Nelly Ménard

Noninvasive population genetics: a review of sample source, diet, fragment length and microsatellite motif effects on amplification success and genotyping error rates

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.

Gorilla susceptibility to Ebola virus: The cost of sociality

Since 1994, there have been nine human Ebola-Zaire virus (EBOV) outbreaks in eastern Gabon and northwestern Congo [1–3]. A majority of them originated from the handling of ape carcasses found by local hunters [4]. The impact of Ebola-Zaire virus on great ape density is suspected to be high [2,5,6], but neither the demographic consequences of outbreaks nor the way the virus spreads within an ape population are well known. The large population of western lowland gorillas, Gorilla gorilla gorilla, monitored since 2001 at the Lokoue clearing, Odzala-Kokoua National Park, Congo, was affected in 2004, providing us with the opportunity to address both questions using an original statistical approach mixing capture–recapture and epidemiological models.

Sex-biased dispersal in western lowland gorillas (Gorilla gorilla gorilla).

We explored two hypotheses related to potential differences between sexes in dispersal behaviour in western lowland gorillas (Gorilla gorilla gorilla). Direct observations suggest that immature females have more opportunities to move between breeding groups than immature males. The distribution of kin dyadic relationships within and between groups does not, however, support this hypothesis. At larger geographical scales, dispersal is likely to be easier for males than females because of the solitary phase most blackbacks experience before founding their own breeding group. However, previous work indicates that males settle preferentially close to male kin. By specifically tracing female and male lineages with mitochondrial and Y‐chromosomal genetic markers, we found that male gorillas in the 6000 km2 area we surveyed form a single population whereas females are restricted to the individual sites we sampled and do not freely move around this area. These differences are more correctly described as differences in dispersal distances, rather than differences in dispersal rates between sexes (both sexes emigrate from their natal group in this species). Differences in resource competition and dispersal costs between female and male gorillas are compatible with the observed pattern, but more work is needed to understand if these ultimate causes are responsible for sex‐biased dispersal distances in western lowland gorillas.

Behavioral responses of Barbary macaques (Macaca sylvanus) to variations in environmental conditions in Algeria

In this study, the behavioral responses of Barbary macaques to seasonal and interhabitat variations in resource availability were analyzed over an entire annual cycle. Two groups, one in an evergreen cedar–oak forest (Djurdjura) and the other in a deciduous oak forest (Akfadou), were observed. In this paper, references to data on resource availability published elsewhere are made. Time budget has been studied. Variations in foraging and moving time, in day–range lengths, and in time moving in trees have been considered to estimate the variations in foraging effort and thus energy expenditure. Great monthly variations in foraging effort and other activities were observed in both habitats. In early spring, when resource availabilities were maximal, foraging effort was low while monkeys maximized their feeding time (about 5 h/day). In June, during the peak of the birth season and the rearing period, monkeys minimized their feeding time to the benefit of social interactions (to 1.6–2.7 h/day), whatever the food availability, which was low in Akfadou and high in Djurdjura. In addition, foraging effort remained low in Djurdjura, while it increased in Akfadou. Thus, at the beginning of the dry summer period, monkeys in Akfadou were in a less favorable position than those in Djurdjura. At both sites, in periods of food shortage in summer or in winter, monkeys displayed two different strategies. In the former case, their foraging effort increased, while in the second one it remained relatively low. Whatever the foraging effort, monkeys did not reach the same amount of feeding time as in early spring. In the poorest site of Akfadou, foraging effort was globally greater than in the richest site of Djurdjura, especially for adults. At both sites, adult males spent more time feeding than juveniles and less time in social interactions. Results are discussed according to rearing period, temperatures, and day length constraints. The limits of adaptability to different habitats are considered in light of the demographic parameters. Am. J. Primatol. 43:285–304, 1997.

Dynamics of fission in a wild barbary macaque group (Macaca sylvanus)

We studied the dynamics of a group of Barbary macaques (Macaca sylvanus) in Algeria from March 1983 to November 1989. Troop fission began in autumn 1987, when group size had more than doubled, to include 76 animals. We observed 11 temporary splits of this group during the mating seasons of 1987 and 1988. The process was interrupted during the 1988 birth season. In June 1989, fission resumed and ended with the formation of three independent groups that included 50, 24, and 13 individuals. Adult females played an important role in the process of fission. They initiated the rapid formation of two, and later three, coherent nuclei, distributed in two or three bisexual subgroups; on several occasions these nuclei also formed subgroups without any adult males. Adult males remained together in a single nucleus for longer periods of time than females did. However, during fission, 35% (N=20) of resident males emigrated to neighboring groups, while 11 strange males immigrated into the focal group; over 6 years, 57% of the male transfers occurred after the beginning of the process. After group fission, maternally related individuals lived together in the new groups. The majority of resident males remained with the largest of the three groups, while most of the immigrant males were in another group. The third group included a single adult male. Possible factors that induce group fission are discussed.

A new 2CTAB/PCI method improves DNA amplification success from faeces of Mediterranean (Barbary macaques) and tropical (lowland gorillas) primates

Animal genomic DNA extracts of sufficient quality to address questions about population biology or behavioural ecology can be obtained from faeces when adequate extraction procedures are used. The presence of PCR inhibitors in extract products appears generally the main factor limiting DNA amplification success. We compared DNA amplification success from faeces of a tropical primate (western lowland gorilla, Gorilla g. gorilla) and a Mediterranean primate (Barbary macaque, Macaca sylvanus) between a standardized extraction technique widely used in animals (QIAamp® stool kit), a technique mainly used in plant species (CTAB) and a new protocol (2CTAB/PCI). Amplification success varied from 51% to 97%, the highest success being reached with the 2CTAB/PCI protocol in both species.

Genetic differentiation within and between isolated Algerian subpopulations of Barbary macaques (Macaca sylvanus): evidence from microsatellites

This study of wild‐living Algerian Barbary macaques (Macaca sylvanus) was designed to examine genetic variability in subpopulations isolated in residual forest patches, in an attempt to obtain data on the effects of habitat fragmentation. The wild population of this species (estimated at a maximum of 15 000) is vulnerable and this study therefore has direct relevance for conservation measures. Data from five microsatellite loci were analysed for 159 individuals from nine different groups living in four isolates in Algeria. Genetic polymorphism was found to be relatively high (4–12 alleles per locus) compared with other genetic markers used in previous studies of this species; mean expected heterozygosity was 65%. The four isolates are all genetically distinct (FST = 0; P < 0.001). Indeed, the results suggest that dispersal is limited even between some social groups within a single isolate. Genetic distances based on models not assuming stepwise mutation (FST and chord distance) gave very similar results and are highly correlated with geographical distances within one isolate but not between isolates. This may indicate that isolation by distance exerts a significant influence within an isolate but that genetic drift prevails between the four isolates. After allowing for variation in sample size, we found no evidence of reduced allelic diversity within small isolates that may have been separated for 250 years or more. The surviving population of Algerian Barbary macaques taken as a whole still shows marked variability in microsatellite alleles, but maintenance of genetic variability over the long term will surely require effective protection of all isolates.

Démographie et reproduction de Macaca sylvanus dans différents habitats en Algérie.

Usually described as a cedar forest monkey, the Barbary macaque in effect has colonized a great variety of habitat types. At the moment, it is not known to what extent these different habitats are suitable for the species’ survival. We tried to answer this question by comparing the demography of three monkey troops: one lives in a deciduous oak forest; the second lives in an nondeciduous cedar-green oak forest while the third is found on rocky ridges of mountains without any arborescent vegetation. In the three sites, there is a true seasonal breeding season with most births taking place in April to May and most matings occurring in November to December. Details are given on reproduction parameters (sexual activity of females; fertility rates; young survival...). Monkeys densities are higher in cedar forest than in deciduous forest. The smallest density is found on mountain ridges. Forest troops are more numerous, highly stable; their growth rate is better and the population is relatively young. The situation is slightly better still in the cedar forest than in the oak forest with a sex ratio more in favor of females and a better survival of the young. The troop of the mountain ridges is an unstable group ranging from 10 to 25 individuals; the population is aging, with a low birth rate and more male infants surviving compared with females. Demographic differences between sites are discussed according to climate, food availability and human influences (tree-clearing and overgrazing). Conclusions are drawn from this situation, for species conservation.

Dietary adaptations of temperate primates : comparisons of Japanese and Barbary macaques

Habitat, diet and leaf chemistry are compared between Japanese and Barbary macaques to reveal the similarities and differences in dietary adaptations of temperate primates living at the eastern and western extremes of the genus Macaca. Tree species diversity and proportion of fleshy-fruited species are much higher in Japan than in North Africa. Both species spend considerable annual feeding time on leaves. Japanese macaques prefer fruits and seeds over leaves, and Barbary macaques prefer seeds. These characteristics are adaptive in temperate regions where fruit availability varies considerably with season, since animals can survive during the lean period by relying on leaf and other vegetative foods. The two species are different with respect to the higher consumption of herbs by Barbary macaques, and the leaves consumed contain high condensed and hydrolysable tannin for Barbary but not for Japanese macaques. Barbary macaques supplement less diverse tree foods with herbs. Because of the low species diversity and high tannin content of the dominant tree species, Barbary macaques may have developed the capacity to cope with tannin. This supports the idea that digestion of leaves is indispensable to survive in temperate regions where fruit and seed foods are not available for a prolonged period during each year.

Ecology, demography, and population genetics of barbary macaques in Algeria

Over a 9-year period from 1982 to 1990 ecological and demographic data were collected on two genetic isolates of Barbary macaques (Macaca sylvanus) in Algeria, from the deciduous oak-forest of Akfadou and from the evergreen cedar-oak forest of the National Park Djurdjura. Macaques at Djurdjura profit from more suitable ecological conditions and have a higher rate of population increase as well as a higher male migration rate than those at Akfadou. Genetic data, gained from 23 genetic markers (blood proteins), proved to be highly influenced by the demographic structure of the groups. The macaque populations of Akfadou and Djurdjura have become genetically differentiated. Group fission, coupled with founder effect (genetic drift) and kin-structured (matrilineal) separation, resulted in a priori genetic diversity between one newly-established group and its parent group.