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Social system of the Alaotran gentle lemur (Hapalemur griseus alaotrensis): Genetic characterization of group composition and mating system

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Social system of the Alaotran gentle lemur (Hapalemur griseus alaotrensis): Genetic characterization of group composition and mating system

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Abstract

Group composition and mating system were investigated in wild Alaotran gentle lemurs (Hapalemur griseus alaotrensis) using genetic markers. These small-bodied herbivorous and cathemeral primates are endemic to the reed and papyrus beds around Lac Alaotra in Madagascar. They live in small groups in small, defended territories. Data were collected during the rainy seasons in 1996, 1997, and 1999, and include 99 individuals from 22 neighboring social groups and an additional 30 animals from other areas representing most of the geographic range. Animals were located by researchers canoeing in the marshes bordering the lake. After a group's size was determined by direct observation, all individuals were captured, marked, and released. During handling each individual was weighed and sexed, and hair samples for DNA extraction were collected. A 342 bp mtDNA control region sequence and 10 nuclear microsatellite loci provided multilocus genotypes that were used to assess pedigree relations and population structure. Alaotran gentle lemurs were found in groups of two to nine individuals (mean: 4.3), comprising one or two breeding females, their offspring, and one reproducing male. Solitary individuals of both sexes were encountered rarely. Breeding females were the permanent core of the social groups, whereas intergroup transfer of reproductive males was relatively frequent. Forty percent of all reproducing groups contained two breeding females, which were related to each other as closely as mother-daughter or full sisters. Parentage assessment revealed a variable mating system ranging from serial monogamy to polygyny within social groups. At least 8% of paternities involved extragroup males. Additional data on life history and reproduction are presented, and the social system of the Alaotran gentle lemur is discussed in the light of the new genetic findings.

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... They found that relatedness among females was greater than among males, both within social groups and within larger neighborhoods, a pattern consistent with behavioral observations of female philopatry and male-biased dispersal. Studies of several other lemurs (reviewed below) revealed a similar pattern (Nievergelt et al., 2002;) (Fig. 2E,F). Among platyrrhines, Nievergelt et al. (2000) also found greater average relatedness among adult females than among adult males for several groups of wild common marmosets (Fig. 2G). ...
... nt males were responsible for most conceptions, suggesting an influence of male dominance rank on reproductive success . Nonetheless, about one-third of offspring were sired by noncentral males. Like red-fronted lemurs, Alaotran gentle lemurs typically live in multimale-multifemale social groups with a small number of adult individuals of each sex. Nievergelt et al. (2002) genotyped and sequenced a portion of the mitochondrial control region for 99 Alaotran gentle lemurs from 22 social groups found at three different sites around Lac Alaotra in northeastern Madacascar. As in redfronted lemurs (), breeding females in each gentle lemur social group invariably shared the same mitochondrial DNA haplotype and ...
... Additionally, over 21% of offspring in the population were sired by former rather than current resident males (who nonetheless tolerated these older juveniles ), suggesting a frequent turnover among male residents. Finally, Nievergelt et al. (2002) found that about 8.5% of offspring in the population (five individuals) were sired by extragroup males; several of these appeared to be cases of inbreeding avoidance , as the resident breeding male was a close relative of the female involved. What emerges from all these studies, and from work on Propithecus (Lawler et al., 2001b; is the clear matrilineal underpinnings to lemur sociality . ...
Article
In the past several decades, the development of novel molecular techniques and the advent of noninvasive DNA sampling, coupled with the ease and speed with which molecular analyses can now be performed, have made it possible for primatologists to directly examine the fitness effects of individual behavior and to explore how variation in behavior and social systems influences primate population genetic structure. This review describes the theoretical connections between individual behavior and primate social systems on the one hand and population genetic structure on the other, discusses the kinds of molecular markers typically employed in genetic studies of primates, and summarizes what primatologists have learned from molecular studies over the past few decades about dispersal patterns, mating systems, reproductive strategies, and the influence of kinship on social behavior. Several important conclusions can be drawn from this overview. First, genetic data confirm that, in many species, male dominance rank and fitness are positively related, at least over the short term, though this relationship need not simply be a reflection of male-male contest competition over mates. More importantly, genetic research reveals the significance of female choice in determining male reproductive success, and documents the efficacy of alternative mating tactics among males. Second, genetic data suggest that the presumed importance of kinship in structuring primate social relationships needs to be evaluated further, at least for some taxa such as chimpanzees in which demographic factors may be more important than relatedness. I conclude this paper by offering several suggestions of additional ways in which molecular techniques might be employed in behavioral and ecological studies of primates (e.g., for conducting "molecular censuses" of unhabituated populations, for studying disease and host-parasite interactions, or for tracking seed fate in studies of seed dispersal) and by providing a brief introduction to the burgeoning field of nonhuman primate behavioral genetics.
... Female gentle lemurs are able to reproduce at 2 years, whereas males are sexually mature at 3 years [wild: (44), captivity: (45)]. The average lifespan in captivity is 17.1 years for females and 12.8 years for males (46). ...
... Gentle lemurs are seasonally polyoestrous and mating occurs over 1 day per sexual cycle (47). They usually deliver offspring once per year (47) after an average gestation period of 145 days (45), with a high rate of twinning (44). In Madagascar the mating season occurs during the dry season [i.e., between April and September (44)], while there is no defined breeding season in captivity (45). ...
... They usually deliver offspring once per year (47) after an average gestation period of 145 days (45), with a high rate of twinning (44). In Madagascar the mating season occurs during the dry season [i.e., between April and September (44)], while there is no defined breeding season in captivity (45). We estimated the breeding and non-breeding periods on the basis of the last parturition of the female and the length of the weaning period (48,49). ...
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The Lake Alaotra gentle lemur (Hapalemur alaotrensis) is one of the 25 most endangered primates in the world and shows low success rate in captive breeding programmes. It is therefore vital to further understand its reproductive biology. We studied a captive troop consisting of five individuals hosted at Jersey Zoo during breeding and non-breeding periods over 1 year. We collected behavioural data (n = 318 h) using all occurrence of some behaviours and ad libitum sampling methods, as well as faecal (n = 54) and anogenital scent (n = 35) samples of the breeding female. We measured sex hormone levels using enzyme immunoassay technique and investigated the volatile component of odour signals using solid-phase microextraction and gas chromatography-mass spectrometry. We observed sexual and aggressive behaviours occasionally during the breeding period. Our regression analysis showed that only period significantly predicted rates of female anogenital scent-marking, whereby the female performed anogenital scent-marking more frequently during the breeding rather than the non-breeding period. In contrast, female hormone levels did not significantly explain variation in rates of neither male nor female olfactory, sexual and affiliative behaviours, suggesting that individuals' behaviour alone is not an effective indicator of the ovulation window. The volatile chemical profile of anogenital odour secretions changed over the study, with four compounds distinguishing the fertile window during the breeding period. In conclusion, our findings suggest that anogenital scent-marking may signal the reproductive status of captive female gentle lemurs.
... The crepuscular lemur shows two distinct activity peaks, one in the early morning, the other in the late afternoon (Mutschler et al. 1998). The social groups of Hapalemur alaotrensis typically consist of two to nine individuals (Nievergelt et al. 2002), while groups of more than 13 have also been reported (Waeber and Hemelrijk 2003). Home ranges of H. alaotrensis vary from two to five hectares depending on group size (Nievergelt et al. 1998). ...
... The gestation period is similar for all bamboo lemurs, being between 137 and 149 days. For H. alaotrensis, the birth season starts in September and ends in February (Mutschler 1999), with births not being synchronized within groups (Nievergelt et al. 2002). ...
... The crepuscular lemur shows two distinct activity peaks, one in the early morning, the other in the late afternoon (Mutschler et al. 1998). The social groups of Hapalemur alaotrensis typically consist of two to nine individuals (Nievergelt et al. 2002), while groups of more than 13 have also been reported (Waeber and Hemelrijk 2003). Home ranges of H. alaotrensis vary from two to five hectares depending on group size (Nievergelt et al. 1998). ...
... The gestation period is similar for all bamboo lemurs, being between 137 and 149 days. For H. alaotrensis, the birth season starts in September and ends in February (Mutschler 1999), with births not being synchronized within groups (Nievergelt et al. 2002). ...
... Studies of strepsirrhine social dynamics have also focused on the most gregarious species (Eulemur spp., ring-tailed lemur, Lemur catta and Verreaux's sifaka, Propithecus verreauxi: van Schaik & Kappeler, 1993;Norscia, Antonacci, & Palagi, 2009;Port, Clough, & Kappeler, 2009). Bamboo lemurs, Hapalemur spp., live in small and/or family-unit-sized groups (Eppley, Ganzhorn, & Donati, 2016d;Grassi, 2006;Nievergelt, Mutschler, Feistner, & Woodruff, 2002;Tan, 1999); within the Lemuridae family, they present an atypical study system. Whereas social rank in a large group confers a higher adaptive value to a dominant individual relative to others (Silk, 2007), there is scant evidence that members of small, familyunit social groups either have similar social standing or maintain strict dominance. ...
... 2000; Nievergelt et al., 2002;Tan, 1999Tan, , 2006. Similarly, in the H. meridionalis population in Mandena both monogamous and polygamous social groups coexist. ...
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Full-text available
It is well established that social rank in a large group confers a higher adaptive value to a dominant individual relative to others, although there is scant evidence that members of small social groups either have similar social standing or maintain strict dominance. We aimed to determine whether members of small social groups, using the southern bamboo lemur, Hapalemur meridionalis, as a model, gain rank-related benefits. We first established a dominance hierarchy through a network-based analysis of win eloss interactions, which showed that adult females maintained social dominance within their groups, similar to many strepsirrhine species. To address whether dominant individuals gained rank-related benefits, we then explored how social dynamics may permit access to resting huddles, which provide a physiological benefit. Social thermoregulation, i.e. huddling, is a behavioural energy conservation mechanism, and among many mammals is a direct response to decreasing ambient temperatures. As such, huddling behaviour may have evolved among social animals because of its potential direct and indirect benefits. To examine the effect of dominance rank within small social groups on huddling inclusion , we used generalized linear mixed-effects models to predict the likelihood of huddling occurring during resting bouts from climatic (e.g. temperature, precipitation), social (e.g. affiliation, dominance rank, grooming) and reproductive (e.g. access, infant protection) variables. We found that lower temperatures , especially during shorter resting bouts, increased the likelihood of huddling. Grooming between partners with a high discrepancy in rank increased huddling. Additionally, huddling increased during the reproductive season, potentially offering greater opportunity for males to gain favour with sexually receptive females, and when new-borns were present, providing essential thermal maintenance and potential antipredator protection to infants. Together, our results suggest that even in small social groups, females gain rank-related benefits by controlling access to huddles, i.e. the intrinsic benefits of social thermoregulation.
... The crepuscular lemur shows two distinct activity peaks, one in the early morning, the other in the late afternoon (Mutschler et al. 1998). The social groups of Hapalemur alaotrensis typically consist of two to nine individuals (Nievergelt et al. 2002), while groups of more than 13 have also been reported (Waeber and Hemelrijk 2003). Home ranges of H. alaotrensis vary from two to five hectares depending on group size (Nievergelt et al. 1998). ...
... The gestation period is similar for all bamboo lemurs, being between 137 and 149 days. For H. alaotrensis, the birth season starts in September and ends in February (Mutschler 1999), with births not being synchronized within groups (Nievergelt et al. 2002). Lake Alaotra, in the central highlands in the Alaotra-Mangoro region, is the biggest shallow fresh-water lake in Madagascar. ...
... The crepuscular lemur shows two distinct activity peaks, one in the early morning, the other in the late afternoon (Mutschler et al. 1998). The social groups of Hapalemur alaotrensis typically consist of two to nine individuals (Nievergelt et al. 2002), while groups of more than 13 have also been reported (Waeber and Hemelrijk 2003). Home ranges of H. alaotrensis vary from two to five hectares depending on group size (Nievergelt et al. 1998). ...
... The gestation period is similar for all bamboo lemurs, being between 137 and 149 days. For H. alaotrensis, the birth season starts in September and ends in February (Mutschler 1999), with births not being synchronized within groups (Nievergelt et al. 2002). ...
... The crepuscular lemur shows two distinct activity peaks, one in the early morning, the other in the late afternoon (Mutschler et al. 1998). The social groups of Hapalemur alaotrensis typically consist of two to nine individuals (Nievergelt et al. 2002), while groups of more than 13 have also been reported (Waeber and Hemelrijk 2003). Home ranges of H. alaotrensis vary from two to five hectares depending on group size (Nievergelt et al. 1998). ...
... The gestation period is similar for all bamboo lemurs, being between 137 and 149 days. For H. alaotrensis, the birth season starts in September and ends in February (Mutschler 1999), with births not being synchronized within groups (Nievergelt et al. 2002). ...
... The crepuscular lemur shows two distinct activity peaks, one in the early morning, the other in the late afternoon (Mutschler et al. 1998). The social groups of Hapalemur alaotrensis typically consist of two to nine individuals (Nievergelt et al. 2002), while groups of more than 13 have also been reported (Waeber and Hemelrijk 2003). Home ranges of H. alaotrensis vary from two to five hectares depending on group size (Nievergelt et al. 1998). ...
... The gestation period is similar for all bamboo lemurs, being between 137 and 149 days. For H. alaotrensis, the birth season starts in September and ends in February (Mutschler 1999), with births not being synchronized within groups (Nievergelt et al. 2002). ...
... The crepuscular lemur shows two distinct activity peaks, one in the early morning, the other in the late afternoon (Mutschler et al. 1998). The social groups of Hapalemur alaotrensis typically consist of two to nine individuals (Nievergelt et al. 2002), while groups of more than 13 have also been reported (Waeber and Hemelrijk 2003). Home ranges of H. alaotrensis vary from two to five hectares depending on group size (Nievergelt et al. 1998). ...
... The gestation period is similar for all bamboo lemurs, being between 137 and 149 days. For H. alaotrensis, the birth season starts in September and ends in February (Mutschler 1999), with births not being synchronized within groups (Nievergelt et al. 2002). ...
... Socionomic sex ratios have been used to sort vertebrate mating systems into categories ( Krebs and Davies 1993): solitary, polygynous, polyandrous, polygynandrous, and monogamous. A primary goal of vertebrate behavioral ecology concerns understanding the selective forces that drive variation in these systems (Crook and Gartland 1966;Eisenberg et al. 1972;Davies and Lundberg 1987;Nunn 1999;Heymann 2000), and the category into which a species falls provides an important predictor of the intensity of mating competition ( Kvarnemo and Ahnesjo 1996;Mitani et al. 1996b;Kappeler 2000), morphology (Harvey and Harcourt 1984;Plavcan et al. 1995) and variance in male reproductive success (Pope 1996(Pope , 2000Nievergelt et al. 2002;Wimmer and Kappeler 2002). ...
Article
Full-text available
Many species fall into specific mating-system categories, and that category is usually associated with a suite of behavioral and morphological characteristics. Several lemur species, including Propithecus diadema edwardsi, have been labeled "idiosyncratic" because variation in socionomic sex ratios among groups is consistent with wide variation in social structure. We used several hypotheses founded in behavioral ecology to assess variability in P. d. edwardsi. First we examined 46 group-mating seasons to quantify variability. We then tested predictions that the number of males per group would increase as the number of adult females increased, and the number of males would increase as female mating synchrony increased. Examining variation in offspring survival relative to the number of adult males in a group may tell us which composition is likely to persist into the future, so we also hypothesized that as the number of males in a group increased, fertility and offspring survival would increase. We found an equal distribution of polygynous, polygynandrous, pairs, and polyandrous groups. Furthermore, female distribution and mating synchrony did not predict the number of males, and offspring survival was not correlated with the number of males. Since infants survived equally well in groups of all compositions, sifakas experienced no pressure to maintain a particular number of adult males per adult female. The small number of adults per group (mean=3.2) may result from balancing feeding competition against predator detection. Augmenting the mate pool available from the group with mates from neighboring groups may promote the notable variability seen in the adult group compositions of sifakas.
... First, 16 trees of the same topology were constructed in which branch lengths were randomly changed by some value between 220 and þ20 MYA, with the restriction that no negative divergence times were allowed and the general topology had to remain the same. We also fitted a model to data including three additional species that were not included in the analyses even when they might be considered pair-living: Microtus ochrogaster [73], Hylobates lar [74] and Canis latrans [75]. (The electronic supplementary material, table S1d provides the reasons why these were not considered pair-living for the analyses). ...
Article
Full-text available
Understanding the evolution of mating systems, a central topic in evolutionary biology for more than 50 years, requires examining the genetic consequences of mating and the relationships between social systems and mating systems. Among pair-living mammals, where genetic monogamy is extremely rare, the extent of extra-group paternity rates has been associated with male participation in infant care, strength of the pair bond and length of the breeding season. This study evaluated the relationship between two of those factors and the genetic mating system of socially monogamous mammals, testing predictions that male care and strength of pair bond would be negatively correlated with rates of extra-pair paternity (EPP). Autosomal microsatellite analyses provide evidence for genetic monogamy in a pair-living primate with bi-parental care, the Azara's owl monkey (Aotus azarae). A phylogenetically corrected generalized least square analysis was used to relate male care and strength of the pair bond to their genetic mating system (i.e. proportions of EPP) in 15 socially monogamous mammalian species. The intensity of male care was correlated with EPP rates in mammals, while strength of pair bond failed to reach statistical significance. Our analyses show that, once social monogamy has evolved, paternal care, and potentially also close bonds, may facilitate the evolution of genetic monogamy.
... Pair-living appears to be much more frequent in Malagasy prosimians than in other primate groups (van Schaik and Kappeler 1993; Wittenberger and Tilson 1980). In fact, it occurs in 4 out of the 8 genera of nocturnal lemurs (Phaner: Charles- Dominique and Petter 1980; Cheirogaleus: Fietz 1999; Lepilemur: Rasoloharijaona et al. 2003; Avahi: Thalmann 2003) and in ≥=3 diurnal lemur genera (Eulemur: Curtis and Zaramody 1999; Hapalemur: Nievergelt et al. 2002; Indri: Powzyk 1997). Indeed, the sparse distribution of small resources typical of Madagascar (Wright 1999) may promote pair-living because it leads to widely spaced females (following the energy conservation hypothesis; Jolly 1998). ...
Article
Full-text available
Researchers have proposed several hypotheses to explain pair-living in primates. In particular, when males are not involved in direct parental care, pair-living may be related to female dispersal, infanticide prevention, or male mate/resource defense. We aimed to evaluate, through a better understanding of the ranging patterns of avahis, which hypotheses may best account for pair-living in these nocturnal lemurs. We collected focal observations over 26 nights, June–September 2004, in a littoral forest (Sainte Luce, southeastern Madagascar) on 4 adult radiocollared avahis [Avahi laniger (Tattersall, I. (1982). The Primates of Madagascar. Columbia University Press, New York.) or Avahi meridionalis (Zaramody in Primate Reports 74:9–22, 2006)]. We followed 2 males and 2 females from 2 groups: B, a male-female couple, and A, comprising the parental pair and 1-yr-old female offspring. The adult females birthed in August. We recorded resting and feeding tree points (via global positioning system) for home range calculation through minimum convex polygon and kernel methods. We provide the first quantitative information on the ranging behavior of 2 male and 2 female avahis. Home range/daily path length values (means) are higher than the ones previously reported for the same and other folivorous pair-living lemur species. On average, the 2 females spent more time feeding and traveled shorter distances than the 2 males did. Male–female cohesion (mean values), possibly enhanced by offspring presence, was higher in A and after births than in B and before births, respectively. Although male avahis may be forced into pair-living owing to energy constraints related to size, locomotion, and diet, females might accept pair-living in exchange for indirect territory defense and mate guarding.
... The development of DNA polymorphic markers has enabled us to carry out parentage analysis, which has made it possible to understand genetic mating systems of a population [Constable et al., 2001]. For example, parentage assessment with microsatellite DNA markers revealed a variable mating system ranging from monogamy to polygyny for the Alaotran gentle lemur (Hapalemur griseus alaotrensis) [Nievergelt et al., 2002]. Gray mouse lemur (Microcebus murinus) populations are characterized by overlapping male and female home ranges, an absence of sexual dimorphism, a short breeding season and high female oestrus synchrony. ...
... Chesser (1991aChesser ( , 1991b noted that such subdivision could occur in social, cooperatively breeding species, where breeding groups act in the same way as subpopulations, but at a finer spatial scale. Several mammalian species exhibit social breeding groups, coupled with male polygyny and female philopatry (Dobson 1998;Emlen 1997;Hayes 2000;Nievergelt et al. 2002). Dispersal among breeding groups should affect the gene dynamics of social mammals, perhaps in a similar manner to dispersal among subpopulations (Sugg et al. 1996). ...
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Using a long-term study of black-tailed prairie dogs (Cynomys ludovicianus), we asked whether subdivision of a subpopulation (colony) into social breeding groups (coteries) influenced gene dynamics. We measured gene dynamics with common statistical tools, F-statistics and effective population size (N(e)), but at a finer scale to account for coteries. We used 2 methods of estimating the gene dynamics of subgroups, and determined if these methods produced similar results that were congruent with an empirical measure of the observed effective population size (N(eO)). Modified F-statistics were estimated from pre- and postdispersal data from pedigrees and allozymes. Both indicated significant genetic substructuring of the colony subpopulation into coterie breeding groups. The rate of inbreeding of individuals relative to the coterie lineage indicated lower than expected inbreeding at the coterie level. Inbreeding of individuals relative to the colony was consistent with random mating. Asymptotic effective size estimates varied substantially. Chesser's method produced estimates of 77 (range 69-90, pedigree) and 86 (range 70-111, allozyme) individuals consistent with the N(eO) of 76 and previous empirical estimates of the instantaneous asymptotic effective size from pedigrees (92.9). Nunney's method produced much lower estimates of approximately one-half the N(eO). Social subdivisions of the colony into coteries clearly influenced gene dynamics. Only the Chesser method accounted for genetic structure introduced by genealogy, both from polygynous mating and matrilines of philopatric females. This may prove important when estimating the rate of loss of genetic variation in highly social mammals.
... Amplification from alien DNA, however, can in a large extent be avoided by using specific primers, and will not be considered any further here (but see Bradley and Vigilant 2002). Finally, various molecules that can inhibit the polymerase chain reaction (PCR) may be present in faeces, a problem that is less likely with hair samples when using only hair roots (but see Nievergelt et al. 2002;Roon et al. 2003). Inhibition levels can vary with diet (Murphy et al. 2003), and most difficulties are met when working with faeces that contain plant remnants (Monteiro et al. 1997, D. Vallet, E. Petit and N. Ménard, unpublished manuscript). ...
Article
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Noninvasive population genetics has found many applications in ecology and conservation biology. However, the technical difficulties inherent to the analysis of low quantities of DNA generally tend to limit the efficiency of this approach. The nature of samples and loci used in noninvasive population genetics are important factors that may help increasing the potential success of case studies. Here we reviewed the effects of the source of DNA (hair vs. faeces), the diet of focal species, the length of mitochondrial DNA fragments, and the length and repeat motif of nuclear microsatellite loci on genotyping success (amplification success and rate of allelic dropout). Locus-specific effects appeared to have the greatest impact, amplification success decreasing with both mitochondrial and microsatellite fragments’ length, while error rates increase with amplicons’ length. Dinucleotides showed best amplification success and lower error rates compared to longer repeat units. Genotyping success did not differ between hair- versus faeces-extracted DNA, and success in faeces-based analyses was not consistently influenced by the diet of focal species. While the great remaining variability among studies implies that other unidentified parameters are acting, results show that the careful choice of genetic markers may allow optimizing the success of noninvasive approaches.
... with an average of around 4 ind. (Nievergelt et al. 2002). H. alaotrensis exhibits cathemeral activity with peaks at the beginning and end of the daylight cycle . ...
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Although monitoring is an essential tool for biodiversity conservation, monitoring programmes are often poorly designed and thus unlikely to produce results that are meaningful for management. Monitoring is especially challenging when dealing with rare and elusive species in areas where conservation resources are particularly limited. In such cases, monitoring techniques aimed at estimating occupancy represent an attractive alternative to traditional methods concerned with estimating population size, as the collection of detection/non-detection data is in general less costly and easier to implement. In this study, we evaluated the use of occupancy as a state variable for the monitoring of the Alaotran gentle lemur Hapalemur alaotrensis, a Critically Endangered primate exclusively inhabiting the dense marshes around Lake Alaotra in Madagascar. We used a likelihood-based modelling approach that explicitly accounts for detectability. This showed that the probability of detection of H. alaotrensis was extremely low and depended on site characteristics that can vary in space and time, confirming the need to account for imperfect detection when monitoring this species. We used our models to explore factors affecting the probability of occupancy and detection to identify management implications, and also developed recommendations for the ongoing monitoring of this species. The method applied in this study provides an efficient tool for the monitoring of an elusive species and has the potential to provide a flexible sampling framework for local community-based monitoring initiatives.
... Invasive genetic sample collection is particularly problematic in the primates, whose capture is considered unethical. Instead, DNA obtained from wadges, faeces, plucked hairs and shed hairs collected from night nests has provided a wealth of data on phylogeography, gene flow, social structure and kinship in wild chimpanzees (Constable et al. 2001;Vigilant et al. 2001), gorillas (Jensen-Seaman and Kidd 2001), bonobos (Gerloff et al. 1999), Hanuman langurs (Launhardt et al. 2001), orangutans (Utami et al. 2002) and lemurs (Nievergelt et al. 2002). Microsatellite genotyping was performed on faecal samples from an Indonesian orangutan (Pongo pygameus abelii) population that has been the subject of a long-term behavioural study with an emphasis on male reproductive strategies (Utami et al. 2002). ...
Article
Obtaining useful information about elusive or endangered species can be logistically difficult, particularly if relying entirely on field signs such as hair, feathers or faeces. However, recent developments in molecular technology add substantially to the utility of such 'non-invasive' samples, which provide a source of DNA that can be used to identify not only species but also individuals and their gender. This provides great potential to improve the accuracy of abundance estimates and determine behavioural parameters, such as home-range size, individual habitat and dietary preferences, and even some forms of social interaction. Non-invasive samples can also be a useful alternative to blood or tissue samples ( the collection of which traditionally has required trapping of animals) as genetic material for applications such as relatedness, population genetic and phylogenetic analyses. Despite the huge potential of non-invasive genetic sampling, the current technology does have limitations. The low quantity and quality of DNA often obtained from such sources results in an increased risk of genotyping errors, which may lead to incorrect inferences, particularly false identification of individuals. Appropriate precautions and pilot studies are required to minimise these risks, and in some cases it may be wise to employ traditional methods when they are adequate.
... However, multi-year studies on identified individuals of purportedly monogamous species have revealed considerable flexibility in their grouping patterns, as well as in their social structure and mating system [Fuentes, 2000;Garber et al., 2015;Reichard et al., 2012;Tecot et al., 2015]. For example, additional breeding females [Nievergelt et al., 2002] or additional mating males [Lappan & Morino, 2014], or both [Garber et al., 2015], have been reported in groups of some socially monogamous species. Such deviations from the nuclear family may arise when mature offspring stay to breed in their natal group [Brockelman et al., 1998] or through immigration of adult individuals [Lappan, 2007]. ...
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We investigated demographic patterns and life history traits from several groups of red titi monkeys (Callicebus discolor) and equatorial sakis (Pithecia aequatorialis) monitored throughout the first 12 years (November 2003 through May 2015) of an ongoing research project in the Yasuní National Park and Biosphere Reserve, Ecuador. The saki groups ranged in size between two and six individuals, comprising either one adult male and one adult female or multiple adult-sized males or females, plus immatures. Deviations from a pair-living structure resulted when two different daughters of the resident female grew up and successfully reproduced in their natal group and when an adult-sized male temporarily immigrated into the group when it already contained an adult male. The titi groups also ranged in size between two and six individuals, but almost exclusively lived in groups with one adult individual of each sex. No titi offspring were observed to breed in their natal groups, and both male and female offspring dispersed when they were between 2.1 and 5.0 years old. In both titi and saki groups, vacant breeding positions resulting from the disappearance of an adult group member were promptly occupied by immigrants of the same sex as the disappeared group member. We recorded nine saki and 28 titi births. Eighty-three percent of the titi births occurred between September and January, suggesting reproductive seasonality. The mean interbirth interval after an infant survived its first 6 months was 21.3 ± SE 1.9 months (N = 3) for sakis and 14.5 ± SE 1.5 months (N = 14) for titis. Saki infant survival was 70%, and juvenile survival 57%. Titi infant survival was 88%, and juvenile survival was 53%. This 12-year study provides important insights into the functioning and maintenance of pair-living and social monogamy in two little-known platyrrhine species. Am. J. Primatol. 9999:XX-XX, 2015. © 2015 Wiley Periodicals, Inc.
... The development of DNA polymorphic markers has enabled us to carry out parentage analysis, which has made it possible to understand genetic mating systems of a population [Constable et al., 2001]. For example, parentage assessment with microsatellite DNA markers revealed a variable mating system ranging from monogamy to polygyny for the Alaotran gentle lemur (Hapalemur griseus alaotrensis) [Nievergelt et al., 2002]. Gray mouse lemur (Microcebus murinus) populations are characterized by overlapping male and female home ranges, an absence of sexual dimorphism, a short breeding season and high female oestrus synchrony. ...
Article
This article reports the first genetic study of the mating system of the Sichuan snub-nosed monkey (Rhinopithecus roxellana), an endemic and endangered species in China. The investigation was carried out in a population (WRT) in the Qinling Mountains using data from both field observation and paternity analysis through microsatellite DNA profiling. During a mating season, a male on an average copulated with 5.7 females. Approximately 18% of the females were observed to copulate with more than one male over the study period. The majority of copulations (94.5%) were initiated by females. Twenty-eight of 430 observed matings were extra-unit copulations. Eight polymorphic microsatellite loci were used for paternity analysis. The number of alleles at each locus ranged from 3 to 7 (mean=4.3). Observed heterozygosity ranged between 0.32 and 0.79. None of the loci showed significant deviation from Hardy-Weinberg equilibrium. Results from paternity exclusion showed that 12 of 21 (57.1%) immature individuals were sired by extra-unit males. Although the basic social unit of snub-nosed monkeys is consistent with a polygynous mating system, both field observation and genetic data suggests that their mating system is polygamous. Infanticide and inbreeding avoidance are the most likely explanations for the promiscuity of female snub-nosed monkeys.
... As expected, given observations of predominantly male exogamy and female philopatry in these taxa, they found that females within social groups were more closely related to one another, on average, than were males. Similar results have been reported for several group-living strepsirrhines (e.g., Verreaux's sifaka: Lawler et al. 1995; Alaotran gentle lemurs: Nievergelt et al. 2002 ; red fronted lemurs: Wimmer and Kappeler 2002). For chimpanzees and bonobos – where observational studies suggest that female exogamy and male philopatry are the rule – males do not generally appear to be more closely related to one another than females, contrary to expectation (Gerloff et al. 1999; Vigilant et al. 2001; Lukas et al. 2005). ...
... Keywords cohabitation; mating system; microsatellites; multiple paternity; relatedness Several factors (e.g., demography, density, resource competition and availability, life-history characteristics, spatial distribution, and dispersal of individuals) influence mating systems of a given species. Consequently, mating strategies may differ across the geographic range of a species (Clutton-Brock 1989;Jones et al. 2001;Nievergelt et al. 2002), especially if ...
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Two hundred twenty-two individuals of the southern plains woodrat (Neotoma micropus) were captured from 198 excavated middens at 10 discrete collecting sites from a single population in south-central Texas. Field data, mitochondrial D-loop haplotypes, and polymorphic microsatellite loci (5-7) were used to determine genetic patterns in parentage, relatedness, and mating strategy. Microsatellite loci were highly polymorphic (average observed heterozygosity = 0.859) and were used to construct genotypes that were unique for each individual (probability of identical genotypes: 1 in 2,104,567). Results indicated a high frequency of multiple paternity (6 of 9 litters), evidence of repeat mating between the same 2 individuals, and no indication of male dominance at any collection site. Examination of these data suggested a promiscuous mating system. Within a site, average relatedness between adult females was similar to that between adult males. A higher level of cohabitation from that previously documented was recorded and finer-scale analyses revealed high levels of relatedness between most cohabiting individuals. Taken with results from other studies of mating behaviors of N. micropus, our results suggest that mating and social behavior of this species are likely influenced by population density.
... Based on our limited knowledge of their population dynamics, the bamboo lemur species at the different sites do not seem to differ in their reproductive output or population dynamics (Eppley et al. 2015b(Eppley et al. , 2016bNievergelt et al. 2002;Tan 2006). Therefore, the surplus of protein ingested from bamboo in Ranomafana is not reflected in higher reproductive rates. ...
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Plants producing toxic plant secondary metabolites (PSMs) deter folivores from feeding on them. Animals that can cope with noxious PSMs have a niche with a competitive advantage over other species. However, the ability to cope with toxic PSMs incurs the costs of detoxification. To assess possible compensations for the ingestion of toxic PSMs, we compare the chemical quality of plants consumed by bamboo lemurs (genera Hapalemur and Prolemur; strepsirrhine primates of Madagascar) in areas with and without bamboo. Some bamboo lemurs consume bamboo containing concentrations of cyanogenic substances 10–50 times above the average lethal dosage for mammals, and we postulate that animals consuming cyanogenic substances need supplementary protein or readily available energy for detoxification. We compared the chemical composition of food consumed by three species of bamboo lemurs that feed mainly (>80% of their time) on bamboo in the evergreen rainforest of Ranomafana (Madagascar) with published data of the diets of bamboo lemurs at two sites without highly cyanogenic plants (reed beds of Lac Alaotra and the evergreen littoral forest of Mandena) and with food of sympatric folivorous lemur species that do not feed on bamboo. Lemurs feeding on bamboo consumed up to twice as much protein as bamboo lemurs in areas without bamboo and sympatric lemur species that feed on leaves of trees. Concentrations of nonstructural carbohydrates (a source of energy) showed the opposite trend. This result supports the hypothesis that feeding on cyanogenic plants is linked to high protein intake, either as a source of protein or for sulfur-containing amino acids that can be used for detoxification. Owing to the high protein concentrations in bamboo, however, we cannot distinguish between the hypothesis that lemurs that eat bamboo target additional food items with higher protein from the hypothesis that lemurs feeding on bamboo unavoidably obtain higher concentrations of protein than animals feeding on leaves of trees, without an added nutritional benefit.
... Understanding marshland fires. Since the early 1990s, Durrell has been engaging mainly in the marshes of Andreba Gare to research the behavior and ecology of Hapalemur alaotrensis ( Mutschler et al. 1998, Nievergelt et al. 1998, Mutschler et al. 2000, Nievergelt et al. 2002a, Nievergelt et al. 2002b, Waeber & Hemelrijk 2003). Since 2003, MWC and Durrell have been working collaboratively. ...
Thesis
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The dissertation takes an interdisciplinary mixed-methods approach to investigate the potential of EE in contributing to conservation in Madagascar. The applied case study therefore focuses on primary schools and communities of Lake Alaotra, and entails a comprehensive survey regarding knowledge, attitudes and perceptions of natural resource users towards nature and conservation in the region, furthermore the drivers and barriers to implement environmental education in public primary schools, as well as significant life experiences of active Malagasy conservationists. The author finally discusses possible measures how environmental education in Madagascar can contribute to biodiversity conservation and sustainable development in the long run.
... Non-monogamous group-living lemur species display a variety of mating systems ( Table 1), some of which vary within species or even within a group's history (Pochron and Wright, 2003). Aloatran gentle lemurs (Hapalemur aloatrensis), for example, appear to occupy a flexible mating system between monogamy and polygyny: intergroup transfer of males commonly occurs, leading to serial monogamy in some groups, while 40% of surveyed groups by Nievergelt et al., (2002) had two breeding females and thus a polygynous mating system. Multiple studies of the red-fronted brown lemur (Eulemur rufifrons) also reveal the complex strategies present within a polygynandrous system. ...
Chapter
Lemurs, a unique primate lineage exclusive to Madagascar, display mating systems encountered across primates and mammals alike, ranging from polygynandrous mating to polygyny and monogamy. However, lemurs demonstrate many unique characteristics which differentiate them from non-Malagasy primates. These include female dominance, a lack of sexual dimorphism, a preponderance of monogamous species, strict breeding seasons, high infant mortality, and sperm competition alongside male-male competition. These and other idiosyncratic traits have been termed the “lemur syndrome” and are believed to have arisen in response to Madagascar’s harsh and unpredictable environment. These traits, as well as examples of lemur species mating systems, are discussed herein.
... Microsatellite loci modelled in the simulations were based on empirically observed allele frequency distributions. Ten different loci were modelled using allele frequency distributions derived from a range of species [one locus each from rock wallabies (Eldridge et al. 2001), harbour seals (Coltman et al. 1998), pipefish (McCoy et al. 2001), gentle lemurs (Nievergelt et al. 2002), sunfish (Dewoody et al. 1998) and tree swallows (Conrad et al. 2001)] and two loci from sperm whales (S. Mesnick pers. ...
Article
Polygynous mating results in nonrandom sampling of the adult male gamete pool in each generation, thereby increasing the rate of genetic drift. In principle, genetic paternity analysis can be used to infer the effective number of breeding males (Nebm). However, this requires genetic data from an exhaustive sample of candidate males. Here we describe a new approach to estimate Nebm using a rejection algorithm in association with three statistics: Euclidean distance between the frequency distributions of maternally and paternally inherited alleles, average number of paternally inherited alleles and average gene diversity of paternally inherited alleles. We quantify the relationship between these statistics and Nebm using an individual-based simulation model in which the male mating system varied continuously between random mating and extreme polygyny. We evaluate this method using genetic data from a natural population of highly polygynous fruit bats (Cynopterous sphinx). Using data in the form of mother-offspring genotypes, we demonstrate that estimates of Nebm are very similar to independent estimates based on a direct paternity analysis that included data on candidate males. Our method also permits an evaluation of uncertainty in estimates of Nebm and thus facilitates inferences about the mating system from genetic data. Finally, we investigate the sensitivity of our method to sample size, model assumptions, adult population size and the mating system. These analyses demonstrate that the rejection algorithm provides accurate estimates of Nebm across a broad range of demographic scenarios, except when the true Nebm is high.
... Among mammals, primates include the highest frequency of monogamous species (29%; Lukas & Clutton-Brock, 2013), usually organized in pair-living groups with immature or even mature offspring (Kappeler & van Schaik, 2002;Reichard & Boesch, 2003). Few studies have investigated the genetic paternity in putatively monogamous primates (not necessarily pair-living as we defined it) and some of them show that EPP occurs, including in tarsiers (Tarsius lariang ;Driller, Perwitasari-Farajallah, Zischler, & Merker, 2009), lemurs (Hapalemur griseus alaotrensis; Nievergelt, Mutschler, Feistner, & Woodruff, 2002;Cheirogaleus medius;Fietz et al., 2000;Phaner furcifer, Schülke, Kappeler, & Zischler, 2004), gibbons (Hylobates lar; Barelli et al., 2013;Nomascus gabriellae;Kenyon, Roos, Binh, & Chivers, 2011). To date, Azara's night monkey (Aotus azarae) and Muller's Bornean gibbon (Hylobates muelleri) are the only two primate species in which no evidence of EPP was found; however, in the latter case, only four offspring were tested (reviewed in Lambert, Solomon, & Sabol, 2018). ...
Article
Monogamy is a rare strategy among mammals but relatively common among primates. The study of the evolution of monogamy in mammals and primates is lacking empirical studies that assess the relationship between a pair‐living social organization and genetic monogamy. Sexual or genetic monogamy can only be assessed by performing molecular analyses and investigating rates of extra‐pair paternity (EPP). Studying the occurrence of EPP can provide valuable insights into reproductive strategies and their adaptive value. The indri is a pair‐living primate that lives in stable groups. Their social units are composed of the reproductive pair and up to four more individuals, but extra‐pair copulation (EPC) can occur. This raises the question of whether this event may or may not lead to EPP. Here, we investigated whether a pair‐living social organization corresponds to genetic monogamy in indris (Indri indri). We analyzed the paternity of 12 offspring from seven pairs using a set of six microsatellite loci on fecal samples (mean number of alleles 11.7 ± 1.8 (mean ± standard deviation). We found that in 92% of cases the genetic profile of the offspring matched the paired male of the group for all the loci considered. In the only case of paternity mismatch, the paternity assignment remained inconclusive. Our results show that I. indri genetic monogamy is the norm and supports the hypothesis that pair‐living social organization is associated with low EPP rate. Also, our results are in contrast with the hypothesis of infertility as a reason to engage in EPC for this species. HIGHLIGHTS • In 92% of cases, the paired male of the group did not have any locus mismatch with the offspring. In the only case of paternity mismatch, we were not able to assign the sire identity. • Our finding suggests that genetic monogamy is the norm in the indri, although EPC can occasionally occur.
... We focus our classification of sociality on the behavior of breeding females, those that are in the later stages of pregnancy or have dependent young and do not consider the behavior of juveniles, males, or adult females who are not breeding. In some species where breeding females commonly aggregate, some breeding groups include a single breeding female, whereas others include several females that breed regularly (Nievergelt et al. 2002;Dalerum 2007;Schradin et al. 2012;Weidt et Where intrapopulation variation of this kind was reported, we classified species as plural breeders if, throughout the breeding season, most breeding females are found in groups where several females breed regularly and as singular breeders if the majority of breeding females were found in groups that included a single breeding female. We used a majority rule to reduce risks of misclassification of rare observations that are likely to be nonadaptive (following Schradin et al. 2018). ...
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In many mammals, breeding females are intolerant of each other and seldom associate closely but, in some, they aggregate in groups that vary in size, stability, and kinship structure. Aggregation frequently increases competition for food, and interspecific differences in female sociality among mammals are commonly attributed to contrasts in ecological parameters, including variation in activity timing, the distribution of resources, as well as the risk of predation. However, there is increasing indication that differences in female sociality are also associated with phylogenetic relationships and with contrasts in life-history parameters. We show here that evolutionary transitions from systems where breeding females usually occupy separate ranges ("singular breeding") to systems where breeding females usually aggregate ("plural breeding") have occurred more frequently in monotocous lineages where females produce single young than in polytocous ones where they produce litters. A likely explanation of this association is that competition between breeding females for resources is reduced where they produce single young and is more intense where they produce litters. Our findings reinforce evidence that variation in life-history parameters plays an important role in shaping the evolution of social behavior.
... Instead, dominant males are able to monopolize reproduction almost completely . In a cross-sectional genetic study of gentle lemur (Hapalemur griseus) population, 91% of infants were also sired by a single resident male (Nievergelt et al. 2002), whereas dominant males reaped 67% of all paternities in redfronted lemurs (Wimmer and Kappeler 2002 ), suggesting the existence of similar processes in other lemur taxa. Because the degree of male reproductive skew observed in this sifaka population equals or exceeds that of highly sexually dimorphic anthropoids living in highly polygynous systems, such as mountain gorillas (Bradley et al. 2005), orang-utans (Utami et al. 2002), mandrills (Charpentier et al. 2005), patas monkeys (Ohsawa et al. 1993), and red howler monkeys (Pope 1990), mechanisms other than exclusion and physical superiority are primary determinants of reproductive success of male sifaka. ...
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The primates of Madagascar (Lemuriformes) are unusual among mammals in that polygynous species lack sexual dimorphism, and females dominate males socially in most species. Moreover, lemur groups are relatively small and characterized by even adult sex ratios despite the fact that one male should be able to exclude other males from the group. One hypothesis to explain this combination of behavioral, morphological, and demographic traits (the “lemur syndrome”) postulates that male–male competition is relaxed and, hence, variance in male reproductive success is low. Reproductive skew theory provides a framework for testing this and several related predictions about lemur social evolution. Specifically, low reproductive skew is also predicted if dominant males or adult females make reproductive concessions to subordinates or if the latter group successfully pursues alternative reproductive tactics. However, suitable data on paternity, demography, and behavior for a conclusive test of these predictions have not been available in the past. In this paper, we show that male reproductive success in ten groups of Verreaux’s sifakas (Propithecus verreauxi) was extremely skewed in favor of the dominant male over 9years. Our genetic analyses also revealed that more than a third of all groups are effectively harem groups because only one male was unrelated to the resident female(s). In groups with two or more non-natal males, the dominant sired 91% of 33 infants. Together, males pursuing one of several alternative reproductive tactics, such as roaming among several groups or immigrating peacefully, sired only 11% of infants. Thus, female sifakas do not control group composition by offering reproductive opportunities to subordinate males as staying incentives, intrasexual selection is not relaxed, and dominant males prevail in a tug-of-war over subordinate males. Because male reproductive skew in sifakas is even more pronounced than in harem-living anthropoids studied to date, intrasexual selection is clearly not relaxed, and the lemur syndrome is more puzzling than ever.
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Tesis doctoral inédita leída en la Universidad Autónoma de Madrid, Facultad de Psicología, Departamento de Psicología Biológica y de la Salud, Fecha de lectura:23 de marzo de 2007 Bibliogr.: p.224-237. Índices
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The Alaotran gentle lemur Hapalemur alaotrensis is a Critically Endangered lemur, which exclusively inhabits the marshes around Lac Alaotra in northeast Madagascar. In the past decades the population of H. alaotrensis has experienced a dramatic decline due to poaching, habitat destruction and degradation. Surveys have been carried out periodically to follow the status of the population. Here we present the results of a survey carried out between May and June 2008 in the southwestern part of the marshes around Alaotra and discuss the key findings derived from the analysis of the data collected. Our study indicates that the probability of detecting the species in an area where it is present is very low and depends on factors that vary in space and time. These results stress the need to account for imperfect detection when monitoring this species, an issue especially relevant when reporting population trends. Our analyses also show that habitat fragmentation is a key determinant of habitat suitability for H. alaotrensis, with fragmented areas of marsh showing low suitability. Finally, our observations and analysis suggest that the protection provided by the local community to H. alaotrensis in Andreba is contributing to the conservation of this Critically Endangered species. This highlights the need to continue working on engaging the local communities in the conservation of the marshes at Lac Alaotra as a critical element to secure the future of H. alaotrensis.
Article
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.
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The competitive dynamics between domestic and native carnivores are poorly studied. We examined competition for food between sympatric populations of free-ranging dogs (Canis familiaris) and Indian foxes (Vulpes bengalensis) through dietary analysis in a protected, dry grassland habitat in central India. We expected significant dietary overlap between dogs and foxes because of clear evidence of interference competition between dogs and foxes in this area. However, dogs subsisted largely on human-derived foods (HDFs) from direct feeding, and scavenging on garbage, crop residue, and livestock carcasses (83% relative occurrence [RO]). Wild-caught foods constituted only 11% RO of the diet of dogs. The majority of the diet of Indian foxes consisted of invertebrates (33% RO), rodents (20% RO), and fruits of Zizyphus (18.5% RO). Indian foxes did not consume HDF, nor did they scavenge from large-mammal carcasses, and included only a small portion of agricultural produce in their diet. The low contribution of HDF and agricultural food sources to the diet of Indian foxes was surprising because this species is a generalist omnivore. Dogs may be preventing foxes from accessing agricultural lands and human-associated foods by interference competition.
Article
Though females are generally more selective in mate choice, males may also derive reproductive benefits from exercising mate selectivity if one or more factors limit male reproductive success and females differ in reproductive potential. I used male mating effort as a proxy for male mate choice in ring-tailed lemurs (Lemur catta). I calculated mating effort as the rate of male-male agonism during each female's estrous period 30 min before and 30 min after the first and last mountings with intromission. I collected data on 1 free-ranging Lemur catta troop during 2 consecutive breeding seasons on St. Catherines Island, USA. In both yrs, male mating effort differed significantly among troop females once I adjusted male-male agonistic rates to reflect agonistic intensity, and I corrected for the number of observed mates per female (2000: X² = 27.43, df = 3, p < 0.0001; 2001: X² = 21.10, df = 3, p < 0.001). Results strongly suggest male mate choice. Contrary to expectation, males did not expend the greatest mating effort for females with the highest dominance status nor the highest reproductive success. Males preferred females that either: (1) belonged to the age class in which fecundity and infant survival is the highest at this site (4-9 yrs), or 2) were older females (=10 yrs) with high reproductive success. Female reproductive potential appears to be an important variable determining male mating effort in Lemur catta.
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In recent years, genetic studies have been used to investigate mating systems of marine turtles, but to date no such research has been conducted on the flatback turtle (Natator depressus). This study investigates paternity of flatback turtle clutches at two rookeries in Queensland, Australia; Peak Island (Keppel Bay), and Mon Repos (Bundaberg). In the 2004–2005 nesting season, tissue samples were taken from either single or multiple clutches (n = 16) of nesting females (n = 8) representing a sampling effort ranging from 25% to 50% offspring per nest. Determination of the extent of multiple paternity was done using a comparative approach that included initial inferences based on observed alleles, Chi-square tests for deviations from Mendelian expectations, and three software programs (PARENTAGE1.0, GERUD2.0 and MER3.0). Results varied depending on the approach, but by calculating a consensus value of the output from these different methods, the null hypothesis of single paternity could be rejected in at least 11 of the 16 clutches (69%). Multiple paternity was thus observed in the clutches of six of nine females (67%), with two or three fathers being the most likely outcome. Analyses of successive clutches illustrated that paternal contribution to clutch fertilization can vary through time, as observed for two females. This first evidence regarding the mating system of flatback turtles indicates that multiple paternity is common in this species and that the observed frequency of multiple paternity is among the higher values reported in marine turtle species. Application of these results to estimates of effective population size (N e) suggests that population size may have been relatively stable over long periods. Continued monitoring of population dynamics is recommended to ensure that future changes in the east coast can be detected.
Chapter
We review available data documenting reproductive skew in the small group of mammals characterized by female dominance over males, focusing mainly on lemurs and spotted hyenas (Crocuta crocuta). Although most females in all lemur species examined here appear to bear young at each opportunity, we know very little about variation in longer-term reproductive success or rates of reproduction among female lemurs. Therefore we cannot draw firm conclusions in regard to reproductive skew among female lemurs except that at present this appears to be slight. However, current data show that female lemurs typically mate with multiple males, and that a substantial fraction of litters containing multiple offspring is sired by more than one male. The extent of reproductive skew in male lemurs varies among species, but there is a slight trend, among the lemur species for which genetic data exist, for male skew to decrease as the intensity of female dominance increases. Variance in reproductive success among female spotted hyenas appears to be substantially greater than it is in male-dominated species in which plural breeding occurs. In this species, female dominance, combined with virilization of the external genitalia, may increase female control over mating to its extreme limit, such that we find very little reproductive skew among males relative to that found in other polygynous mammals. The most dominant male hyenas often achieve very little reproductive success. Overall, reproductive skew among females in female-dominated mammals appears to be the same as or slightly greater than that in male-dominated species, whereas skew among males in female-dominated species generally tends to be relatively low.
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The evolution of social monogamy has intrigued biologists for over a century. Here, we show that the ancestral condition for all mammalian groups is of solitary individuals and that social monogamy is derived almost exclusively from this social system. The evolution of social monogamy does not appear to have been associated with a high risk of male infanticide, and paternal care is a consequence rather than a cause of social monogamy. Social monogamy has evolved in nonhuman mammals where breeding females are intolerant of each other and female density is low, suggesting that it represents a mating strategy that has developed where males are unable to defend access to multiple females.
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Male mammals often kill conspecific offspring. The benefits of such infanticide to males, and its costs to females, probably vary across mammalian social and mating systems. We used comparative analyses to show that infanticide primarily evolves in social mammals in which reproduction is monopolized by a minority of males. It has not promoted social counterstrategies such as female gregariousness, pair living, or changes in group size and sex ratio, but is successfully prevented by female sexual promiscuity, a paternity dilution strategy. These findings indicate that infanticide is a consequence, rather than a cause, of contrasts in mammalian social systems affecting the intensity of sexual conflict.
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Following the introduction of DNA fingerprinting in the 1980s, studies have repeatedly revealed mismatches between the mating system inferred from social behaviour and the mating system revealed through genetic relationships. In this study, we examined the occurrence of extragroup paternities (EGPs) in gelada monkeys at Guassa, Ethiopia and explored how EGPs may be acquired in this species, which is conventionally considered to have a single breeding male (‘leader’) per social group (‘unit’). We found that while leaders sired most offspring, a substantial proportion (17 of 88 offspring, 19%) were sired by extra-unit males. Offspring were more likely to be sired by extra-unit males when they were: (1) conceived in the 6 months following the start of peak rainfall (July–December) and (2) the first successful conception for a mother. Furthermore, eight of the 17 extra-unit paternities were directly or indirectly the result of a single infertile leader, indicating that infertility plays an important role in the occurrence of EGPs. Compiling published data revealed that the 19% EGP rate observed among Guassa geladas was also the median for polygynous nonhuman primates (range 0–57%, N = 5 populations), in contrast to geladas in the Simien Mountains, where EGPs are absent or rare. Thus, intraspecific variation in EGP rates in geladas encompasses much of the range described across polygynous primates more broadly. The Guassa gelada EGP rate was similar to the median rate reported for mammals. Primates generally had a lower median rate of EGPs, more similar to the median rate reported for birds. Understanding variation in EGP rates requires understanding the outcomes of competing interests of males and females within the same species, as well as how these features contribute to the evolution of social systems and influence variation in EGP rates at higher taxonomic levels.
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Natural resource management problems typically involve a multitude of stakeholders with diverse sets of needs and interests, and often conflicting worldviews in an environment with growing uncertainty. Such problems are termed " wicked " problems, where there are no right or wrong solutions, only more or less acceptable ones. In the case of Lake Alaotra, growing agricultural pressures have a negative impact on the wetland biodiversity and especially on the Alaotra gentle lemur (Hapalemur alaotrensis) restricted to these marshlands. The species survival is highly uncertain because of increased habitat loss caused mainly by marshland fires. The conservation work for this unique lemur is complex and complicated and requires the involvement and collaboration of decision-making institutions, NGOs, universities and riverine communities. From the inception of projects to their implementation phase, all parties need clearly defined responsibilities and transparency in communication in order to run projects successfully. This article describes the approach that Madagascar Wildlife Conservation has been implementing during the past ten years at Lake Alaotra, discussing the plan of action and challenges for environmental education, ecotourism and alternative livelihoods. RÉSUMÉ Les problèmes de gestion des ressources naturelles impliquent généralement une multitude d'intervenants avec divers ensembles de besoins et d'intérêts, et souvent, les visions du monde contradictoires dans un environnement avec une incertitude croissante. Ces problèmes sont appelés problèmes sournois, 'wicked problems' en anglais, où il n'y a pas de bonnes ou de mauvaises solutions, seules plus ou moins acceptables. Dans le cas du lac Alaotra, la croissance des pressions agricoles a un impact négatif sur la biodiversité des zones humides, et en particulier sur l'Alaotra lémurien douce (Hapalemur alaotrensis) limitée à ces marais. La survie de l'espèce est très incertaine en raison de l'augmentation de la perte d'habitat causée principalement par les feux de marais. Les travaux de conservation pour ce lémurien unique sont complexes et compliqués, et nécessitent l'implication et la collaboration sur la prise de décision des institutions, des ONG, des universités et des communautés riveraines. Cela implique que toutes les parties, depuis la création de projets à leur phase de mise en oeuvre, partagent un terrain d'entente avec les avantages clairement définis de pouvoir de décision, les responsabilités et la transparence dans la communication. Madagascar Wildlife Conservation a travaillé sur le lac depuis plus de dix ans, y compris l'éducation environnementale, l'écotourisme et les moyens de subsistance alternatifs dans le plan d'action. Cet article met en évidence l'approche adoptée et examine ses défis.
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Monogamy as a social system has been both a scientific puzzle and a sociocultural issue for decades. In this review, we examine social monogamy from a comparative perspective with a focus on primates, our closest genetic relatives. We break down monogamy into component elements, including pair-bonding and partner preference, mate guarding or jealousy, social attachment, and biparental care. Our survey of primates shows that not all features are present in species classified as socially monogamous, in the same way that human monogamous relationships may not include all elements—a perspective we refer to as “monogamy à la carte.” Our review includes a survey of the neurobiological correlates of social monogamy in primates, exploring unique or common pathways for the elemental components of monogamy. This compilation reveals that the components of monogamy are modulated by a suite of androgenic steroids, glucocorticoid hormones, the nonapeptide hormones oxytocin and vasopressin, and other neurotransmitter systems (e.g., dopamine and opioids). We propose that efforts to understand the biological underpinnings of complex human and animal sociosexual relationships will be well served by exploring individual phenotypic traits, as opposed to pursuing these questions with the assumption that monogamy is a unitary trait or a species-specific characteristic.
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In most mammalian species, females regularly interact with kin, and it may thus be difficult to understand the evolution of some aggressive and harmful competitive behaviour among females, such as infanticide. Here, we investigate the evolutionary determinants of infanticide by females by combining a quantitative analysis of the taxonomic distribution of infanticide with a qualitative synthesis of the circumstances of infanticidal attacks in published reports. Our results show that female infanticide is widespread across mammals and varies in relation to social organization and life-history, being more frequent where females breed in group and invest much energy into reproduction. Specifically, female infanticide occurs where the proximity of conspecific offspring directly threatens the killer's reproductive success by limiting access to critical resources for her dependent progeny, including food, shelters, care or a social position. In contrast, infanticide is not immediately modulated by the degree of kinship among females, and females occasionally sacrifice related juveniles. Our findings suggest that the potential direct fitness rewards of gaining access to reproductive resources have a stronger influence on the expression of female aggression than the indirect fitness costs of competing against kin.
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In most mammalian species, females regularly interact with kin, which is expected to reduce aggressive competitive behaviour among females. It may thus be difficult to understand why infanticide by females has been reported in numerous species and is sometimes perpetrated by groupmates. Here, we investigate the evolutionary determinants of infanticide by females by combining a quantitative analysis of the taxonomic distribution of infanticide with a qualitative synthesis of the circumstances of infanticidal attacks in published reports. Our results show that female infanticide is widespread across mammals and varies in relation to social organization and life history, being more frequent where females breed in groups and have intense bouts of high reproductive output. Specifically, female infanticide occurs where the proximity of conspecific offspring directly threatens the killer's reproductive success by limiting access to critical resources for her dependent progeny, including food, shelters, care or a social position. By contrast, infanticide is not immediately modulated by the degree of kinship among females, and females occasionally sacrifice closely related infants. Our findings suggest that the potential direct fitness rewards of gaining access to reproductive resources have a stronger influence on the expression of female aggression than the indirect fitness costs of competing against kin. This article is part of the theme issue ‘The evolution of female-biased kinship in humans and other mammals’.
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Extant lemuriform and anthropoid primates differ dramatically in social behavior, grouping patterns, social structure, and sexual dimorphism In this paper, we analyze and contrast grouping and bonding patterns among lemurs, and suggest determinants of social organization that explain many of these differences. Lemurs exhibit three main grouping patterns: solitary individuals, bonded pairs, and larger groups. Transitions between pairs and larger groups occur within several species and even within populations in some of Eulemur species and in Varecia. Larger groups of these species have an equal adult sex ratio, and spatial associations and social behavior suggest the existence of male-female pair bonds. Larger groups of the consistently diurnal Lemur and Propithecus also show equal adult sex ratios, but no evidence for pair-bonding. These differences among lemurs are likely due to variation in the activity periods of the cathemeral species, whose groups are hypothesized to break up into pairs during periods of nocturnal activity. The pair bond is therefore the fundamental umt of many lemur groups. This is a special case of the permanent male-female associations found among the great majority of primate species. We suggest that the evolution of permanent male-female associations is favored by selection for infanticide prevention, because the male can effectively protect the females against infanticide attempts by other males. Where females live alone permanently or part of their time (the cathemeral species), this association takes the form of a pair bond. Where they live in groups, it takes the form of permanently bisexual groups. This hypothesis leads us to predict no male-female association in species with absentee maternal care. This prediction is confirmed: the interspecific variation in infant care (carry vs hide) covaries perfectly with grouping pattern among prosimians, as well as among other primate radiations. We conclude that activity period and type of infant care determine grouping and bonding patterns in both prosimian and anthropoid societies. Both cathemeral activity periods and infant carrying among primates were probably made possible by increased precociality.
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Research on lemurs contributes importantly to evaluation of hypotheses on primate development and evolution. A central question about social behavior has asked why adult females in many lemur species socially dominate males while this trait is rare among Anthropoids and other mammals. At present, the favored hypothesis—that female lemurs undertake unusually costly reproduction and dominance over males is necessary for females to access sufficient nutrition throughout Madagascar’s dry season—has both supporters and detractors. We propose that confusion concerning female dominance in lemurs derives from failing to appreciate that adaptation should have minimized prospects for seasonal stress and that success during months of food abundance, not months of food scarcity, is most likely to be the primary foraging factor influencing relative fitness among today’s lemurs. Analyses of hair growth, somatic growth, food intake, fatness, and two metabolically-active hormones (thyroxine and insulin-like growth factor 1) revealed that Lemur catta and Eulemur fulvus rufus prepare during the photoperiod of Madagascar’s annual wet season for upcoming dry seasons and also make adjustments during dry seasons that make life less expensive.
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Infant killing by primates is highly controversial. Sexual selection of infanticidal males has been disputed, especially for seasonally breeding species, in which death of an infant does not advance conception of the next infant. We report attacks, infants found wounded, and predation in seasonally breeding Eulemur and Lemur at Berenty, Beza Mahafaly and Duke University Primate Center, and review cases seen elsewhere. Observed attacks leading to wounds or death conservatively total twelve by extratroop males, two by troop males, and seven by troop females. Eulemur are occasional vertebrate predators, whose prey includes infant Lemur catta. Wounds inflicted by lemurs are usually abdominal canine slashes or bites to the head, with rare eating, a pattern distinct from carnivore and raptor kills. Infant killing as inferred from corpses is more frequent than previously thought, but still rare. Adaptive advantages of killing plausibly include eliminating resource competitors of females, and sexual selection on males.
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Cheirogaleids are one of the most primitive extant primate taxa in the world. Their lifestyle and mating system, therefore, have been considered to be representative for social systems in primate ancestors. Accepted models of social evolution in primates state that pair-bonding has evolved secondarily from diurnal group-living taxa and should therefore be constrained primarily to diurnal species. In contrast to these assumptions, the nocturnal fat-tailed dwarf lemur (Cheirogaleus medius) lives in permanent pairs, with obligate paternal care probably representing the evolutionary basis of pair-living. In this sociobiological field study, we analyzed the reproduction strategy of C. medius in the tropical forest of western Madagascar. In the rainy seasons from 1995 to 1999, 173 individuals of C. medius were captured and individually marked and 131 were genetically characterized through seven microsatellite loci. Additionally, 36 of these individuals were radio-tracked and observed. For 53 genotyped individuals, including 16 offspring, information about pair-bonding and family structure was known from field observations. Genetic analyses revealed that yearlings and infants living with an adult pair were in all cases sibs of the social mother. However, C. medius does not restrain from extra-pair copulations (EPCs) and a high rate of extra-pair paternity (44%) was detected. Males sired offspring with their female partners as well as with extra-pair females within the same year, indicating that males may increase their reproductive success by EPCs without necessarily running the risk of cuckoldry. Females on the other hand do not seem to run the risk of reduced paternal care, either because males cannot detect relatedness of young, or because they might even increase their inclusive fitness by raising offspring of closely related males. Since females reproduce preferentially with territory holders and no paternity could be assigned to floating males, superior genetic quality of the males might be crucial for female choice.
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Paternity determination by DNA fingerprinting is reported for a long-term study group of semi-free-ranging ringtailed lemurs (Lemur catta), together with behavioral data collected independently. In 1985, fraternal twin males unfamiliar and unrelated to the resident ringtailed lemurs were introduced to the forest enclosure. Every mature resident male attacked the immigrants frequently across the next 5 months, whereas no female ever did. All observed estrous females showed sexual proceptivity toward the' immigrant males; three solicited copulation exclusively from them. Each female repelled sons, matrilineal brothers, and other resident males from attempting to copulate. Over a 5-year period, four of five females always reproduced with distantly related or unrelated males (Fig. 3). Despite low dominance status throughout the case study, an immigrant sired the off-spring of each female that was proceptive toward only the immigrants, demonstrating that female choice can override male dominance relations to determine reproductive success among male ringtailed lemurs. In the birth season following the 1985–1986 immigration, each of four females targeted one or two particular adult males for consistent attack across the period of infant dependency, beginning days after parturition. Paternity determinations, colony records, and subsequent study of two groups allowed 66 cases of this mode of maternal aggression to be documented. In each, the targeted male had not fathered the protected infant, and almost invariably, he was unrelated to the infant's mother. New mothers attacked every male that immigrated following their infants' conceptions and a few familiar males with whom they had not been seen to copulate during the previous breeding season. Recent attempts by immigrant males to kill infants confirmed the anti-infanticidal function of maternal targeting of males. All results were interpreted together to advance a prospective model of the mating system of ringtailed lemurs. Female avoidance of incest has led to the evolution of natal male dispersal. Subsequently, males should prefer to transfer into groups containing few and/or status-vulnerable males. We predict that, by killing others' infants, males simultaneously increase chances for success in females' next reproductive efforts and terminate current fathers' reproductive eligibility in a group. Basic hypotheses that await testing are that (a) raising an infant through weaning reduces a female's chances for reproductive success the following year and (b) males that demonstrate the capacity to promote the survival of infant offspring are most attractive to females as mates.
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Data from wild and semifree-ranging groups of ringtailed lemurs (Lemur catta) were combined to evaluate the hypothesis that female ringtailed lemurs exhibit asynchrony of estrus within seasonal synchrony of estrous cycles. Photoperiodic and probably social entrainments lead all females within social groups of ringtailed lemurs to experience estrus annually within periods of 7 to 20 days. Among an average of five adult females in each of 11 group-years, however, only 2 separate instances of dyadic estrous overlap were observed. Computer simulations of estrus occurring independently among group-living females revealed that this was unlikely to have occurred by chance. Recent research on social enhancement and suppression of ovarian cycles in mammals suggests that a single pheromone-based signal-response system could mediate both ringtailed lemurs' remarkable annual estrous synchrony and the subsidiary asynchrony reported here. Asynchrony of estrus probably functions to maximize each female's ability to exercise mate choice by circumventing temporal conflict among females. Asynchrony of estrus and female mate choice cause current models to explain male membership in primate groups to fail for ringtailed lemurs. Such results highlight the need for detailed information on behavioral and physiological reproductive tactics before generally applicable models of reproductive strategies can be developed.
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The lemurs of Madagascar typically exhibit a strictly seasonal pattern of breeding, with a limited number of successive estrous cycles occurring at a particular time of the year, which varies from species to species. Previous reports indicated that aye-ayes also exhibit such a strictly seasonal polyestrous pattern. Data from the author's 2-year field study of aye-ayes on the island of Nosy Mangabe, combined with information from recently initiated captive breeding programs, now indicate that this species in fact shows an extended breeding season or even year-round breeding. Actual mating or signs of estrus were observed in the field throughout a 5-month period (October-February). Further, data from captured pregnant females and young offspring indicate that births take place during the period from February to September. Apart from aye-ayes, extended breeding periods have been reported for wild Eulemur coronatus and for captive Eulemur fulvus and Mirza coquereli. Analysis of information on seasonal variation in food availability for aye-ayes and other lemurs provides no clear evidence that the degree of seasonality of breeding is directly dependent on ecological factors.
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We report new evidence that bears decisively on a long-standing controversy in primate systematics. DNA sequence data for the complete cytochrome b gene, combined with an expanded morphological data set, confirm the results of a previous study and again indicate that all extant Malagasy lemurs originated from a single common ancestor. These results, as well as those from other genetic studies, call for a revision of primate classifications in which the dwarf and mouse lemurs are placed within the Afro-Asian lorisiforms. The phylogenetic results, in agreement with paleocontinental data, indicate an African origin for the common ancestor of lemurs and lorises (the Strepsirrhini). The molecular data further suggest the surprising conclusion that lemurs began evolving independently by the early Eocene at the latest. This indicates that the Malagasy primate lineage is more ancient than generally thought and places the split between the two strepsirrhine lineages well before the appearance of known Eocene fossil primates. We conclude that primate origins were marked by rapid speciation and diversification sometime before the late Paleocene.
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Most lemurs yet studied in detail exhibit some mode of adult female social dominance over males. The known exception, a brown lemur subspecies known as rufous or redfronted lemurs (Eulemur fulvus rufus), forms multimale-multifemale social groups within which unambiguous dominance relations are not observed among adults. Resting groups of redfronted lemurs consistently include huddling adult male-female pairs whose males selectively scentmark and rub their heads in the scentmarks of their female huddling partners. Quantitative observations confirmed that some of these male-female pairs maintain special relationships satisfying all criteria originally developed in research on cercopithecine monkeys. Observations before, during, and after mating season, intergroup encounters, male transfers, and changes in male-female affiliations illuminated developmental and functional aspects of male-female partnerships. Each adult female in two semi-free-ranging study groups shared high rates of association, grooming, and agonistic support and low rates of agonistic interaction with one unrelated or distantly related adult male partner. Such affinity characterized small proportions of adult male-female relationships. Several males directed not only support but also aggression toward adult females with whom they sought to affiliate. All bonded males sought to copulate with their partners, and some appeared to ignore estrus in nonpartners. All females accepted copulation attempts from partners and some seemed to prefer their partners as mates. Partial synchronization of brief estrus periods together with concealed ovulation appeared to minimize chances for polygynous mating. Results support the view that the male-female pair is the fundamental social unit of E. fulvus and suggest that female partnership with individual males obviates dominance behavior, including female dominance, in this lemurid primate.
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Year-round association between adult males and females is common in primates, even though internal gestation and lactation predispose males to mate-desertion in the majority of mammals. Because there is little a priori support for alternative explanations, we hypothesized that permanent male-female association in primates serves to reduce the risk of infanticide by strange males whenever females and infants are closely associated. For a phylogenetic test of this hypothesis, we reconstructed the evolution of male-female and female-infant association among primates. The results of Maddison's concentrated changes test confirmed the prediction that mother-infant association, as opposed to infant parking, and female-male association did not evolve independently. Changes in litter size and activity, in contrast, were not significantly associated with evolutionary changes in male-female association. Thus, we demonstrate a fundamental link between primate life history and social behaviour, explain the most basic type of variation in primate social organization, and propose an additional determinant of social organization that may also operate in other mammals.
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A new method is described for estimating genetic relatedness from genetic markers such as protein polymorphisms. It is based on Grafen's (1985) relatedness coefficient and is most easily interpreted in terms of identity by descent rather than as a genetic regression. It has several advantages over methods currently in use: it eliminates a downward bias for small sample sizes; it improves estimation of relatedness for subsets of population samples; and it allows estimation of relatedness for a single group or for a single pair of individuals. Individual estimates of relatedness tend to be highly variable but, in aggregate, can still be very useful as data for nonparametric tests. Such tests allow testing for differences in relatedness between two samples or for correlating individual relatedness values with another variable.
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Chapter
The Alaotran Gentle LemurHapalemur griseus alaotrensis isrestricted to the marshes around Lac Alaotra. It is threatened by habitat destruction and fragmentation and by hunting for food and pets. Since 1990 a conservation program for this lemur—now a flagship for the Alaotran wetlands—has been developed. It has a multidisciplinary approach involving captive breeding(inandex situ)research on captive animals (infant development, nutrition), field research (distribution, census, conservation status, behavioral ecology, ranging, diet, social organization), socioeconomic studies, community education, and genetics. The development of this program is described and illustrates how a small-scale yet holistic approach to species conservation can be effective.
Chapter
Seasonal behavioral variation has been described in lemur species throughout Madagascar, and has been related to pronounced island-wide environmental seasonality. Although there are regional differences in rainfall patterns, ambient temperature appears to vary in consistent, seasonal cycles throughout Madagascar. Data collected during a field study of black and white ruffed lemurs (Varecia variegata variegata) in northeastern Madagascar demonstrated that ruffed lemurs reduced activity levels and travel distances, and increased feeding, sunning, and hunched sitting during the months with the lowest temperatures. Lemurs appear to respond to predictable annual cycles of temperature change with behavioral and social mechanisms rather than purely physiological ones. Ambient temperature is proposed to be a major determinant of seasonal variation in lemur behavior. These hypotheses have implications for the evolution of lemur social organization. The goal of this paper is to focus attention on the relationship between thermoregulation and behavior in lemurs and to suggest a set of issues that merit detailed study.
Chapter
Hapalemur griseus alaotrensisa relatively small-bodied (1240 ± 140 g, n = 58), folivorous lemur, was studied over a period of 15 months at Lac Alaotra. The study showed thatH. g. alaotrensishad an exclusively folivorous diet and mainly fed on leaves and stems of grasses and sedges. However, since folivorous diets are known to be poor sources of readily available energy and small-bodied animals generally have high metabolic requirementsH. g. alaotrensisis expected to have adaptations at several levels (morphological, physiological, behavioral) to resolve this conflict. The present study onH. g. alaotrensisshowed that dietary diversity was extremely low and food choice highly selective, but chemical composition of the food items yielded no evidence thatH. g. alaotrensisselected higher quality foods than larger folivores, nor was there evidence thatH. g. alaotrensisminimized energy expenditure at the behavioral or physiological level. This lack of behavioral or physiological adaptations to folivory imply that the digestive ability ofH. g. alaotrensismay be higher than predicted for an animal of its size.
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A new method is described for estimating genetic relatedness from genetic markers such as protein polymorphisms. It is based on Grafen's (1985) relatedness coefficient and is most easily interpreted in terms of identity by descent rather than as a genetic regression. It has several advantages over methods currently in use: it eliminates a downward bias for small sample sizes; it improves estimation of relatedness for subsets of population samples; and it allows estimation of relatedness for a single group or for a single pair of individuals. Individual estimates of relatedness tend to be highly variable but, in aggregate, can still be very useful as data for nonparametric tests. Such tests allow testing for differences in relatedness between two samples or for correlating individual relatedness values with another variable.
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A model suggests that female-bonded (FB) groups have evolved as a result of competition for high-quality food patches containing a limited number of feeding sites. These relationships are beneficial based on cooperative relationships among females. These relationships are beneficial because cooperators act together to supplant others from preferred food patches. Ecological data support the model for most FB species, but not for Theropithecus gelada or Colobus guereza, whose foods are not found in high-quality patches with limited feeding sites. Non-FB species conform to expectation, either because they do not use high-quality patches, or because feeding competition has disruptive effects during periods of food scarcity. Multi-male groups tend to be found in non-territorial FB species. The presence of several males per group is suggested to benefit females by raising the competitive ability of the group in inter-group interactions. Competitive relationships among females are more strongly marked in FB groups.-from AuthorTheropithecus gelada Colobus guereza
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The Alaotran gentle lemur Hapalemur griseus alaotrensis is found only in the marsh vegetation surrounding Lac Alaotra in Madagascar. This habitat is shrinking and becoming fragmented due to conversion to rice cultivation. In addition, lemurs are hunted for pets and food. There is no protected area within their limited range. This paper presents the results of a 6-month field study assessing the distribution, population size and conservation status of the lemur. The population consists of about 7500 animals, split into at least two subpopulations. If no conservation action is taken in the near future, drainage of the remaining 13,000 ha block of marsh vegetation will probably lead to the extinction in the wild of this primate taxon.
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The Alaotran gentle lemur Hupuletnur griseus ahotrensis is currently classified as Critically Endangered (IUCN, 1996). In 1988 a captive-breeding programme was considered of highest priority and in November 1990 Jersey Wildlife Preservation Trust. under its accord with the government of Madagascar, imported 6.4 animals. The first captive birth for the species occurred in 1993 and in April 1997 a further 6.4 were imported. As at 1 March 1998 14.8 animals were maintained at Jersey. This paper describes husbandry, enclosure design, diet, reproduction and infant development in H. g. aluotrensis.
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The results of a field census of Alaotran gentle lemurs Hapalemur griseus alaotrensis carried out in February and March 1999 are reported. The results are compared with a census carried out 5 years earlier in 1994. Both censuses followed the same methods and were carried out by the same team, using direct observation from canoe. Mean group encounter rates for the lemur were assessed in each location, which allowed us to calculate the relative group density in each site. Qualitative information on habitat condition (on the basis of plant diversity, vegetation height and evidence of burning) was gathered at each site. Additional information, mainly on lemur hunting, was acquired through interviews with local people. In most sites group encounter rate was at least 50 per cent lower than 5 years before. Taking into account unusually low water levels because of a drought at Lac Alaotra in 1999, we estimate that these encounter rates reflect a 30 per cent decline in the total population size over the last 5 years. The main cause of this dramatic decrease was human-induced fire (habitat degradation) coupled with heavy hunting (poaching of lemurs for food). The importance of assessing regularly both population status and threats, and of adjusting conservation actions accordingly is emphasized.
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In this contribution, we present baseline data on the existing level of genetic diversity in the wild Alaotran gentle lemur population, and evaluate its evolutionary divergence from its most closely related subspecies, H. g. griseus. We studied sequence variation in the rapidly evolving control region of the mitochondrial DNA (mtDNA) to describe the phylogeographic structure of nine populations representative of the Alaotran gentle lemur's geographic range.
Book
Spectacular progress has been made recently in the study of evolution at the molecular level, primarily due to new biochemical techniques such as gene cloning and DNA sequencing. In this book, the author summarizes new developments and seeks to unify studies of evolutionary histories of organisms and the mechanisms of evolution into a single science - molecular evolutionary genetics.
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Recent developments of statistical methods in molecular phylogenetics are reviewed. It is shown that the mathematical foundations of these methods are not well established, but computer simulations and empirical data indicate that currently used methods such as neighbor joining, minimum evolution, likelihood, and parsimony methods produce reasonably good phylogenetic trees when a sufficiently large number of nucleotides or amino acids are used. However, when the rate of evolution varies extensively from branch to branch, many methods may fail to recover the true topology. Solid statistical tests for examining the accuracy of trees obtained by neighbor joining, minimum evolution, and least-squares method are available, but the methods for likelihood and parsimony trees are yet to be refined. Parsimony, likelihood, and distance methods can all be used for inferring amino acid sequences of the proteins of ancestral organisms that have become extinct.
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Existing DNA sequence data on the Sry gene, the mammalian sex-determining locus in the Y chromosome, were analyzed for primates, rodents, and bovids. In all three taxonomic groups, the terminal sequences evolved faster than the HMG (high mobility group) boxes, and this applies both to synonymous (Ks) and nonsynonymous (Ka) nucleotide substitutions. Similar intragenic correlation between synonymous and nonsynonymous substitution rates was not found either in other mammalian genes that contain a conservative box (Sox, Msx) or in the MADS-box genes of plants. The rate of nonsynonymous substitutions exceeds significantly that of synonymous substitutions in the terminal Sry sequences of apes. We did not find good support for the hypothesis that the high evolutionary rate of Sry would be associated with a promiscuous mating system.
Article
The aim of this review is to summarize newly available information on lemur social systems, to contrast it with the social organization of other primates and to relate it to existing models of primate social evolution. Because of their evolutionary history, the primates of Madagascar constitute a natural experiment in social evolution. During millions of years of isolation, they converged with other primates only in the most fundamental way in the evolution of solitary, pair-living and group-living species, but deviate in several respects within these basic categories of social organization. Solitary lemurs remain poorly studied, but their social organization appears to be broadly similar to that of other solitary primates, even though the unexpected lack of sexual dimorphism may indicate that similar types of social organization can give rise to different mating systems. The determinants of a solitary lifestyle remain elusive. Pair-living lemurs show striking convergences with other monogamous primates in several behavioural traits, but also deviate in that the majority of species are at least partly nocturnal and do not exhibit direct paternal care of dependent young. Group-living lemurs have not evolved single-male groups, male-bonded and multi-level societies, and polyandrous groups may also be lacking. Female philopatry is common, but female bonds are generally weakly developed and eviction of females from natal groups is not unusual. Group-living lemurs also differ from anthropoids in that their groups have even adult sex ratios, smaller average size and may split up on a seasonal basis. Feeding competition, predation risk and reproductive competition can not fully explain these unusual aspects of lemur social organization. It has therefore been suggested that the social consequences of the risk of infanticide and of recent changes in activity may be ultimately responsible for these idiosyncracies of group-living lemurs, an explanation largely supported by the available evidence. Thus, social factors and fundamental life-history traits, in addition to ecological factors, contribute importantly to variation in social systems among lemurs, and possibly other primates. However, neither the diversity of lemur social systems, nor the evolutionary forces and mechanisms operating in these and other primates are yet fully understood.
Article
How small-bodied (500-1,200 g) folivorous prosimian primates cope with large amounts of foliage in their diet seasonally has yet to be determined for many species such as Hapalemur griseus, which specializes on bamboo. To address this issue, we present results on seasonal variation in activity and diet from a wild group of H. griseus in southeastern Madagascar. Throughout the study (which was conducted from July-November 1994 and July 1995-February 1996), H. griseus primarily fed on new growth from three species of bamboo: two species of liana bamboo and Cephalostachyum perrieri. Bamboo species were used in different ways seasonally; liana bamboo was consumed more during the dry, cool season, and C. perrieri was eaten more often during the wet, warm season. H. griseus also spent more of their time feeding and traveling than nocturnal folivores of similar body size during the dry season. During the warm wet season, H. griseus decreased the amount of time spent feeding and traveling and rested more often. We hypothesize that seasonal changes in activity may be primarily related to the distribution and availability of food sources and/or reproductive cycles.
Article
Lemur societies have been described as convergent with those of anthropoids, including Papio-like female-bonded multi-male groups. Recent research, however, shows at least 5 pair-bonded species among the Lemuridae and Indriidae. Three more, Eulemur mongoz, Eulemur fulvus and Varecia variegata, have societies combining aspects of pairing with aspects of troop life. The best-known female-bonded societies, those of Lemur catta, Propithecus diadema edwardsi and Propithecus verreauxi, may be assemblages of mother-daughter dyads, capable of high aggression towards other females, but derived from more solitary female ancestors, perhaps also living as pairs. The internal structure of such lemur groups differs from the more extensive kin groups of catarrhines. This in turn may relate to the lemurs' level of social intelligence and to lemur female dominance over males.
Article
Paternity inference using highly polymorphic codominant markers is becoming common in the study of natural populations. However, multiple males are often found to be genetically compatible with each offspring tested, even when the probability of excluding an unrelated male is high. While various methods exist for evaluating the likelihood of paternity of each nonexcluded male, interpreting these likelihoods has hitherto been difficult, and no method takes account of the incomplete sampling and error-prone genetic data typical of large-scale studies of natural systems. We derive likelihood ratios for paternity inference with codominant markers taking account of typing error, and define a statistic delta for resolving paternity. Using allele frequencies from the study population in question, a simulation program generates criteria for delta that permit assignment of paternity to the most likely male with a known level of statistical confidence. The simulation takes account of the number of candidate males, the proportion of males that are sampled and gaps and errors in genetic data. We explore the potentially confounding effect of relatives and show that the method is robust to their presence under commonly encountered conditions. The method is demonstrated using genetic data from the intensively studied red deer (Cervus elaphus) population on the island of Rum, Scotland. The Windows-based computer program, CERVUS, described in this study is available from the authors. CERVUS can be used to calculate allele frequencies, run simulations and perform parentage analysis using data from all types of codominant markers.
Article
The Alaotran gentle lemur Hapalemur griseus alaotrensis is a poorly known primate found in the reed and papyrus beds around Lac Alaotra, Madagascar. Because of its restricted distribution, which does not contain any protected areas, it was classified as of highest conservation priority in the Lemur Action Plan [1]. Little is known about this taxon, it having been studied only briefly in 1969 [2]and 1984 [3]. These studies were based on limited direct observation and most information was derived from interviews with local people.
Article
To test whether plucked hairs are a reliable source of DNA for genotyping microsatellite loci, we carried out experiments using one, three, or 10 hairs per extract for 50 alpine marmots. For each extract, seven independent genotypings were performed for the same locus (multiple-tubes approach). Two types of genotyping errors were recorded: a false homozygote defined as the detection of only one allele of a true heterozygote, and a false allele defined as a PCR-generated allele that was not one of the alleles of the true genotype. Using DNA extracted from one, three, or 10 hairs the overall error rate was 14.00%, 4.86%, and 0.29%, respectively. Based on our results, we conclude that 10 hairs should be used to obtain consistently reliable genotypings using the single-tube approach, and that a single plucked hair could represent a reliable source of DNA if the multiple-tubes approach is used. For future studies of dinucleotide repeat diversity using DNA extracted from one to three shed or plucked hairs, we strongly recommend initiating an appropriate pilot study to quantify the error rate and to determine the reliability of the single-tube approach.