Introgression of exotic Cervus (nippon and canadensis) into red deer (Cervus elaphus) populations in Scotland and the English Lake District

Since the mid‐19th century, multiple introductions of Japanese sika deer (Cervus nippon nippon) and North American wapiti (C. canadensis) have taken place in the British Isles. While wapiti have generally been unsuccessful, sika have been very successful, especially in Scotland where they now overlap at least 40% of the range of native red deer (C. elaphus). Hybridization between these two species and red deer has been demonstrated in captivity and in the wild. Using a panel of 22 microsatellite loci that are highly diagnostic between red deer and sika, and moderately diagnostic between red deer and wapiti, we investigated the extent of introgression between these species in 2,943 deer sampled from around Scotland and from the English Lake District using the Bayesian clustering software STRUCTURE. We also used a diagnostic mitochondrial marker for red deer and sika. Our survey extends previous studies indicating little introgression of wapiti nuclear alleles into red deer, in particular in Northern Scotland, Kintyre, and the Lake District. We found a new area of extensive sika introgression in South Kintyre. In the North Highlands, we show for the first time geographically scattered evidence of past hybridization followed by extensive backcrossing, including one red‐like individual with sika introgression, two sika‐like individuals with red deer introgression, and six individuals that were apparently pure sika at the nuclear markers assessed but which carried red deer mitochondria. However, there has not been a collapse of assortative mating in this region. Similarly, in the English Lake District red deer, we found only traces of past sika introgression. No sika alleles were detected in the Central Highlands or the Hebridean red deer refugia. We make suggestions for management to prevent further spread of sika alleles into red deer and vice versa.     

A phylogenetic comparison of red deer and wapiti using mitochondrial DNA

A phylogeny was constructed for red deer/wapiti (Cervus elaphus) subspecies using sequence data from the control region of mitochondrial DNA (mtDNA). The tree was rooted using Cervus nippon (sika deer), Cervus albirostris (Thorold's white-lipped deer), and several Odocoileinae species. A division between the mtDNA haplotypes of red deer (European) and wapiti (Asian/North American) corresponds to subspecies found on opposite sides of the Himalayan Mountains and Gobi, which suggests wapiti should be reconsidered for the status of C. canadensis. Using parsimony and distance analysis, red deer and wapiti are derived from a single recent common ancestor, which is consistent with current taxonomy that recognizes the subspecies of Cervus elaphus as monophyletic group. However, maximum-likelihood analysis using weighted transitional substitutions caused red deer to form a sister group to sika deer (Cervus nippon) and wapiti. A phenetic comparison revealed wapiti also share more nucleotide similarities with sika deer, although approximately 5% sequence divergence separates wapiti, sika, and red deer. Phylogenetic evidence from the cytochrome b sequences corroborated observations from the control region. Observations from this study suggest that the species status of wapiti should be reinstated.     

Phylogenetic relationships among european red deer, wapiti, and sika deer inferred from mitochondrial DNA sequences

We determined the mitochondrial cytochrome b gene sequences (1140 bp) of one subspecies of the European red deer (Cervus elaphus in Europe), three subspecies of the wapiti (C. elaphus in Asia and North America), and six subspecies of the sika deer (C. nippon in Japan). Our phylogenetic analysis revealed the monophyly of the European red deer, that of the wapiti, and that of the sika deer. The wapiti, however, was shown to be more closely related to the sika deer than to the European red deer. This is in conflict with traditional morphological results, which suggest a close sister group relationship between the wapiti and the European red deer. The divergence time between the European red deer and the wapiti plus the sika deer was estimated to be approximately 0.80 Ma, and that between the wapiti and the sika deer was estimated to be 0.57 Ma. The sika deer was subdivided into two subspecies groups, and the wapiti was also found to consist of an Asian group and a North American group.     

Phylogeography of red deer (Cervus elaphus): Analysis of MtDNA cytochrome b polymorphism

Analysis of MtDNA cytochrome b gene (1140 bp) polymorphism of 106 samples red deer (Cervus elaphus) from different regions of Eurasia was performed; the phylogenetic relationships of groups throughout the entire inhibiting area (including North America) were reconstructed. Totally 75 haplotypes were detected, 33 of which were found in the European and 42 in the Asian part of the area. There were no identical haplotypes for these two parts of the area found. The close relatedness between Siberian red deer (C. e. sibirica) and North American wapiti (C. e. canadensis) was confirmed. Red deer inhibiting Yakutia were close to the Siberian red deer from Altai and Tuva, whereas red deer inhibiting Krasnoyarsk and Irkutsk regions formed a separate clade. Overall, the reconstructed phylogeographic pattern of the species was significantly different from the subspecies differentiation based on morphological traits.     

Characterization of the erythrocyte superoxide dismutase allozymes in the deer Cervus elaphus

The cDNA sequences for Cu,Zn superoxide dismutase from two Cervus elaphus subspecies, North American wapiti and European red deer, were determined. The derived amino acid sequences showed two differences: residue 8 was Leu in wapiti and Met in red deer and residue 25 was His in wapiti and Asn in red deer. The extra positive charge at position 25 in the wapiti isoform accounted for its greater mobility towards the cathode during non-denaturing electrophoresis, a procedure widely used in the genetic analysis of deer. There was no difference in specific activity between the two Cu,Zn superoxide dismutase isoforms, but the wapiti isoform was slightly more susceptible to heat denaturation.     

A new form of wapiti Cervus canadensis Erxleben, 1777 (Cervidae,Mammalia) from the Late Pleistocene of France

A well-preserved antlered braincase of wapiti (Cervus canadensis) from the Late Pleistocene of Saint-Hippolyte (Puy de Dôme, France) is described herein. The specific morphology of antlers suggests peculiar adaptations to the open landscapes of periglacial tundra-steppe that permitted to identify a new fossil subspecies Cervus canadensis combrayicus n. ssp. The specimen attests the occurrence of Cervus canadensis in the paleontological record of Western Europe and helps to clarify the systematical position of some disputed findings of Cervus from Western Europe. The revised systematic position of some fossil and sub-fossil cervid findings reveals the paleobiogeographic story of wapiti in Western Europe during the Last Glacial Maximum and the postglacial time. The treeless Alpine altitudes and Sweden are proposed as the glacial refugia for the last European wapiti. The medium-sized deer from Capri Island is regarded as an insular dwarfed wapiti C. canadensis tyrrhenicus closely related to the continental form C. canadensis palmidactyloceros from the alpine refugium.     

A survey of the hybridisation status of Cervus deer species on the island of Ireland

Red deer (Cervus elaphus) did not recolonise Ireland after the last glaciation, but the population in Co. Kerry is descended from an ancient (c. 5000 BP) introduction and merits conservation. During the mid-19th century exotic species including North American wapiti (C. canadensis) and Japanese sika deer (C. nippon nippon) were introduced to Ireland, mainly via Powerscourt Park, Co. Wicklow. While wapiti failed to establish, sika thrived, dispersed within Co. Wicklow and were translocated to other sites throughout Ireland. Red deer and sika are known to have hybridised in Ireland, particularly in Co. Wicklow, but an extensive survey with a large, highly diagnostic marker panel is required to assess the threat hybridisation potentially poses to the Co. Kerry red deer population. Here, 374 individuals were genotyped at a panel of 22 microsatellites and at a single mtDNA marker that are highly diagnostic for red deer and Japanese sika. The microsatellites are also moderately diagnostic for red deer and wapiti. Wapiti introgression was very low [trace evidence in 2 (0.53 %) individuals]. Despite long-standing sympatry of red deer and sika in the area, no red deer-sika hybrids were detected in Co. Kerry suggesting strong assortative mating by both species in this area. However, 80/197 (41 %) of deer sampled in Co. Wicklow and 7/15 (47 %) of deer sampled in Co. Cork were red-sika hybrids. Given their proximity and that hybrids are less likely to mate assortatively than pure individuals, the Co. Cork hybrids pose a threat to the Co. Kerry red deer.     

Red and sika deer in the British Isles,current management issues and management policy

The red deer (Cervus elaphus) is one of the most widely distributed species of deer in Europe. Due to its economic value as game species or its negative impacts on forestry, agriculture and conservation areas, most populations are currently managed, with strategies and intensity of the management varying between countries. In Britain, and less certainly in Ireland, red deer have been continuously present since the end of the last glaciation and constitute the largest population of red deer in Europe. Although they thrived in the past when forests were abundant, the current distribution of red deer in the British Isles is uneven, with the largest numbers being found in Scotland and few and more localised populations in England, Wales and the Republic of Ireland. In the British Isles, as in many other parts of Europe, there is a long history of man interacting with deer populations including local extinctions, multiple translocations and introductions of exotic species of deer. Among introduced exotic species of deer, the Japanese sika (Cervus nippon) is the one of most concern. After introduction of small numbers at multiple locations in Britain and Ireland from 1860 onwards, sika have increased in population number and range in areas with good forest cover, and where they overlap with red deer there is a risk of hybridisation. Due to recent increases in numbers and range of red and sika deer, both species pose a range of management challenges which are not easy to solve. In this review we summarise the history and status of these two species in Great Britain and Ireland, describe current management and discuss management options for the future.     

Insights into the evolutionary history of Cervus (Cervidae,tribe Cervini) based on Bayesian analysis of mitochondrial marker sequences,with first indications for a new species

Molecular phylogeny and evolutionary history of Cervus, the most successful and widespread cervid genus, have been extensively addressed in Europe, fairly in eastern Asia, but scarcely in central Asia, where some populations have never been phylogenetically investigated with DNA‐based methods. Here, we applied a coalescent Bayesian approach to most Cervus taxa using complete mitochondrial cytochrome b gene and control region to provide a temporal framework for species differentiation and dispersal, with special emphasis on the central Asian populations from the Tarim Basin (C. elaphus bactrianus, C. elaphus yarkandensis) and Indian Kashmir (C. elaphus hanglu) aiming at assessing their phylogenetic and phylogeographic patterns. Red deer (C. elaphus), wapiti (C. canadensis) and sika deer (C. nippon) are confirmed as highly differentiated taxa, with genetic distances, divergence times and phylogenetic positions compatible with the rank of species. Similarly, the red deer of the Tarim group, hitherto considered as subspecies of C. elaphus, showed a comparable pattern of genetic distinction in the phylogeny and, according to our results, are thus worthy of being raised to the species level. The systematic position of the endangered red deer from Indian Kashmir is assessed here for the first time, and implications for its conservation are also outlined. Based on phylogeny and divergence time estimates, we propose a novel evolutionary pattern for the genus Cervus during the Mio/Pliocene, in the light of palaeo‐climatological information.     

Genetic variation and structure in Scandinavian red deer (Cervus elaphus): influence of ancestry,past hunting,and restoration management

In the 19^th century, the red deer (Cervus elaphus) population in Sweden experienced a rapid decline in numbers and distribution. A small population was, however, remnant in the southernmost province (Skåne) of the country, presumably corresponding to the nominate form of red deer (Cervus elaphus elaphus Linnaeus, 1758). After management, reintroductions, and supplementary release during the 20^th century the Swedish C. elaphus population recovered. The recovery was partially uncontrolled, and included introductions of C. elaphus of continental origin. In northern central Sweden (Jämtland) the current C. elaphus population may stem from natural colonization from Norway and/or from specimens of Swedish origin that have escaped from enclosures. To evaluate the status of the current, partially separated populations, we investigated variation at microsatellite markers in 157 C. elaphus specimens from ten locations in Sweden and Norway. Analyses suggest that the highest‐likelihood phylogenetic structure among the individuals sampled is described four distinct genetic clusters: (1) animals from the province of Västergötland in south‐western Sweden; (2) deer from the southernmost province of Skåne; (3) deer from the provinces Jämtland, Blekinge, and Västmanland; and (4) Norwegian deer. Cervus elaphus from a captive herd at the Skåne Zoo cluster with deer from Skåne or deer from Västergötland, depending on the method of analysis. A number of populations in Sweden may genetically match the nominate form of red deer (C. e. elaphus). The recently established C. elaphus population in Jämtland seems to stem mainly from escapees from enclosures, with a mixed ancestry from the wild remnant population in Skåne and continental deer, whereas the influx from Norway is minor, if any. Our results show the need for a detailed assessment of genetic differentiation, and emphasize the value of local management plans when planning and managing introductions. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 43–53.     

Genetic structure of red deer population in northeastern Poland in relation to the history of human interventions

We studied the genetic structure of a red deer (Cervus elaphus) population in 8 woodlands of northeastern Poland and 1 in western Belarus and compared it with the documented history of the population in the region. Red deer nearly went extinct in the region in the 18th and 19th centuries. In the mid-19th century, reintroductions began and continued until the mid-1960s. Animals were translocated from various sites in Poland and other European countries. We genotyped 303 individuals using 14 microsatellite loci and sequenced 253 individuals for a fragment of the control region (mitochondrial DNA [mtDNA]). The microsatellite analyses demonstrate that 3 genetically separate subpopulations exist, but 4 according to mtDNA. All haplotypes found in northeastern Poland are closely related to haplotypes from northern and northwestern Europe. The only individuals that could have originated from autochthonous red deer populations, rather than introductions, were found in Napiwoda Forest. The present regional genetic structure of the species is consistent with the known history of red deer translocations. Current patterns of genetic diversity in these populations are determined by the interaction of past human management and contemporary natural migrations. © 2012 The Wildlife Society.     

The anatomy of vocal divergence in North American Elk and European red deer

Loud and frequent vocalizations play an important role in courtship behavior in Cervus species. European red deer (Cervus elaphus) produce low‐pitched calls, whereas North American elk (Cervus canadensis) produce high‐pitched calls, which is remarkable for one of the biggest land mammals. Both species engage their vocal organs in elaborate maneuvers but the precise mechanism is unknown. Vocal organs were compared by macroscopic and microscopic dissection. The larynx is sexually dimorphic in red deer but not in elk. The laryngeal lumen is more constricted in elk, and narrows further during ontogeny. Several elements of the hyoid skeleton and two of four vocal tract segments are longer in red deer than in elk allowing greater vocal tract expansion and elongation. We conclude that elk submit the larynx and vocal tract to much higher tension than red deer, whereby, enormously stressed vocal folds of reduced effective length create a high resistance glottal source. The narrow, high impedance laryngeal vestibulum matches glottal and vocal tract impedance allowing maximum power transfer. In red deer longer and relaxed vocal folds create a less resistant glottal source and a wider vestibulum matches the low glottal impedance to the vocal tract, thereby also ensuring maximum power transfer. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

Gastropod availability and habitat utilization by wapiti and white-tailed deer sympatric on range enzootic for meningeal worm

Gastropod occurrence and the utilization of habitat by sympatric populations of wapiti (Cervus elephus) and white-tailed deer (Odocoileus virginianus) on range enzootic for meningeal worm (Parelaphostrongylus tenuis) were studied on Cookson Hills Wildlife Management Area (WMA) in eastern Oklahoma. Visual observations and fecal pellet group transect data indicated that wapiti spent the majority of their time in open fields and meadows where we recovered the least numbers of gastropods. Although deer were frequently observed in open areas, visual sightings and transect data indicated that they spent more time in forested areas where we recovered the most gastropods. Gastropods harbored low numbers of P. tenuis larvae (0.00 to 0.06 larvae/gastropod) in all habitat types with the greatest recovery from red oak white oak-hickory forests (0.34 larvae/gastropod). Our results indicate that the reason a viable wapiti herd exists on Cookson Hills WMA in a P. tenuis enzootic area is at least partially because of the habitat preference by wapiti and the reduced availability of infected gastropods in the selected areas prefered by the wapiti. We were not able to detect any free-ranging wapiti that were shedding P. tenuis larvae nor were we able to detect past or sub-clinical infections with P. tenuis in wapiti.     

Mitochondrial D-loop phylogeny signals two native Iberian red deer (Cervus elaphus) Lineages genetically different to Western and Eastern European red deer and infers human-mediated translocations

Native red deer (Cervus elaphus) in Western Europe might at least partially derive from refugial populations which survived in the Iberian Peninsula during the last glacial maximum, and that expanded northwards at the onset of the Holocene. However, the phylogeny and genetic structure of red deer populations in the Iberian Peninsula are still poorly known. This study was planned, in a first step, to reconstruct the phylogenetic relationship of the main red deer populations extant in Spain by the analyses of an extensive sample of mitochondrial DNA sequences. Results indicate that sequences from these populations can be assigned to one of two deeply divergent mtDNA lineages (South-Western and Central-Eastern) with molecular divergence nearby the 2 %. In each lineage were respectively found sixteen and thirteen different haplotypes. It was evidenced that they may be allopatrically distributed in Spain with 86.6 % sequences of the South-Western lineage at the South-Western side and the 65 % sequences of Central-Eastern lineage in the Central-Eastern side. These mitochondrial lineages might have originated in two distinct refugial populations during the last glacial maximum. Genetic data also reveal instances of admixture between native populations and translocated European red deer, which belong to at least three distinct subspecies. Gene introgression was mainly due to red deer from Western European populations. The genetic contribution of red deer translocated from Eastern Europe (C. e. hippelaphus) or North Africa (C. e. corsicanus, C. e. barbarus) was apparently less deep. The extant phylogenetic relationship and evidences of genetic admixture suggest that sound conservation actions for the native Iberian red deer should severely restrict the introduction of alien red deer and, when possible, avoid admixture between the South-Western and Central-Eastern mtDNA lineages.     

Positioning the Red Deer (Cervus elaphus) Hunted by the Tyrolean Iceman into a Mitochondrial DNA Phylogeny

In the last years several phylogeographic studies of both extant and extinct red deer populations have been conducted. Three distinct mitochondrial lineages (western, eastern and North-African/Sardinian) have been identified reflecting different glacial refugia and postglacial recolonisation processes. However, little is known about the genetics of the Alpine populations and no mitochondrial DNA sequences from Alpine archaeological specimens are available. Here we provide the first mitochondrial sequences of an Alpine Copper Age Cervus elaphus. DNA was extracted from hair shafts which were part of the remains of the clothes of the glacier mummy known as the Tyrolean Iceman or Ötzi (5,350–5,100 years before present). A 2,297 base pairs long fragment was sequenced using a mixed sequencing procedure based on PCR amplifications and 454 sequencing of pooled amplification products. We analyzed the phylogenetic relationships of the Alpine Copper Age red deer''s haplotype with haplotypes of modern and ancient European red deer. The phylogenetic analyses showed that the haplotype of the Alpine Copper Age red deer falls within the western European mitochondrial lineage in contrast with the current populations from the Italian Alps belonging to the eastern lineage. We also discussed the phylogenetic relationships of the Alpine Copper Age red deer with the populations from Mesola Wood (northern Italy) and Sardinia.     

Haplotype diversity of Bulgarian red deer (Cervus elaphus L.)

To estimate the hyplotype diversity of red deer (Cervus elaphus L.) from the Balkan Peninsula, a fragment of cytochrome b (427 bp) was analyzed. Six haplotypes were revealed in the investigated red deer from Bulgaria (16 individuals). In all, 32 sequences were included in the comparative analyses (15 from Genbank and 17 of our samples from different locations of the Cervus elaphus area). As an outgroup we used a C. e. xanthopygus sequence. Four Bulgarian red deer haplotypes were closely related to other European haplotypes, where two other haplotypes formed a separate branch, and also encompassed two samples from Sardinia and Tunisia. Thus, our results indicated the existence at least two different genetic lines of red deer in Bulgaria.     

Tracing the genetic roots of the sika deer Cervus nippon naturalized in Germany and Austria

To determine the geographical origin of the sika deer (Cervus nippon) naturalized in Germany and Austria, we sequenced the mitochondrial control region for 214 individuals. Adding these sequences to previously published data from native sika deer across its natural geographic range, the total comes to 245, extending what is already known about the geographical variation in this sequence in Cervus nippon. From these sequences, a neighbour-joining tree was constructed. This tree showed that the 49 different mitochondrial (mt)DNA types are grouped into three distinct phylogenetic clusters, which correspond to different geographic areas. Similarities between sequences of the naturalized sika deer and those described from native sika deer from both southern Honshu, Kyushu with associated islands, and northern Honshu suggest that the ancestors of the sika deer populations in Germany and Austria originated from the Japanese archipelago. In contrast, there is no evidence that female sika deer of Chinese, Taiwanese or north Vietnamese origin were involved in the ancestry of the present sika population in Germany and Austria.     

Relative Effect of Food Supplementation and Natural Resources on Female Red Deer Distribution in a Mediterranean Ecosystem

ABSTRACT Supplementary feeding is a widespread game management practice in several red deer (Cervus elaphus) populations, with important potential consequences on the biology of this species. In Mediterranean ecosystems food supplementation occurs in the rutting period, when it may change mating system characteristics. We studied the role of food supplementation relative to natural resources in the spatial distribution, aggregation, and mean harem size of females in Iberian red deer (Cervus elaphus hispanicus) during the rut. We studied 30 red deer populations of southwestern Spain, 63% of which experienced supplementary feeding. Using multivariate spatial analyses we found that food supplementation affected distribution of females in 95% of the populations in which it occurred. Green meadows present during the mating season acted as an important natural resource influencing female distribution. Additionally, the level of female aggregation and mean harem size were significantly higher in those populations in which food supplementation determined female distribution than in populations in which female distribution did not depend on supplementary feeding. Because female aggregation and mean harem size are key elements in sexual selection, supplementary feeding may constitute an important anthropogenic element with potential evolutionary implications for populations of Iberian red deer.     

Bull bellows and bugles: a remarkable convergence of low and high-frequency vocalizations between male domestic cattle Bos taurus and the rutting calls of Siberian and North American wapiti

Whereas low-frequency bellows (below 200 Hz) have been investigated in detail in both male and female domestic cattle (Bos taurus), male high-frequency bugle calls (over 800 Hz) have not been described so far in any large bovid species. In this study, high-frequency bugles and low-frequency bellows were recorded from three crossbred free-ranging domestic cattle bulls and analysed spectrographically. The maximum fundamental frequency of bellows was 113.6 Hz, whereas the maximum fundamental frequency of bugles was 958.4 Hz, ranging from 801 to 1125 Hz in different males. These amazingly high fundamental frequencies of bull bugles are comparable with those reported for Siberian wapiti Cervus elaphus sibiricus, but lower than reported values for some subspecies of North American wapiti Cervus canadensis. The similarity with both Siberian and North American wapiti was also observed in the production of bull biphonic bugles with two fundamental frequencies: the low and the high one. We suggest that bugles of domestic cattle bulls provide an excellent model for comparative research with cervid bugles concerning the mechanism of vocal production and the underlying anatomical and behavioural adaptations.     

Wear Fast,Die Young: More Worn Teeth and Shorter Lives in Iberian Compared to Scottish Red Deer

Teeth in Cervidae are permanent structures that are not replaceable or repairable; consequently their rate of wear, due to the grinding effect of food and dental attrition, affects their duration and can determine an animal''s lifespan. Tooth wear is also a useful indicator of accumulative life energy investment in intake and mastication and their interactions with diet. Little is known regarding how natural and sexual selection operate on dental structures within a species in contrasting environments and how these relate to life history traits to explain differences in population rates of tooth wear and longevity. We hypothesised that populations under harsh environmental conditions should be selected for more hypsodont teeth while sexual selection may maintain similar sex differences within different populations. We investigated the patterns of tooth wear in males and females of Iberian red deer (Cervus elaphus hispanicus) in Southern Spain and Scottish red deer (C. e. scoticus) across Scotland, that occur in very different environments, using 10343 samples from legal hunting activities. We found higher rates of both incisor and molar wear in the Spanish compared to Scottish populations. However, Scottish red deer had larger incisors at emergence than Iberian red deer, whilst molars emerged at a similar size in both populations and sexes. Iberian and Scottish males had earlier tooth depletion than females, in support of a similar sexual selection process in both populations. However, whilst average lifespan for Iberian males was 4 years shorter than that for Iberian females and Scottish males, Scottish males only showed a reduction of 1 year in average lifespan with respect to Scottish females. More worn molars were associated with larger mandibles in both populations, suggesting that higher intake and/or greater investment in food comminution may have favoured increased body growth, before later loss of tooth efficiency due to severe wear. These results illustrate how independent selection in both subspecies, that diverged 11,700 years BP, has resulted in the evolution of different longevity, although sexual selection has maintained a similar pattern of relative sex differences in tooth depletion. This study opens interesting questions on optimal allocation in life history trade-offs and the independent evolution of allopatric populations.