Origin of, and conservation units in, the Irish red squirrel (Sciurus vulgaris) population

Knowledge of genetic relationships among wildlife populations is fundamental to their conservation, particularly where translocations are concerned. This study involved a survey of mitochondrial DNA variation in the Irish red squirrel population. Our main aims were: (1) to determine whether the Irish red squirrel population is distinct from that found in Britain, given known translocations that took place from Britain in the 1800’s; and (2) whether inclusion of Irish data into a reanalysis of European red squirrel data could reveal patterns of postglacial spread in Ireland. We found evidence that the current Irish red squirrel population may be a mixture of native and translocated stock, and relationships between Irish and European haplotypes supported a number of colonisation events of the island. Although only one haplotype was common to both Ireland and Britain, it is probable that the most common haplotypes in Ireland are British introductions that have since become extinct in Britain. There was a significant regional genetic structure in Ireland (P < 0.001), as well as between all Irish and British regions. Although it is likely that the red squirrel will not be fundamental in tracing the colonisation of Ireland by mammals, the data demonstrated that individual regions within Ireland, as well as the Irish population as a whole, are distinct both from the British population and from each other and, therefore, these populations should be treated as separate Management Units (MU) in conservation strategies.     

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.     

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.     

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.     

Genetic drift and the population history of the Irish travellers

The Irish Travellers are an itinerant group in Ireland that has been socially isolated. Two hypotheses have been proposed concerning the genetic origin of the Travellers: (1) they are genetically related to Roma populations in Europe that share a nomadic lifestyle or (2) they are of Irish origin, and genetic differences from the rest of Ireland reflect genetic drift. These hypotheses were tested using data on 33 alleles from 12 red blood cell polymorphism loci. Comparison with other European, Roma, and Indian populations shows that the Travellers are genetically distinct from the Roma and Indian populations and most genetically similar to Ireland, in agreement with earlier genetic analyses of the Travellers. However, the Travellers are still genetically distinct from other Irish populations, which could reflect some external gene flow and/or the action of genetic drift in a small group that was descended from a small number of founders. In order to test the drift hypothesis, we analyzed genetic distances comparing the Travellers to four geographic regions in Ireland. These distances were then compared with adjusted distances that account for differential genetic drift using a method developed by Relethford (Hum Biol 68 ( 1996 ) 29–44). The unadjusted distances show the genetic distinctiveness of the Travellers. After adjustment for the expected effects of genetic drift, the Travellers are equidistant from the other Irish samples, showing their Irish origins and population history. The observed genetic differences are thus a reflection of genetic drift, and there is no evidence of any external gene flow. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

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.     

Modelled larval dispersal and measured gene flow: seascape genetics of the common cockle Cerastoderma edule in the southern Irish Sea

The role of marine currents in shaping population connectivity in the common cockle Cerastoderma edule was investigated in the southern Irish Sea. C. edule is one of the most valuable and exploited shellfish species in the area, yet very little is known about its population dynamics. In the present study, coupled hydrodynamic and particle tracking models are used in conjunction with genetic data collected at twelve microsatellite loci to estimate the influence of the Celtic Sea front on larval transport between the coasts of Britain and Ireland. Genetic analysis highlights the presence of at least three genetic clusters partitioned within locations, suggesting a contact zone between separate subpopulations. Samples collected from the Irish coast are most similar to each other. On the British coast, the Burry Inlet appears genetically isolated while samples collected from the coast of Pembrokeshire show evidence of connectivity between Britain and Ireland. These results agree with the model’s predictions: away from the coastal zone, residual baroclinic currents develop along tidal mixing fronts and act as conduit systems, transporting larvae great distances. Larvae spawned in south Wales are capable of travelling west towards Ireland due to the Celtic Sea front residual current, confirming the action of the Celtic Sea front on larval transport. Sheltered, flood-dominant estuaries such as the Burry Inlet promote self-recruitment. The validation of the model using genetic data represents progress towards a sustainable future for the common cockle, and paves the way for a more effective approach to management of all Irish Sea shellfisheries.     

Movements of salmon Salmo salar (L.) to and from Irish waters

Fish tagged as kelts at a number of Irish stations have been recaptured outside Irish waters along the coasts of Great Britain, Norway and West Greenland. Salmon tagged as smolts in three Irish rivers have been recaptured off the coast of West Greenland and one off the Faroes. Sixteen fish tagged as smolts in Denmark, Great Britain and Sweden were recaptured in Irish rivers or on the coastline of Ireland. Clean salmon tagged in the open sea have travelled to the coasts of Great Britain and a single fish travelled to southern Sweden. Feeding salmon tagged off West Greenland, in the Labrador sea and off the Faroes have been recaptured in Irish waters.     

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.     

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.     

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.     

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.     

A genetic analysis of grey squirrel (Sciurus carolinensis) populations in Ireland

Biological Invasions - The grey squirrel (Sciurus carolinensis) is an invasive rodent in Ireland that has had detrimental impacts on the native Irish red squirrel (S. vulgaris) as well as on...     

Adaptive and neutral genetic differentiation among Scottish and endangered Irish red grouse (<Emphasis Type="Italic">Lagopus lagopus scotica</Emphasis>)

Studying patterns of intra-specific genetic variation among populations allows for a better understanding of population structure and local adaptation. However, those patterns may differ according to the genetic markers applied, as neutral genetic markers reflect demographic processes and random genetic drift, whereas adaptive markers also carry the footprint of selection. In combination, neutral and adaptive genetic markers permit to assess the relative roles of drift and selection in shaping population structure. Among the best understood adaptive genetic loci are the genes of the major histocompatibility complex (MHC). We here study variation and differentiation at neutral SNP markers and MHC class II genes in red grouse (Lagopus lagopus scotica) from Ireland and Scotland. Irish red grouse populations are fragmented and drastically declining, but red grouse are abundant in Scotland. We find evidence for positive selection acting on the MHC genes and variation in MHC gene copy numbers among Irish individuals. Furthermore, there was significant population differentiation among red grouse from Ireland and Scotland at the neutral SNP markers (F_ST = 0.084) and the MHC-BLB genes (F_ST: BLB1 = 0.116, BLB2 = 0.090, BLB3 = 0.104). Differentiation at the MHC-BLB1 was significantly higher than at the neutral SNP markers, suggesting that selection plays an important role in shaping MHC variation, in addition to genetic drift. We speculate that the observed differentiation pattern might be due to local adaptation to different parasite regimes. These findings have strong conservation implications and we advise against the introduction of Scottish red grouse to supplement Irish populations.     

Sourcing Eurasian beaver Castor fiber stock for reintroductions in Great Britain and Western Europe

• 1 Eurasian beavers Castor fiber, formerly threatened with extinction, have been widely reintroduced since the 1920s. Reintroductions and studies of possible reintroductions are continuing.
• 2 The International Union for Conservation of Nature (IUCN) guidelines for reintroductions state that ‘the source population should ideally be closely related genetically to the original native stock’.
• 3 Palaeoecological studies suggest that the species survived the last Ice Age in two refugia: in the west in Iberia and Southern France and in the east in the Black Sea region. The post‐Ice Age population of Western Europe, including Great Britain, recolonized from the western refugium. Recent mitochondrial deoxyribonucleic acid studies strongly support this view, and extant beaver populations are clearly divided into eastern and western evolutionarily significant units (ESUs).
• 4 The western ESU is composed of three stocks which survived the 19th and early 20th century as very small, isolated populations. They are very closely related to each other. Each is genetically depauperate, apparently as a result of genetic drift at low population levels.
• 5 There is evidence of inbreeding depression and of phenotypic abnormalities in beaver populations descended from unmixed stocks.
• 6 The evidence suggests three coherent management options for sourcing reintroduction stock for Great Britain and for unoccupied areas of western continental Europe. These are (i) use animals from a single western ESU stock; (ii) intentionally mix animals from two or all three of the surviving western ESU stocks; (iii) make an informed exception to the IUCN guidelines and reintroduce animals of mixed eastern and western ESU provenance.
• 7 These options are discussed with regard to IUCN guidelines, conservation biology and animal welfare considerations. It would be advantageous if a common policy on the origin of reintroduction stock were agreed by the national agencies responsible.

     

Genetic variability and phylogeography of the invasive zebra mussel, Dreissena polymorpha (Pallas)

The zebra mussel, Dreissena polymorpha (Pallas), a bivalve species originally native to the Black and Caspian seas, has invaded Ireland in the last decade. Five microsatellite loci were used to investigate genetic diversity and population structure in 10 populations across Europe (Ireland, UK, the Netherlands and Romania) and the Great Lakes (Lake Ontario and Lake St Clair). Levels of allelic diversity and mean expected heterozygosity were high for all populations (mean number of alleles/locus and H(E) were 10-15.2 and 0.79-0.89, respectively). High levels of polymorphism observed in Irish populations suggest that the Irish founder population(s) were large and/or several introductions took place after foundation. Significant deficits of heterozygotes were recorded for all populations, and null alleles were the most probable factor contributing to these deficits. Pairwise comparisons using Fisher exact tests and F(ST) values revealed little genetic differentiation between Irish populations. The UK sample was not significantly differentiated from the Irish samples, most probably reflecting an English origin for Irish zebra mussels. No significant differentiation was detected between the two Great Lakes populations. Our data support a northwest rather than a central or east European source for North American zebra mussels.     

Genetic diversity within and between British and Irish breeds: The maternal and paternal history of native ponies

The UK and Ireland have many native pony breeds with historical and cultural importance as well as being a source of uncharacterized genetic diversity. However, there is a lack of comprehensive research investigating their genetic diversity and phylogenetic interrelationships. Many studies contain a limited number of pony breeds or small sample sizes for these breeds. This may result in erroneous grouping of pony breeds that otherwise have intricate interrelationships with each other and are not evaluated correctly when placed as a token subset of a larger dataset. This is the first study that specifically investigates the genetic diversity within and between British and Irish native pony breeds using large sample numbers from locations of their native origin. This study used a panel of microsatellite markers and sequence analysis of the mitochondrial control region to analyze the genetic diversity within and between 11 pony breeds from Britain and Ireland. A large dataset was collected (a total of 485 animals were used for mtDNA analysis and 450 for microsatellite analysis), and previously published data were used to place the British and Irish ponies in a global context. The native ponies of Britain and Ireland were found to have had a complex history, and the interrelationships between the breeds were revealed. Overall, high levels of genetic diversity were maintained in native breeds, although some reduction was evident in small or isolated populations (Shetland, Carneddau, and Section C). Unusual mitochondrial diversity distribution patterns were apparent for the Carneddau and Dartmoor, although among breeds and global haplogroups there was a high degree of haplotype sharing evident, well‐represented within British and Irish ponies. Ancestral maternal diversity was maintained by most populations, particularly the Fells and Welsh ponies, which exhibited rare and ancient lineages. The maternal and paternal histories of the breeds are distinct, with male‐biased crossings between native breeds, and other shared influences, likely Arabs and Thoroughbreds, are apparent. The data generated herein provide valuable information to guide and implement the conservation of increasingly rare native genetic resources.     

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, ?? , ??–??.     

Effects of Parasitism and Morphology on Squirrelpox Virus Seroprevalence in Grey Squirrels (Sciurus carolinensis)

Invasive species have been cited as major causes of population extinctions in several animal and plant classes worldwide. The North American grey squirrel (Sciurus carolinensis) has a major detrimental effect on native red squirrel (Sciurus vulgaris) populations across Britain and Ireland, in part because it can be a reservoir host for the deadly squirrelpox virus (SQPV). Whilst various researchers have investigated the epizootiology of SQPV disease in grey squirrels and have modelled the consequent effects on red squirrel populations, less work has examined morphological and physiological characteristics that might make individual grey squirrels more susceptible to contracting SQPV. The current study investigated the putative relationships between morphology, parasitism, and SQPV exposure in grey squirrels. We found geographical, sex, and morphological differences in SQPV seroprevalence. In particular, larger animals, those with wide zygomatic arch widths (ZAW), males with large testes, and individuals with concurrent nematode and/or coccidial infections had an increased seroprevalence of SQPV. In addition, males with larger spleens, particularly those with narrow ZAW, were more likely to be exposed to SQPV. Overall these results show that there is variation in SQPV seroprevalence in grey squirrels and that, consequently, certain individual, or populations of, grey squirrels might be more responsible for transmitting SQPV to native red squirrel populations.     

Mitogenomic analysis of the Australian lungfish (<Emphasis Type="Italic">Neoceratodus forsteri</Emphasis>) reveals structuring of indigenous riverine populations and late Pleistocene movement between drainage basins

Neoceratodus forsteri: is a freshwater species of Dipnoan currently listed as ‘vulnerable to extinction’ under Australian legislation. The species is restricted to at least two indigenous riverine populations in southeastern Queensland, and several other putatively translocated populations. Current understanding of genetic relationships among populations is based on studies of allozymes, microsatellites and mitochondrial DNA (mtDNA) fragments. A notable feature of all these datasets was low genetic variability. Here we sequence the complete mitogenome of 71 N. forsteri individuals from five populations to improve resolution of mtDNA diversity, examine relationships among populations, and evaluate recent demographic history. We recorded 137 variable positions forming 41 haplotypes in the 16,573 bp mitogenome alignment. Strong genetic structure was observed among riverine samples (global Φ_ST?=?0.342) in a pattern consistent with translocation history. Tinana Creek was confirmed as an isolated and genetically unique subpopulation that should be recognized as a distinct management unit. Two previously unreported mtDNA clades (0.46% mean divergence) were found and suggest that genetic exchange among coastal catchments may have been facilitated by riverine connections on the exposed continental shelf during the late Pleistocene. Extended Bayesian skyline analysis showed no evidence for recent historical change in female effective population size, and codon-based selection tests found no evidence for positive selection in coding genes. Overall, our results emphasise the utility of the full mtDNA molecule for capturing population structure in taxa with low genetic diversity. In such cases, informative variation may be scattered across disparate parts of the mitogenome. Surveying relatively short fragments of mtDNA may lead to significant underestimates of population structure when applied to threatened species with low genetic diversity.