The lemur syndrome unresolved: extreme male reproductive skew in sifakas (Propithecus verreauxi), a sexually monomorphic primate with female dominance

Abstract

The primates of Madagascar (Lemuriformes) are unusual among mammals in that polygynous species lack sexual dimorphism, and females dominate males socially in most species. Moreover, lemur groups are relatively small and characterized by even adult sex ratios despite the fact that one male should be able to exclude other males from the group. One hypothesis to explain this combination of behavioral, morphological, and demographic traits (the "lemur syndrome") postulates that male-male competition is relaxed and, hence, variance in male reproductive success is low. Reproductive skew theory provides a framework for testing this and several related predictions about lemur social evolution. Specifically, low reproductive skew is also predicted if dominant males or adult females make reproductive concessions to subordinates or if the latter group successfully pursues alternative reproductive tactics. However, suitable data on paternity, demography, and behavior for a conclusive test of these predictions have not been available in the past. In this paper, we show that male reproductive success in ten groups of Verreaux's sifakas (Propithecus verreauxi) was extremely skewed in favor of the dominant male over 9 years. Our genetic analyses also revealed that more than a third of all groups are effectively harem groups because only one male was unrelated to the resident female(s). In groups with two or more non-natal males, the dominant sired 91% of 33 infants. Together, males pursuing one of several alternative reproductive tactics, such as roaming among several groups or immigrating peacefully, sired only 11% of infants. Thus, female sifakas do not control group composition by offering reproductive opportunities to subordinate males as staying incentives, intrasexual selection is not relaxed, and dominant males prevail in a tug-of-war over subordinate males. Because male reproductive skew in sifakas is even more pronounced than in harem-living anthropoids studied to date, intrasexual selection is clearly not relaxed, and the lemur syndrome is more puzzling than ever.

Cues to kinship and close relatedness during infancy in white-faced capuchin monkeys, Cebus capucinus

“…As a consequence of both the high degree of male reproductive skew seen at Lomas and the stability in male alpha rank, alpha status is an excellent marker of the paternal descent of infants in this population. In another primate with extreme male reproductive skew toward alpha males, Verreaux's sifakas (Propithecus verreauxi), dominant non-natal males residing in groups containing other non-natal adult males sire approximately 91% of offspring (Kappeler & Schäffler, 2008). Alpha male status should thus also be an informative marker for close relatedness, and more specifically paternity in these sifakas.…”

“…Alpha male status should thus also be an informative marker for close relatedness, and more specifically paternity in these sifakas. Indeed, there is some evidence for later father-daughter discrimination in the species in the form of inbreeding avoidance (Kappeler & Schäffler, 2008).…”

“…2009), bonobos (Gerloff et al, 1999), mountain gorillas (Bradley et al, 2005), mandrills Setchell et al, 2005), red howler monkeys (Pope, 1990), white-faced capuchins (Jack & Fedigan, 2006;Muniz et al, 2006Muniz et al, , 2010, red-fronted lemurs (Kappeler & Port, 2008), and sifakas (Kappeler & Schäffler, 2008)). If male dominance rank and group membership can remain relatively stable for longer than the typical gestation length for their species, then male dominance rank can serve as a cue to paternity for infants.…”

Mate-Guarding as a Male Reproductive Tactic in Propithecus verreauxi

“…Although the number of reproducing females within a group is small (1-3 individuals; Kubzdela 1997;Lewis 2005;Richard et al 2002), dominant males do not exclude rival males from group membership, resulting in a tendency toward an even adult sex ratio. Despite the presence of multiple males within groups, according to genetic paternity analysis, reproduction in the Kirindy Forest population is highly skewed in favor of dominant individuals with dominant males siring almost all offspring (91% of 33 infants; Kappeler and Schäffler 2008). In contrast, paternity analysis results for a population of Propithecus verreauxi at Beza Mahafaly revealed that extragroup fertilizations occur more frequently (Lawler 2007).…”

“…We studied 9 groups of well habituated sifakas living in one of these study areas. All individuals in the study population are marked with either unique nylon collars and pendants or radio collars (Kappeler and Schäffler 2008). Group size and composition varied across the 9 study groups over the 2 sampling periods (Table I).…”