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2019, Royal Anthropological Institute - Occasional Paper - Dunbar's Number
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16 pages
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There has been a long history of attempts to explain the evolution of monogamy in mammals in general (Kleiman 1977), and primates in particular (Alexander 1979), partly because of the implications that it may have for the evolution of monogamy in humans. Monogamy is a complex term though, with some species invariably found in pairs (such as owl monkeys), whereas other species can be monogamous, but flexibly take up other mating systems (such as callitrichid monkeys). Humans fit with the latter flexible group, as well as having the additional distinction between their mating system and their marriage system. However, it is fairly well established that monogamy is common in birds (90% of species) (Lack 1968) due to the short time period between mating and egg laying that allows a male to increase his reproductive success through sharing high levels of offspring care (incubating, hatching and rearing), rather than leaving the female he has just mated with to look for other females with whom to mate. The particular reproductive strategy of mammals, with a long gestation period followed by lactation, reduces the opportunities for a male to provide direct care for his offspring, therefore most males move on after mating to seek other fertile females. As a result, monogamy is rare among mammals (5% of species) (Lukas and Clutton-Brock 2013). It is surprising, then, that monogamy is unusually prevalent in one particular mammal order, namely the primates (where 30% of species are monogamous) (Opie, et al. 2013a), with monogamy occurring in all the major primate families (Opie, et al. 2012).
1992
In the first study conducted on a monogamous neotropical primate, the titi monkey Callicebus moloch, Mason [1] already touched on the topics and problems to be dealt with in the following paper. Mason found that (a) titi monkey groups usually consist of an adult pair and one or more young, (b) there are many indications that the bond between mates is strong and enduring, and (c) the adult male carried the infant at virtually all times. This citation illustrates three levels at which we can deal with monogamy, namely the sociographic, the motivational, and the functional level. Traditionally, behavioral studies rely on all three levels, and commonly provide a basis from which the entire social system or mating system of a given species is inferred [for a detailed discussion of such problems when dealing with the topic of monogamy, see ref. 2]. There was, however, an additional observation reported in Mason's paper, namely that'animals will occasionally copulate with members of adjacent groups', which brings us to the genetic level of monogamy and vividly illustrates the fact that grouping pattern and behavioral mechanisms do not necessarily reflect the genetic reiationships within a social unit. In other words, it is almost impogsible to establish genetic relationships in field studies by using behavioral observations alone. Wickler [3] wrote: 'If the term monogamy is to remain biologically meaningful it must imply that one or both partner(s) will produce offspring exclusively with the otherregardless by what behaviour mechanism this exclusiveness is ensured'. From this, it
American Anthropologist, 1998
Researchers propose hypotheses for the occurrence of monogamy as a social system in primates based on the assumption that there are a group of primates, including humans, which live exclusively in "nuclear families" and share a similar set of social behaviors. Examining the primates purported to be "monogamous" reveals that they cover a wide range of grouping types, mating patterns, taxonomic groups, and evolutionary grades. While there are a few primate species that do live in small, two-adult groups and share a similar set of social behaviors, the vast majority of the supposed "monogamous" primates, including humans, do not. [monogamy, social systems, evolution, variability in social organization]
Proceedings of the National Academy of Sciences.
Although common in birds, social monogamy, or pair-living, is rare among mammals because internal gestation and lactation in mammals makes it advantageous for males to seek additional mating opportunities. A number of hypotheses have been proposed to explain the evolution of social monogamy among mammals: as a male mate-guarding strategy, because of the benefits of biparental care, or as a defense against infanticidal males. However, comparative analyses have been unable to resolve the root causes of monogamy. Primates are unusual among mammals because monogamy has evolved independently in all of the major clades.
Proceedings of the Royal Society B: Biological Sciences, 2014
Understanding the evolution of mating systems, a central topic in evolutionary biology for more than 50 years, requires examining the genetic consequences of mating and the relationships between social systems and mating systems. Among pair-living mammals, where genetic monogamy is extremely rare, the extent of extra-group paternity rates has been associated with male participation in infant care, strength of the pair bond and length of the breeding season. This study evaluated the relationship between two of those factors and the genetic mating system of socially monogamous mammals, testing predictions that male care and strength of pair bond would be negatively correlated with rates of extra-pair paternity (EPP). Autosomal microsatellite analyses provide evidence for genetic monogamy in a pair-living primate with bi-parental care, the Azara's owl monkey (Aotus azarae). A phylogenetically corrected generalized least square analysis was used to relate male care and strength of the pair bond to their genetic mating system (i.e. proportions of EPP) in 15 socially monogamous mammalian species. The intensity of male care was correlated with EPP rates in mammals, while strength of pair bond failed to reach statistical significance. Our analyses show that, once social monogamy has evolved, paternal care, and potentially also close bonds, may facilitate the evolution of genetic monogamy.
American Journal of Physical Anthropology, 2005
Behavioral Ecology and Sociobiology, 2011
The evolution of social monogamy in larger mammals is difficult to explain because males usually do not invest much in direct offspring care and might achieve greater fitness by deserting a pregnant female to reproduce with additional females elsewhere. It has been hypothesized that socially monogamous males remain with the female year-round to protect their offspring from infanticide by new immigrant males. We investigated this idea by analyzing all cases of infant loss in a wild population of white-handed gibbons (Hylobates lar; Primates), in which most groups were socially monogamous and some polyandrous (137.5 group years). We examined the influence of (a) male intruder pressure on male immigration rates and (b) the presence of a new male in the group on infant loss. We found no relation between intruder pressure and male immigration rates. Infant loss was lowest (4.5%) for stable monogamy (probable father stayed from conception through infancy) and intermediate (25.0%; p=0.166) for stable polyandry. If a new male immigrated after conception, however, the infant was lost in all cases (p<0.01) independent of the presumed father's presence. Overall, 83.3% of infant losses were associated with the presence of a presumably unrelated male. Although the sample size is small, our results provide the first true support for the idea that the risk of infanticide is an important factor in the evolution of social monogamy in larger mammals.
Frontiers in Ecology and Evolution, 2018
Background: We still do not understand the key drivers or prevalence of genetic monogamy in mammals despite the amount of attention that the evolution of mammalian monogamy has received. There have been numerous reviews of the hypotheses proposed to explain monogamy, some of which focused on animals in general, while others focused on particular classes like birds or mammals, or on specific orders within a class. Because monogamy is rare in mammals overall but relatively common in some of the orders in which it has been observed (e.g., Primates, Macroscelidea, and Carnivora), mammals provide a unique taxon in which to study the evolution and maintenance of monogamy However, the term "monogamy" encompasses related but separate phenomena; i.e., social monogamy (pair-living by opposite-sex conspecifics) and genetic monogamy or reproductive monogamy (mating exclusivity). A recent review of mammalian monogamy reported that 226 species (9%) in 9 orders (35%) were socially monogamous, although socially monogamous mammals are not necessarily genetically monogamous. Methods: Since factors that predispose socially monogamous mammals to be genetically monogamous are still subject to debate, we conducted meta-analyses using model selection to determine the relative importance of several life history, demographic, and environmental factors in predicting genetic monogamy. Results: We found sufficient data to include 41 species in our analysis, about 2x more than have been included in previous analyses of mammalian genetic monogamy. We found that living as part of a socially monogamous pair vs. in a group was the best predictor of genetic monogamy, either by itself or in combination with high levels of paternal care. A male-biased sex ratio and low population density were inversely related to the number of pairs that were genetically monogamous, but not to the production of intra-pair young or litters. Conclusion: Our results agree with the results of some previous analyses but suggest that more than one factor may be important in driving genetic monogamy in mammals.
Frontiers in Ecology and Evolution, 2020
Editorial on the Research Topic What's Love Got to Do With It: The Evolution of Monogamy Monogamy and pair-bonding are central to the human experience in the majority of cultures worldwide (Schacht and Kramer), which might explain the long-running fascination scientists have for understanding monogamy within mammals and across other taxa. The inherent interest in monogamy in western cultures, in part, may be a result of anthropomorphism and a belief that who we mate with defines us. Nevertheless, monogamy captivates the human mind and has been the subject matter in art, religion and literature for centuries. It is a topic that has brought together researchers from diverse backgrounds including anthropology, behavioral ecology, psychology, psychiatry, pediatrics, neurobiology, endocrinology, and molecular biology. There is still much we do not understand about monogamy. A collective, systematic, and concerted effort toward answering questions surrounding the meaning of monogamy is overdue. This Research Topic aimed to bring experts, from a variety of disciplines and conceptual approaches, together to showcase our current understanding of monogamy. This issue is composed of articles focusing on the specific and general aspects of monogamy within a variety of species, and taking empirical, methodological, conceptual, or theoretical approaches to provide a deeper and more complete understanding of aspects of behavior that comprise monogamy, its evolution, and its meaning. The term "monogamy" can be used in very different contexts or ways, emphasizing the need to carefully delineate or define terminology. This is a critical concern because not only can there be confusion between different forms of monogamy (e.g., "social" and "genetic" monogamy), but also about the particular behaviors that should be included within the concept of monogamy. Thus, consistent and clearly defined terminology is crucial, especially when conducting comparative analyses (Huck et al.; Kappeler and von Schaik, 2002). Early studies of monogamy often assumed that animals with a high degree of spatio-temporal overlap mated exclusively with each other (Wittenberger and Tilson, 1980). Since the advent of molecular techniques enabling parentage determination, it has become clear that exclusive mating with a social partner (i.e., genetic monogamy) is much rarer than social partnerships in which mating outside the pair occurs (e.g., eastern bluebirds, Silia silis, Gowaty and Karlin, 1984, indigo buntings, Passerina cyanea, Westneat, 1987; fat-tailed dwarf lemur, Cheirogalaus medius, Fietz et al., 2000). Thus, the propensity for two opposite sexed individuals to live together need not relate to an exclusive mating relationship, in itself requiring a reevaluation of the common understanding of monogamy. Social monogamy can be defined in terms of spatial overlap of one adult male and one adult female that live as a pair. Advances in methods to study such behavior in nature, particularly among cryptic subterranean species (like rodents), provide accurate and more refined determinations of behavior that can significantly improve assessment of the behaviors that define monogamy. For example, Sabol et al. demonstrated that incorporating automated radio frequency identification
Frontiers in Ecology and Evolution
Explanations for the evolution of social monogamy in mammals typically emphasise one of two possibilities: females are overdispersed (such that males cannot defend access to more than one female at a time) or males provide a service to the female. However, the first claim has never been formally tested. I test it directly at three levels using population-level data from primates and ungulates. First, I show that the females of monogamous genera do not have territories that are significantly larger, either absolutely or relatively, than those of polygynous genera. Second, using two indices of territorial defendability, I show that, given their typical day journey lengths, males of most monogamous species could easily defend an area large enough to allow them to monopolise as many as 5–10 females if they ranged solitarily. Finally, I use a model of male mate searching strategies to show that the opportunity cost incurred by pairbonded males is typically 5–10 times the reproductive suc...
Explanations for the evolution of monogamy in mammals typically emphasise one of two possibilities: monogamy evolves when females are overdispersed (such that males cannot defend more than one female at a time) or when males provide a service to the female. However, the first claim has never been directly tested. I test it directly at three levels using data from primates and ungulates. First, I show that the females of monogamous genera do not have territories that are significantly larger, either absolutely or relatively, than those of polygamous genera. Second, using both the Mitani-Rodman and Lowen-Dunbar inequalities, I show that, given their typical day journey lengths, males of most monogamous species could easily defend an area large enough to allow them to monopolise as many as 5-10 females if these ranged solitarily. Finally, I use a model of male mate searching strategies to show that, unlike the males of socially-living polygamous species, the opportunity cost that monog...
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