Génétique du paysage de populations fragmentées de lémuriens à Madagascar : conservation du propithèque à couronne dorée (Propithecus tattersalli) dans la région de Daraina

Parce que la fragmentation de l'habitat favorise la diminution de la taille des patches de ressources et la réduction de leur connectivité, ce processus est l'une des principales causes d'extinction des espèces en milieu tropical. Dans cette thèse, nous nous sommes intéressés au cas du propithèque à couronne dorée (Propithecus tattersalli), une espèce rare et menacée de lémurien du Nord-Est de Madagascar dont les populations évoluent dans un habitat forestier restreint et fortement fragmenté. Cette espèce sociale, endémique de la région enclavée de Daraina, n'a été découverte qu'il y a une vingtaine d'années (Simons 1988) et peu d'informations sont disponibles sur sa résilience à l'ouverture croissante de son habitat. Afin de fournir des informations pertinentes pour la mise en place de stratégies de conservation pour cette espèce, nous avons 1) étudié sa distribution et mesuré les densités des principales populations et 2) caractérisé sa structure génétique globale grâce au développement de marqueurs microsatellites spécifiques et à l'échantillonnage des fèces de 403 individus appartenant à 118 groupes sociaux répartis sur l'ensemble de l'aire de distribution. Les résultats des analyses démographiques suggèrent une importante variabilité de densité entre les fragments forestiers prospectés (entre 34 et 90 individus/km²) et une abondance totale du propithèque à couronne dorée comprise entre 11.000 et 26.000 individus, avec probablement plus de 18.000 individus. En combinant des analyses spatiales et génétiques, nous avons mis en évidence que la rivière Manankolana est à l'origine de la principale discontinuité génétique et joue probablement le rôle de barrière de flux de gènes pour cette espèce, alors que la route nationale non goudronnée semble peu entraver la dispersion des individus. Nos résultats suggèrent également une forte influence de l'isolement par la distance et une faible influence de la connectivité structurelle de l'habitat forestier sur les patterns de dispersion à l'échelle du paysage, même si l'une des populations au Nord de l'aire de distribution est très différenciée, suggérant un fort effet local de la fragmentation de l'habitat. À l'échelle des patches de ressources, nous avons observé un apparentement important à l'intérieur des groupes sociaux et mis en évidence que l'essentiel des dispersions se font entre groupes voisins, comme le suggèrent les données comportementales (Meyers 1993). Enfin, l'étude de l'histoire démographique de P. tattersalli a permis de mettre en évidence que les populations ont subi un goulot d'étranglement à une période située entre 1500 et 3000 ans BP, à l'origine d'une réduction drastique de la taille efficace de la population (de plusieurs milliers d'individus à quelques centaines d'individus par population). Ainsi, contrairement à ce qui a été observé pour d'autres espèces de lémuriens moins mobiles (Microcebus spp ; Lepilemur edwardsi), P. tattersalli n'a pas subi d'importantes réductions de taille au cours des derniers siècles, et a donc peu souffert de la déforestation anthropique récente. Lorsque nous confrontons nos résultats aux données paléoclimatiques, archéologiques et historiques disponibles pour le Nord de Madagascar, il apparaît que ce goulot d'étranglement pourrait être lié à la fois à l'aridification climatique de l'environnement avant l'arrivée des premiers hommes et aux dégradations anthropiques qui ont marqué le premier millénaire de colonisation par l'Homme. En effet, ces deux facteurs pourraient avoir contribué aux importantes modifications de l'habitat forestier et de la distribution des communautés de primates dans le Nord de Madagascar. Comme attendu pour une espèce non chassée, semi-arboricole et présentant une importante flexibilité de régime alimentaire, nos résultats semblent indiquer que P. tattersalli est relativement résilient au niveau actuel d'hétérogénéité de son habitat. Cependant, nous suggérons un suivi régulier de la viabilité des populations puisque leur habitat est très restreint et promis à d'importantes perturbations anthropiques dans les années à venir, comme le goudronnage de la route principale et l'installation d'une importante compagnie minière.Since habitat fragmentation reduces the size of habitat patches and decreases their level of connectivity, this process is among the greatest threats faced by species in tropical regions. Here, we studied the case of the golden-crowned sifaka (Propithecus tattersalli), a rare and threatened species of lemur from northeastern Madagascar, whose populations are only found in a small and highly fragmented forest habitat. This socially-organized species, endemic to the Daraina area, was only discovered twenty years ago (Simons, 1988) and little is know about its resiliency to the growing habitat openness. To provide relevant information to set up appropriate conservation strategies for this species, we 1) studied its distribution and assessed the density of its main populations and 2) characterized its global genetic structure isolating new specific microsatellites and collecting faeces from 403 putative individuals (118 social groups) sampling in the whole distribution area. The results of the demographic analyses suggest a large heterogeneity of density among surveyed forest patches (between 34 and 90 individuals/km²) and a total species size between 11,000 and 26,000 individuals and most likely above 18,000 individuals. Combining spatial and genetic analyses, we showed that the Manankolana River is the main geographical feature shaping P. tattersalli 's genetic diversity, and that it probably played a role as a barrier to gene flow whereas the national road does not seem to strongly impede the dispersal of individuals. Our results also suggested a strong influence of the isolation by distance and a weak influence of the forest habitat structural connectivity on dispersal patterns at the landscape scale even though one of the population in north of the distribution area is highly differentiated suggesting a strong local impact of habitat fragmentation. At the resource patch scale, we found that individuals within social groups are closely related and that most of the dispersal events occur between adjacent social groups as suggested by behavioural information (Meyers, 1993). Lastly, the study of the P. tattersalli demographic history revealed that the populations underwent a bottleneck at a period between 1500 and 3000 years ago leading to a drastic reduction of effective population size (from several thousand individuals to a few hundred individuals per population). Thus, contrary to what was observed for other less mobile lemur species such as Microcebus spp. or Lepilemur edwardsi, P. tattersalli probably did not undergo a strong population collapse in the last centuries and thus did not suffer from recent anthropogenic deforestation. Using paleoclimatic, archaeological and historical data from the North of Madagascar, it appears that the uncovered bottleneck could be related to both climate desiccation of the environment in pre-human times and to anthropogenic degradation during the first millennium of human colonization. Indeed, both could have contributed to a large shift of forest habitat and primate communities' distribution that is observed in the north of the Island. As expected for a non hunted and semi-arboreal species exhibiting large feeding behaviour flexibility, our results suggested that P. tattersalli is relatively resilient to the current level of habitat heterogeneity. However, we suggest a regular monitoring of the populations viability since their habitat is very small and is likely to be affected by large anthropogenic disturbances in near future such as the tarring of the national road and the installation of an important gold mining company)

Propithecus_tattersalli_GPS_coordinates

This file contains the geographic coordinates of the 230 Propithecus tattersalli individuals genotyped and studied in the current paper as well as in Quéméré et al., 2010, 2012. The individuals ID correspond to those in the genetic data file. For further details see Quemere, Erwan, et al. "Landscape genetics of an endangered lemur (Propithecus tattersalli) within its entire fragmented range." Molecular Ecology 19.8 (2010): 1606-1621.and Quéméré, Erwan, et al. "Genetic data suggest a natural prehuman origin of open habitats in northern Madagascar and question the deforestation narrative in this region." Proceedings of the National Academy of Sciences 109.32 (2012): 13028-13033

Climate change and human colonization triggered habitat loss and fragmentation in Madagascar

International audienceThe relative effect of past climate fluctuations and anthropogenic activities on current biome distribution is subject to increasing attention, notably in biodiversity hot spots. In Madagascar, where humans arrived in the last similar to 4 to 5,000years, the exact causes of the demise of large vertebrates that cohabited with humans are yet unclear. The prevailing narrative holds that Madagascar was covered with forest before human arrival and that the expansion of grasslands was the result of human-driven deforestation. However, recent studies have shown that vegetation and fauna structure substantially fluctuated during the Holocene. Here, we study the Holocene history of habitat fragmentation in the north of Madagascar using a population genetics approach. To do so, we infer the demographic history of two northern Madagascar neighbouring, congeneric and critically endangered forest dwelling lemur speciesPropithecus tattersalli and Propithecus perrieriusing population genetic analyses. Our results highlight the necessity to consider population structure and changes in connectivity in demographic history inferences. We show that both species underwent demographic fluctuations which most likely occurred after the mid-Holocene transition. While mid-Holocene climate change probably triggered major demographic changes in the two lemur species range and connectivity, human settlements that expanded over the last four millennia in northern Madagascar likely played a role in the loss and fragmentation of the forest cover

Data from: Climate change and human colonization triggered habitat loss and fragmentation in Madagascar.

The relative effect of past climate fluctuations and anthropogenic activities on current biome distribution is subject to increasing attention, notably in biodiversity hot spots. In Madagascar, where humans arrived in the last ~4 to 5,000 years, the exact causes of the demise of large vertebrates that cohabited with humans are yet unclear. The prevailing narrative holds that Madagascar was covered with forest before human arrival and that the expansion of grasslands was the result of human-driven deforestation. However, recent studies have shown that vegetation and fauna structure substantially fluctuated during the Holocene. Here, we study the Holocene history of habitat fragmentation in the north of Madagascar using a population genetics approach. To do so, we infer the demographic history of two northern Madagascar neighbouring, congeneric and critically endangered forest dwelling lemur species—Propithecus tattersalli and Propithecus perrieri—using population genetic analyses. Our results highlight the necessity to consider population structure and changes in connectivity in demographic history inferences. We show that both species underwent demographic fluctuations which most likely occurred after the mid-Holocene transition. While mid-Holocene climate change probably triggered major demographic changes in the two lemur species range and connectivity, human settlements that expanded over the last four millennia in northern Madagascar likely played a role in the loss and fragmentation of the forest cover

Propithecus_perrieri_GPS_coordinates

This file contains the geographic coordinates of the 42 Propithecus perrieri individuals genotyped and studied in the current paper as well as in Salmona et al., 2015. The individuals ID correspond to those in the genetic data file. Salmona, J, et al. "Genetic Diversity, Population Size, and Conservation of the Critically Endangered Perrier’s Sifaka (Propithecus perrieri)." International Journal of Primatology 36.6 (2015): 1132-1153

Propithecus_perrieri_24loci_3pop

This file contains the microsatellite genotype data used in the current paper as well as in Salmona et al. 2015. The file is in .gtx format and can be opened and analyzed easily in Genetix, R, or with a common text editor. The file contains the data of 42 Propithecus perrieri individuals genotyped over 24 polymorphic microsatellites markers. The individuals are further classified in three "populations" that relates to sampling sites. Salmona et al. 2015 showed little differentiation between the three sampling sites, therefore the three "population" individuals can not be considered as belonging to the same population. A file containing the geographic coordinates of the samples is associated to this file. For further details on how the data was generated see Salmona, Jordi, et al. "Genetic Diversity, Population Size, and Conservation of the Critically Endangered Perrier’s Sifaka (Propithecus perrieri)." International Journal of Primatology 36.6 (2015): 1132-1153

Propithecus_tattersalli_230ind_13loc

This file contains the microsatellite genotype data used in the current paper as well as in Quéméré et al 2010, 2012. The file is in .gtx format and can be opened and analyzed easily in Genetix, R, or with a common text editor. The file contains the data of 230 Propithecus tatersalli individuals genotyped over 13 polymorphic microsatellites markers. The individuals are further classified in three "populations" that relates to the main genetic structure described in Quéméré et al 2010. A file containing the geographic coordinates of the samples is associated to this file. For further details on how the data was generated see Quemere, Erwan, et al. "Landscape genetics of an endangered lemur (Propithecus tattersalli) within its entire fragmented range." Molecular Ecology 19.8 (2010): 1606-1621.and Quéméré, Erwan, et al. "Genetic data suggest a natural prehuman origin of open habitats in northern Madagascar and question the deforestation narrative in this region." Proceedings of the National Academy of Sciences 109.32 (2012): 13028-13033

Genetic consequences of social structure in the golden-crowned sifaka

International audienceMany species are structured in social groups (SGs) where individuals exhibit complex mating strategies. Yet, most population genetic studies ignore SGs either treating them as small random-mating units or focusing on a higher hierarchical level (the population). Empirical studies acknowledging SGs have found an overall excess of heterozygotes within SGs and usually invoke inbreeding avoidance strategies to explain this finding. However, there is a lack of null models against which ecological theories can be tested and inbreeding avoidance quantified. Here, we investigateinbreeding(deviation from random mating) in an endangered forest-dwelling pair-living lemur species (Propithecus tattersalli). In particular, we measure the inbreeding coefficient (F-IS) in empirical data at different scales: SGs, sampling sites and forest patches. We observe high excess of heterozygotes within SGs. The magnitude of this excess is highly dependent on the sampling scheme: while offspring are characterised by a high excess of heterozygotes (F-IS < 0), the reproductive pair does not show dramatic departures from Hardy-Weinberg expectations. Moreover, the heterozygosity excess disappears at larger geographic scales (sites and forests). We use a modelling framework that incorporates details of the sifaka mating system but does not include active inbreeding avoidance mechanisms. The simulated data show that, although apparent "random mating" or eveninbreedingmay occur at the "population" level, outbreeding is maintained within SGs. Altogether our results suggest that social structure leads to high levels of outbreeding without the need for active inbreeding avoidance mechanisms. Thus, demonstrating and measuring the existence of active inbreeding avoidance mechanisms may be more difficult than usually assumed

Data from: The demographic history of populations experiencing asymmetric gene flow: combining simulated and empirical data.

Population structure can significantly affect genetic-based demographic inferences, generating spurious bottleneck-like signals. Previous studies have typically assumed island or stepping-stone models, which are characterized by symmetric gene flow. However, many organisms are characterized by asymmetric gene flow. Here, we combined simulated and empirical data to test whether asymmetric gene flow affects the inference of past demographic changes. Through the analysis of simulated genetic data with three methods (i.e. bottleneck, M-ratio and msvar), we demonstrated that asymmetric gene flow biases past demographic changes. Most biases were towards spurious signals of expansion, albeit their strength depended on values of effective population size and migration rate. It is noteworthy that the spurious signals of demographic changes also depended on the statistical approach underlying each of the three methods. For one of the three methods, biases induced by asymmetric gene flow were confirmed in an empirical multispecific data set involving four freshwater fish species (Squalius cephalus, Leuciscus burdigalensis, Gobio gobio and Phoxinus phoxinus). However, for the two other methods, strong signals of bottlenecks were detected for all species and across two rivers. This suggests that, although potentially biased by asymmetric gene flow, some of these methods were able to bypass this bias when a bottleneck actually occurred. Our results show that population structure and dispersal patterns have to be considered for proper inference of demographic changes from genetic data

The demographic history of populations experiencing asymmetric gene flow: combining simulated and empirical data

International audiencePopulation structure can significantly affect genetic-based demographic inferences, generating spurious bottleneck-like signals. Previous studies have typically assumed island or stepping-stone models, which are characterized by symmetric gene flow. However, many organisms are characterized by asymmetric gene flow. Here, we combined simulated and empirical data to test whether asymmetric gene flow affects the inference of past demographic changes. Through the analysis of simulated genetic data with three methods (i.e. bottleneck, M-ratio and msvar), we demonstrated that asymmetric gene flow biases past demographic changes. Most biases were towards spurious signals of expansion, albeit their strength depended on values of effective population size and migration rate. It is noteworthy that the spurious signals of demographic changes also depended on the statistical approach underlying each of the three methods. For one of the three methods, biases induced by asymmetric gene flow were confirmed in an empirical multispecific data set involving four freshwater fish species (Squalius cephalus, Leuciscus burdigalensis, Gobio gobio and Phoxinus phoxinus). However, for the two other methods, strong signals of bottlenecks were detected for all species and across two rivers. This suggests that, although potentially biased by asymmetric gene flow, some of these methods were able to bypass this bias when a bottleneck actually occurred. Our results show that population structure and dispersal patterns have to be considered for proper inference of demographic changes from genetic data