Insect secretions determine habitat use patterns by a female lesser mouse lemur (Microcebus murinus)

The lesser mouse lemur (Microcebus murinus) is one of six sympatric nocturnal primates found in the Kirindy forest, west-Madagascar. Each of these species is reported to consume a secretion produced during the austral winter by the Homopteran insect Flatidia coccinea. In July and August 1993 a study was conducted to determine the importance of this food resource in the ecology of female M. murinus. At this study site, animals were distributed only along the forest edge where insect secretions are significantly more abundant than in the forest interior. Abundances of arboreal and nocturnal flying insects do not differ between the forest edge and interior. Experimental resource removal from a 25 × 25 m plot in one female's home range caused a significant shift in the animals' pattern of habitat use while no change occurred in a control plot. Thus, at this study site and time of year, the ranging behavior of a female M. murinus was strongly influenced by the presence of Homopteran secretions. © 1995 Wiley-Liss, Inc.     

Daily torpor in the gray mouse lemur (Microcebus murinus) in Madagascar: energetic consequences and biological significance

Patterns and energetic consequences of spontaneous daily torpor were measured in the gray mouse lemur (Microcebus murinus) under natural conditions of ambient temperature and photoperiod in a dry deciduous forest in western Madagascar. Over a period of two consecutive dry seasons, oxygen consumption (VO₂) and body temperature (T _b) were measured on ten individuals kept in outdoor enclosures. In all animals, spontaneous daily torpor occurred on a daily basis with torpor bouts lasting from 3.6 to 17.6 h, with a mean torpor bout duration of 9.3 h. On average, body temperatures in torpor were 17.3±4.9°C with a recorded minimum value of 7.8°C. Torpor was not restricted to the mouse lemurs’ diurnal resting phase: entries occurred throughout the night and arousals mainly around midday, coinciding with the daily ambient temperature maximum. Arousal from torpor was a two-phase process with a first passive, exogenous heating where the T _b of animals increased from the torpor T _b minimum to a mean value of 27.1°C before the second, endogenous heat production commenced to further raise T _b to normothermic values. Metabolic rate during torpor (28.6±13.2 ml O₂ h^–1) was significantly reduced by about 76% compared to resting metabolic rate (132.6±50.5 ml O₂ h^–1). On average, for all M. murinus individuals measured, hypometabolism during daily torpor reduced daily energy expenditure by about 38%. In conclusion, all these energy-conserving mechanisms of the nocturnal mouse lemurs, with passive exogenous heating during arousal from torpor, low minimum torpor T _bs, and extended torpor bouts into the activity phase, comprise an important and highly adapted mechanism to minimize energetic costs in response to unfavorable environmental conditions and may play a crucial role for individual fitness. Received: 8 July 1999 / Accepted: 3 December 1999     

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.     

Female dominance in captive gray mouse lemurs (Microcebus murinus)

Female dominance or female feeding priority seem to be characteristic for many lemur species, but are rare traits in other primates and mammals in general. The nocturnal lemur species, however, are underrepresented in the quantitative studies on social dominance. The aim of this study is to investigate the pattern of intersexual dominance relationships in the gray mouse lemur (Microcebus murinus), a species that is generally thought to possess a number of ancestral lemur traits. The context, distribution, and outcome of intersexual conflicts are analyzed in four captive groups of gray mouse lemurs. Intersexual conflicts occurred in the study groups in different behavioral contexts and were mostly spatial interactions (chasing/fleeing, approach/avoidance). The majority of conflicts were decided, and were in all but one case won by females. This is the first evidence suggesting unconditional female dominance in a cheirogaleid primate. The existence of female dominance in most families of the Lemuriformes suggests it is an ancient trait that evolved in their common ancestor.     

Daily energy expenditure of the grey mouse lemur (Microcebus murinus): a small primate that uses torpor

We aimed to investigate the pattern of utilisation of torpor and its impact on energy budgets in free-living grey mouse lemurs (Microcebus murinus), a small nocturnal primate endemic to Madagascar. We measured daily energy expenditure (DEE) and water turnover using doubly labelled water, and we used temperature-sensitive radio collars to measure skin temperature (T _sk) and home range. Our results showed that male and female mouse lemurs in the wild enter torpor spontaneously over a wide range of ambient temperatures (T _a) during the dry season, but not during the rainy season. Mouse lemurs remained torpid between 1.7–8.9 h with a daily mean of 3.4 h, and their T _sk s fell to a minimum of 18.8 °C. Mean home ranges of mouse lemurs which remained normothermic were similar in the rainy and dry season. During the dry season, the mean home range of mouse lemurs showing daily torpor was significantly smaller than that of animals remaining normothermic. The DEE of M. murinus remaining normothermic in the rainy season (122 ± 65.4 kJ day⁻¹) was about the same of that of normothermic mouse lemurs in the dry season (115.5 ± 27.3 kJ day⁻¹). During the dry season, the mean DEE of M. murinus that utilised daily torpor was 103.4 ± 32.7 kJ day⁻¹ which is not significantly different from the mean DEE of animals remaining normothermic. We found that the DEE of mouse lemurs using daily torpor was significantly correlated with the mean temperature difference between T _sk and T _a (r ²=0.37) and with torpor bout length (r ² =0.46), while none of these factors explained significant amounts of variation in the DEE of the mouse lemurs remaining normothermic. The mean water flux rate of mouse lemurs using daily torpor (13.0 ± 4.1 ml day⁻¹) was significantly lower than that of mouse lemurs remaining normothermic (19.4 ± 3.8 ml day⁻¹), suggesting the lemurs conserve water by entering torpor. Thus, this first study on the energy budget of free-ranging M. murinus demonstrates that torpor may not only reflect its impact on the daily energy demands, but involve wider adaptive implications such as water requirements. Accepted: 29 August 2000     

Association between major histocompatibility complex class II DRB alleles and parasite load in the hairy-footed gerbil, Gerbillurus paeba, in the southern Kalahari

We investigated the importance of the MHC-constitution (major histocompatibility complex-constitution) on the endoparasite load in free-range hairy-footed gerbils (Gerbillurus paeba) in the southern Kalahari Desert. While the number of alleles of the duplicated DRB exon 2 gene had no significant effects on the individual status of being 'not infected' or 'infected' and on the number of helminth morphotype infections per individual, it significantly affected the faecal egg count values. One allele (Gepa-DRB*15) was only found in uninfected mice. Our results support the hypotheses that MHC polymorphism in G. paeba is maintained by pathogen-driven selection. The present study is the first investigation on associations between duplicated DRB gene loci and the parasite load in mammals.     

Signals of major histocompatibility complex overdominance in a wild salmonid population

The major histocompatibility complex (MHC) contains the most variable genes in vertebrates, but despite extensive research, the mechanisms maintaining this polymorphism are still unresolved. One hypothesis is that MHC polymorphism is a result of balancing selection operating by overdominance, but convincing evidence for overdominant selection in natural populations has been lacking. We present strong evidence consistent with MHC-specific overdominance in a free-living population of Arctic charr (Salvelinus alpinus) in northernmost Europe. In this population, where just two MHC alleles were observed, MHC heterozygous fish had a lower parasite load, were in better condition (as estimated by a fatness indicator) and had higher survival under stress than either of the homozygotes. Conversely, there was no consistent association between these fitness measures and assumedly neutral microsatellite variability, indicating an MHC-specific effect. Our results provide convincing empirical evidence consistent with the notion that overdominance can be an important evolutionary mechanism contributing to MHC polymorphism in wild animal populations. They also support a recent simulation study indicating that the number of alleles expected to be maintained at an MHC loci can be low, even under strong heterozygote advantage.     

Microsatellite analyses reveal fine-scale genetic structure in grey mouse lemurs (Microcebus murinus)

Information on genetic structure can be used to complement direct inferences on social systems and behaviour. We studied the genetic structure of the solitary grey mouse lemur (Microcebus murinus), a small, nocturnal primate endemic to western Madagascar, with the aim of getting further insight on its breeding structure. Tissue samples from 167 grey mouse lemurs in an area covering 12.3 km2 in Kirindy Forest were obtained from trapping. The capture data indicated a noncontinuous distribution of individuals in the study area. Using 10 microsatellite markers, significant genetic differentiation in the study area was demonstrated and dispersal was found to be significantly male biased. Furthermore, we observed an overall excess of homozygotes in the total population (F(IT) = 0.131), which we interpret as caused by fine-scale structure with breeding occurring in small units. Evidence for a clumped distribution of identical homozygotes was found, supporting the notion that dispersal distance for breeding was shorter than that for foraging, i.e. the breeding neighbourhood size is smaller than the foraging neighbourhood size. In conclusion, we found a more complex population structure than what has been previously reported in studies performed on smaller spatial scales. The noncontinuous distribution of individuals and the effects of social variables on the genetic structure have implications for the interpretation of social organization and the planning of conservation activities that may apply to other solitary and endangered mammals as well.     

Dynamics of Estrous Synchrony in Captive Gray Mouse Lemurs (Microcebus murinus)

Estrous synchrony in seasonal breeders can in principle be based on and shaped by environmental, internal, and/or social cues. We analyzed the dynamics of estrous synchrony for the first time in a seasonal, nocturnal primate species, the gray mouse lemur (Microcebus murinus). We compared successive estrous cycles and different levels of spatial proximity over two reproductive seasons in a captive population in order to identify possible social influences on estrous synchrony. The females exhibited a marked estrous synchrony at the beginning of each reproductive season, but we found no indication of a process of socially induced synchronization among them. Females housed in the same cage/room were not more strongly synchronized than females housed in different cages/rooms. Moreover, cycles desynchronized from the first to the second estrus of the season. Estrous cycle length did not depend on age, parity, or social housing conditions, but instead mainly on the individuality of the lemurs. This individuality, shown for the first time in a nocturnal primate species, is likely to be based on an endogenous rhythm with a genetic basis. We discuss possible social advantages, e.g., communal rearing, and disadvantages, e.g., mate choice and female-female competition, of estrous synchrony for nocturnal primates living in a dispersed individualized social network, and propose that a moderate flexibility within the individual cycle lengths probably enables the females to compromise between the different socioecological pressures.     

Differential expression of alloantigens of the major histocompatibility complex on unfertilized and fertilized mouse eggs

Mouse oocytes at the dictyate and metaphase II stages as well as fertilized eggs have been studied by indirect immunofluorescence for the expression of H-2 histocompatibility antigens on surface membranes. Serologically specific reactivity to H-2 antibody was observed as patchy fluorescence distributed over the surface of the oocyte membrane. In contrast, one-cell zygotes exhibited variable reactivity, and early two-cell stages were negative. Absorption studies confirmed the serologic specificity of the reactivity on oocytes, which could be shown to be due to H-2 antibody. The results suggest that fertilization results in altered expression of major histocompatibility complex surface antigens, and confirms earlier studies that cleavage stage mouse embryos are not reactive with H-2 antibody.     

Feeding ecology and seed dispersal of sympatric cheirogaleid lemurs (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major) in the littoral rainforest of south-east Madagascar

The lemurs of Madagascar are known for their extraordinary species diversity. The mechanisms that allow the coexistence of these species are still poorly known. Here feeding patterns were investigated for three small nocturnal lemur species of Cheirogaleidae ( Microcebus murinus , Cheirogaleus medius and Cheirogaleus major ) occurring sympatrically in a littoral rainforest in south-east Madagascar. During three rainy seasons, the plant species eaten by these three lemurs were described in relation to morphological and biochemical characteristics. All three species were mainly frugivorous and fed on 68 different plant species with small- and medium-sized fruits. A total of 91% of these forage plant species was visited by all three lemur species. Fruits larger than 25–30 mm were avoided. Seeds of a total of 51 food plant species were swallowed and passed the gut unharmed. Thus, even these smaller lemur species play an important role in seed dispersal. There were no differences in the morphological and biochemical characteristics of fruits eaten between the three species, but the feeding height was significantly different between the species. Thus, competition avoidance and niche separation are presumably not based on different feeding patterns of M. murinus , C. medius and C. major in the littoral rainforest, but on different habitat utilization.     

Divergent selection on locally adapted major histocompatibility complex immune genes experimentally proven in the field

Although crucial for the understanding of adaptive evolution, genetically resolved examples of local adaptation are rare. To maximize survival and reproduction in their local environment, hosts should resist their local parasites and pathogens. The major histocompatibility complex (MHC) with its key function in parasite resistance represents an ideal candidate to investigate parasite-mediated local adaptation. Using replicated field mesocosms, stocked with second-generation lab-bred three-spined stickleback hybrids of a lake and a river population, we show local adaptation of MHC genotypes to population-specific parasites, independently of the genetic background. Increased allele divergence of lake MHC genotypes allows lake fish to fight the broad range of lake parasites, whereas more specific river genotypes confer selective advantages against the less diverse river parasites. Hybrids with local MHC genotype gained more body weight and thus higher fitness than those with foreign MHC in either habitat, suggesting the evolutionary significance of locally adapted MHC genotypes.     

猪主要组织相容性复合体研究进展

主要组织相容性复合体（major histocompatibility complex,MHC）分子首先作为主要组织相容性抗原被发现,进而以此命名。随着其抗原结合分子及T细胞信使生物学功能本质的揭示,关于MHC结构与功能的研究就进入了一个崭新时代,并在这一领域中取得了许多可喜的成果。论述了近年来猪MHC（SLA）结构与功能方面的研究进展,包括SLA的分类及多态性、SLA分子结构特点、SLA分子功能及SLA分子相关领域的最新研究进展。     

The major histocompatibility complex and mating preferences in wild house mice (mus domesticus)

This study examined the relationship between the major histocompatibilitycomplex (MHC) genes and mate choice by wild house mice in acontrolled laboratory setting in an attempt to understand themechanisms maintaining natural MHC diversity. Three rearinggroups of wild test mice were produced: nonfostered controlmice, mice fostered into families of an inbred laboratory mousestrain, and mice fostered into families of a second mouse straindiffering genetically from the first only within the MHC region.At maturity, test mice were given a choice of two opposite-sexstimulus mice of the two MHC-congenic strains used for fostering.Test mice were scored for several measures of preference includingamount of time spent with either stimulus mouse, and ejaculationwith a stimulus mouse. Females in two of three rearing groupsspent more time with one MHC type regardless of rearing environment,suggesting that females did not prefer mates dissimilar fromfamily MHC type. Time preferences tended to be stronger in femalesthan in males. Male test mice ejaculated indiscriminantly. Femalewild mice mated to ejaculation more often in longer trials,but these matings were still too infrequent to assess preferences.Fostering had little or no effect on MHC-based mate preferencesof wild house mice, and no evidence suggested that MHC was usedto avoid inbreeding. Wild female mice may still choose matesbased on MHC haplotypes (but do not necessarily prefer MHC-dissimilarmates); other cues are probably also used. Based on these results,inbreeding avoidance does not seem a strong mechanism for maintainingnatural MHC diversity     

Sexual selection explains more functional variation in the mammalian major histocompatibility complex than parasitism

Understanding drivers of genetic diversity at the major histocompatibility complex (MHC) is vitally important for predicting how vertebrate immune defence might respond to future selection pressures and for preserving immunogenetic diversity in declining populations. Parasite-mediated selection is believed to be the major selective force generating MHC polymorphism, and while MHC-based mating preferences also exist for multiple species including humans, the general importance of mate choice is debated. To investigate the contributions of parasitism and sexual selection in explaining among-species variation in MHC diversity, we applied comparative methods and meta-analysis across 112 mammal species, including carnivores, bats, primates, rodents and ungulates. We tested whether MHC diversity increased with parasite richness and relative testes size (as an indicator of the potential for mate choice), while controlling for phylogenetic autocorrelation, neutral mutation rate and confounding ecological variables. We found that MHC nucleotide diversity increased with parasite richness for bats and ungulates but decreased with parasite richness for carnivores. By contrast, nucleotide diversity increased with relative testes size for all taxa. This study provides support for both parasite-mediated and sexual selection in shaping functional MHC polymorphism across mammals, and importantly, suggests that sexual selection could have a more general role than previously thought.     

Cloning of the bovine major histocompatibility complex class II genes

Summary. Class II genes of the bovine major histocompatibility complex (MHC) have been cloned from a genomic library. The library was constructed in the bacteriophage Λ vector EMBL3 and comprises approximately 10 times the equivalent of the haploid genome. Half the library was screened with the human DQA, DQB, DRA and DRB cDNA probes. Of the 100 positively hybridizing phage clones, 37 were eventually fully characterized and mapped by means of Southern blot analysis. The exons encoding the first, second and transmembrane domain of all different A and B genes were subcloned and mapped in more detail. These analyses showed that these 37 clones were derived from five different A and 10 different B genes. The hybridization studies indicate that we have cloned and mapped two DQA genes, one DRA gene, two other A genes, four DQB genes, three DRB genes and three other B genes. Since the library was made from a heterozygous animal, this would suggest that there are at least one DQA, one DRA one other undefined A, two DQB, two DRB and one or two other undefined B genes in the haploid genome of Holstein Friesian cattle.     

Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata)

Our understanding of the evolution of genes of the major histocompatibility complex (MHC) is rapidly increasing, but there are still enigmatic questions remaining, particularly regarding the maintenance of high levels of MHC polymorphisms in small, isolated populations. Here, we analyze the genetic variation at eight microsatellite loci and sequence variation at exon 2 of the MHC class IIB (DAB) genes in two wild populations of the Trinidadian guppy, Poecilia reticulata. We compare the genetic variation of a small (Ne, 100) and relatively isolated upland population to that of its much larger (Ne approximately 2400) downstream counterpart. As predicted, microsatellite diversity in the upland population is significantly lower and highly differentiated from the population further downstream. Surprisingly, however, these guppy populations are not differentiated by MHC genetic variation and show very similar levels of allelic richness. Computer simulations indicate that the observed level of genetic variation can be maintained with overdominant selection acting at three DAB loci. The selection coefficients differ dramatically between the upland (s > or = 0.2) and lowland (s < or = 0.01) populations. Parasitological analysis on wild-caught fish shows that parasite load is significantly higher on upland than on lowland fish, which suggests that large differences in selection intensity may indeed exist between populations. Based on the infection intensity, a substantial proportion of the upland fish would have suffered direct or indirect fitness consequences as a result of their high parasite loads. Selection by parasites plays a particularly important role in the evolution of guppies in the upland habitat, which has resulted in high levels of MHC diversity being maintained in this population despite considerable genetic drift.     

First evidence for relocation of stationary food resources during foraging in a strepsirhine primate (Microcebus murinus)

Field observations suggest that the diet of the Malagasy gray mouse lemur consists not only of non-stationary animal prey (invertebrates or small vertebrates), but also of stationary food resources such as gum or homopteran larvae secretions (HLS). We studied the foraging behavior of five mouse lemurs radiotelemetrically, each during six consecutive nights in the dry season, to explore to which extent they use these food resources and whether there is evidence for their relocation. We found that animals used all three different food categories. Mouse lemurs fed on gums and spent 68.5% (range 20.1-99.7%) of their feeding time eating this item. They were observed eating HLS in 8.4% (range 0-71.5%) of the feeding time and consuming small animals in 8.4% (range 0.3-26%) of their feeding time. The animals relocated stationary feeding sites significantly more frequently than non-stationary ones. They revisited the relocated stationary food sites about five times over the six nights. Furthermore, departure directions when leaving the sleeping site at dusk were not randomly distributed but showed a preferred orientation. Altogether, we provided first evidence for the relocation of stationary food resources in nature and thereby for the potential significance of spatial memory during foraging in a strepsirhine primate.