Rare in mammals but more common in primates, there remains a considerable controversy concerning whether primate species traditionally described as monogamous actually express this highly specialized breeding pattern. Unfortunately the definition of "monogamy" varies greatly, inhibiting our understanding of this trait and two related traits with which monogamy is often conflated: pair-living and pair-bonding. Strepsirrhine primates are useful models to study factors that select for pair-living, pair-bonding, and monogamy because this taxon exhibits high incidences of each trait, in addition to species that exhibit behaviors that reflect combinations of these traits. Several hypotheses have been articulated to help explain the evolution of "monogamy," but again, these hypotheses often conflate pair-living, pair-bonding, and/or monogamy. In this review, we (1) propose clear, discrete, and logical definitions for each trait; (2) review variation in strepsirrhines with respect to these three traits; (3) clarify which of these traits can be explained by existing hypotheses; and (4) provide an example of the applicability of the Resource Defense Hypothesis (RDH) to understand two of these traits, pair-living and pair-bonding, in the red-bellied lemur (Eulemur rubriventer). Available data support the RDH for pair-living in red-bellied lemurs. They live in stable family groups with one adult pair. Both sexes actively codefend territories that overlap little with other pairs' territories. Agonism is extremely rare within groups and intergroup and interspecific agonism varies with food availability. Available data also support the RDH for pair-bonding. Pair-bonds are cohesive year-round. Pairs coordinate behaviors to defend territories with auditory and olfactory signals. Cohesion increases with food abundance and both sexes reinforce bonds. We indicate where additional data will help to more rigorously test the RDH for each trait and encourage others to test alternative hypotheses.
Which factors select for long juvenile periods in some species is not well understood. One potential reason to delay the onset of reproduction is slow food acquisition rates, either due to competition (part of the ecological risk avoidance hypothesis), or due to a decreased foraging efficiency (a version of the needing to learn hypothesis). Capuchins provide a useful genus to test the needing to learn hypothesis because they are known for having long juvenile periods and a difficult-to-acquire diet. Generalized, linear, mixed models with data from 609 fruit forage focal follows on 49, habituated, wild Cebus capucinus were used to test two predictions from the needing-to-learn hypothesis as it applies to fruit foraging skills: 1) capuchin monkeys do not achieve adult foraging return rates for difficult-to-acquire fruits before late in the juvenile period; and 2) variance in return rates for these fruits is at least partially associated with differences in foraging skill. In support of the first prediction, adults, compared with all younger age classes, had significantly higher foraging return rates when foraging for fruits that were ranked as difficult-to-acquire (return rates relative to adults: 0.30–0.41, p-value range 0.008–0.016), indicating that the individuals in the group who have the most foraging experience also achieve the highest return rates. In contrast, and in support of the second prediction, there were no significant differences between age classes for fruits that were ranked as easy to acquire (return rates relative to adults: 0.97–1.42, p-value range 0.086–0.896), indicating that strength and/or skill are likely to affect return rates. In addition, fruits that were difficult to acquire were foraged at nearly identical rates by adult males and significantly smaller (and presumably weaker) adult females (males relative to females: 1.01, p = 0.978), while subadult females had much lower foraging efficiency than the similarly-sized but more experienced adult females (subadults relative to adults: 0.34, p = 0.052), indicating that skill, specifically, is likely to have an effect on return rates. These results are consistent with the needing to learn hypothesis and indicate that long juvenile periods in capuchins may be the result of selection for more time to learn foraging skills for difficult-to-acquire fruits.
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