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Abstract Background Diversity at the Major Histocompatibility Complex (MHC) is critical to health and fitness, such that MHC genotype may predict an individual’s quality or compatibility as a competitor, ally, or mate. Moreover, because MHC products can influence the components of bodily secretions, an individual’s body odors may signal its MHC composition and influence partner identification or mate choice. Here, we investigated MHC-based signaling and recipient sensitivity by testing for odor-gene covariance and behavioral discrimination of MHC diversity and pairwise dissimilarity in a strepsirrhine primate, the ring-tailed lemur (Lemur catta). Methods First, we coupled genotyping of the MHC class II gene, DRB, with gas chromatography-mass spectrometry of genital gland secretions to investigate if functional genetic diversity is signaled by the chemical diversity of lemur scent secretions. We also assessed if the chemical similarity between individuals correlated with their MHC-DRB similarity. Next, we assessed if lemurs discriminated this chemically encoded, genetic information in opposite-sex conspecifics. Results We found that both sexes signaled overall MHC-DRB diversity and pairwise MHC-DRB similarity via genital secretions, but in a sex- and season-dependent manner. Additionally, the sexes discriminated absolute and relative MHC-DRB diversity in the genital odors of opposite-sex conspecifics, suggesting that lemur genital odors function to advertise genetic quality. Conclusions In summary, genital odors of ring-tailed lemurs provide honest information about an individual’s absolute and relative MHC quality. Complementing evidence in humans and Old World monkeys, we suggest that reliance on scent signals to communicate MHC quality may be important across the primate lineage.

The study of human chemical communication benefits from comparative perspectives that relate humans, conceptually and empirically, to other primates. All major primate groups rely on intraspecific chemosignals, but strepsirrhines present the greatest diversity and specialization, providing a rich framework for examining design, delivery and perception. Strepsirrhines actively scent mark, possess a functional vomeronasal organ, investigate scents via olfactory and gustatory means, and are exquisitely sensitive to chemically encoded messages. Variation in delivery, scent mixing and multimodality alters signal detection, longevity and intended audience. Based on an integrative, 19-species review, the main scent source used (excretory versus glandular) differentiates nocturnal from diurnal or cathemeral species, reflecting differing socioecological demands and evolutionary trajectories. Condition-dependent signals reflect immutable (species, sex, identity, genetic diversity, immunity and kinship) and transient (health, social status, reproductive state and breeding history) traits, consistent with socio-reproductive functions. Sex reversals in glandular elaboration, marking rates or chemical richness in female-dominant species implicate sexual selection of olfactory ornaments in both sexes. Whereas some compounds may be endogenously produced and modified (e.g. via hormones), microbial analyses of different odorants support the fermentation hypothesis of bacterial contribution. The intimate contexts of information transfer and varied functions provide important parallels applicable to olfactory communication in humans. [ABSTRACT FROM AUTHOR]

Background: The de novo assembly of repeat-rich mammalian genomes using only high-throughput short read sequencing data typically results in highly fragmented genome assemblies that limit downstream applications. Here, we present an iterative approach to hybrid de novo genome assembly that incorporates datasets stemming from multiple genomic technologies and methods. We used this approach to improve the gray mouse lemur (Microcebus murinus) genome from early draft status to a near chromosome-scale assembly. Methods: We used a combination of advanced genomic technologies to iteratively resolve conflicts and super-scaffold the M. murinus genome. Results: We improved the M. murinus genome assembly to a scaffold N50 of 93.32 Mb. Whole genome alignments between our primary super-scaffolds and 23 human chromosomes revealed patterns that are congruent with historical comparative cytogenetic data, thus demonstrating the accuracy of our de novo scaffolding approach and allowing assignment of scaffolds to M. murinus chromosomes. Moreover, we utilized our independent datasets to discover and characterize sequences associated with centromeres across the mouse lemur genome. Quality assessment of the final assembly found 96% of mouse lemur canonical transcripts nearly complete, comparable to other published high-quality reference genome assemblies. Conclusions: We describe a new assembly of the gray mouse lemur (Microcebus murinus) genome with chromosome-scale scaffolds produced using a hybrid bioinformatic and sequencing approach. The approach is cost effective and produces superior results based on metrics of contiguity and completeness. Our results show that emerging genomic technologies can be used in combination to characterize centromeres of non-model species and to produce accurate de novo chromosome-scale genome assemblies of complex mammalian genomes. [ABSTRACT FROM AUTHOR]

Across species, diversity at the major histocompatibility complex ( MHC) is critical to individual disease resistance and, hence, to population health; however, MHC diversity can be reduced in small, fragmented, or isolated populations. Given the need for comparative studies of functional genetic diversity, we investigated whether MHC diversity differs between populations which are open, that is experiencing gene flow, versus populations which are closed, that is isolated from other populations. Using the endangered ring-tailed lemur ( Lemur catta) as a model, we compared two populations under long-term study: a relatively 'open,' wild population ( n = 180) derived from Bezà Mahafaly Special Reserve, Madagascar (2003-2013) and a 'closed,' captive population ( n = 121) derived from the Duke Lemur Center ( DLC, 1980-2013) and from the Indianapolis and Cincinnati Zoos (2012). For all animals, we assessed MHC- DRB diversity and, across populations, we compared the number of unique MHC- DRB alleles and their distributions. Wild individuals possessed more MHC- DRB alleles than did captive individuals, and overall, the wild population had more unique MHC- DRB alleles that were more evenly distributed than did the captive population. Despite management efforts to maintain or increase genetic diversity in the DLC population, MHC diversity remained static from 1980 to 2010. Since 2010, however, captive-breeding efforts resulted in the MHC diversity of offspring increasing to a level commensurate with that found in wild individuals. Therefore, loss of genetic diversity in lemurs, owing to small founder populations or reduced gene flow, can be mitigated by managed breeding efforts. Quantifying MHC diversity within individuals and between populations is the necessary first step to identifying potential improvements to captive management and conservation plans. [ABSTRACT FROM AUTHOR]

Periods of reproduction are linked to changes in male behaviour, physiology and physical parameters. Although high androgen concentrations hold numerous advantages, especially during reproductive periods, chronically elevated androgen concentrations over long periods may be costly and thus need to be regulated. As such seasonal breeders will display temporary elevated androgen concentrations, increased testis levels and mating behaviour only during important reproductive periods. We studied a captive as well as a free-ranging population of the polygamous strepsirrhine primate, the African lesser bushbaby Galago moholi, to clarify the link between androgen concentration, reproductive behaviour and testis size and the importance of the two mating periods observed in the species. To monitor androgen patterns, we used faecal sampling and quantification of faecal androgen metabolites ( fAM). We additionally collected testicular measurements and behavioural data. G. moholi displayed a strong degree of reproductive seasonality, with maximum fAM concentration, testicular volume ( TV) and behavioural activity focused on the mating periods. In contrast to other studies, TV increased prior to fAM, with reproductive activity being initiated only when fAM concentrations reached high levels. Changes in TV and fAM concentrations were not significantly different between both mating periods. Based on the absence of a significant difference between mating seasons, it is likely that male G. moholi attempt to maximize their reproductive success by utilizing both mating periods equally. This study is the first to describe the reproductive endocrine pattern linked to physical changes and mating behaviour in any galago species, increasing our understanding of the reproductive biology of nocturnal, polygamous primates. [ABSTRACT FROM AUTHOR]

Background: The gut microbiome (GMB) is the first line of defense against enteric pathogens, which are a leading cause of disease and mortality worldwide. One such pathogen, the protozoan Cryptosporidium, causes a variety of digestive disorders that can be devastating and even lethal. The Coquerel's sifaka (Propithecus coquereli) - an endangered, folivorous primate endemic to Madagascar - is precariously susceptible to cryptosporidiosis under captive conditions. If left untreated, infection can rapidly advance to morbidity and death. Objective: To gain a richer understanding of the pathophysiology of this pathogen while also improving captive management of endangered species, we examine the impact of cryptosporidiosis on the GMB of a flagship species known to experience a debilitating disease state upon infection. Design: Using 16S sequencing of DNA extracted from sifaka fecal samples, we compared the microbial communities of healthy sifakas to those of infected individuals, across infection and recovery periods. Results: Over the course of infection, we found that the sifaka GMB responds with decreased microbial diversity and increased community dissimilarity. Compared to the GMB of unaffected individuals, as well as during pre-infection and recovery periods, the GMB during active infection was enriched for microbial taxa associated with dysbiosis and rapid transit time. Time to recovery was inversely related to age, with young animals being slowest to recover GMB diversity and full community membership. Antimicrobial treatment during infection caused a significant depletion in GMB diversity. Conclusions: Although individual sifakas show unique trajectories of microbial loss and recolonization in response to infection, recovering sifakas exhibit remarkably consistent patterns, similar to initial community assembly of the GMB in infants. This observation, in particular, provides biological insight into the rules by which the GMB recovers from the disease state. Fecal transfaunation may prove effective in restoring a healthy GMB in animals with specialized diets. [ABSTRACT FROM AUTHOR]

Animals communicating via scent often deposit composite signals that incorporate odorants from multiple sources; however, the function of mixing chemical signals remains understudied. We tested both a ‘multiple-messages’ and a ‘fixative’ hypothesis of composite olfactory signalling, which, respectively, posit that mixing scents functions to increase information content or prolong signal longevity. Our subjects—adult, male ring-tailed lemurs (Lemur catta)—have a complex scent-marking repertoire, involving volatile antebrachial (A) secretions, deposited pure or after being mixed with a squalene-rich paste exuded from brachial (B) glands. Using behavioural bioassays, we examined recipient responses to odorants collected from conspecific strangers. We concurrently presented pure A, pure B and mixed A + B secretions, in fresh or decayed conditions. Lemurs preferentially responded to mixed over pure secretions, their interest increasing and shifting over time, from sniffing and countermarking fresh mixtures, to licking and countermarking decayed mixtures. Substituting synthetic squalene (S)—a well-known fixative—for B secretions did not replicate prior results: B secretions, which contain additional chemicals that probably encode salient information, were preferred over pure S. Whereas support for the ‘multiple-messages’ hypothesis underscores the unique contribution from each of an animal's various secretions, support for the ‘fixative’ hypothesis highlights the synergistic benefits of composite signals.

The role of androgens in shaping "masculine" traits in males is a core focus in behavioral endocrinology, but relatively little is known about an androgenic role in female aggression and social dominance. In mammalian models of female dominance, including the ring-tailed lemur (Lemur catta), links to androgens in adulthood are variable. We studied the development of ring-tailed lemurs to address the behavioral basis and ontogenetic mechanisms of female dominance. We measured behavior and serum androgen concentrations in 24 lemurs (8 males, 16 females) from infancy to early adulthood, and assessed their 'prenatal' androgen milieu using serum samples obtained from their mothers during gestation. Because logistical constraints limited the frequency of infant blood sampling, we accounted for asynchrony between behavioral and postnatal hormone measurements via imputation procedures. Imputation was unnecessary for prenatal hormone measurements. The typical sex difference in androgen concentrations in young lemurs was consistent with adult conspecifics and most other mammals; however, we found no significant sex differences in rough-and-tumble play. Female (but not male) aggression increased beginning at approximately 15 months, coincident with female puberty. In our analyses relating sexually differentiated behavior to androgens, we found no relationship with activational hormones, but several significant relationships with organizational hormones. Notably, associations of prenatal androstenedione and testosterone with behavior were differentiated, both by offspring sex and by type of behavior within offspring sexes. We discuss the importance of considering (1) missing data in behavioral endocrinology research, and (2) organizational androgens other than testosterone in studies of female dominance. • Androgens may influence female aggression and dominance. • Across species, links between androgens and female dominance are variable. • We collected longitudinal data on juvenile Lemur catta and their mothers. • Despite typical androgenic sex differences, female aggression rises during development. • Maternal androgens predict offspring play and aggression. [ABSTRACT FROM AUTHOR]

Animals communicating via scent often deposit composite signals that incorporate odorants from multiple sources; however, the function of mixing chemical signals remains understudied. We tested both a 'multiple-messages' and a 'fixative' hypothesis of composite olfactory signalling, which, respectively, posit that mixing scents functions to increase information content or prolong signal longevity. Our subjects-adult, male ring-tailed lemurs (Lemur catta)-have a complex scent-marking repertoire, involving volatile antebrachial (A) secretions, deposited pure or after being mixed with a squalene-rich paste exuded from brachial (B) glands. Using behavioural bioassays, we examined recipient responses to odorants collected from conspecific strangers. We concurrently presented pure A, pure B and mixed A + B secretions, in fresh or decayed conditions. Lemurs preferentially responded to mixed over pure secretions, their interest increasing and shifting over time, from sniffing and countermarking fresh mixtures, to licking and countermarking decayed mixtures. Substituting synthetic squalene (S)-a well-known fixative-for B secretions did not replicate prior results: B secretions, which contain additional chemicals that probably encode salient information, were preferred over pure S. Whereas support for the 'multiple-messages' hypothesis underscores the unique contribution from each of an animal's various secretions, support for the 'fixative' hypothesis highlights the synergistic benefits of composite signals.