Monogamy In Mammals Research Articles

Monogamy or monogamish? Re-examining monogamy in Peromyscus californicus

California mice have been widely recognized as one of the few examples of ‘true’ genetic monogamy in mammals and are one of only four mammalian species considered to be both genetically and socially monogamous. The mating system of this species, first described by David O. Ribble (1991), was initially investigated in a single population by integrating both behavioral data and DNA fingerprinting to classify P. californicus as monogamous. Here, we investigated the parentage of field sampled litters of California mice across 4 populations using both classic field methods and modern microsatellite analyses. We putatively identified male-female mouse pairs in the field using capture localities and transfer of fluorescent pigment between individuals. We then used microsatellite loci to genotype pregnant adult females, their embryos, and the adult males identified in the field as the partners of those females. We identified occurrences of extra-pair paternity in 3 out of the 4 populations of California mice, calling in to question the designation of this species as genetically monogamous (Figure 1 and Table 1). We suggest a careful re-examination of the mating system of this species using modern molecular methods to analyze a greater number of samples representing multiple sampling localities. Future studies of this species should prove particularly informative regarding the correlates of extra-pair mating and, hence, the adaptive bases for the maintenance of male-female pair bonds in the absence of true genetic monogamy.

Female Dispersion Is Necessary, but Not Sufficient, for Pairbonded Monogamy in Mammals

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 success they actually obtain by being obligately monogamous. This suggests that the selection pressure dissuading them from pursuing a roving male strategy must be very considerable. At present, the evidence is undecided as to whether mitigating predation or infanticide risk is the primary function, but estimates of their impacts suggest that both are in fact plausible.

Space use and the evolution of social monogamy in eastern rock sengis

AbstractLimiting resources often differ between males and females. Reproductive success in females is constrained by resources such as food and shelter, while the availability of receptive females determines male reproductive success. In addition to limiting resources, low intra‐sexual tolerances among females can affect their spacing. High intolerances coinciding with low population densities have been suggested as a cause for the evolution of monogamy in mammals, but the evidence for female intolerance is limited. We investigated long‐term space use patterns (measured as home range sizes and centers of activity) in a wild population of eastern rock sengis (Elephantulus myurus) from Limpopo, South Africa. Between March 2012 and March 2016, we recorded capture locations for 93 sengis and home range size for 22 sengis and evaluated the contributions of study year, sex, and season on these measures. Sex had no significant effect on home range size, but ranges were significantly greater during the breeding compared to the non‐breeding season, consistent with the increased energetic demands during reproduction. We found corroborative support for the role of energetic demands on home range size fluctuations. The activity centers of female–female dyads were further apart than those of male–male or mixed‐sex dyads, suggesting lower female–female tolerances in the study species. Our results offer evidence that intolerances may affect female spacing behavior and may have contributed to the evolution of monogamy in sengis.

Evidence of genetic monogamy in the lemur Indri (Indri indri).

Monogamy is a rare strategy among mammals but relatively common among primates. The study of the evolution of monogamy in mammals and primates is lacking empirical studies that assess the relationship between a pair-living social organization and genetic monogamy. Sexual or genetic monogamy can only be assessed by performing molecular analyses and investigating rates of extra-pair paternity (EPP). Studying the occurrence of EPP can provide valuable insights into reproductive strategies and their adaptive value. The indri is a pair-living primate that lives in stable groups. Their social units are composed of the reproductive pair and up to four more individuals, but extra-pair copulation (EPC) can occur. This raises the question of whether this event may or may not lead to EPP. Here, we investigated whether a pair-living social organization corresponds to genetic monogamy in indris (Indri indri). We analyzed the paternity of 12 offspring from seven pairs using a set of six microsatellite loci on fecal samples (mean number of alleles 11.7 ± 1.8 (mean ± standard deviation). We found that in 92% of cases the genetic profile of the offspring matched the paired male of the group for all the loci considered. In the only case of paternity mismatch, the paternity assignment remained inconclusive. Our results show that I. indri genetic monogamy is the norm and supports the hypothesis that pair-living social organization is associated with low EPP rate. Also, our results are in contrast with the hypothesis of infertility as a reason to engage in EPC for this species.

The Monogamy Paradox: What Do Love and Sex Have to Do With It?

Genetic monogamy is rare-at least at the level of a species-and monogamy can exist in the absence of sexual fidelity. Rather than focusing on mating exclusivity, it has become common to use the term "social monogamy" to describe a cluster of social features, including the capacity for selective and lasting social bonds, central to what humans call "love." Socially monogamous mammals often exhibit selective aggression toward strangers and form extended families. These features of social monogamy in mammals are supported by patterns of hormonal function originating in the neurobiology of maternity, including oxytocin, as well as a more primitive vasopressin pathway. Another key feature of social monogamy is reduced sexual dimorphism. Processes associated with sexual differentiation offer clues to the mysteries surrounding the evolution of monogamy. Although there is consistency in the necessary ingredients, it is likely that there is no single recipe for social monogamy. As reviewed here, genes for steroids and peptides and their receptors are variable and are subject to epigenetic regulation across the lifespan permitting individual, gender and species variations and providing substrates for evolution. Reduced sensitivity to gonadal androgens, and a concurrent increased reliance on vasopressin (for selective defense) and oxytocin (for selective affiliation) may have offered pathways to the emergence of social monogamy.

The Bold, Silent Type: Predictors of Ultrasonic Vocalizations in the Genus Peromyscus

An ongoing question related to the evolution of monogamy is how behavioral traits that characterize individuals in monogamous species evolve, and whether monogamy influences the evolution of these traits. One of the most important models for the study of monogamy in mammals is the California mouse (Peromyscus californicus) that uses ultrasonic vocalizations (USVs) in multiple behavioral contexts, including pair-bonding and courtship. Because the genus Peromyscus has many species that both use USVs and express a variety of mating systems, we were able to examine the relationship among USVs, and other ecological (e.g., xeric habitat), physiological (testosterone), and behavioral (e.g., boldness) traits across species. We measured USVs from seven species at the Peromyscus Genetic Stock Center and derived character traits associated with the species' ecology, physiology, and behavior from published studies, including those that had used stocks from the Peromyscus Genetic Stock Center. We determined whether there were USV traits that were particular to monogamous species or whether traits other than mating system best predicted USVs. The trait that best predicted USVs was not related to mating system, but rather, species boldness. Bold species produced few aggressive barks (likely a defensive agonistic USV type) at a higher mean fundamental frequency than less bold species. In relation to mating system, the barks in monogamous species were shorter in duration than the barks in non-monogamous species. Our results suggest that boldness of a species has a higher selection on USVs than the species mating system, ecology, or physiology and that selection has acted on agonistic acoustic signals. Because another type of USV, the sustained vocalization or SV type, did not differ among species in spite of mating system differences, and because all species produced bark types, we suggest that the USVs in rodents evolved as general signals that have generally been co-opted for particular functions within the mating system context that differs across species, as opposed to signals that have been shaped by mating system type.

Genetic Monogamy in Socially Monogamous Mammals Is Primarily Predicted by Multiple Life History Factors: A Meta-Analysis

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 versus 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.

Comparative studies need to rely both on sound natural history data and on excellent statistical analysis.

We certainly agree with Schradin [1] that comparative studies need to use the best information available—as well as clear definitions, up-to-date statistical techniques and common sense. We have divided our response into two sections: the first dealing with Schradin's critique of our 2017 paper and the classification of the social organization of shrews; the second dealing with three general issues that his commentary raises. The paper that Schradin is commenting on [2] asks whether cooperative breeders (which we define as species where non-breeding helpers assist breeders to raise their young) in mammals are more commonly found in arid environments than monogamous species (defined as species where breeding pairs of males and females remain together for more than one season) from which cooperative breeders appear to be derived [3]. It shows that, as in birds, cooperative breeders tend to live in relatively arid habitats compared to monogamous species. As we describe below, these conclusions are unaffected by differences between our classification of the social organization of shrews and the classification suggested by Schradin. Schradin's first criticism is that the categorizations of shrews that we have used in this analysis were based on one paper on a single species. This is incorrect, for our categorization of shrews was based on more than 70 separate sources (see electronic supplementary material, appendix S1). When we published our dataset [4], we were required to reduce the associated reference list by the editors of the journal and, to comply, we removed around 75% of our 2000+ sources, often listing a single reference per species or group of species, and frequently using generic reviews for particular groups where these were available: for example, for many rodent species, we simply listed Wolff and Sherman's Rodent Societies [5], and …

Sex Discrimination via Anal Gland Secretion in a Territorial Monogamous Mammal

Monogamy in mammals is relatively unusual, only occurring in 3–5% and to an even lesser degree in rodents. Monogamy exists in two forms, facultative which evolved due to female dispersion and obligate when male care is needed for offspring survival. Most monogamous rodents use scent marking as a form of territorial defence to obtain exclusive access to vital resources. Intrasexual competition occurs in many species to maintain pair bonds and also to signal presence within a territory. In this study, we tested the hypothesis that resident obligate monogamous Eurasian beaver (Castor fiber) can discriminate between the sexes when investigating anal gland secretions (AGS) from unknown (stranger) mated pairs. We predicted that, due to intrasexual competition, dominant territorial male and female beavers will display a stronger response to AGS of same-sex conspecifics. Territorial intrusion by mated pair strangers was simulated by the formation of experimental scent mounds (ESM) with AGS. Our results showed that both sexes (1) displayed a stronger response to the male AGS in sniffing duration, (2) physically responded for longer durations towards male AGS and (3) overmarked male AGS more frequently. We infer that obligate monogamous mammals can determine the sexual identity of intruding conspecifics of a mated pair via AGS and that intruding males may pose more of a threat to resident males via intrasexual competition and resident females due to the long-term costs, such as infanticide and abortion, of a new dominant male.

The Evolution of Social Monogamy in Mammals

The evolution of social monogamy has intrigued biologists for over a century. Here, we show that the ancestral condition for all mammalian groups is of solitary individuals and that social monogamy is derived almost exclusively from this social system. The evolution of social monogamy does not appear to have been associated with a high risk of male infanticide, and paternal care is a consequence rather than a cause of social monogamy. Social monogamy has evolved in nonhuman mammals where breeding females are intolerant of each other and female density is low, suggesting that it represents a mating strategy that has developed where males are unable to defend access to multiple females.

Determinants of Pair-Living in Red-Tailed Sportive Lemurs (Lepilemur ruficaudatus).

Pair-living and a monogamous mating strategy are rare and theoretically unexpected among mammals. Nevertheless, about 10% of primate species exhibit such a social system, which is difficult to explain in the absence of paternal care. In this study, we investigated the two major hypotheses proposed to explain the evolution of monogamy in mammals, the female defence hypothesis (FDH) and the resource defence hypothesis (RDH), in red-tailed sportive lemurs (Lepilemur ruficaudatus), a nocturnal primate from Madagascar. We analysed behavioural data from eight male–female pairs collected during a 24-mo field study to illuminate the determinants of pair-living in this species. Male and female L. ruficaudatus were found to live in dispersed pairs, which are characterised by low cohesion and low encounter rates within a common home range. Social interactions between pair partners were mainly agonistic and characterised by a complete absence of affiliative interactions – body contact was only observed during mating. During the short annual mating season, males exhibited elevated levels of aggression towards mates, as well as extensive mate guarding and increased locomotor activity. In addition, males were exclusively responsible for the maintenance of proximity between pair partners during this period, and they defended their territories against neighbouring males but not against females. Together, these results point towards the importance of female defence in explaining pair-living in L. ruficaudatus. We discuss the spatial and temporal distribution of receptive females in relation to the female defence strategies of males and suggest possible costs that prevent male red-tailed sportive lemurs from defending more than one female.

Spatial dynamics and the evolution of social monogamy in mammals

Social monogamy is an uncommon mating system among mammalian species, and several hypotheses have been suggested to explain its evolution. It is generally thought that low local population densities and widely spaced female home ranges, particularly small home ranges, may facilitate social monogamy. We tested these expectations with a complete data set on local density, home range area, and body mass for 64 mammalian species, 22 of which were described as socially monogamous and 42 as not socially monogamous (socially polygynous or polygynandrous). Larger samples were examined separately for local density (84 species) and home range size (129 species). We found that with or without statistical adjustments for body size and phylogeny, socially monogamous and nonmonogamous species appeared similar in local density and home range area. Thus, we found no support for the idea that low population densities and wide dispersion of small home ranges have favored the evolution of social monogamy. Given support for different hypotheses in studies of different species, we suggest multiple causes of social monogamy among mammalian species.

Laboratory and field evidence of paternal care in the Algerian mouse (Mus spretus)

Paternal care is generally, although not exclusively, associated with monogamy in mammals. The Algerian mouse, Mus spretus, is a nocturnal murid living in xeric habitats in northern Africa, the Iberian peninsula and the south of France. We compared the amount of paternal care induced by removing young in Mus spretus and in the polygamous house mouse M. musculus domesticus in terms of the evolution of paternal care during the first 10-days post-partum and absolute (father alone) and relative (both parents) values. We then recovered indirect evidence of young being cared for by males from field data. The results were unambiguous in showing that the two species differed dramatically in paternal behaviour, with no variation being observed during the initial pup development. Mus spretus dedicated half of its time to caring from the young against less than 10% in M. m. domesticus. The former species showed the same number of retrieving acts and direct care bouts both in the presence and in the absence of the mother. Merging these results with field observations of spatial association “male-young” until subadult age, we drew conclusions on the likely occurrence of paternal care in M. spretus. Taken together with our previous results on socio-spatial organisation and pair bonding, we propose that social monogamy is advanced for this species.

Social but not genetic monogamy is associated with greater breeding success in prairie voles

Much attention has focused on distinguishing between social and genetic monogamy in avian taxa. However, surprisingly few studies have directly investigated this distinction among mammals. We investigated the genetic mating system of the prairie vole, Microtus ochrogaster, a popular model for mammalian monogamy and human attachment. We used space use patterns to define paired and single animals and assessed paternity using microsatellite loci. Prairie voles in this study engaged in significantly more extrapair fertilizations than predicted under genetic monogamy but fewer than predicted under random mating, demonstrating social but not genetic monogamy. Furthermore, we found that paired individuals were more likely to produce offspring than were unpaired individuals of either sex. This finding was true for both sexes and was attributable to differences in fertilization rates rather than litter sizes. Among mated individuals, however, faithful animals were no more successful than those that mated outside a pair. Taken together, our data demonstrate that paired prairie voles have greater breeding success than single voles, but such success is not contingent on mating exclusively with a social partner. If this species is to serve as a model for human love, our findings emphasize the need to distinguish between mammalian social attachment and sexual fidelity.

Behavioral Monogamy and Fruit Aavailability in the Large Treeshrew (Tupaia tana) in Sabah, Malaysia

Behavioral monogamy in mammals varies from male–female pairs that spend most of their time in close spatial contact (associated pair-living) to pairs that occupy exclusive territories but travel, forage, and sleep alone (dispersed pair-living). We present radiotelemetry data on 46 adult large treeshrews (Tupaia tana) from 2 populations in Sabah, Malaysia, that indicate that this species forms dispersed pairs across a range of ecological conditions. Dispersed pair-living was the primary behavioral mating system in primary forest during a major fruit masting event, in nonmasting primary forest, and in selectively logged forest with significantly higher fruitfall than in primary forest. Territories of behavioral partners were spatially concordant, but both male and female territories typically overlapped the boundaries of 1–3 extra-pair territories. Comparison between masting and nonmasting forests indicated that females exhibited better body condition during masting, whereas males exhibited larger home-range areas and longer daily movements. Both males and females exhibited better body condition in selectively logged versus primary forests, but ranging patterns were not significantly different between these habitats. We argue that intraspecific foraging competition is the most likely explanation for the evolution of dispersed pair-living in T. tana.

Morphological, Genetic, and Behavioral Comparisons of Two Prairie Vole Populations in the Field and Laboratory

Reports of geographic variation in behavior and morphology among prairie voles (Microtus ochrogaster) from Illinois, Kansas, and Tennessee have led to the belief that these animals vary in their mating strategies and the degree to which they are monogamous. Despite this, few studies have directly compared behavior between populations. Because the prairie vole is commonly discussed as a model for mammalian monogamy, understanding how aspects of social attachment and the mating system vary could provide further insight into the evolution of monogamy. We therefore conducted a series of experiments in the laboratory and field to assess morphological, behavioral, or genetic differences between 2 populations of this species. Voles from Illinois were morphologically similar to voles from Tennessee and exhibited comparable social and mating behavior under both laboratory and field conditions. Although genetically distinct, the 2 populations demonstrated similar levels of heterozygosity and allelic richness. Sexual dimorphism, a common indicator of mating strategy, was absent in voles from 7 widely distributed regions from across their geographic range. In the context of these results, we question the degree to which the previously described population differences are ecologically meaningful. If differences between prairie voles from Kansas and Illinois do indeed exist, examination of our data suggests that those from Kansas are atypical of prairie voles overall.

Long-term pair-bonds without mating fidelity in a mammal

AbstractMost mammals are polygynous and are characterised by male-biased sexual size dimorphism. One hallmark of mammalian monogamy is the lack of such dimorphism. Bobucks, or mountain brushtail possums, Trichosurus cunninghami, lack sexual size dimorphism; however, few behavioural data exist for this species. We studied the mating system of a bobuck population in south-eastern Australia. Adult bobucks were strongly paired: pair-members had exclusive access to a suite of den-trees and overlapped in home range on average by 70%. Pair-members rested together in the same tree-hollow on approximately 70% of days during the breeding season and 47% of days during the non-breeding season. While active, pair-members remained within approximately 8 m of one another during the breeding season and within 31 m of one another during the non-breeding season. Females established pair-bonds at 2-5 years of age; pair-bonds ended only as a result of the death of one pair member. However, molecular paternity analysis established that 35% of young were the result of extra-pair copulations (EPCs). This is the first study to provide strong evidence of long-term pair-bonds in a marsupial and raises questions about the relative benefits of pairing to males and females in this population.

Mammalian monogamy is not controlled by a single gene.

Complex social behavior in Microtus voles and other mammals has been postulated to be under the direct genetic control of a single locus: the arginine vasopressin 1a receptor (avpr1a) gene. Using a phylogenetic approach, we show that a repetitive element in the promoter region of avpr1a, which reportedly causes social monogamy, is actually widespread in nonmonogamous Microtus and other rodents. There was no evidence for intraspecific polymorphism in regard to the presence or absence of the repetitive element. Among 25 rodent species studied, the element was absent in only two closely related nonmonogamous species, indicating that this absence is certainly the result of an evolutionarily recent loss. Our analyses further demonstrate that the repetitive structures upstream of the avpr1a gene in humans and primates, which have been associated with social bonding, are evolutionarily distinct from those in rodents. Our evolutionary approach reveals that monogamy in rodents is not controlled by a single polymorphism in the promoter region of the avpr1a gene. We thus resolve the contradiction between the claims for an evolutionarily conserved genetic programming of social behavior in mammals and the vast evidence for highly complex and flexible mating systems.

Monogamy: Mating Strategies and Partnerships in Birds, Humans and Other Mammals

U. H. Reichard, C. Boesch (eds.). 2003. Monogamy: Mating Strategies and Partnerships in Birds, Humans and Other Mammals. Cambridge University Press, Cambridge, United Kingdom, 267 pp. ISBN 0-521-52577-2, price (paper), $45.00. Understanding the evolution of monogamy in mammals has challenged behavioral ecologists for decades, because in most cases males are predicted to experience higher fitness through polygynous mating. In contrast to birds, gestation and lactation limit the potential fitness benefits of paternal care for all but a handful of species. Individuals that live in monogamous pairs but mate with extra-pair partners present an additional puzzle. Monogamy: Mating Strategies and Partnerships in Birds, Humans and Other Mammals brings together the most recent comparative analyses and long-term field studies that address the evolution of monogamy in mammals. A book-length review of this topic is very welcome. The conceptual framework for thinking about mating systems in mammals for nearly a decade and a half (Clutton-Brock 1989; Davies 1991) has been rooted in Kleiman's (1977) seminal review of monogamy and Emlen and Oring's (1977) ecological framework of mating system evolution. These reviews overemphasized the role of parental care, now believed to have evolved after the evolution of monogamy in most cases, and de-emphasized the role of female choice in favor of male control of female reproduction. The advent of molecular techniques for parentage assignment has ushered in a new understanding of the costs and benefits of monogamy for individuals that …

Multiple paternity in socially monogamous prairie voles (Microtus ochrogaster)

Prairie voles (Microtus ochrogaster (Wagner, 1842)) exhibit behavioral, morphological, and neuroendocrinological traits associated with monogamy and are considered a model system to examine the biological foundations of monogamy in mammals. We examined allelic polymorphism at microsatellite loci to assess mating exclusivity in wild prairie voles sampled in east-central Illinois and found evidence of multiple paternity in five of nine litters (56%) analyzed. Thus, a female in this socially monogamous mammal with extensive mechanisms for pair bonding does not always mate solely with its partner and raises the paradox of why some pair-bonded females mate multiply.