Discussion
The link between mating system, mate choice and dispersal has rarely
been studied in pair-living mammals. Here, we demonstrated that coppery
titi monkeys, despite exhibiting no relatedness- or heterozygosity-based
mate choice, are genetically monogamous, with no cases of EPP found
across 18 offspring born in 9 family groups. Furthermore, we found that
although dispersal was opportunistic and often local, relatedness
between pair mates remained very low and they never shared the same
mtDNA haplotypes. Our results suggest that even opportunistic dispersal
can generate sufficient genetic dissimilarity between opposite-sex
animals, rendering both active inbreeding avoidance during mate choice
and extra-pair matings unnecessary.
Coppery titis are only the second primate species and the seventh
pair-living mammal with no evidence of EPP found in a study with an
adequate sample size (the study on Bornean gibbon was based on just 4
infants from 4 family groups (Oka & Takenaka, 2001), Table 1). The
finding of genetic monogamy in titis is not unexpected, as they are
consistently pair-living, pair mates spend most of the day within a few
meters from each other, sleep together at night and engage in frequent
joint visual displays and duetting at the territorial borders
(Dolotovskaya et al., 2019; Fernandez-Duque et al., 2013; Kinzey &
Robinson, 1983; Kinzey & Wright, 1982; Spence-Aizenberg, Di Fiore, &
Fernandez-Duque, 2016). This high level of proximity and coordination
should make mate guarding easy and effective enough to prevent EPC. The
opportunities for EPC are likely very limited, too. The home ranges of
our study groups have very little overlap (Fig. 3), and to find
extra-pair mates, individuals would need to intrude into the neighboring
home ranges, risking aggression from the same-sex residents. Another way
to obtain EPC could be mating with “floaters”, solitary
non-territorial individuals ranging over a wide area after having
dispersed from their natal groups. There is accumulating evidence for
the importance of floaters in population dynamics of both birds and
mammals (Fernandez-Duque & Huck, 2013; Penteriani, Ferrer, & Delgado,
2011). In Azara’s owl monkeys, Aotus azarae , who are very similar
to titis in all aspects of their social system, mated individuals
experience intense intra-sexual competition from floaters of both sexes
(Fernandez-Duque & Huck, 2013; Huck & Fernandez-Duque, 2012). However,
the presence of floaters in owl monkeys does not lead to EPP but rather
to “serial monogamy”, as floaters expel and replace mated individuals.
Evidence from other mammals and birds indicate that generally floaters
do not copulate with the mated animals as often as might be intuitively
expected, and EPP are attributed to the neighboring individuals in most
cases (e.g., Barelli et al., 2013; Nimje et al., 2019; Petrie &
Kempenaers, 1998; but see Cohas, Yoccoz, Da Silva, Goossens, & Allainé,
2006; Kenyon, Roos, Binh, & Chivers, 2011). In titis, only anecdotal
reports of replacements by intruders exist (Lawrence, 2007; Rodman &
Bossuyt, 2007), but given the difficulty of detecting floaters, it is
highly possible that they are present in titi populations, too. However,
given the high levels of proximity and coordination between pair mates,
EPC with the floaters are probably not easier to obtain than EPC with
the neighboring individuals.
It should be noted that we cannot fully exclude the possibility of a low
EPP rate in our study population. With our sample size of 18 offspring,
the maximum possible EPP level (assuming no EPP has been found and
estimated with 95% confidence) is 15.2%, calculated as y =
1–(1–x)18, where y is the probability of producing
at least one extra-pair offspring (0.95); x is the frequency of EPP, and
n is the sample size (Brotherton, Pemberton, Komers, & Malarky, 1997).
To narrow down the confidence interval to at least 5% of EPP, we would
need a sample size of 58, which is difficult to achieve in a pair-living
mammal giving singleton birth once a year in a reasonable period.
Contrary to our predictions, we did not find evidence for relatedness-
or heterozygosity-based mate choice in our study population. In
pair-living animals with biparental care, such as titis, mate choice is
indeed likely to be severely constrained. What is intriguing, however,
is how titis avoid inbreeding under the situation of constrained mate
choice and a strictly monogamous mating system. In our study population,
despite the lack of evidence for active inbreeding avoidance through
mate choice, the pair mates were on average not related (mean r =
-0.033) and never shared the same mtDNA haplotype (Supplementary Table
1, Fig. 1). Although active inbreeding avoidance through mate choice has
been demonstrated both in birds and mammals (e.g., Hoffman et al., 2007;
Leedale et al., 2020; Wheelwright, Freeman-Gallant, & Mauck, 2006), it
does not seem to be universal. In fact, in most pair-living species, no
evidence for relatedness-based assortative mating was found
(García-Navas et al., 2009; Hansson et al., 2007; Schwensow, Fietz,
Dausmann, & Sommer, 2008; Sommer, 2005). In some species, mate choice
was based on similarity in certain MHC genes rather than on genome-wide
relatedness (e.g., Schwensow et al., 2008). In the absence of active
mate choice, one way to avoid incest in natural populations is natal
dispersal. By creating gene flow across physical and social landscapes,
dispersal can generate sufficient genetic diversity to ensure low
relatedness between pair mates even in the absence of active
relatedness-based mate choice. This has been demonstrated both in birds
and mammals (Hansson et al., 2007; Huchard et al., 2010; Szulkin &
Sheldon, 2008); furthermore, the reverse situations, when constrained
dispersal leads to active inbreeding avoidance via mate choice or
increases inbreeding risks in the absence of active inbreeding
avoidance, are also known (Leedale et al., 2020; Schultz et al., 2020).
These findings are further confirmed by data indicating that mate choice
patterns depend on the local factors, such as population density, adult
sex ratio or presence of kin, all of which are ultimately related to
dispersal (Blyton, Shaw, Peakall, Lindenmayer, & Banks, 2016).
In our study population, both sexes dispersed opportunistically, i.e.
migrated over varying distances. There was no obvious difference in
dispersal distances between sexes: while mtDNA haplotype diversity was
similar in both sexes, indicating longer dispersal distances in females,
mean relatedness was similar between sexes, suggesting more equal
dispersal. Partly it can be attributed to the scale of our study being
relatively confined, with distances between home-range centers varying
from 215 to 3200 m. In other pair-living mammals, evidence for
sex-biased dispersal is mixed. On one hand, it can be expected that
similar levels of intra-sexual competition in socially monogamous
species will lead to similar rates of dispersal among sexes. On the
other hand, it has been suggested that in pair-living animals with
biparental care, females should disperse further, because males, in
addition to participating in offspring care, need to acquire and defend
resources to attract females, and thus will benefit the most from
staying in a familiar area (Greenwood, 1980). Female-biased dispersal
was demonstrated in two pair-living mammals, California mouse,Peromyscus californicus , and white-toothed shrews,Crocidura russula (Favre et al., 1997; Ribble, 1992). In Azara’s
owl monkeys, however, dispersal was opportunistic, with both sexes
travelling similar distances (Fernandez-Duque, 2009), and in Eurasian
and North American (Castor canadensis ) beavers, some populations
had no sex bias in dispersal, whereas others had female-biased or
male-biased dispersal (Mayer et al., 2017). Interestingly, in humans,
who are most often described as socially monogamous, dispersal patterns
also vary among societies, although most (about 70%) of societies
practice patrilocality (Burton, Moore, Whiting, & Romney, 1996). All
these findings suggest that dispersal patterns, like mate choice, also
partly depend on local factors, such as population density, adult sex
ratio, or food availability (Bowler & Benton, 2005). The population
density at our study site was 34 individuals per km2(unpublished data), falling within the range of population densities
reported for undisturbed populations of titi species (Bicca-Marques &
Heymann, 2013).
Another intriguing question is why, under the condition of constrained
mate choice, titis do not engage in EPC. In many bird species,
individuals paired with more closely related or MHC-similar mates were
shown to be more likely to engage in EPC (e.g., Arct et al., 2015;
Blomqvist et al., 2002; Foerster et al., 2003). In mammals, however,
there is very limited evidence for this strategy. EPP rates were
correlated with genetic similarity of pair mates in two species with
high degree of breeding monopolization by a dominant pair, Alpine
marmots, Marmota marmota and meerkats, Suricata suricatta(Cohas et al., 2008; Leclaire, Nielsen, Sharp, & Clutton-Brock, 2013).
But, to our knowledge, the only pair-living mammal species for which
this effect has been demonstrated is fat-tailed dwarf lemurs,Cheirogaleus medius , where females sharing more MHC-supertypes
with their social partner engaged in more EPCs (Schwensow et al., 2008).
The costs of engaging in EPCs in pair-living animals with biparental
care are likely high and include the risks of acquiring sexually
transmitted diseases, aggression from same-sex adults and, for females,
the retaliatory withholding of parental care by males (Westneat &
Stewart, 2003). Alternatively, to escape the constraints of mate choice,
animals can switch mates, or “divorce”, and this strategy was shown to
be advantageous in many pair-living birds and some human societies
(Dubois & Cézilly, 2002; Mulder, 2009). However, in Azara’s owl monkeys
and Alpine marmots, the replacement of mated individuals by floaters was
never voluntary and had strong negative effects on the reproductive
success of both partners (Fernandez-Duque & Huck, 2013; Lardy, Cohas,
Figueroa, & Allainé, 2011). In pair-living mammals with very high level
of male care and seasonal singleton births, such as titi monkeys and owl
monkeys, this should be a strong selective force promoting animals to
keep long-term stable pair bonds instead of seeking EPC or “better
options”.
The current study is the first to examine the link between mating
system, mate choice and dispersal in a wild population of a pair-living
primate. Using a newly designed set of microsatellite loci universally
applicable to New World monkeys, we showed that coppery titis, despite
exhibiting no relatedness- or heterozygosity-based mate choice, still
had very low relatedness between pair mates and did not engage in
extra-pair matings. Our results indicate that dispersal, even
opportunistic and partly local, can create sufficient genetic
dissimilarity between opposite sexes to render active mate choice and
extra-pair copulations unnecessary. These findings have implications for
the evolution of mating systems, suggesting that limited opportunities
for extra-pair copulations and their high costs, together with
sufficient level of dispersal, can maintain and facilitate the evolution
of genetic monogamy in pair-living animals.