-bellied lemurs, and redbellied lemurs that form social groups containing at least three adults such as might occur in the case of delayed dispersal, would help determine if pairs actually have an advantage over solitary individuals and multi-adult groups. Based on data presented by Overdorff [1993a], red-bellied lemur groups are able to exploit smaller trees than sympatric, closely related species who live in larger groups and have similar diets, and who may deplete resources in small tree crowns faster [e.g., red-fronted brown lemur, Overdorff, 1993a], though they still have to contend with other red-bellied lemur groups. Applicability of Alternative Hypotheses in Red-Bellied Lemurs While we found some support for the RDH, it is possible that other hypotheses also may help explain pair-living and pair-bonding, as well as monogamy, in the red-bellied lemur. The Optimal Group Size Hypothesis is very similar to the RDH in suggesting that resource competition drives pair-living, but it also considers predation pressure in regulating group size, and does not require that pairs work together to defend resources (N.B. pair-bonding is not under selective pressure under this hypothesis). Additional research comparing predation rates on solitary individuals versus pair-bonded groups, and groups with three or more adults will help test this hypothesis, though the fact that pairs work together in resource defense suggests that the RDH may be a better fit. It is possible that a combination of these two hypotheses is at play. The Infant Care Hypothesis may explain the maintenance of pair-living, pair-bonding, and monogamy in red-bellied lemurs, but does not likely explain their evolution. Traits associated with paternal care indicate a strong bond that reinforces pair-living, but several lines of evidence suggest that paternal care likely evolved after pair-living and pair-bonding in these primates [Komers & Brotherton, 1997; Lukas & Clutton-Brock, 2013; Opie et al., 2013]. Once pairs are bonded throughout the year, males likely have less opportunity to find additional mates, which can result in strong pressure for monogamy, and increased paternity certainty. In

RNP, inter-birth intervals in red-bellied lemurs are approximately 24 months, and though singletons are most common, twinning occurs regularly (one pair in 5.6 births) [see Tecot, 2010]. Some fathers and siblings help with infant carrying to varying degrees [Hosey et al., 2003; Overdorff, 1991; Tecot et al., 2012,13; Tecot and Baden, unpublished data], particularly when twins are present. It has been suggested that faster rates of infant growth and time to reach developmental landmarks in red-bellied lemurs, relative to congeneric species who lack paternal and sibling care, may explain these different infant care strategies [Overdorff, 1996]. However, the precise factors that select for this facultative infant care in red-bellied lemurs, and whether faster development is a cause or consequence of shared infant care, remain unclear [De Michelis et al., 1999; Overdorff, 1991; but see Tecot et al., 2012]. More research on the context in which facultative paternal (and sibling) care occurs will help us determine the environmental pressures promoting these behaviors. Infanticide avoidance is not a likely pressure selecting for pair-living and pair-bonding in relatively large-bodied lemurs in general because reproduction is highly responsive to photoperiod; infanticide will not bring a female into ovulation sooner. In contrast, red-bellied lemurs have shown greater flexibility in the timing of reproduction with infants born in eight different months, and 23.3% of infants born outside of the birth peak [Tecot, 2010]. The mechanism affecting the timing of ovulation in redbellied lemurs is as yet unknown [Tecot, 2010]. Infanticide has not been reported in red-bellied lemurs in RNP, and based on 28 individuals in six social groups, there is genetic evidence that pairs mate monogamously [Merenlender, 1993]. The pairbond in red-bellied lemurs persists for several years. Pairs are agonistic toward both adult extra-group males and females (and other species). Females help defend against intruders of both sexes, and are not significantly different in body mass from males; therefore they likely do not require males to defend them. The Mate Defense Hypothesis can explain the evolution of pair-living in some primate species [e.g., Brotherton & Komers, 2003; Fuentes, 2000; Gursky, 2003; Hilgartner et al., 2008; Hilgartner et al., 2012; Palombit, 1996; Palombit, 1999]. In red-bellied lemurs, this hypothesis can be difficult to assess: over the course of 25 years of study by D. Durham, R. Jacobs, D. Overdorff, B. O. Razafindratsima, B. Singletary, S. Tecot, and numerous local field technicians with whom they work, there have been only two instances (both in 2014) in which mating was observed in red-bellied lemurs (J. Krauss, personal communication; Tecot and Baden, unpublished data). In each instance, mating lasted approximately 15 sec, no extra-group males were observed, and no inter-group interactions occurred. Aside from

Am. J. Primatol.

12 / Tecot et al.

these anecdotes, whether mates are guarded is unknown. There is, however, no evidence of extrapair copulations as indicated by genetic paternity analysis as noted above [Merenlender 1993]. Pairs are cohesive year-round, both sexes are equally responsible for maintaining proximity, and males (and females) direct agonism toward both male and female conspecifics [Tecot, unpublished data], as well as toward individuals of other species who are not potential mates. Thus, resources seem to be the stronger pressure for pair-living (N.B. pairbonding is not under selective pressure under the Mate Defense Hypothesis, Table 1). CONCLUSIONS Using clearly defined terms is critical to investigate and compare differences and similarities in traits associated with reproductive and social bonding in primates. Different evolutionary pressures may lead to the appearance of pair-living, pairbonding, or monogamy, as exemplified by variation in their co-occurrence in strepsirrhine primates (Table S1). If we continue to conflate these traits, we may miss important evolutionary processes acting on species, or misinterpret what shapes the patterns we see today. Future research will better elucidate the selective pressures maintaining the expression of pair-living, pair-bonding, and monogamy in primates if researchers studying a broad range of taxa coordinate their efforts and collect systematic measures to quantify the strength of bonds, ancestral states, and intraspecific variation in pair-living, pair-bonding, and monogamy [Kappeler 2014]. Efforts to operationalize measures of pair-living, pair-bonding, and monogamy will allow us to test current hypotheses and generate new hypotheses regarding the costs and benefits of alternative reproductive and social strategies. Only then will we be equipped to more fully explain the evolution of such distinctive traits in primates. ACKNOWLEDGMENTS We thank Karen Bales and Samuel DiazMunoz for their kind invitation to contribute to the symposium at the American Society of Primatologists conference that resulted in this special issue, and their feedback. We are also grateful for the thoughtful comments of Paul Garber and anonymous reviewers on earlier drafts. We thank Deborah Overdorff for the initial inspiration and collaboration that led to this work. We are grateful to Madagascar National Parks, the Ministere des Eaux et Forets, the Universite de Madagascar, Centre ValBio, Institute for the Conservation of Tropical Environmetns (USA and Madagascar), and Erin Ehmke and the DLC for support and permission to conduct research. We thank Rakotonirina L, Telo A, Rasendrinirina V, Rakotonirina TE,

Am. J. Primatol.

Rakotoniaina JF, Waters D, Calhoon T, Hall A, Cortes N, and M. Silva for their help, dedication, and expertise. ST also thanks Luecke L, Muchlinski M, Pavao-Zuckerman B, and Zhang Q for support. Research complied with protocols approved by Animal Care and Use Committees at UT-Austin and UA/DLC, Duke University, and adhered to Madagascar’s national laws. REFERENCES Anzenberger G. 1992. Monogamous social systems and paternity in primates. In: Martin R, Dixson A, Wickings E, editors. Paternity in primates: genetic tests and theories. Basel: Karger Press. p 203–224. Anzenberger G, Mendoza SP, Mason WA. 1986. Comparative studies of social behavior in Callicebus and Saimiri: behavioral and physiological responses of established pairs to unfamiliar pairs. American Journal of Primatology 11:37–51. Bartlett TQ. 2003. Intragroup and intergroup social interactions in white-handed gibbons. International Journal of Primatology 24:239–259. Bogart MH, Kumamoto AT, Lasley B. 1977. A comparison of the reproductive cycle of three species of lemur. Folia Primatologica 28:134–143. Bollen A, Donati G. 2005. Phenology of the littoral forest of Sainte Luce, southeastern Madagascar. Biotropica 37:32– 43. Bonadonna G, Torti V, Randrianarison RM, Martinet N, Gamba M, Giacoma C. 2014. Behavioral correlates of extra-pair copulation in Indri indri. Primates 55:119– 123. Brotherton PN, Komers PE. 2003. Mate guarding and the evolution of social monogamy in mammals. In: Reichard U, Boesch C, editors. Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge: Cambridge University Press. p 42–58. Clutton-Brock T. 1989. Review lecture: mammalian mating systems. Proceedings of the Royal Society of London B: Biological Sciences 236:339–372. Clutton-Brock T, Harvey PH. 1978. Mammals, resources and reproductive strategies. Nature 273:191–195. Clutton-Brock TH, Janson C. 2012. Primate socioecology at the crossroads: past, present, and future. Evolutionary Anthropology 21:136–150. Colquhoun IC. 2011. A review and interspecific comparison of nocturnal and cathemeral strepsirhine primate olfactory behavioural ecology. International Journal of Zoology 36:362976. Curtis D, Zaramody A. 1999. Social structure and seasonal variation in the behaviour of Eulemur mongoz. Folia Primatologica 70:79–96. De Michelis S, De Trani C, Moisson P. 1999. Preliminary results on the behavioural development of three new-born lemurs (Eulemur rubriventer, Eulemur macaco flavifrons) at Mulhouse Zoo. Folia Primatologica 70:215–216. de Winter I. 2014. The coexistence of two congeneric lemur species: niche separation and competition as underlying mechanisms [MA Thesis] Netherlands: Wageningen University. delBarco-Trillo J, Sacha CR, Dubay GR, Drea CM. 2012. Eulemur, me lemur: the evolution of scent-signal complexity in a primate clade. Philosophical Transactions of the Royal Society B: Biological Sciences 367:1909– 1922. Dewar RE, Richard AF. 2007. Evolution in the hypervariable environment of Madagascar. Proceedings of the National Academy of Sciences 104:13723–13727.

Pair-Living, Pair-Bonding, and Monogamy / 13

Dewsbury DA. 1988. The comparative psychology of monogamy. In: Leger D, editor. Comparative perspectives in modern psychology: Nebraska symposium on motivation, 1987. Lincoln: University of Nebraska Press. p 1–50. Digby LJ, Kahlenberg SM. 2002. Female dominance in blueeyed black lemurs (Eulemur macaco flavifrons). Primates 43:191–199. Dr€ oscher I, Kappeler P. 2014. Competition for food in a solitarily foraging folivorous primate (Lepilemur leucopus)? American Journal of Primatology 76:842–854. Dunbar RI, Shultz S. 2007. Evolution in the social brain. Science 317:1344–1347. Emlen ST, Oring LW. 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223. Fernandez-Duque E. 2015. Social monogamy in wild owl monkeys (Aotus azarae) of Argentina: the potentail influences of resource distribution and ranging patterns. American Journal of Primatology. In press. Fietz J. 1999. Monogamy as a rule rather than exception in nocturnal lemurs: the case of the fat-tailed dwarf lemur, Cheirogaleus medius. Ethology 105:255–272. Fietz J, Dausmann KH. 2003. Costs and potential benefits of parental care in the nocturnal fat-tailed dwarf lemur (Cheirogaleus medius). Folia Primatologica 74:246–258. Fietz J, Zischler H, Schwiegk C, Tomiuk J, Dausmann KH, Ganzhorn JU. 2000. High rates of extra-pair young in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius. Behavioral Ecology and Sociobiology 49:8–17. Fuentes A. 1998. Re-evaluating primate monogamy. American Anthropologist 100:890–907. Fuentes A. 2000. Hylobatid communities: changing views on pair bonding and social organization in hominoids. American Journal of Physical Anthropology 113:33–60. Fuentes A. 2002. Patterns and trends in primate pair bonds. International Journal of Primatology 23:953–978. Ganzhorn JU, Arrigo-Nelson S, Boinski S, et al. 2009. Possible fruit protein effects on primate communities in Madagascar and the Neotropics. PLoS One 4:e8253. Garber P. A., Porter L. M., Spross J, Di Fiore A. D. 2015. Tamarins: insights into monogamous and non-monogamous single female social and breeding systems. American Journal of Primatology. doi: 10.1002/ajp.22370 Geissmann T, Mutschler T. 2006. Diurnal distribution of loud calls in sympatric wild indris (Indri indri) and ruffed lemurs (Varecia variegata): implications for call functions. Primates 47:393–396. Goldizen AW. 2003. Social monogamy and its variations in callitrichids: do these relate to the costs of infant care. In: Reichard UH, Boesch C, editors. Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge: Cambridge University Press. p 232– 247. Gould L. 1994. Patterns of affiliative behavior in adult male ringtailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve, Madagascar [Dissertation] St. Louis, MO: Washington University in St. Louis. Gould L. 1996. Male-female affiliative relationships in naturally occurring ringtailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve, Madagascar. American Journal of Primatology 39:63–78. Gowaty PA. 1996. Battles of the sexes and origins of monogamy. In: Black J, editor. Partnerships in birds: the study of monogamy. Oxford: Oxford University Press. p 21– 52. Gursky S. 2003. Territoriality in the spectral tarsier, Tarsius spectrum. In: Wright P, Simons E, Gursky S, editors. The tarsiers: past, present and future. New Brunswick, NJ: Rutgers University Press. p 221–236. Hemingway CA, Overdorff DJ. 1999. Sampling effects on food availability estimates: phenological method, sample size, and species composition. Biotropica 31:354–364.

Hilgartner R, Zinner D, Kappeler PM. 2008. Life history traits and parental care in Lepilemur ruficaudatus. American Journal of Primatology 70:2–11. Hilgartner R, Fichtel C, Kappeler PM, Zinner D. 2012. Determinants of pair-living in red-tailed sportive lemurs (Lepilemur ruficaudatus). Ethology 118:466–479. Hosey G, Hughes J, Bournes E. 2003. Observations on some rare infant lemurs. Zoologische Garten 73:55–58. Huck M, Fernandez-Duque E, Babb P, Schurr T. 2014. Correlates of genetic monogamy in socially monogamous mammals: insights from Azara’s owl monkeys. Proceedings of the Royal Society B: Biological Sciences 281:20140195. Jolly A. 1966. Lemur behavior: a madagascar field study. Chicago: University of Chicago Press. Kappeler P. 2014. Lemur behavior informs the evolution of social monogamy. Trends in Ecology and Evolution 29:591– 593. Kappeler PM, van Schaik CP. 2002. Evolution of primate social systems. International Journal of Primatology 23:707–740. Kinzey WG, Wright PC. 1982. Grooming behavior in the titi monkey (Callicebus torquatus). American Journal of Primatology 3:267–275. Kleiman DG. 1977. Monogamy in mammals. Quarterly Review of Biology 39–69. Kleiman DG, Malcolm J. 1981. The evolution of male parental investment in mammals. In: Gubernick D, Klopfer P, editors. Parental care in mammals. New York: Plenum Press. p 347–387. Komers PE, Brotherton PN. 1997. Female space use is the best predictor of monogamy in mammals. Proceedings of the Royal Society of London B: Biological Sciences 264:1261– 1270. Lack D. 1968. Ecological adaptations for breeding in birds. London: Methuen. Low BS. 2003. Ecological and social complexities in human monogamy. In: Reichard UH, Boesch C, editors. Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge, UK: Cambridge University Press. p 161–176. Lowen C, Dunbar R. 1994. Territory size and defendability in primates. Behavioral Ecology and Sociobiology 35: 347–354. Lukas D, Clutton-Brock TH. 2013. The evolution of social monogamy in mammals. Science 341:526–530. Marlowe F. 2000. Paternal investment and the human mating system. Behavioural Processes 51:45–61. Marolf B, McElligott AG, M€ uller AE. 2007. Female social dominance in two Eulemur species with different social organizations. Zoo Biology 26:201–214. Merenlender A. 1993. The Effects of sociality on the demography and genetic structure of Lemur fulvus rufus (polygamous) and Lemur rubriventer (monogamous) and the conservation implications [Dissertation] Rochester, NY: University of Rochester. Mitani JC, Rodman PS. 1979. Territoriality: the relation of ranging pattern and home range size to defendability, with an analysis of territoriality among primate species. Behavioral Ecology and Sociobiology 5:241–251. M€ uller AE, Thalmann URS. 2000. Origin and evolution of primate social organisation: a reconstruction. Biological Reviews 75:405–435. Norscia I, Borgognini-Tarli SM. 2008. Ranging behavior and possible correlates of pair-living in southeastern avahis (Madagascar). International Journal of Primatology 29:153–171. Opie C, Atkinson QD, Dunbar RIM, Shultz S. 2013. Male infanticide leads to social monogamy in primates. Proceedings of the National Academy of Sciences 110:13328– 13332. Orians GH. 1969. On the evolution of mating systems in birds and mammals. American Naturalist 103:589–603.

Am. J. Primatol.

14 / Tecot et al.

Overdorff D. 1988. Preliminary report on the activity cycle and diet of the red-bellied lemur (Lemur rubriventer) in Madagascar. American Journal of Primatology 16:143–153. Overdorff DJ. 1991. Ecological correlates to social structure in two prosimian primates: Eulemur fulvus rufous and Eulemur rubriventer in Madagascar [Dissertation] Durham, NC: Duke University. Overdorff DJ. 1993a. Ecological and reproductive correlates to range use in red-bellied lemurs (Eulemur rubriventer) and rufous lemurs (Eulemur fulvus rufus). In: Kappeler P, Ganzhorn J, editors. Lemur social systems and their ecological basis. New York: Springer. p 167–178. Overdorff DJ. 1993b. Similarities, differences, and seasonal patterns in the diets of Eulemur rubriventer and Eulemur fulvus rufus in the Ranomafana National Park, Madagascar. International Journal of Primatology 14:721–753. Overdorff DJ. 1996. Ecological correlates to social structure in two lemur species in Madagascar. American Journal of Physical Anthropology 100:487–506. Overdorff DJ, Tecot SR. 2006. Social pair-bonding and resource defense in wild red-bellied lemurs (Eulemur rubriventer). In: Gould L, Sauther M, editors. Lemurs: ecology and adaptation. New York: Springer. p 235–254. Palombit RA. 1996. Pair bonds in monogamous apes: a comparison of the siamang Hylobates syndactylus and the white-handed gibbon Hylobates lar. Behaviour 133:321– 356. Palombit RA. 1999. Infanticide and the evolution of pair bonds in nonhuman primates. Evolutionary Anthropology Issues News and Reviews 7:117–129. Palombit RA. 2000. Infanticide and the evolution of malefemale bonds in animals. In: van Schaik C, Janson C, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p 239–268. Pereira ME, Kappeler PM. 1997. Divergent systems of agonistic behaviour in lemurid primates. Behaviour 134:225–274. Pereira ME, Seeligson ML, Macedonia JM. 1988. The behavioral repertoire of the black-and-white ruffed lemur, Varecia variegata variegata (Primates: Lemuridae). Folia Primatologica 51:1–32. Petter-Rousseaux A. 1980. Seasonal activity rhythms, reproduction, and body weight variations in five sympatric nocturnal prosimians, in simulated light and climatic conditions. In: Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, editors. Nocturnal Malagasy primates. New York: Academic Press. p 137– 152. Pollock JI. 1986. The song of the indris (Indri indri; Primates: Lemuroidea): natural history, form, and function. International Journal of Primatology 7:225–264. Powzyk JA. 1997. The Socio-ecology of two sympatric indriids: Propithecus diadema diadema and Indri indri, a comparison of feeding strategies and their possible repercussions on species-specific behaviors [Dissertation] Durham, NC: Duke University. Rasoloharijaona S, Randrianambinina B, Joly-Radko M. 2010. Does nonnutritive tree gouging in a rainforest-dwelling lemur convey resource ownership as does loud calling in a dry forest-dwelling lemur? American Journal of Primatology 72:1062–1072. Rehg JA. 2006. Seasonal variation in polyspecific associations among Callimico goeldii, Saguinus labiatus, and S. fuscicollis in Acre, Brazil. International Journal of Primatology 27:1399–1428. Reichard UH. 2003. Monogamy: past and present. In: Reichard UH, Boesch C, editors. Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge, UK: Cambridge University Press. p 3–25. Rutberg AT. 1983. The evolution of monogamy in primates. Journal of Theoretical Biology 104:93–112.

Am. J. Primatol.

Schilling A. 1979. Olfactory communication in prosimians. In: Dayle G, Martin R, editors. The study of Prosimian behavior. New York: Academic Press. p 461–542. Sch€ ulke O. 2005. Evolution of pair-living in Phaner furcifer. International Journal of Primatology 26:903–919. Sch€ ulke O, Kappeler PM. 2003. So near and yet so far: territorial pairs but low cohesion between pair partners in a nocturnal lemur, Phaner furcifer. Animal Behaviour 65:331–343. Sch€ ulke O, Kappeler PM, Zischler H. 2004. Small testes size despite high extra-pair paternity in the pair-living nocturnal primate Phaner furcifer. Behavioral Ecology and Sociobiology 55:293–301. Shultz S, Opie C, Atkinson QD. 2011. Stepwise evolution of stable sociality in primates. Nature 479:219–222. Singletary B. 2013. Monogamy, pair-bonding, and complex signal use: a review of the primate order and a preliminary case study of Eulemur rubriventer [MA Thesis] Tucson, AZ: The University of Arizona. Smuts BB, Gubernick DJ. 1992. Male-infant relationships in nonhuman primates: paternal investment or mating effort. In: Hewlett B, editor. Father-child relations: cultural and biosocial contexts. Brunswick, NJ: Transaction Publishers. p 1–30. Stanger-Hall KF. 1997. Phylogenetic affinities among the extant Malagasy lemurs (Lemuriformes) based on morphology and behavior. Journal of Mammalian Evolution 4:163– 194. Suwanvecho U, Brockelman WY. 2012. Interspecific territoriality in gibbons (Hylobates lar and H. pileatus) and its effects on the dynamics of interspecies contact zones. Primates 53:97–108. Tecot S. 2008. Seasonality and predictability: the hormonal and behavioral responses of the red-bellied lemur, Eulemur rubriventer, in southeastern Madagascar [Dissertation] Austin, TX: The University of Texas at Austin. Tecot S. 2010. It’s all in the timing: birth seasonality and infant survival in Eulemur rubriventer. International Journal of Primatology 31:715–735. Tecot S. 2013. Variable energetic strategies in disturbed and undisturbed rain forests: Eulemur rubriventer fecal cortisol levels in south-eastern Madagascar. In: Masters J, Gamba M, Genin F, Tuttle R, editors. Leaping ahead: advances in prosimian biology (Developments in primatology: progress and prospects). New York: Springer. p 185–195. Tecot S, Romine N. 2012. Leading ladies: leadership of group movements in a pair-living, co-dominant, monomorphic primate across reproductive stages and fruit availability seasons. American Journal of Primatology 74:591–601. Tecot S, Baden A, Romine N, Kamilar J. 2012. Infant parking and nesting, not allomaternal care, influence Malagasy primate life histories. Behavioral Ecology and Sociobiology 66:1375–1386. Tecot S, Baden A, Romine N, Kamilar J. 2013. Reproductive strategies in Malagasy strepsirhines. In: Clancy K, Hinde K, Rutherford J, editors. Building babies: primate development in proximate and ultimate perspective (Developments in primatology: progress and prospects). New York: Springer. p 321–359. Terborgh J, Janson C. 1986. The socioecology of primate groups. Annual Review of Ecology and Systematics 17:111– 136. Thalmann U. 2001. Food resource characteristics in two nocturnal lemurs with different social behavior: Avahi occidentalis and Lepilemur edwardsi. International Journal of Primatology 22:287–324. Thompson CL, Norconk MA. 2011. Within-group social bonds in white-faced saki monkeys (Pithecia pithecia) display male-female pair preference. American Journal of Primatology 73:1051–1061.

Pair-Living, Pair-Bonding, and Monogamy / 15

Thornhill R, Alcock J. 1983. The evolution of insect mating systems. Cambridge, MA: Harvard University Press. Torti V, Gamba M, Rabermanajara Z, Giacoma C. 2013. The songs of the indris (Mammalia: Primates: Indridae): contextual variation in the long-distance calls of a lemur. Italian Journal of Zoology 80:596–607. Trivers RL. 1972. Parental investment and sexual selection. In: Campbell B, editor. Sexual selection and the descent of man 1871–1971. Chicago: Aldine -Atherton. p 136–179. van Schaik C, Dunbar R. 1990. The evolution of monogamy in large primates: a new hypothesis and some crucial tests. Behaviour 115:30–62. van Schaik CP, Kappeler PM. 1997. Infanticide risk and the evolution of male-female association in primates. Proceedings of the Royal Society of London B: Biological Sciences 264:1687–1694. Weatherhead PJ, Robertson RJ. 1979. Offspring quality and the polygyny threshold: “the sexy son hypothesis”. American Naturalist 113:201–208. Wickler W, Seibt U. 1983. Monogamy: an ambiguous concept. In: Bateson P, editor. Mate choice. Cambridge: Cambridge University Press. p 33–50. Wittenberger JF, Tilson RL. 1980. The evolution of monogamy: hypotheses and evidence. Annual Review of Ecology and Systematics 11:197–232. Wolff JO, Macdonald DW. 2004. Promiscuous females protect their offspring. Trends in Ecology and Evolution 19:127– 134. Wolovich CK, Evans S, Green SM. 2010. Mated pairs of owl monkeys (Aotus nancymaae) exhibit sex differences in response to unfamiliar male and female conspecifics. American Journal of Primatology 72:942–950. Wrangham R. 1979. On the evolution of ape social systems. Social Science Information 18:336–368. Wright PC. 1986. Ecological correlates of monogamy in Aotus and Callicebus. In: Else JG, Lee PC, editors. Primate ecology and conservation. Cambridge: Cambridge University Press. p 159–167.

Wright PC. 1990. Patterns of paternal care in primates. International Journal of Primatology 11:89–102. Wright PC. 1999. Lemur traits and Madagascar ecology: coping with an island environment. American Journal of Physical Anthropology 110:31–72. Wright PC. 2006. Considering climate change effects in lemur ecology and conservation. In: Gould L, Sauther ML, editors. Lemurs: ecology and adaptation. New York: Springer. p 385–401. Wright PC, Razafindratsita VR, Pochron ST, Jernvall J, Boubli J. 2005. The key to Madagascar frugivores. In: Dew L, editor. Tropical fruits and frugivores: the search for strong interactors. Netherlands: Springer. p 121–138. Wright PC, Tecot SR, Erhart EM, Baden AL, King SJ, Grassi C. 2011. Frugivory in four sympatric lemurs: implications for the future of Madagascar’s forests. American Journal of Primatology 73:585–602. Wynne-Edwards KE. 1987. Evidence for obligate monogamy in the Djungarian hamster, Phodopus campbelli: pup survival under different parenting conditions. Behavioral Ecology and Sociobiology 20:427–437. Zahavi A. 1977. The testing of a bond. Animal Behaviour 25:246–247. Zahavi A. 1987. The theory of signal selection and some of its implications. In: Delfino V, editor. International symposium of biological evolution. Bari, Italy: Adriatica Editrice. p 305– 327. Zinner D, Hilgartner RD, Kappeler PM, Pietsch T, Ganzhorn JU. 2003. Social organization of Lepilemur ruficaudatus. International Journal of Primatology 24: 869–888.

Supporting Information Additional supporting information may be found in the online version of this article at the publisher’s web-site.

Am. J. Primatol.

Why "monogamy" isn't good enough.

Rare in mammals but more common in primates, there remains a considerable controversy concerning whether primate species traditionally described as mo...
381KB Sizes 0 Downloads 7 Views