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.