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Lemur behaviour informs the evolution of social
monogamy
Peter M. Kappeler1,2
1
Behavioral Ecology and Sociobiology Unit, German Primate Centre, Göttingen, Germany
2
Department Sociobiology/Anthropology, University of Göttingen, 37077 Göttingen, Germany
Recent comparative analyses reached contradictory con-
clusions about the evolutionary origins of social monog-
amy in primates and other mammals, but they ignored
variation in social bond quality between pair-partners.
Recent field studies of Malagasy primates (lemurs) with
variable intersexual bonds indicate independent evolu-
tionary transitions to pair-living from solitary and group-
living ancestors, respectively, as well as four cumulative
steps in evolutionary transitions from a solitary life style
to pair-living that resolve some contradictory results of
previous studies.
The study of the evolution of mammalian monogamy con-
tinues to generate much interest and controversy [1–
3]. Mammalian monogamy represents an evolutionary
puzzle because males have a much higher potential for
producing offspring per unit time than females, making it
necessary to identify selective advantages that would more
than compensate for the loss of potential reproduction
suffered by males that confine their reproductive activities
to a single female [4]. This problem is also of particular
interest to humans because transitions to monogamy have
occurred repeatedly in human evolution [5], especially in
recent centuries in various cultures [6]. Nonetheless, the
relative importance of the evolutionary forces favouring
the origins and maintenance of monogamy remain obscure
and controversial.
Muddled origins of mammalian social monogamy
Two recent comparative studies across all mammals [1]
and primates [2], respectively, tested hypotheses about the
relative importance of paternal care, including protection
from infanticide risk, and male mate guarding strategies in
promoting social monogamy. According to one study, 29%
of living primates are socially monogamous, evolutionary
transitions to social monogamy occurred seven times, and
in all but one case from solitary ancestors [1], whereas the
other study classified 19% of primate species as pair-living
(16% according to another classification by the same
authors [2]) and identified six transitions to monogamy,
all from group-living ancestors [7]. These studies also
yielded opposite conclusions regarding the importance of
infanticide risk [2] and ecological factors [1] driving evolu-
tionary transitions to monogamy, which were not resolved
Corresponding author: Kappeler, P.M. (pkappel@gwdg.de).
Keywords: monogamy; social evolution; primates.
0169-5347/
ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2014.09.005
by subsequent mutual re-analyses [8]. Thus, controversy
continues over which factors promoted how many transi-
tions to monogamy from which ancestral social system and
which factors subsequently stabilised its maintenance.
These discrepancies clearly call for generally agreed-
upon classifications of social systems for comparative anal-
yses. Variable operational definition of social monogamy
(e.g., distribution of breeding females vs. composition of
social units), inclusion of species for which no primary data
or only anecdotal reports exist, and divergent arbitrary
rules for operationally dealing with intraspecific variation
in the composition of social units have all contributed to
discrepancies in species classifications, reconstructions of
state transitions and outcomes of functional analyses
[1,2,9]. Using insights from recent lemur field studies, I
argue here that consideration of behavioural details of
male-female tolerance and bonding can contribute to a
constructive resolution of this controversy.
Diversity of lemur social monogamy
The primates of Madagascar represent a speciose primate
lineage (> 100 species) in which pair-living evolved inde-
pendently in four out of five families and independently
from monkeys and apes. Importantly, in contrast to mon-
keys and apes, intersexual cohesion is highly variable
among pair-living lemurs, ranging from species where pair
partners actively avoid each other and only interact during
mating, to others where males and females are highly
cohesive, interact regularly and even cooperate in parental
care [9,10]. Because it is unlikely that all components of a
social system arise simultaneously, and because evolution-
ary change in social systems is more likely stepwise,
cumulative and based on exaptations [5,9], ordination of
snapshots of types of male-female associations found
among living lemur species can suggest a scenario for
step-wise evolution of the components and functions of
this social system that can also guide future comparative
analyses in other mammals.
Because the ancestral primates and mammals were
nocturnal and solitary [1,7], females of some solitary spe-
cies presumably first became more territorial in an initial
step towards pair-living (Table 1). It is conceivable that in
an initial crucial step from a solitary life to pair-living,
territorial females were joined by males, who shared their
ranges, but actively avoided females and never affiliated or
rested with them (Pair I). Such dispersed pairs are also
found at the next level, where cohesion remains low, but
pair-partners interact occasionally, coordinate their activ-
ities only when in visual contact with each other, and share
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Table 1. Two evolutionary transitions to pair-living in lemursa

Solitary I Solitary II Pair I Pair II Pair III Pair IV Pair V Groups
Female range overlap 10 11 1-2 12 0 13 0 14,15 0-1 16,17 0 18,19 0 20 n.a.
22
Intersexual range 10 11 8 21 1 13 1 14,15 1 16,17 1 18,19 1 n.a.
overlap
Co-sleeping 0 23 34 24 0 13 26 (2-83) 25 52 (14-92) 26 98 18 permanent permanent
36 (0-78) 15 60 17 70 19
11 12 13
Intersexual cohesion No No 7 15 27 27* 17 continuous 28 permanent permanent
9 15
30
Duetting No No No No 29 Yes 16 ? Yes No
35 35
Paternal care No 31 No No 13 No 32, 33 ? Yes 34 Yes No
14 36 36
Polygynous units n.a. n.a. 28 13 10 0 16 0 18 35 85
0 17 11 19
Activity N N N N N N D or C D or C
Factors facilitating Female territoriality Male mating strategy Paternal care Female competition
transitions Interspecific competition
Direction of transition

Examples

Microcebus Microcebus Lepilemur Lepilemur Lepilemur Avahi Eulemur Eulemur

murinus, berthae leucopus ruficaudatus, edwardsi, occidentalis, rubriventer, coronatus,
Microcebus Phaner Avahi Cheirogaleus Hapalemur Lemur catta,
ravelobensis pallescens meridionalis medius griseus, Propithecus
Indri indri verreauxi
a
For each category of solitary and pair-living species, key features of the social system are contrasted. Four types of pair-living (light green) can be distinguished
among nocturnal species that can be derived from solitary ancestors; a fifth type of pairs (dark green) evolved from group-living ancestors. Female range overlap:
average number of other adult females with which female ranges overlap. Intersexual range overlap: average number of adult males overlapping the home range of a
female. Co-sleeping: proportion (mean; range) of days males and females share a sleeping shelter simultaneously. Intersexual cohesion: proportion of time (%) pair-
partners spend within 10m (*20m) of each other. Duetting: presence of stereotyped antiphonal calling between pair partners. Paternal care: regular presence of male
behaviours that benefit infants. Polygynous units: proportion (%) of social units composed of 1 male and 2 females. For Pair V and Groups: proportion of social units
with  2 females. Activity: nocturnal (N), diurnal (D), or cathemeral (C). Numbers refer to exemplary references listed in the supplementary electronic material.

sleeping sites on some days (Pair II). Next, cohesion
increases, especially following births, and pair-partners
in some pairs share sleeping sites on most days (Pair
III). Male polygynous tendencies also decrease, as reflected
by a decrease in the proportion of social units containing
two females. Finally, male-female cohesion is nearly per-
manent, also during periods of inactivity, most interactions
are affiliative, and males can exhibit paternal care (Pair
IV). In contrast, diurnal pair-living lemurs of the genera
Eulemur, Hapalemur and Indri (Pair V) all exhibit close
and permanent intersexual cohesion, thus converging in
this respect with pair-living monkeys and apes [9].
Two alternative routes to different types of social
monogamy
Because of the necessity of classifying species into broad
categories, previous quantitative comparative analyses
ignored fine-grained interspecific behavioural variation
in intersexual tolerance and cohesion. The above scenar-
io suggests that the initial transition from a solitary life
to pair-living along one conduit was triggered by ecologi-
cal factors promoting female territoriality, followed by a
shift in male mating strategies. Because these males
never associate with females within their overlapping
ranges, effective protection from infanticide is difficult to
envisage at these initial stages. Only once intersexual
tolerance and cohesion increase, and females carry
infants, rather than parking them, males can protect
females effectively from infanticide [9]. Because preda-
tion risk promotes strong cohesion in diurnal species,
intersexual cohesion was already high in those pair-
living species evolving along another conduit from
group-living ancestors. As group-living lemurs exhibit
adaptations to reduce infanticide risk, this alternative
transition might have been facilitated by a reduction in
female group size in response to female competition [10],
and thus ultimately also by ecological factors, rather
than by a sudden change in infanticide risk.
Concluding remarks
The present review (i) emphasises different evolutionary
conduits to two types of pair-living, (ii) indicates four
cumulative steps in evolutionary transitions towards
pair-living from solitary ancestors, (iii) suggests that eco-
logical factors triggered the formation of dispersed pairs
from solitary ancestors, and (vi) indicates that benefits of
infanticide avoidance might have been of limited impor-
tance during the origins of both types of pair-living. More
generally, this analysis should alert future studies on the
evolution of social systems to the importance of beha-
vioural mechanisms and to variation within apparently
simple social systems.
Acknowledgements
I thank the Deutsche Forschungsgemeinschaft for supporting my
research on pair-living lemurs (Ka 1082-6 and 21) and two anonymous
referees for helpful comments.

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Spotlight
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in the online
version, at http://dx.doi.org/10.1016/j.tree.2014.09.005.
References
1 Lukas, D. and Clutton-Brock, T.H. (2013) The evolution of social
monogamy in mammals. Science 341, 526–530
2 Opie, C. et al. (2013) Male infanticide leads to social monogamy in
primates. Proc. Natl. Acad. Sci. U.S.A. 110, 13328–13332
3 de Waal, F.B.M. and Gavrilets, S. (2013) Monogamy with a purpose.
Proc. Natl. Acad. Sci. U.S.A. 110, 15167–15168
4 Kappeler, P.M. (2013) Why male mammals are monogamous. Science
341, 469–470
5 Chapais, B. (2013) Monogamy, strongly bonded groups, and the
evolution of human social structure. Evol. Anthropol. 22, 52–65
6 Henrich, J. et al. (2012) The puzzle of monogamous marriage. Philos.
Trans. R. Soc. Lond. B 367, 657–669
Trends in Ecology & Evolution xxx xxxx, Vol. xxx, No. x
7 Shultz, S. et al. (2011) Stepwise evolution of stable sociality in
primates. Nature 479, 219–222
8 Lukas, D. and Clutton-Brock, T.H. (2014) Evolution of social
monogamy in primates is not consistently associated with male
infanticide. and: Opie, C. et al. Reply to Lukas and Clutton-Brock:
Infanticide still drives primate monogamy. Proc. Natl. Acad. Sci.
U.S.A. 111, E1674–E1675
9 van Schaik, C.P. and Kappeler, P.M. (2003) The evolution of social
monogamy in primates. In Monogamy: Mating Strategies and
Partnerships in Birds, Humans and Other Mammals (Reichard,
U.H. and Boesch, C., eds), pp. 59–80, Cambridge: Cambridge
University Press
10 Kappeler, P.M. (2012) The behavioral ecology of strepsirrhines and
tarsiers. In The evolution of primate societies (Mitani, J.C. et al., eds),
pp. 17–42, Chicago: University of Chicago Press