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Revealing the maternal demographic history of Panthera leo using ancient DNA and a spatially explicit genealogical analysis.

ABSTRACT: BACKGROUND: Understanding the demographic history of a population is critical to conservation and to our broader understanding of evolutionary processes. For many tropical large mammals, however, this aim is confounded by the absence of fossil material and by the misleading signal obtained from genetic data of recently fragmented and isolated populations. This is particularly true for the lion which as a consequence of millennia of human persecution, has large gaps in its natural distribution and several recently extinct populations. RESULTS: We sequenced mitochondrial DNA from museum-preserved individuals, including the extinct Barbary lion (Panthera leo leo) and Iranian lion (P. l. persica), as well as lions from West and Central Africa. We added these to a broader sample of lion sequences, resulting in a data set spanning the historical range of lions. Our Bayesian phylogeographical analyses provide evidence for highly supported, reciprocally monophyletic lion clades. Using a molecular clock, we estimated that recent lion lineages began to diverge in the Late Pleistocene. Expanding equatorial rainforest probably separated lions in South and East Africa from other populations. West African lions then expanded into Central Africa during periods of rainforest contraction. Lastly, we found evidence of two separate incursions into Asia from North Africa, first into India and later into the Middle East. CONCLUSIONS: We have identified deep, well-supported splits within the mitochondrial phylogeny of African lions, arguing for recognition of some regional populations as worthy of independent conservation. More morphological and nuclear DNA data are now needed to test these subdivisions.

SUBMITTER: Barnett R

PROVIDER: S-EPMC3997813 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Revealing the maternal demographic history of Panthera leo using ancient DNA and a spatially explicit genealogical analysis.

Barnett Ross R Yamaguchi Nobuyuki N Shapiro Beth B Ho Simon Y W SY Barnes Ian I Sabin Richard R Werdelin Lars L Cuisin Jacques J Larson Greger G

BMC evolutionary biology 20140402 1

<h4>Background</h4>Understanding the demographic history of a population is critical to conservation and to our broader understanding of evolutionary processes. For many tropical large mammals, however, this aim is confounded by the absence of fossil material and by the misleading signal obtained from genetic data of recently fragmented and isolated populations. This is particularly true for the lion which as a consequence of millennia of human persecution, has large gaps in its natural distribu ...[more]

PMID: 24690312

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Project description:Background:The long-term success of ex-situ conservation programmes depends on species-appropriate husbandry and enrichment practices complemented by an accurate welfare assessment protocol. Zoos and conservation breeding programmes should employ a bottom-up approach to account for intraspecific variations in measures of animal welfare. We studied 35 (14:21) captive Asiatic lions in Sakkarbaug Zoological Garden, Junagadh, India to understand the implications of individual variations on welfare measures. We categorized the subjects based on personality traits (bold or shy), rearing history (wild-rescued or captive-raised), sex, and social-grouping. We explored the association of these categorical variables on welfare indices such as behavioural diversity, latency to approach novel objects, enclosure usage and aberrant repetitive behaviours. Further, we assessed the inter-relationships between different behavioural measures of welfare. Results:Our results show that intraspecific variations based on rearing-history and personality traits are significantly associated with the welfare states of captive Asiatic lions. Asiatic lions with bold personality traits (M = 0.50, SD = 0.12, N = 21) and those raised in captivity (M = 0.47, SD = 0.12, N = 16) used enclosure space more homogenously compared to shy (M = 0.71, SD = 0.15, N = 14) and wild-rescued (M = 0.67, SD = 0.15, N = 19) animals. Behaviour diversity was significantly higher in captive-raised (M = 1.26, SD = 0.3, N = 16) and bold (M = 1.23, SD = 0.26, N = 21) subjects compared to wild-rescued (M = 0.83, SD = 0.35, N = 19) and shy (M = 0.73, SD = 0.34, N = 14) individuals. Aberrant repetitive behaviours (stereotypy) were significantly lower in bold (M = 7.01, SD = 4, N = 21) and captive-raised (M = 7.74, SD = 5.3) individuals compared to wild-rescued (M = 13.12, SD = 6.25, N = 19) and shy (M = 16.13, SD = 5.4, N = 16) lions. Sex and social-grouping of subjects did not show significant associations with behavioural welfare indices. Interestingly, behaviour diversity was reliably predicted by the enclosure usage patterns and aberrant repetitive behaviours displayed by subjects. Discussion:Our findings underline the importance of individual-centric, behaviour-based, and multi-dimensional welfare assessment approaches in ex-situ conservation programmes. The results suggest that behavioural welfare indices complemented with individual variations can explain inter-individual differences in behavioural welfare measure outcomes of Asiatic lions. These findings also provide zoo managers with a non-invasive tool to reliably assess and improve husbandry practices for Asiatic lions. Understanding the unique welfare requirement of individuals in captivity will be crucial for the survival of the species.

Project description:Recent advances in sequencing technologies have allowed for the retrieval of ancient DNA data (aDNA) from skeletal remains, providing direct genetic snapshots from diverse periods of human prehistory. Comparing samples taken in the same region but at different times, hereafter called "serial samples", may indicate whether there is continuity in the peopling history of that area or whether an immigration of a genetically different population has occurred between the two sampling times. However, the exploration of genetic relationships between serial samples generally ignores their geographical locations and the spatiotemporal dynamics of populations. Here, we present a new coalescent-based, spatially explicit modelling approach to investigate population continuity using aDNA, which includes two fundamental elements neglected in previous methods: population structure and migration. The approach also considers the extensive temporal and geographical variance that is commonly found in aDNA population samples.We first showed that our spatially explicit approach is more conservative than the previous (panmictic) approach and should be preferred to test for population continuity, especially when small and isolated populations are considered. We then applied our method to two mitochondrial datasets from Germany and France, both including modern and ancient lineages dating from the early Neolithic. The results clearly reject population continuity for the maternal line over the last 7500 years for the German dataset but not for the French dataset, suggesting regional heterogeneity in post-Neolithic migratory processes.Here, we demonstrate the benefits of using a spatially explicit method when investigating population continuity with aDNA. It constitutes an improvement over panmictic methods by considering the spatiotemporal dynamics of genetic lineages and the precise location of ancient samples. The method can be used to investigate population continuity between any pair of serial samples (ancient-ancient or ancient-modern) and to investigate more complex evolutionary scenarios. Although we based our study on mitochondrial DNA sequences, diploid molecular markers of different types (DNA, SNP, STR) can also be simulated with our approach. It thus constitutes a promising tool for the analysis of the numerous aDNA datasets being produced, including genome wide data, in humans but also in many other species.

Project description:The retrieval of ancient DNA from osteological material provides direct evidence of human genetic diversity in the past. Ancient DNA samples are often used to investigate whether there was population continuity in the settlement history of an area. Methods based on the serial coalescent algorithm have been developed to test whether the population continuity hypothesis can be statistically rejected by analysing DNA samples from the same region but of different ages. Rejection of this hypothesis is indicative of a large genetic shift, possibly due to immigration occurring between two sampling times. However, this approach is only able to reject a model of full continuity model (a total absence of genetic input from outside), but admixture between local and immigrant populations may lead to partial continuity. We have recently developed a method to test for population continuity that explicitly considers the spatial and temporal dynamics of populations. Here, we extended this approach to estimate the proportion of genetic continuity between two populations, using ancient genetic samples. We applied our original approach to the question of the Neolithic transition in Central Europe. Our results confirmed the rejection of full continuity, but our approach represents an important step forward by estimating the relative contribution of immigrant farmers and of local hunter-gatherers to the final Central European Neolithic genetic pool. Furthermore, we show that a substantial proportion of genes brought by the farmers in this region were assimilated from other hunter-gatherer populations along the way from Anatolia, which was not detectable by previous continuity tests. Our approach is also able to jointly estimate demographic parameters, as we show here by finding both low density and low migration rate for pre-Neolithic hunter-gatherers. It provides a useful tool for the analysis of the numerous ancient DNA data sets that are currently being produced for many different species.

Dataset Information

Revealing the maternal demographic history of Panthera leo using ancient DNA and a spatially explicit genealogical analysis.

Publications

Revealing the maternal demographic history of Panthera leo using ancient DNA and a spatially explicit genealogical analysis.

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