Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in northwestern Madagascar

We investigated the sleeping site ecology of two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in northwestern Madagascar during the second half of the dry season with respect to the type, quality, and usage pattern of the sleeping sites, as well as to social sleeping habits and response to potential threats. The type and quality of the sleeping sites differed between the two species. M. murinus used protected wooden shelters (tree holes) more frequently than M. ravelobensis, and M. ravelobensis used a broader variety of less protected sites (e.g., branches, lianas, and leaves) than M. murinus. Whereas male M. murinus usually slept alone, and female M. murinus mostly slept in groups, both sexes of M. ravelobensis slept in mixed-sex sleeping groups. M. murinus relied on crypsis in their sleeping sites, whereas M. ravelobensis regularly showed a flight response to the approach of an observer. This behavioral difference could indicate an adaptation to a higher predation risk in less protected sleeping sites. Whereas female M. murinus showed a high site fidelity, male M. murinus and both sexes of M. ravelobensis frequently changed their sleeping sites, which may also be interpreted as an antipredator strategy. The results are discussed with respect to three possible ecological explanations: interspecies competition, restricted resource availability, and niche differentiation. The latter is the most likely explanation for these interspecific differences.     

Isolation of new microsatellite markers and application in four species of mouse lemurs (Microcebus sp.)

We report the development of 13 new microsatellite markers for mouse lemurs (Microcebus sp.). Two markers were isolated from the fat tailed dwarf lemur (Cheirogaleus medius) and 11 from the grey mouse lemur (Microcebus murinus). A total of 561 individuals from four different species of mouse lemurs was genotyped with the newly developed markers. All markers showed Mendelian inheritance in 21 families of mouse lemurs. All markers show polymorphism in several species of mouse lemurs and seven amplified in C. medius. Among these new markers are the first 10 published for M. berthae and the first 11 for M. griseorufus.     

Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis)

Affiliation/agonism and social dominance are central factors determining social organization in primates. The aim of our study is to investigate and describe, for the first time, the intersexual relations in a nocturnal and cohesive pair‐living prosimian primate, the western woolly lemur (Avahi occidentalis), and to determine to what extent phylogeny, activity mode, or the cohesiveness of pair partners shape the quality of social interactions. Six pairs of western woolly lemurs were radio‐collared in the dry deciduous forest of northwestern Madagascar. More than 874 hr of focal animal sampling were conducted. All occurrences of social interactions involving a focal animal were recorded. The rate of affiliation between pair partners was significantly higher than the rate of agonism. Western woolly lemur pairs' interactions were extremely peaceful. All decided agonistic conflicts (N = 15) were exclusively initiated and won by the female. No female showed spontaneous submission toward her male partner. These results are in line with those of diurnal cohesive pair‐living anthropoid primates. Findings support the hypothesis that social relations in pair‐living primates are linked to the cohesiveness of pair partners in time and space irrespective of phylogeny and activity mode. Am. J. Primatol. 73:1261–1268, 2011. © 2011 Wiley Periodicals, Inc.     

Diet and nutrition in wild mongoose lemurs (Eulemur mongoz) and their implications for the evolution of female dominance and small group size in lemurs

Data collected on the feeding behavior, food intake, and chemical analyses of plant foods were used to document seasonal variation in diet and nutrition in Eulemur mongoz in northwestern Madagascar. E. mongoz conforms to the general Eulemur dietary pattern, with a predominantly frugivorous diet supplemented mainly by leaves, flowers, and nectar. Phytochemical analysis revealed high water contents in all the main plant foods; mature fruit and flowers contained the most water-soluble carbohydrates; immature leaves were richest in protein and essential amino acids; the limiting amino acids in all plant foods were methionine and cystine; ash (mineral) content was highest in petioles and mature leaves; crude lipid content was highest in seeds; and crude fiber content was indistinguishable between immature and mature fruit and leaves. High-fiber foods were eaten during both seasons; the wet season diet was dominated by high-energy foods (mature fruit, nectar, and seeds), while the dry season diet contained foods high in energy (mature fruit and flowers) and high in protein (immature leaves) and minerals (mature leaves and petioles). However, nutrient intake did not vary between seasons, implying that nutrient requirements are met throughout the year. These results suggest we draw more conservative conclusions when interpreting dietary variability in the absence of chemical analysis, and also draw into question the idea that nutritional stress is a factor in the timing of reproduction in lemurs and, by extension, is linked to the prevalence of female dominance and small group size in lemurs.     

Noninvasive molecular sexing: An evaluation and validation of the SRY‐ and amelogenin‐based method in three new lemur species

Many lemur species are arboreal, elusive, and/or nocturnal and are consequently difficult to approach, observe and catch. In addition, most of them are endangered. For these reasons, non‐invasive sampling is especially useful in primates including lemurs. A key issue in conservation and ecological studies is to identify the sex of the sampled individuals to investigate sex‐biased dispersal, parentage, social organization and population sex ratio. Several molecular tests of sex are available in apes and monkeys, but only a handful of them work in the lemuriform clade. Among these tests, the coamplification of the SRY gene with the amelogenin X gene using strepsirhine‐specific X primers seems particularly promising, but the reliability and validity of this sexing test have not been properly assessed yet. In this study, we (i) show that this molecular sexing test works on three additional lemur species (Microcebus tavaratra, Propithecus coronatus and P. verreauxi) from two previously untested genera and one previously untested family, suggesting that these markers are likely to be universal among lemurs and other strepsirrhines; (ii) provide the first evidence that this PCR‐based sexing test works on degraded DNA obtained from noninvasive samples; (iii) validate the approach using a large number of known‐sex individuals and a multiple‐tubes approach, and show that mismatches between the field sex and the final molecular consensus sex occur in less than 10% of all the samples and that most of these mismatches were likely linked to incorrect sex determinations in the field rather than genotyping errors. Am J Phys Anthropol, 2013. © 2013 Wiley Periodicals, Inc.     

The evolution of social philopatry in female primates

The transition from solitary life to sociality is considered one of the major transitions in evolution. In primates, this transition is currently not well understood. Traditional verbal models appear insufficient to unravel the complex interplay of environmental and demographic factors involved in the evolution of primate sociality, and recent phylogenetic reconstructions have produced conflicting results. We therefore analyze a theoretical model for the evolution of female social philopatry that sheds new light on the question why most primates live in groups. In individual-based simulations, we study the evolution of dispersal strategies of both resident females and their offspring. The model reveals that social philopatry can evolve through kin selection, even if retention of offspring is costly in terms of within-group resource competition and provides no direct benefits. Our model supports the role of predator avoidance as a selective pressure for group-living in primates, but it also suggests that a second benefit of group-living, communal resource defense, might be required to trigger the evolution of sizable groups. Lastly, our model reveals that seemingly small differences in demographic parameters can have profound effects on primate social evolution.     

Feeding enrichment by self‐operated food boxes for white‐fronted lemurs (Eulemur fulvus albifrons) in the Masoala exhibit of the Zurich Zoo

In the new Masoala exhibit of the Zurich Zoo four self‐operated food boxes were installed to encourage arboreal behavior and higher activity levels, and to increase the attractiveness to visitors of a group of three white‐fronted lemurs (Eulemur fulvus albifrons) and one Alaotran gentle lemur (Hapalemur griseus alaotrensis). Data obtained by direct observations with and without food boxes present were compared. In addition, visitors were surveyed to investigate attractiveness of the lemurs. Overall activity and locomotor behavior increased due to food box presentation. Furthermore, the visitor survey documented that the lemurs were spotted more often in trees when the food boxes were present. Because behavior patterns of the subjects approached natural levels with food boxes, the presentation of self‐operated food boxes seems a valuable tool to improve the captive environment of lemurs. Zoo Biol 0:1–10, 2005. © 2005 Wiley‐Liss, Inc.     

Predominant contribution of cis‐regulatory divergence in the evolution of mouse alternative splicing

Divergence of alternative splicing represents one of the major driving forces to shape phenotypic diversity during evolution. However, the extent to which these divergences could be explained by the evolving cis‐regulatory versus trans‐acting factors remains unresolved. To globally investigate the relative contributions of the two factors for the first time in mammals, we measured splicing difference between C57BL/6J and SPRET/EiJ mouse strains and allele‐specific splicing pattern in their F1 hybrid. Out of 11,818 alternative splicing events expressed in the cultured fibroblast cells, we identified 796 with significant difference between the parental strains. After integrating allele‐specific data from F1 hybrid, we demonstrated that these events could be predominately attributed to cis‐regulatory variants, including those residing at and beyond canonical splicing sites. Contrary to previous observations in Drosophila, such predominant contribution was consistently observed across different types of alternative splicing. Further analysis of liver tissues from the same mouse strains and reanalysis of published datasets on other strains showed similar trends, implying in general the predominant contribution of cis‐regulatory changes in the evolution of mouse alternative splicing.     

The evolution of female multiple mating in social hymenoptera

Abstract The evolution of female multiple mating is a highly controversial topic, especially in social insects. Here we analyze, using comparative analyses and simulation models, the merits of two major contending hypotheses for the adaptive value of polyandry in this group. The hypotheses maintain that, respectively, the resulting genotypic diversity among offspring within a colony: (1) mitigates against the effects of parasites; or (2) favors adaptive division of labor. Only two of 11 phylogenetically uncontrolled comparative analyses supported an association between polyandry and the complexity of division of labor (measured here using worker caste polymorphism or polyethism) as proposed by hypothesis 2, and after controlling for phylogeny there were no significant associations. In contrast, a previous study demonstrated such an association for parasite load as expected under hypothesis 1. In addition, we used simulation models to track the spread of an initially rare allele for double mating in a population of single-mating alleles, thus analyzing the crucial first step from monandry to polyandry. We find that double mating evolves consistently under antagonistic coevolution given that parasites exert sufficient selection intensity. In contrast, selection for enhanced division of labor resulted in only an erratic appearance of polyandry in highly (and mostly negatively) autocorrelated environments where no coevolutionary dynamics were allowed. Together, we interpret these results to suggest that parasites, and the antagonistic coevolutionary pressures they exert, may play an important role in the evolution of polyandry in social hymenopteran populations.     

Sex‐dependent effects of Cacna1c haploinsufficiency on juvenile social play behavior and pro‐social 50‐kHz ultrasonic communication in rats

As cross‐disorder risk gene, CACNA1C is implicated in the etiology of all major neuropsychiatric disorders characterized by deficits in social behavior and communication and there is evidence for sex‐dependent influences of single‐nucleotide polymorphisms within CACNA1C on diagnosis, course, and recovery in humans. In this study, we aimed, therefore, at further exploring the role of Cacna1c in regulating behavioral phenotypes, focusing on sex‐specific differences in social behavior and communication during the critical developmental period of adolescence in rats. Specifically, we compared rough‐and‐tumble play, concomitant emission of pro‐social 50‐kHz ultrasonic vocalizations, and social approach behavior in response to playback of 50‐kHz ultrasonic vocalizations between constitutive heterozygous Cacna1c ^+/? females and wildtype Cacna1c ^+/+ littermate controls, and contrasted present female findings to data previously reported in males. Our results show for the first time that partial depletion of Cacna1c leads to sex‐dependent alterations in social behavior and communication in rats. In females, Cacna1c haploinsufficiency led to hypermasculinization, with rough‐and‐tumble play behavior, in general, and pinning behavior, in particular, being even higher than in males without affecting concomitant 50‐kHz ultrasonic vocalizations. In males, in contrast, rough‐and‐tumble play behavior was not altered, yet emission of 50‐kHz ultrasonic vocalizations was diminished following partial Cacna1c depletion. The behavioral responses elicited by playback of 50‐kHz ultrasonic vocalizations were reduced upon partial Cacna1c depletion in both sexes. It thus can be concluded that Cacna1c plays a prominent sex‐dependent role in regulating juvenile rat social play behavior and pro‐social 50‐kHz ultrasonic communication with relevance to sex‐specific effects seen in neuropsychiatric disorders.     

The importance of genomic novelty in social evolution

Insect societies dominate the natural world: They mould landscapes, sculpt habitats, pollinate plants, sow seeds and control pests. The secret to their success lies in the evolution of queen (reproductive) and worker (provisioner and carer) castes (Oster & Wilson 1978 ). A major problem in evolutionary biology is explaining the evolution of insect castes, particularly the workers (Darwin 1859 ). Next‐generation sequencing technologies now make it possible to understand how genomic material is born, lost and reorganized in the evolution of alternative phenotypes. Such analyses are revealing a general role for novel (e.g. taxonomically restricted) genes in phenotypic innovations across the animal kingdom (Chen et al. 2013). In this issue of molecular ecology, Feldmeyer et al. (2014) provide overwhelming evidence for the importance of novel genes in caste evolution in an ant. Feldmeyer et al.'s study is important and exciting because it cements the role of genomic novelty, as well as conservation, firmly into the molecular jigsaw of social evolution. Evolution is eclectic in its exploitation of both old and new genomic material to generate replicated phenotypic innovations across the tree of life.     

Aggression Levels Affect Social Interaction in the Non‐Breeding Territorial Aggression of the Weakly Electric Fish,Gymnotus omarorum

Animals typically decide whether to fight or retreat from conspecifics based on their individual estimates of the costs and benefits of fighting. Theoretical models predict how contenders solve a conflict, but the evaluation processes involved in these decisions depend on multiple factors that are difficult to explore experimentally. We addressed these questions using the non‐breeding territorial aggression of Gymnotus omarorum, in which subordinates make three distinctive decisions to signal their submission during a fight: (1) interruption of their electric discharges to hide from the dominant, (2) stop attacking and retreat, and (3) emission of ‘chirps’, transient submissive electric signals. We confirmed that subordinates take into account the aggressive performance of dominants to shape their own agonistic decisions and performance. The intensity of aggression is highly correlated with an agonistic dyad, and the decision of subordinates to retreat is influenced by the attack rates of dominants. When we lowered the aggression of expected dominants with a 5‐HT_1A receptor agonist, the correlation between the two contenders' aggression levels was lost and subordinates completely stopped emitting electric chirp signals. The aforementioned results contribute to the understanding of the decision‐making strategies driven by social challenge inherent to agonistic encounters.     

Maternal and offspring methylenetetrahydrofolate‐reductase genotypes interact in a mouse model to induce autism spectrum disorder‐like behavior

Individuals with autism constitute a variable population whose members are spread along the autism spectrum. Subpopulations within that spectrum exhibit other conditions, such as anxiety, intellectual disabilities, hyperactivity and epilepsy, with different severities and co‐occurrences. Among the genes associated with the increased risk for autism is the methylenetetrahydrofolate‐reductase (MTHFR) 677C>T polymorphism, which impairs one‐carbon (C1) metabolic pathway efficiency. The frequency of the MTHFR677TT homozygote is markedly higher among autism patients and their mothers than in the general population. Here, we report on the Mthfr heterozygous knockout (KO) mouse as a rodent model of autism that shows the contributions of maternal and offspring genotypes to the development of autistic‐like behaviors. Maternal Mthfr‐deficiency was associated with developmental delays in morphogenic features and sensory‐motor reflexes in offspring. In the adult male mouse, behaviors representing core autism symptoms, such as repetitive behavior and restricted interest, were affected by maternal genotype while social behaviors were affected by both maternal and offspring genotypes. In females and males, behaviors associated with autism such as memory impairment, social aggression and anxiety were affected by both the maternal and offspring Mthfr genotypes, with sex‐dependent differences. Mthfr‐deficient male mice with observable impacts on behavior presented a particular laminar disturbance in parvalbumin interneuron density and innervation in superficial and deep layers of the cingulate cortex. This mouse model of autism will help to elucidate the molecular mechanisms that predispose a significant subgroup of autistic patients to abnormal development and to distinguish between the in‐utero and autonomous factors involved in autism.