A 24-Year Record of Female Reproductive Dynamics in Two Sympatric Mouse Lemur Species in Northwestern Madagascar

Seasonal reproduction is widespread among primates but the degree of reproductive synchrony and plasticity can vary, even between closely related species. This study compares the dynamics of female reproductive seasonality in two mouse lemur species, Microcebus murinus and M. ravelobensis, in Ankarafantsika National Park, Madagascar, across 24 years. We collected 4321 records of female reproductive state from 1033 individual females (319 M. murinus, 714 M. ravelobensis). The analyses revealed disparate reproductive schedules: While female M. murinus showed high degrees of reproductive synchrony throughout all years, leading to the production of two successive litters, the seasonal onset of estrus (= reproductive activation) in female M. ravelobensis was more flexible than in M. murinus, starting 2-4 weeks earlier, varying by up to 4 weeks between years, and being less synchronized. M. ravelobensis females became reproductively active later in years with more rainfall, in particular rain in February, but the timing of reproductive activation was not related to differences in temperatures. The likelihood of early conception was significantly lower in M. ravelobensis than in M. murinus. This was partly due to delayed reproductive activation in young animals, and a lower likelihood of early conception for females with low body mass in M. ravelobensis. Our results suggest high, adaptive reproductive plasticity in M. ravelobensis that may enable individuals to respond flexibly to yearly environmental changes and expand the reproductive period under favorable conditions. These species differences in reproductive schedules may be the result of the divergent evolutionary histories of the two mouse lemur species in different parts of Madagascar.

Linking cognition to ecology in wild sympatric mouse lemur species

Cognitive abilities covary with both social and ecological factors across animal taxa. Ecological generalists have been attributed with enhanced cognitive abilities, but which specific ecological factors may have shaped the evolution of which specific cognitive abilities remains poorly known. To explore these links, we applied a cognitive test battery (two personality, ten cognitive tests; n = 1104 tests) to wild individuals of two sympatric mouse lemur species ( n = 120 Microcebus murinus, n = 34 M. berthae ) varying in ecological adaptations but sharing key features of their social systems. The habitat and dietary generalist grey mouse lemurs were more innovative and exhibited better spatial learning abilities; a cognitive advantage in responding adaptively to dynamic environmental conditions. The more specialized Madame Berthe's mouse lemurs were faster in learning associative reward contingencies, providing relative advantages in stable environmental conditions. Hence, our study revealed key cognitive correlates of ecological adaptations and indicates potential cognitive constraints of specialists that may help explain why they face a greater extinction risk in the context of current environmental changes.

Enriched sleep environments lengthen lemur sleep duration

Characteristics of the sleep-site are thought to influence the quality and duration of primate sleep, yet only a handful of studies have investigated these links experimentally. Using actigraphy and infrared videography, we quantified sleep in four lemur species (Eulemur coronatus, Lemur catta, Propithecus coquereli, and Varecia rubra) under two different experimental conditions at the Duke Lemur Center (DLC) in Durham, NC, USA. Individuals from each species underwent three weeks of simultaneous testing to investigate the hypothesis that comfort level of the sleep-site influences sleep. We obtained baseline data on normal sleep, and then, in a pair-wise study design, we compared the daily sleep times, inter-daily activity stability, and intra-daily activity variability of individuals in simultaneous experiments of sleep-site enrichment and sleep-site impoverishment. Over 164 24-hour periods from 8 individuals (2 of each species), we found evidence that enriched sleep-sites increased daily sleep times of lemurs, with an average increase of thirty-two minutes. The effect of sleep-site impoverishment was small and not statistically significant. Though our experimental manipulations altered inter-daily stability and intra-daily variability in activity patterns relative to baseline, the changes did not differ significantly between enriched and impoverished conditions. We conclude that properties of a sleep-site enhancing softness or insulation, more than the factors of surface area or stability, influence lemur sleep, with implications regarding the importance of nest building in primate evolution and the welfare and management of captive lemurs.

RADseq data reveal a lack of admixture in a mouse lemur contact zone contrary to previous microsatellite results

Despite being one of the most fundamental biological processes, the process of speciation remains poorly understood in many groups of organisms. Mouse lemurs are a species-rich genus of small primates endemic to Madagascar, whose diversity has only recently been uncovered using genetic data and is primarily found among morphologically cryptic, allopatric populations. To assess to what extent described species represent reproductively isolated entities, studies are needed in areas where mouse lemur taxa come into contact. Hybridization has previously been reported in a contact zone between two closely related mouse lemur species (Microcebus murinus and M. griseorufus) based on microsatellite data. Here, we revisit this system using RADseq data for populations in, near, and far from the contact zone, including many of the individuals that had previously been identified as hybrids. Surprisingly, we find no evidence for admixed nuclear ancestry in any of the individuals. Re-analyses of microsatellite data and simulations suggest that previously inferred hybrids were false positives and that the program NewHybrids can be particularly sensitive to erroneously inferring hybrid ancestry. Using coalescent-bases analyses, we also show an overall lack of recent gene flow between the two species, and low levels of ancestral gene flow. Combined with evidence for local syntopic occurrence, these data indicate that M. murinus and M. griseorufus are reproductively isolated. Finally, we estimate that they diverged less than a million years ago, suggesting that completion of speciation is relatively rapid in mouse lemurs. Future work should focus on the underpinnings of reproductive isolation in this cryptic primate radiation, which are mostly unknown. Our study also provides a cautionary tale for the inference of hybridization with microsatellite data.

Enriched sleep environments lengthen lemur sleep duration

Characteristics of the sleep-site are thought to influence the quality and duration of primate sleep, yet only a handful of studies have investigated these links experimentally. Using actigraphy and infrared videography, we quantified sleep in four lemur species ( Eulemur coronatus, Lemur catta, Propithecus coquereli, and Varecia rubra ) under two different experimental conditions at the Duke Lemur Center (DLC) in Durham, NC, USA. Individuals from each species underwent three weeks of simultaneous testing to investigate the hypothesis that comfort level of the sleep-site influences sleep. We obtained baseline data on normal sleep, and then, in a pair-wise study design, we compared the daily sleep times of individuals in simultaneous experiments of sleep-site enrichment and sleep-site impoverishment. Over 163 24-hour periods from 8 individuals (2 of each species), we found strong evidence that enriched sleep-sites increased daily sleep times of lemurs, with an average increase of thirty-one minutes. The effect of sleep-site impoverishment was small and not statistically significant. We conclude that properties of a sleep-site enhancing softness or insulation, more than the factors of surface area or stability, influence lemur sleep, with implications regarding the importance of nest building in primate evolution and the welfare and management of captive lemurs.

I Like the Way You Eat It: Lemur (Indri indri) Gut Mycobiome and Geophagy

Here, we investigated the possible linkages among geophagy, soil characteristics, and gut mycobiome of indri (Indri indri), an endangered lemur species able to survive only in wild conditions. The soil eaten by indri resulted in enriched secondary oxide-hydroxides and clays, together with a high concentration of specific essential micronutrients. This could partially explain the role of the soil in detoxification and as a nutrient supply. Besides, we found that soil subject to geophagy and indris’ faeces shared about 8.9% of the fungal OTUs. Also, several genera (e.g. Fusarium, Aspergillus and Penicillium) commonly associated with soil and plant material were found in both geophagic soil and indri samples. On the contrary, some taxa with pathogenic potentials, such as Cryptococcus, were only found in indri samples. Further, many saprotrophs and plant-associated fungal taxa were detected in the indri faeces. These fungal species may be involved in the digestion processes of leaves and could have a beneficial role in their health. In conclusion, we found an intimate connection between gut mycobiome and soil, highlighting, once again, the potential consequent impacts on the wider habitat.