Retracing the history and planning the future of the red squirrel (<Emphasis Type="Italic">Sciurus vulgaris</Emphasis>) in Ireland using non-invasive genetics

The Eurasian red squirrel’s (Sciurus vulgaris) history in Ireland is largely unknown, but the original population is thought to have been driven to extinction by humans in the seventeenth century, and multiple records exist for its subsequent reintroduction in the nineteenth century. However, it is currently unknown how these reintroductions affect the red squirrel population today, or may do so in the future. In this study, we report on the development of a DNA toolkit for the non-invasive genetic study of the red squirrel. Non-invasively collected red squirrel samples were combined with other samples collected throughout Ireland and previously published mitochondrial DNA (mtDNA) data from Ireland, Great Britain and Continental Europe to give an insight into population genetics and historical introductions of the red squirrel in Ireland. Our findings demonstrate that the Irish red squirrel population is on a national scale quite genetically diverse, but at a local level contains relatively low levels of genetic diversity, and there is also evidence of genetic structure. This is likely an artefact of the introduction of a small number of genetically similar animals to specific sites. A lack of continuous woodland cover in Ireland has prevented further mixing with animals of different origins that may have been introduced even to neighbouring sites. Consequently, some of these genetically isolated populations are or may in the future be at risk of extinction. The Irish red squirrel population contains mtDNA haplotypes of both a British and Continental European origin, the former of which are now extinct or simply not recorded in contemporary Great Britain. The Irish population is therefore important in terms of red squirrel conservation not only in Ireland, but also for Great Britain, and should be appropriately managed.     

Morphological diversity of the red squirrel, <Emphasis Type="Italic">Sciurus vulgaris</Emphasis>, in Ireland

The red squirrel in Britain and Ireland has been described as a separate subspecies, Sciurus vulgaris leucourus, based on bleaching of the tail and ear tufts. However, recent investigations in northern England found this light colour confined to one area, probably due to the rapid spread of introduced continental European red squirrels. This study reports the first detailed survey of tail colour and cranial measurements in the Irish red squirrel population to (1) investigate the distribution of the light colour morph in Ireland and (2) determine whether the Irish red squirrel population is morphologically divergent from populations elsewhere in the species range. The light tail colour was found in 57% of individuals and in all regions, although it was most common in the northwest. The mixture of different colour morphs indicates the Irish population is a mixture of different subspecies, including S. vulgaris leucourus, while the cranial measurements suggest the Irish squirrel may be morphologically divergent from populations elsewhere. Combined, these results support previous suggestions that conservation measures seek to maintain the diversity within the Irish red squirrel population.     

Conservation of genetic uniqueness in remaining populations of red squirrels (Sciurus vulgaris L.) in the South of England

The Eurasian red squirrel (Sciurus vulgaris) is an emblematic species for conservation, and its decline in the British Isles exemplifies the impact that alien introductions can have on native ecosystems. Indeed, red squirrels in this region have declined dramatically over the last 60 years due to the spread of squirrelpox virus following the introduction of the gray squirrel (Sciurus carolinensis). Currently, red squirrel populations in Britain are fragmented and need to be closely monitored in order to assess their viability and the effectiveness of conservation efforts. The situation is even more dramatic in the South of England, where S. vulgaris survives only on islands (Brownsea Island, Furzey Island, and the Isle of Wight). Using the D‐loop, we investigated the genetic diversity and putative ancestry of the squirrels from Southern England and compared them to a European dataset composed of 1,016 samples from 54 populations. We found that our three populations were more closely related to other squirrels from the British Isles than squirrels from Europe, showed low genetic diversity, and also harbored several private haplotypes. Our study demonstrates how genetically unique the Southern English populations are in comparison with squirrels from the continental European range. We report the presence of four private haplotypes, suggesting that these populations may potentially harbor distinct genetic lineages. Our results emphasize the importance of preserving these isolated red squirrel populations for the conservation of the species.     

Genetic structure of Eurasian badgers Meles meles (Carnivora: Mustelidae) and the colonization history of Ireland

The present study examined the contemporary genetic composition of the Eurasian badger, Meles meles, in Ireland, Britain and Western Europe, using six nuclear microsatellite loci and a 215‐bp fragment of the mitochondrial DNA control region. Significant population structure was evident within Europe (global multilocus microsatellite F_ST = 0.205, P < 0.001; global mitochondrial control region Φ_ST = 0.399, P < 0.001). Microsatellite‐based cluster analyses detected one population in Ireland, whereas badgers from Britain could be subdivided into several populations. Excluding the island populations of Ireland and Britain, badgers from Western Europe showed further structuring, with evidence of discrete Scandinavian, Central European, and Spanish populations. Mitochondrial DNA cluster analysis grouped the Irish population with Scandinavia and Spain, whereas the majority of British haplotypes grouped with those from Central Europe. The findings of the present study suggest that British and Irish badger populations colonized from different refugial areas, or that there were different waves of colonization from the source population. There are indications for the presence of an Atlantic fringe element, which has been seen in other Irish species. We discuss the results in light of the controversy about natural versus human‐mediated introductions. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Museum samples provide novel insights into the taxonomy and genetic diversity of Irish red grouse

The taxonomic status of red grouse in Ireland has been the subject of considerable debate over the past century. Irish red grouse are usually classified as Lagopus lagopus scoticus, which is the same subspecies as that found in Britain, but some ornithologists believe that native Irish red grouse constitute an endemic subspecies, namely L. lagopus hibernicus. The considerable decline of Irish red grouse over the past century, along with possible hybridization with introduced grouse from Britain, have highlighted the need to resolve their taxonomic status as part of a biodiversity management plan. However, genetic analysis of samples from a single point in time will provide limited insight into potentially confounding historical events such as hybridization and introgression. We therefore compared mtDNA sequences from both current and historical samples of the two putative subspecies, scoticus and hibernicus, to see if they are or were genetically distinct. Red grouse from Britain and Ireland shared mitochondrial haplotypes, and our historical data suggest that this is unlikely to be the result of recent hybridization and introgression. These findings, combined with a general lack of documented differences in behaviour and ecology, suggest that Irish red grouse should remain classified as L. lagopus scoticus. At the same time, we found evidence that a significant amount of genetic diversity has been lost from Irish red grouse over the past century, presumably as a result of diminishing population sizes and fragmentation of extant populations. A loss of habitat, combined with the declining numbers and genetic diversity of Irish red grouse, justify their designation as an All-Ireland Priority (Red List) species and a Northern Ireland Priority Species for conservation.     

Genetic variation among endangered Irish red grouse (<Emphasis Type="Italic">Lagopus lagopus hibernicus</Emphasis>) populations: implications for conservation and management

Extant populations of Irish red grouse (Lagopus lagopus hibernicus) are both small and fragmented, and as such may have an increased risk of extinction through the effects of inbreeding depression and compromised adaptive potential. Here we used 19 microsatellite markers to assay genetic diversity across 89 georeferenced samples from putatively semi-isolated areas throughout the Republic of Ireland and we also genotyped 27 red grouse from Scotland using the same markers. The genetic variation within Ireland was low in comparison to previously published data from Britain and the sample of Scottish red grouse, and comparable to threatened European grouse populations of related species. Irish and Scottish grouse were significantly genetically differentiated (F_ST = 0.07, 95% CI = 0.04–0.10). There was evidence for weak population structure within Ireland with indications of four distinct genetic clusters. These correspond approximately to grouse populations inhabiting suitable habitat patches in the North West, Wicklow Mountains, Munster and Cork, respectively, although some admixture was detected. Pair-wise F_ST values among these populations ranged from 0.02 to 0.04 and the overall mean allelic richness was 5.5. Effective population size in the Munster area was estimated to be 62 individuals (95% CI = 33.6–248.8). Wicklow was the most variable population with an AR value of 5.4 alleles/locus. Local (Munster) neighbourhood size was estimated to 31 individuals corresponding to an average dispersal distance of 31 km. In order to manage and preserve Irish grouse we recommend that further fragmentation and destruction of habitats need to be prevented in conjunction with population management, including protection of the integrity of the existing population by refraining from augmenting it with individuals from mainland Britain to maximise population size.     

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.     

Population crash in an invasive species following the recovery of a native predator: the case of the American grey squirrel and the European pine marten in Ireland

In Ireland, the UK and Italy, the invasive North American grey squirrel, Sciurus carolinensis, threatens the survival of the Eurasian red squirrel, Sciurus vulgaris, as the effects of competition and disease almost inevitably lead to total replacement of red squirrel populations. However the results of a recent national squirrel survey suggested that the normally invasive grey squirrel had gone into decline in the Irish midlands, which was anecdotally attributed to an increase in European pine marten, Martes martes, range and numbers. This study aimed to quantify changes in squirrel distribution in Ireland and to investigate the role, if any, of the pine marten in red and grey squirrel population dynamics. A distribution survey of the midlands was carried out which confirmed the grey squirrel population has crashed in approximately 9,000 km² of its former range and the red squirrel is common after an absence of up to 30 years. At landscape level, pine marten and red squirrel abundance were positively correlated, whereas a strong negative correlation between pine marten and grey squirrel presence at woodland level was found to exist. Squirrel demographics were determined by means of live trapping programs which confirmed that the red squirrel in the midlands is now in competitive release and the grey squirrel is present at unusually low density. This study provides the first evidence of a regional grey squirrel population crash and suggests that European pine marten abundance may be a critical factor in the American grey squirrel’s success or failure as an invasive species.     

Genetic Structure of the French Red Squirrel Populations: Implication for Conservation

The decline of the red squirrel (Sciurus vulgaris) in several European countries due to the introduction of the American grey squirrel (S. carolinensis) and the predicted arrival of the grey squirrel in France in the near future has lead to the development of a preventative conservation project in this country. In this study, we conducted an extensive survey of mitochondrial DNA variation in French red squirrels using a fragment of the mitochondrial D-loop and we compared the results with previously published data from other European populations. Our main aims were: (1) to determine whether genetically differentiated populations, which could represent prioritized units for conservation purposes, were present in France and (2) to determine whether the French population, which is currently largely undisturbed, could provide information on the postglacial recolonization history of the species. We found that French D-loop haplotypes show almost no tendency to cluster by geographic origin, be it region or country, suggesting that French red squirrels have not been isolated from other populations during an evolutionarily significant period and that they do not constitute an Evolutionary Significant Unit. The French red squirrels showed strong signals of population expansion, the opposite to what is observed in most other European populations, making them of particular interest to study the postglacial expansion history of the species.     

Population genetic structure of Bombus terrestris in Europe: Isolation and genetic differentiation of Irish and British populations

The genetic structure of the earth bumblebee (Bombus terrestris L.) was examined across 22 wild populations and two commercially reared populations using eight microsatellite loci and two mitochondrial genes. Our study included wild bumblebee samples from six populations in Ireland, one from the Isle of Man, four from Britain and 11 from mainland Europe. A further sample was acquired from New Zealand. Observed levels of genetic variability and heterozygosity were low in Ireland and the Isle of Man, but relatively high in continental Europe and among commercial populations. Estimates of F_st revealed significant genetic differentiation among populations. Bayesian cluster analysis indicated that Irish populations were highly differentiated from British and continental populations, the latter two showing higher levels of admixture. The data suggest that the Irish Sea and prevailing south westerly winds act as a considerable geographical barrier to gene flow between populations in Ireland and Britain; however, some immigration from the Isle of Man to Ireland was detected. The results are discussed in the context of the recent commercialization of bumblebees for the European horticultural industry.     

Patterns of genetic diversity in the red squirrel (Sciurus vulgaris L.): Footprints of biogeographic history and artificial introductions

British S. vulgaris are classified as aseparate subspecies, S. v. leucourus, tomainland Europe. While S. vulgaris is notunder threat across most of its Eurasian range,in Britain, Ireland and Italy populations aredeclining, mainly due to the introduction ofthe American grey squirrel (S.carolinensis). In this study, we conducted anextensive survey of mitochondrial DNA variationin British S. vulgaris populations and apreliminary survey of continental Europeanpopulations. Our main aims were to determinethe extent to which any populations of S.vulgaris in Britain are partially or whollythe product of artificial translocation of redsquirrels from continental Europe, and whethercontinental population variation will provideinformation on post-glacial reafforestationpatterns in Europe. We found that the majorityof extant populations of British S.vulgaris are of continental ancestry, manywith a very recent (last 40 years) Scandinavianancestry. The Scandinavian haplotype hasrapidly become the most dominant innortheastern Britain, despite not appearing innorthern English populations until 1966. Thissuggests that these squirrels may have anadaptive advantage in the non-native sprucedominated conifer plantations of northernEngland. Our preliminary examination ofcontinental populations demonstrated that theyare sufficiently differentiated to allow aphylogeographic study of this species.     

Grey squirrels in central Italy: a new threat for endemic red squirrel subspecies

A new population of the invasive American Eastern grey squirrel (Sciurus carolinensis) has recently settled in central Italy from an accidental release in Perugia, Umbria in the early 2000s. The grey squirrel is known to compete with and exclude native red squirrels (S. vulgaris) in the British Isles and Northern Italy, so it represents a potentially important new conservation threat to the red squirrel subspecies of south and central Italy, S. vulgaris italicus and S. v. meridionalis, which are endemic to peninsular Italy. The grey squirrel population range in Perugia is currently expanding at a rate of about 0.29 km/year (SD 0.19), slower than grey squirrel invasions elsewhere in Europe. Nuclear DNA analysed at 12 different microsatellite loci revealed that the grey squirrels in Perugia have extremely low genetic diversity, consistent with a small founder size. Genetic assignment tests indicate that the Perugia population was founded by translocations from an established population in Piedmont, Italy. No genetic substructure is evident yet in the Perugia population. These results together have serious consequences for the management of the grey squirrel invasion in Perugia and the conservation of the red squirrel subspecies: the Perugia grey squirrel population should be eradicated if politically feasible; otherwise new releases of grey squirrels, especially from sources other than the Piedmont population, should be prevented because such introductions could increase genetic diversity, thereby potentially increasing population range expansion rate to the much higher levels seen for more diverse grey squirrel populations elsewhere in Europe.     

Unique mitochondrial DNA lineages in Irish stickleback populations: cryptic refugium or rapid recolonization?

Repeated recolonization of freshwater environments following Pleistocene glaciations has played a major role in the evolution and adaptation of anadromous taxa. Located at the western fringe of Europe, Ireland and Britain were likely recolonized rapidly by anadromous fishes from the North Atlantic following the last glacial maximum (LGM). While the presence of unique mitochondrial haplotypes in Ireland suggests that a cryptic northern refugium may have played a role in recolonization, no explicit test of this hypothesis has been conducted. The three‐spined stickleback is native and ubiquitous to aquatic ecosystems throughout Ireland, making it an excellent model species with which to examine the biogeographical history of anadromous fishes in the region. We used mitochondrial and microsatellite markers to examine the presence of divergent evolutionary lineages and to assess broad‐scale patterns of geographical clustering among postglacially isolated populations. Our results confirm that Ireland is a region of secondary contact for divergent mitochondrial lineages and that endemic haplotypes occur in populations in Central and Southern Ireland. To test whether a putative Irish lineage arose from a cryptic Irish refugium, we used approximate Bayesian computation (ABC). However, we found no support for this hypothesis. Instead, the Irish lineage likely diverged from the European lineage as a result of postglacial isolation of freshwater populations by rising sea levels. These findings emphasize the need to rigorously test biogeographical hypothesis and contribute further evidence that postglacial processes may have shaped genetic diversity in temperate fauna.     

Zebra mussels (Dreissena polymorpha) in Ireland, AFLP-fingerprinting and boat traffic both indicate an origin from Britain

1. The zebra mussel (Dreissena polymorpha) is an aquatic nuisance species that invaded Ireland around 1994. We studied the invasion of the zebra mussel combining field surveys and genetic studies, to determine the origin of invasion and the vector of introduction. 2. Field surveys showed that live zebra mussels, attached to the hulls of pleasure boats, were transported from Britain to Ireland. These boats were lifted from British waters onto trailers, transported to Ireland by ferry and lifted into Irish waters within a day. Length‐frequency distributions of dead and living mussels on one vessel imported 3 months earlier revealed a traumatic occurrence caused by the overland, air‐exposed transportation. Results show that a large number of individuals survived after re‐immersion in Irish waters and continued to grow. 3. Zebra mussels from populations in Ireland, Great Britain, the Netherlands, France and North America, were analysed using amplified fragment length polymorphisms (AFLP)‐fingerprinting to determine the origin of the Irish invasion. Phylogenetic analysis revealed that Irish and British mussels clustered closely together, suggesting an introduction from Britain. 4. Ireland remained un‐invaded by the zebra mussel for more than 150 year. The introduction of the zebra mussel to Ireland occurred following the abolition of value added tax in January 1993 on imported second‐hand boats from the European Union (UK and continental Europe). This, together with a favourable monetary exchange rate at that time, may have increased the risk of invasion of the zebra mussel.     

Origin and colonization history of the white-clawed crayfish,Austropotamobius pallipes,in Ireland

The presence of the white-clawed crayfish Austropotamobius pallipes complex in Ireland is suspected to be a result of human translocations. Two hypotheses have been formulated about the origin of the crayfish: from British populations or from western French populations. In order to resolve this question, nine Irish crayfish populations (a total of 124 individuals) were sampled along a south-north cline and investigated by combining two molecular markers: mtDNA and RAPDs. The mtDNA marker, analysed by RFLP on the entire molecule, showed an absence of polymorphism within and among Irish populations. The RFLP haplotype found in Irish populations was only recorded in western French populations and was different from those found in English populations. This result may be explained by a human introduction of crayfish to Ireland from western French populations. RAPD analysis showed a clinal reduction of genetic variability within Irish populations from south to north, associated with an increase in their genetic differentiation. A stepwise model of translocation from the south to the north of Ireland is proposed and discussed.     

Stoats (Mustela erminea) provide evidence of natural overland colonization of Ireland

The current Irish biota has controversial origins. Ireland was largely covered by ice at the Last Glacial Maximum (LGM) and may not have had land connections to continental Europe and Britain thereafter. Given the potential difficulty for terrestrial species to colonize Ireland except by human introduction, we investigated the stoat (Mustela erminea) as a possible cold-tolerant model species for natural colonization of Ireland at the LGM itself. The stoat currently lives in Ireland and Britain and across much of the Holarctic region including the high Arctic. We studied mitochondrial DNA variation (1771 bp) over the whole geographical range of the stoat (186 individuals and 142 localities), but with particular emphasis on the British Isles and continental Europe. Irish stoats showed considerably greater nucleotide and haplotype diversity than those in Britain. Bayesian dating is consistent with an LGM colonization of Ireland and suggests that Britain was colonized later. This later colonization probably reflects a replacement event, which can explain why Irish and British stoats belong to different mitochondrial lineages as well as different morphologically defined subspecies. The molecular data strongly indicate that stoats colonized Ireland naturally and that their genetic variability reflects accumulation of mutations during a population expansion on the island.     

Genetic diversity and phylogenetic analysis of native mountain ponies of Britain and Ireland reveals a novel rare population

The conservation of unique populations of animals is critical in order to preserve valuable genetic diversity and, where populations are free‐living, maintain their irreplaceable influence upon habitat ecology. An accurate assessment of genetic diversity and structure within and between populations is crucial in order to design and implement conservation strategies in natural and domesticated species. Moreover, where it is possible to identify relic populations that are related to a structured breed an ideal opportunity presents itself to model processes that reveal historical factors that have shaped genetic diversity. The origins of native UK mountain and moorland ponies are uncertain, but they may have directly descended from prehistoric populations and potentially harbour specific adaptations to the uplands of Britain and Ireland. To date, there have been no studies of population structure and genetic diversity present within a free‐living group of ponies in the Carneddau mountain range of North Wales. Herein, we describe the use of microsatellites and SNPs together with analysis of the mitochondrial control region to quantify the extent and magnitude of genetic diversity present in the feral Carneddau pony and relate this to several recognised British and Irish pony breeds. Our results establish that the feral Carneddau ponies represent a unique and distinctive population that merits recognition as a defined population and conservation priority. We discuss the implications for conservation of this population as a unique pool of genetic diversity adapted to the British uplands and potentially of particular value in maintaining the biodiversity of these habitats.     

Grauhörnchen vs. Eichhörnchen

Competition for resources in Europe's forests – grey versus red squirrels As a result of the introduction of the north American grey squirrel in Britain, Ireland and Italy in the 19th and 20th century, the sole native tree squirrel species in Europe – the red squirrel – faced a completely novel competitor. In order to understand the interactions between the two species and to develop a conservation strategy, the two species' biology and ecology was the focus of intense research over the last 25 years. We provide an overview of research findings and the complex competitive interactions for resources and the curcial role of disease in the replacement of native red by introduced grey squirrels. Key factors in the competitive replacement process are habitat composition and patterns of seed food availability, which directly influence individual body condition and reproductive success. In addition, in the British Isles a squirrelpox virus for which grey squirrels act as a reservoir and vector has a drastic impact on the competitive interactions between the two species.     

Route,speed and mode of oak postglacial colonisation across the British Isles: Integrating molecular ecology,palaeoecology and modelling approaches

Summary

This paper describes the route, speed and mode of colonisation of oaks by integrating a number of independent analyses using molecular ecology, palaeoecology and simulation modelling approaches. Using a synthetic map of the contemporary distribution of chloroplast DNA (integrating several published and unpublished data sets and describing variation in 1468 trees from 313 autochthonous stands of Q. robur and Q. petraea from Britain and Ireland), and considering the postglacial topographic landscape, the most likely routes of postglacial colonisation across the British Isles are suggested. The overall pattern of these directions agrees with previous interpretations, but several routes, particularly those into Ireland, differ from previous interpretations and benefit here from using a single synthesised data set. Interestingly, the Atlantic oakwoods appear to have been colonised by individuals bearing a single haplotype (type 12). Two palaeoecology data sets, published separately for Britain and Ireland, are synthesised here and used to infer the timing of first arrival of oaks across the British Isles (between 9500 and 6000 years before present). The maximum observed colonisation speed within the British Isles is approximately 500 m year^-1 in central and southern England. Outputs from a simulation model, which mimics postglacial colonisation processes, and which has been parameterised for the colonisation rate observed from the pollen core record and contemporary cpDNA structure, predict that the rapid colonisation rate observed, for at least the southern portion of the British Isles, can only be achieved via very rare (an approximate frequency 0.01%), very long distance seed dispersal events (up to 100 km). Potential agents of such dispersal events are birdsor major meteorological disturbances, e.g. hurricanes. Additional simulation modelling and genetic analysis of latitudinally stratified populations indicate that non-synchronous colonisation fronts, topographic barriers and temperature related survival may also have had an effect on the speed of migration and resulting genetic structure. Finally, in an attempt to record predicted long distance seed dispersal events, a novel curve fitting technique is applied to molecular parentage assignment data for field established seedlings from a contemporary population. A notable discrepancy is recorded between contemporary field estimates (just over 1 km) and those predicted by simulation modelling, and is discussed in detail. A concluding section describes future research priorities.