Need for speed: Sexual maturation precedes social maturation in gray mouse lemurs

Abstract

The life history of mammals underlies a fast-slow continuum, ranging from "slow" species with large body size, delayed sexual maturation, low fertility, and long lifespan, to "fast" species showing the opposite traits. Primates fall into the "slow" category, considering their relatively low offspring numbers and delayed juvenile development. However, social and sexual maturation processes do not necessarily have to be completed simultaneously. The comparison of the timeframes for sexual and social maturation is largely lacking for primates, with the prominent exception of humans. Here, we compare both maturation processes in a basal primate, the gray mouse lemur, which ranges in many aspects at the fast end of the slow-fast life history continuum among primates. We compared the patterns and frequencies of various social and solitary behaviors in young adults (YA, 12-13 months old) and older individuals (A, ≥2 years) of both sexes outside estrus. Observations were conducted during mix-sexed dyadic encounter experiments under controlled captive conditions (eight dyads per age class). Results indicate that although all young adults were sexually mature, social maturation was not yet completed in all behavioral domains: Age-dependent differences were found in the number of playing dyads, female marking behavior, female aggression, and social tolerance. Thus, this study provides a first indication that social maturation lags behind sexual maturation in an ancestral nocturnal primate model, indicating that these two developmental schemes may have been decoupled early and throughout the primate lineage.

Mouse lemurs’ and degraded habitat

“…In addition, although several studies reported mouse lemurs’ poaching (Gardner & Davies, 2014; Jenkins et al, 2011) and its negative effects on DF use (Figure 3, Table 1), it seems not be as frequent as for larger-bodied lemur species (Jenkins et al, 2011; Lehman & Ratsimbazafy, 2001). Mouse lemur populations are likely to be less susceptible to poaching than larger-bodied lemurs because of their shorter generation time and higher reproductive rate (Hohenbrink, Zimmermann, & Radespiel, 2015; Zimmermann & Radespiel, 2013). Therefore, mouse lemur harvesting needs to be formally evaluated to determine under which conditions sustainability can be achieved (Gardner & Davies, 2014; Golden, 2009).…”

Sources of variation in social tolerance in mouse lemurs (Microcebus spp.)

“…It is known from the gray mouse lemur ( M. murinus ) that males can compete severely for the access to estrous females under natural conditions ( M. murinus , [15]) and in captivity ( M. murinus , [67]), and that conflict rates among the sexes are higher and female dominance is more expressed in the reproductive season than in the non-reproductive season, at least in captivity ( M. murinus , M. lehilahytsara , [42]). It was therefore predicted that social tolerance (i.e.…”

“…Not much is known about the social relationships in these dispersed social networks from the wild, although occasional nocturnal affiliative and agonistic encounters have been observed in several species [20, 29, 31, 37–39]. However, recent work from captivity suggests that female dominance that is untypical for mammals but formerly thought to be typical for most lemur species [40, 41], may be much more variable and plastic in mouse lemurs than expected [24, 25, 42]. For example, conflict rates, the probability for females to win conflicts, and the proportion of females being dominant over males varied between species ( M. murinus , M. lehilahytsara ) and season (reproductive vs. non-reproductive) and furthermore depended on age and breeding experience [25, 42].…”

“…However, recent work from captivity suggests that female dominance that is untypical for mammals but formerly thought to be typical for most lemur species [40, 41], may be much more variable and plastic in mouse lemurs than expected [24, 25, 42]. For example, conflict rates, the probability for females to win conflicts, and the proportion of females being dominant over males varied between species ( M. murinus , M. lehilahytsara ) and season (reproductive vs. non-reproductive) and furthermore depended on age and breeding experience [25, 42]. Whether this diverse, plastic and complex behavioral phenomenon is the outcome of adaptive evolutionary trajectories of different species [25, 43] or resulted from phylogenetic constraints [41], could not be clarified so far.…”

Characterisation of urinary WFDC12 in small nocturnal basal primates, mouse lemurs (Microcebus spp.)

“…Mouse lemurs possess a functional vomeronasal organ (VNO 22 23 ) and have a repertoire of over 200 vomeronasal receptor genes 24 25 that are expressed in the VNO but also partially in the main olfactory epithelium 22 . Olfaction may be involved in various contexts of intraspecific communication, as in marking group ownership of sleeping sites 19 , or in many aspects of reproduction, and may be used within and between the sexes 20 26 27 28 29 .…”