Jordi Salmona

Genomics and the challenging translation into conservation practice

The global loss of biodiversity continues at an alarming rate. Genomic approaches have been suggested as a promising tool for conservation practice as scaling up to genome-wide data can improve traditional conservation genetic inferences and provide qualitatively novel insights. However, the generation of genomic data and subsequent analyses and interpretations remain challenging and largely confined to academic research in ecology and evolution. This generates a gap between basic research and applicable solutions for conservation managers faced with multifaceted problems. Before the real-world conservation potential of genomic research can be realized, we suggest that current infrastructures need to be modified, methods must mature, analytical pipelines need to be developed, and successful case studies must be disseminated to practitioners.

Signature of a Pre-Human Population Decline in the Critically Endangered Reunion Island Endemic Forest Bird Coracina newtoni

The exceptional biodiversity of Reunion Island is threatened by anthropogenic landscape changes that took place during the 350 years of human colonization. During this period the human population size increased dramatically from 250 to 800,000. The arrival of humans together with the development of agriculture, invasive species such as rats and cats, and deforestation has lead to the extinction of more than half of the original vertebrate species of the island. For the remaining species, significant work is being carried out to identify threats and conservation status, but little genetic work has been carried on some of the most endangered species. In the last decade theoretical studies have shown the ability of neutral genetic markers to infer the demographic history of endangered species and identify and date past population size changes (expansions or bottlenecks). In this study we provide the first genetic data on the critically endangered species the Reunion cuckoo-shrike Coracina newtoni. The Reunion cuckoo-shrike is a rare endemic forest bird surviving in a restricted 12-km2 area of forested uplands and mountains. The total known population consists of less than one hundred individuals out of which 45 were genotyped using seventeen polymorphic microsatellite loci. We found a limited level of genetic variability and weak population structure, probably due to the limited geographic distribution. Using Bayesian methods, we identified a strong decline in population size during the Holocene, most likely caused by an ancient climatic or volcanic event around 5000 years ago. This result was surprising as it appeared in apparent contradiction with the accepted theory of recent population collapse due to deforestation and predator introduction. These results suggest that new methods allowing for more complex demographic models are necessary to reconstruct the demographic history of populations.

Effective population size dynamics and the demographic collapse of Bornean orang-utans.

Bornean orang-utans experienced a major demographic decline and local extirpations during the Pleistocene and Holocene due to climate change, the arrival of modern humans, of farmers and recent commercially-driven habitat loss and fragmentation. The recent loss of habitat and its dramatic fragmentation has affected the patterns of genetic variability and differentiation among the remaining populations and increased the extinction risk of the most isolated ones. However, the contribution of recent demographic events to such genetic patterns is still not fully clear. Indeed, it can be difficult to separate the effects of recent anthropogenic fragmentation from the genetic signature of prehistoric demographic events. Here, we investigated the genetic structure and population size dynamics of orang-utans from different sites. Altogether 126 individuals were analyzed and a full-likelihood Bayesian approach was applied. All sites exhibited clear signals of population decline. Population structure is known to generate spurious bottleneck signals and we found that it does indeed contribute to the signals observed. However, population structure alone does not easily explain the observed patterns. The dating of the population decline varied across sites but was always within the 200–2000 years period. This suggests that in some sites at least, orang-utan populations were affected by demographic events that started before the recent anthropogenic effects that occurred in Borneo. These results do not mean that the recent forest exploitation did not leave its genetic mark on orang-utans but suggests that the genetic pool of orang-utans is also impacted by more ancient events. While we cannot identify the main cause for this decline, our results suggests that the decline may be related to the arrival of the first farmers or climatic events, and that more theoretical work is needed to understand how multiple demographic events impact the genome of species and how we can assess their relative contributions.

Density Estimates of Two Endangered Nocturnal Lemur Species From Northern Madagascar: New Results and a Comparison of Commonly Used Methods

Very little information is known of the recently described Microcebus tavaratra and Lepilemur milanoii in the Daraina region, a restricted area in far northern Madagascar. Since their forest habitat is highly fragmented and expected to undergo significant changes in the future, rapid surveys are essential to determine conservation priorities. Using both distance sampling and capture–recapture methods, we estimated population densities in two forest fragments. Our results are the first known density and population size estimates for both nocturnal species. In parallel, we compare density results from four different approaches, which are widely used to estimate lemur densities and population sizes throughout Madagascar. Four approaches (King, Kelker, Muller and Buckland) are based on transect surveys and distance sampling, and they differ from each other by the way the effective strip width is estimated. The fifth method relies on a capture–mark–recapture (CMR) approach. Overall, we found that the King method produced density estimates that were significantly higher than other methods, suggesting that it generates overestimates and hence overly optimistic estimates of population sizes in endangered species. The other three distance sampling methods provided similar estimates. These estimates were similar to those obtained with the CMR approach when enough recapture data were available. Given that Microcebus species are often trapped for genetic or behavioral studies, our results suggest that existing data can be used to provide estimates of population density for that species across Madagascar. Am. J. Primatol. 74:414‐422, 2012.

New density estimates of a threatened sifaka species (Propithecus coquereli) in Ankarafantsika National Park

Propithecus coquereli is one of the last sifaka species for which no reliable and extensive density estimates are yet available. Despite its endangered conservation status [IUCN, 2012] and recognition as a flagship species of the northwestern dry forests of Madagascar, its population in its last main refugium, the Ankarafantsika National Park (ANP), is still poorly known. Using line transect distance sampling surveys we estimated population density and abundance in the ANP. Furthermore, we investigated the effects of road, forest edge, river proximity and group size on sighting frequencies, and density estimates. We provide here the first population density estimates throughout the ANP. We found that density varied greatly among surveyed sites (from 5 to ∼100 ind/km2) which could result from significant (negative) effects of road, and forest edge, and/or a (positive) effect of river proximity. Our results also suggest that the population size may be ∼47,000 individuals in the ANP, hinting that the population likely underwent a strong decline in some parts of the Park in recent decades, possibly caused by habitat loss from fires and charcoal production and by poaching. We suggest community‐based conservation actions for the largest remaining population of Coquerels sifaka which will (i) maintain forest connectivity; (ii) implement alternatives to deforestation through charcoal production, logging, and grass fires; (iii) reduce poaching; and (iv) enable long‐term monitoring of the population in collaboration with local authorities and researchers. Am. J. Primatol. 76:515–528, 2014.

Reply to Garner et al.

Genomics in Conservation : Case Studies and Bridging the Gap between Data and Application Reply

Noninvasive molecular sexing: An evaluation and validation of the SRY‐ and amelogenin‐based method in three new lemur species

Many lemur species are arboreal, elusive, and/or nocturnal and are consequently difficult to approach, observe and catch. In addition, most of them are endangered. For these reasons, non-invasive sampling is especially useful in primates including lemurs. A key issue in conservation and ecological studies is to identify the sex of the sampled individuals to investigate sex-biased dispersal, parentage, social organization and population sex ratio. Several molecular tests of sex are available in apes and monkeys, but only a handful of them work in the lemuriform clade. Among these tests, the coamplification of the SRY gene with the amelogenin X gene using strepsirhine-specific X primers seems particularly promising, but the reliability and validity of this sexing test have not been properly assessed yet. In this study, we (i) show that this molecular sexing test works on three additional lemur species (Microcebus tavaratra, Propithecus coronatus and P. verreauxi) from two previously untested genera and one previously untested family, suggesting that these markers are likely to be universal among lemurs and other strepsirrhines; (ii) provide the first evidence that this PCR-based sexing test works on degraded DNA obtained from noninvasive samples; (iii) validate the approach using a large number of known-sex individuals and a multiple-tubes approach, and show that mismatches between the field sex and the final molecular consensus sex occur in less than 10% of all the samples and that most of these mismatches were likely linked to incorrect sex determinations in the field rather than genotyping errors.

Genetic Diversity, Population Size, and Conservation of the Critically Endangered Perrier’s Sifaka (Propithecus perrieri)

Genetic data can be combined with ecological data to study the demographic history of a species, identify landscape features that influence migration patterns, and guide conservation efforts. Perrier’s sifaka (Propithecus perrieri) is a Critically Endangered, rare, and elusive social lemur living in a very restricted, fragmented landscape. To assess the effect of habitat loss and fragmentation on the genetic diversity of the Perrier’s sifaka population we examined 24 microsatellite markers genotyped for 67 samples corresponding to 42 individuals. Perrier’s sifaka shows a low current effective population size (ca. 52–105) and a strong heterozygosity excess, suggesting a historically large but dwindling population. Moreover, we identified a pattern of isolation by distance, typical of continuous habitat, suggesting that sifakas were still able to cross the grasslands between forest fragments in the recent past. Our study calls for a unified conservation plan covering the two protected areas where the species is still present, if not the whole area of its past distribution. Further studies inferring the past demographic history of Perrier’s sifaka may confirm the population decline and shed light on its potential causes.

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.