Publications

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    ABSTRACT: 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. 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. 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.
    BMC Evolutionary Biology 01/2014; 14(1):70. · 3.29 Impact Factor
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    ABSTRACT: Estimations of species extinction dates are rarely definitive, yet declarations of extinction or extirpation are important as they define when conservation efforts may cease. Erroneous declarations of extinctions not only destabilize conservation efforts but also corrode local community support. Mismatches in perceptions by the scientific and local communities risk undermining sensitive, but important partnerships. We examine observations relating to the decline and extinction of Barbary lions in North Africa. Whilst the extinction predates the era of the scientific conservation movement, the decline is relatively well documented in historical records. Recently unearthed accounts suggest Barbary lions survived later than previously assumed. We use probabilistic methods to estimate a more recent extinction date for the subspecies. The evidence presented for a much later persistence of lions in North Africa, including generations when sightings were nil, suggests caution when considering felid populations as extinct in the wild. The case raises the possibility that captive animals descended from the Moroccan royal collection are closer contemporaries to wild Barbary lions. Furthermore, our results highlight the vulnerability of very small lion populations and the significance of continued conservation of remnant lion populations in Central and West Africa.
    PLoS ONE 04/2013; 8(4). · 3.53 Impact Factor
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    ABSTRACT: Recent advances in multivariate statistics, and in ancient DNA techniques, have greatly increased understanding of tiger phylogeography. However, regardless of advances in analytical methodology, researchers will continue to need access to specimens for morphological measurements and sampling for genetic analysis. The tiger has become increasingly endangered, and out of the nine putative tiger subspecies, three (Javan, Balinese, and Caspian) have become extinct in the last 100 years, leaving the specimens kept in natural history collections as the only materials available for research. Frustratingly little information is widely available concerning the specimens of these extinct tiger subspecies. We conducted an extensive search for specimens of extinct tiger subspecies, and also developed a simple on-site method to assign unprovenanced and probable Indonesian specimens to either Javan/Balinese or Sumatran subspecies. We located a total of 88 Javan, 11 Balinese, and 46 Caspian tigers, including seven new Javan tigers, and three Balinese tigers that were not widely known previously. These specimens are critical for research in order to understand the intraspecific phylogeny and evolutionary history of the tiger.
    Mammal Study 01/2013; 38:187-198. · 0.67 Impact Factor
  • Nobuyuki Yamaguchi, Afra Al-Hajri, Hayat Al-Jabiri
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    ABSTRACT: There is little information pertaining to the breeding behaviour and reproductive biology of free-ranging hedgehog populations outside of Europe. We monitored the seasonal changes in courtship behaviour and the presence of new young animals from a free-ranging Ethiopian hedgehog population in Qatar between 2010 and 2012. Based on frequencies of courtship behaviour and deduced frequencies of successful mating, the mating season of the Ethiopian hedgehog is believed to start in January and continue through until July with a clear peak during the February/March period. We propose the existence of two mating peaks, one in February/March and the second in June, suggesting that free-ranging Ethiopian hedgehogs breed more than twice a year in Qatar. Successful mating in late winter/early spring may be more important for the increasing the inclusive fitness of the parents based on the number of young individuals that survive beyond one month of age.
    Journal of Arid Environments 01/2013; 99:1–4. · 1.77 Impact Factor
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    ABSTRACT: The wildcat (Felis silvestris ssp.) is a conservation concern largely due to introgressive hybridization with its congener F. s. catus, the common domestic cat. Because of a recent divergence and entirely overlapping ranges, hybridization is common and pervasive between these taxa threatening the genetic integrity of remaining wildcat populations. Identifying pure wildcats for inclusion in conservation programs using current morphological discriminants is difficult because of gross similarity between them and the domestic, critically hampering conservation efforts. Here, we present a vetted panel of microsatellite loci and mitochondrial polymorphisms informative for each of the 5 naturally evolved wildcat subspecies and the derived domestic cat. We also present reference genotypes for each assignment class. Together, these marker sets and corresponding reference genotypes allow for the development of a genetic rational for defining "units of conservation" within a phylogenetically based taxonomy of the entire F. silvestris species complex. We anticipate this marker panel will allow conservators to assess genetic integrity and quantify admixture in managed wildcat populations and to be a starting point for more in-depth analysis of hybridization.
    The Journal of heredity 01/2011; 102 Suppl 1:S87-90. · 2.05 Impact Factor
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    ABSTRACT: The last representatives of the Barbary lion (Panthera leo leo), once numerous in North Africa but exterminated from the wild by the 1940s, are believed to be the captive lions descended from the Moroccan Royal Collection, numbering less than 90 animals in zoos worldwide. The genetic fitness of these captive “Royal Lions” may now be under threat since, although most zoos have avoided hybridisation with animals of other origin, no formal breeding programme currently exists and several institutions have halted breeding activities. This situation has arisen since the distinctiveness of Barbary lions and the representative status of Royal Lions remain inconclusive and definitive molecular studies have yet to be completed. Previously, in the 1970s, morphological and phenotypic traits were used to match Royal Lions and the historic Barbary lion and an ex situ breeding programme was initiated involving a number of selected “founder” animals. This paper outlines the status of the descendent population within zoos in Morocco and Europe, including all known pure-bred descendents from the Royal Palace collection. Founder representation is shown to be greater across European collections than the Moroccan collection. Breeding exchanges are recommended between institutions in order to improve genetic diversity and maintain the genetic health of the population and a studbook for European zoo animals has been developed to support this action. This analysis serves as a benchmark for guiding effective maintenance of the captive population, thereby allowing time to clarify the conservation value of Royal Lions and their relevance to North African ecology.
    European Journal of Wildlife Research 01/2010; 56(1):21-31. · 1.36 Impact Factor
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    ABSTRACT: Intraspecific encephalization of the lion and the tiger is investigated for the first time using a very large sample. Using cranial volume as a measure of brain size, the tiger has a larger brain relative to greatest length of skull than the lion, the leopard and the jaguar. The Asian lion has a relatively much smaller brain compared with those of sub-Saharan lions, between which there are few differences. The Balinese and Javan tigers had relatively larger brains compared with those of Malayan and Sumatran tigers, even although these four putative subspecies occupy adjacent ranges in south-eastern Asia. Differences in brain size do not appear to correlate with any known differences in behaviour and ecology and, therefore, may reflect only chance differences in intrageneric and intraspecific phylogeny. However, captive-bred big cats generally have a reduced brain size compared with that of wild animals, so that an animal's life history and living conditions may affect brain size and, hence, functional or environmental explanations should be considered when linking brain size differences to intraspecific phylogenies. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 85–93.
    Biological Journal of the Linnean Society 08/2009; 98(1):85 - 93. · 2.41 Impact Factor
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    ABSTRACT: In order to conserve mammalian top predators in human-dominated landscapes, large scale habitat requirements and food habits of the Japanese weasel (Mustela itatsi) were studied using 237 faecal samples, from a 901 km2 area in the vicinity of Mito City, Ibaraki Prefecture, Japan between 1999 and 2001. Findings show a significant difference in the faeces distribution among the nine biotope types surveyed, with a marked preference for rice fields and conifer plantations, coupled with an avoidance of farming and urban areas. In terms of weasel diet, mammals occured most frequently in relative volume and single occupancy in faeces and most often observed in conifer plantations along river banks. Second, Orthoptera insects, crustaceans, fruits, Coleoptera insects and fish were also found both in high frequency and relative volume, most often in rice fields and riparian habitats along river banks. Third, a high frequency of occurrence among combinations of (1) mammals with Coleoptera insects and (2) crustaceans with Orthoptera insects suggests the necessity of interaction among habitats. Artificial items were rare. These patterns provide evidence that weasels require diverse landscapes and further suggest weasels do not use urban areas because of their predatory preference for fresh animal food. This has implications for weasel conservation strategies.
    Mammal Study 07/2009; · 0.67 Impact Factor
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    ABSTRACT: The American mink, Neovison vison, is an established, alien invasive species in the United Kingdom that originally colonized the country at a time when two native mustelids (otters, Lutra lutra, and polecats, Mustela putorius) were largely absent. Both of these species are now recovering their populations nationally. We compared the relative abundance and the behavior of mink in the 1990s and in the 2000s in an area of southern England where both otters and polecats were absent in the 1990s but reappeared in the intervening years. We found that mink were still abundant in the 2000s in the presence of otters and polecats, but that they appeared to have altered some aspects of their behavior. In accordance with previous studies, we found that mink consumed fewer fish in the presence of otters. We also found that mink were predominantly nocturnal in the 1990s (in the absence of competitors) but were predominantly diurnal in the 2000s (in the presence of competitors). We hypothesize that this temporal shift may be an avoidance mechanism allowing the coexistence of mink with the otter and the polecat, although we are unable to attribute the shift to one or the other species. We also found that mink in the presence of competitors weighed less but remained the same size, suggesting the possibility of a competitor-mediated decline in overall body condition. This is one of very few field studies demonstrating a complete temporal shift in apparent response to competitors. The implications of this study are that recovering otter populations may not lead to significant and long-term reductions in the number of invasive mink in the United Kingdom as has been suggested in the media, although we cannot exclude the possibility of a decline in mink in the longer-term.
    Ecology 06/2009; 90(5):1207-16. · 5.18 Impact Factor
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    ABSTRACT: Lions were the most widespread carnivores in the late Pleistocene, ranging from southern Africa to the southern USA, but little is known about the evolutionary relationships among these Pleistocene populations or the dynamics that led to their extinction. Using ancient DNA techniques, we obtained mitochondrial sequences from 52 individuals sampled across the present and former range of lions. Phylogenetic analysis revealed three distinct clusters: (i) modern lions, Panthera leo; (ii) extinct Pleistocene cave lions, which formed a homogeneous population extending from Europe across Beringia (Siberia, Alaska and western Canada); and (iii) extinct American lions, which formed a separate population south of the Pleistocene ice sheets. The American lion appears to have become genetically isolated around 340 000 years ago, despite the apparent lack of significant barriers to gene flow with Beringian populations through much of the late Pleistocene. We found potential evidence of a severe population bottleneck in the cave lion during the previous interstadial, sometime after 48 000 years, adding to evidence from bison, mammoths, horses and brown bears that megafaunal populations underwent major genetic alterations throughout the last interstadial, potentially presaging the processes involved in the subsequent end-Pleistocene mass extinctions.
    Molecular Ecology 04/2009; 18(8):1668-77. · 6.28 Impact Factor
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    ABSTRACT: The Caspian tiger (Panthera tigris virgata) flourished in Central Asian riverine forest systems in a range disjunct from that of other tigers, but was driven to extinction in 1970 prior to a modern molecular evaluation. For over a century naturalists puzzled over the taxonomic validity, placement, and biogeographic origin of this enigmatic animal. Using ancient-DNA (aDNA) methodology, we generated composite mtDNA haplotypes from twenty wild Caspian tigers from throughout their historic range sampled from museum collections. We found that Caspian tigers carry a major mtDNA haplotype differing by only a single nucleotide from the monomorphic haplotype found across all contemporary Amur tigers (P. t. altaica). Phylogeographic analysis with extant tiger subspecies suggests that less than 10,000 years ago the Caspian/Amur tiger ancestor colonized Central Asia via the Gansu Corridor (Silk Road) from eastern China then subsequently traversed Siberia eastward to establish the Amur tiger in the Russian Far East. The conservation implications of these findings are far reaching, as the observed genetic depletion characteristic of modern Amur tigers likely reflects these founder migrations and therefore predates human influence. Also, due to their evolutionary propinquity, living Amur tigers offer an appropriate genetic source should reintroductions to the former range of the Caspian tiger be implemented.
    PLoS ONE 02/2009; 4(1):e4125. · 3.53 Impact Factor
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    ABSTRACT: A divided infraorbital foramen is an important morphological feature in lion taxonomy and has previously been considered to occur only in the Asian lion, Panthera leo persica. Based on an examination of 498 lion skulls from museum collections in Europe and southern Africa, we report for the first time on the prevalence of the divided infraorbital foramen in African lions, as well as its occurrence in the tiger, P. tigris and the extinct Pleistocene European cave lion, P. leo spelaea. The higher frequency of this characteristic in Asian lions may have occurred after the lion colonised Asia, and can be considered an important morphological feature characterising this population. It is not clear whether recent anthropogenic population bottlenecks have influenced changes in its prevalence over the last 200 years.
    Contributions To Zoology - CONTRIB ZOOL. 01/2009; 78(2):77-83.
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    ABSTRACT: A territorial intruder often poses more of a threat to the territory holder of the same sex as itself. As territorial aggression is associated with costs, aggression shown by birds towards territorial intruders of the opposite sex deserves investigation. This behaviour could arise due to the reproductive value of a mate or through mutualism between members of a pair. We investigated these hypotheses by presenting mated pairs of Tawny Owls Strix aluco with playback of male calls, female calls and a male and female duetting, and recording the number and intensity of responses by the male and female territory holders. Females responded significantly more often to female than to male calls. Males responded equally often to male and female playback. Males which had previously bred successfully with their mate were significantly more likely to respond to female playback in the spring, which suggested males were responding to female playback due to the reproductive value of their mate. There was no evidence of mutualism between members of a pair.
    Ibis 06/2008; 141(1):91 - 99. · 2.36 Impact Factor
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    Ross Barnett, Nobuyuki Yamaguchi, Beth Shapiro, Richard Sabin
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    ABSTRACT: The Royal Menagerie of England was established at the Tower of London in the 13 th Century and served as a home of exotic animals until it was closed on behalf of the Duke of Wellington in 1835. Two well-preserved lion skulls recovered from the moat of the Tower of London were recently radiocarbon-dated to AD 1280-1385 and AD 1420-1480, making them the earliest confirmed lion remains in the British Isles since the extinction of the Pleistocene cave lion. Using ancient DNA techniques and cranio-morphometric analysis, we identify the source of these first English lions to lie in North Africa, where no natural lion population remains today.
    Contributions to zoology Bijdragen tot de dierkunde 01/2008; 77:7-16. · 2.45 Impact Factor
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    ABSTRACT: The world's domestic cats carry patterns of sequence variation in their genome that reflect a history of domestication and breed development. A genetic assessment of 979 domestic cats and their wild progenitors-Felis silvestris silvestris (European wildcat), F. s. lybica (Near Eastern wildcat), F. s. ornata (central Asian wildcat), F. s. cafra (southern African wildcat), and F. s. bieti (Chinese desert cat)-indicated that each wild group represents a distinctive subspecies of Felis silvestris. Further analysis revealed that cats were domesticated in the Near East, probably coincident with agricultural village development in the Fertile Crescent. Domestic cats derive from at least five founders from across this region, whose descendants were transported across the world by human assistance.
    Science 08/2007; 317(5837):519-23. · 31.20 Impact Factor
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    R. Barnett, N. Yamaguchi, B. Shapiro, V. Nijman
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    ABSTRACT: In natural history collections throughout Europe, there are many old lion specimens of unknown origin. If these specimens can be shown to have originated from now-extinct populations their value would significantly increase, as would the value of the collections. Recently, a 200-year old mounted skeleton in the Zoological Museum Amsterdam has been identified as the extinct Cape lion Panthera leo melanochaita (Smith, 1842), based primarily on morphological information inferred from a painting of this specimen while it was still alive. To test this hypothesis, we used ancient DNA (aDNA) techniques to extract and sequence mitochondrial DNA (mtDNA) from this specimen, and compared the genetic results with previously published lion mtDNA sequences. Our results show that the specimen is not a Cape lion, but that it instead possesses the mtDNA haplotype of the Asiatic lions P. l. persica (Meyer, 1826) from India. This Indian origin hypothesis is further supported by an investigation of its cranial morphology. As the amount of genetic information available for lions increases, in particular data from across their historic distribution, the potential for aDNA techniques to identify the origins of previously unassigned museum specimens continues to grow.
    Contributions to zoology Bijdragen tot de dierkunde 01/2007; 76:87-94. · 2.45 Impact Factor
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    Ross Barnett, Nobuyuki Yamaguchi, Ian Barnes, Alan Cooper
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    ABSTRACT: Understanding the phylogeographic processes affecting endangered species is crucial both to interpreting their evolutionary history and to the establishment of conservation strategies. Lions provide a key opportunity to explore such processes; however, a lack of genetic diversity and shortage of suitable samples has until now hindered such investigation. We used mitochondrial control region DNA (mtDNA) sequences to investigate the phylogeographic history of modern lions, using samples from across their entire range. We find the sub-Saharan African lions are basal among modern lions, supporting a single African origin model of modern lion evolution, equivalent to the 'recent African origin' model of modern human evolution. We also find the greatest variety of mtDNA haplotypes in the centre of Africa, which may be due to the distribution of physical barriers and continental-scale habitat changes caused by Pleistocene glacial oscillations. Our results suggest that the modern lion may currently consist of three geographic populations on the basis of their recent evolutionary history: North African-Asian, southern African and middle African. Future conservation strategies should take these evolutionary subdivisions into consideration.
    Proceedings of the Royal Society B: Biological Sciences 10/2006; 273(1598):2119-25. · 5.68 Impact Factor
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    Ross Barnett, Nobuyuki Yamaguchi, Ian Barnes, Alan Cooper
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    ABSTRACT: Two of the eight recognized lion subspecies, North African Barbary lion (Panthera leo leo) and South African Cape lion (Panthera leo melanochaita), have become extinct in the wild in the last 150years. Based on sequences of mitochondrial DNA (mtDNA) control region (HVR1) extracted from museum specimens of four Barbary and one Cape lion, the former was probably a distinct population characterized by an invariable, unique mtDNA haplotype, whilst the latter was likely a part of the extant southern African lion population. Extinction of the Barbary line, which may still be found in “generic” zoo lions, would further erode lion genetic diversity. Therefore, appropriate management of such animals is important for maintaining the overall genetic diversity of the species. The mtDNA haplotype unique to the Barbary lion, in combination with the small size of the HVR1 analyzed (c. 130bp), makes it possible and cost-effective to identify unlabelled Barbary specimens kept in museums and “generic” captive lions that may carry the Barbary line. An initial study of five samples from the lion collection of the King of Morocco, tested using this method, shows that they are not maternally Barbary.
    Conservation Genetics 07/2006; 7(4):507-514. · 2.18 Impact Factor

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