Population structure and dispersal patterns in Scottish Golden Eagles Aquila chrysaetos revealed by molecular genetic analysis of territorial birds

Conservation management of species distributed across fragmented habitats requires consideration of population genetic structure and relative levels of genetic diversity throughout the relevant geographical range. The Golden Eagle Aquila chrysaetos is monitored within Scotland to ensure its survival in the face of land‐use pressure, persecution and future climate change. In this study we constructed DNA profiles for 271 individual birds using a collection of over 1600 moulted feathers collected from 148 territories, representing 34% of known Scottish territories in the largest population genetic study of Golden Eagles undertaken to date. The results, based on data from 10 nuclear microsatellite loci, revealed previously unreported genetic structure between the islands of the Outer Hebrides and the rest of Scotland (F_ST = 0.03), together with evidence of reduced genetic diversity in the Outer Hebridean population compared with mainland Scotland. Analysis of gene flow supports a hypothesis of limited, predominantly male‐mediated, dispersal from the Outer Hebrides to mainland Scotland. The persistence of this pattern is discussed with respect to variation in population density and persecution pressure across Scotland. A finding of non‐random mating within the Outer Hebrides is interpreted as evidence of natal philopatry that was revealed by more intensive sampling in these islands, and is likely to be accentuated by the apparent degree of isolation of the islands from the rest of Scotland.     

A Y chromosome census of the British Isles

The degree of population replacement in the British Isles associated with cultural changes has been extensively debated. Recent work has demonstrated that comparisons of genetic variation in the British Isles and on the European Continent can illuminate specific demographic processes in the history of the British Isles. For example, Wilson et al. used the similarity of Basque and Celtic Y chromosomes to argue for genetic continuity from the Upper Palaeolithic to the present in the paternal history of these populations (see also ). Differences in the Y chromosome composition of these groups also suggested genetic signatures of Norwegian influence in the Orkney Islands north of the Scottish mainland, an important center of Viking activities between 800 and 1300 A.D. More recently, Weale et al. argued for substantial Anglo-Saxon male migration into central England based on the analysis of eight British sample sets collected on an east-west transect across England and Wales. To provide a more complete assessment of the paternal genetic history of the British Isles, we have compared the Y chromosome composition of multiple geographically distant British sample sets with collections from Norway (two sites), Denmark, and Germany and with collections from central Ireland, representing, respectively, the putative invading and the indigenous populations. By analyzing 1772 Y chromosomes from 25 predominantly small urban locations, we found that different parts of the British Isles have sharply different paternal histories; the degree of population replacement and genetic continuity shows systematic variation across the sampled areas.     

Density compensation in allopatric populations of the pygmy shrewSorex minutus on Gotland and the outer hebrides: evidence for the effect of interspecific competition

Pygmy shrewsSorex minutus occur allopatrically in Ireland, the Outer Hebrides and Gotland in Sweden, and sympatrically with common shrewsS. minutus on the European mainland and in England. Competition theory redicts higher population density in allopatric populations as a consequence of relaxed competition. Here this prediction is tested by comparing allopatric populations of pygmy shrews in the Outer Hebrides and in Gotland with sympatric populations on the Swedish mainland. Population densities were higher in allopatry than in sympatry. Lower summed densities in allopatry, which is predicted by niche theory, was found on the Outer Hebrides, but not on Gotland. Size distributions of carabids, which are important food items, could not explain the differences in population densities. Since both avian predators and snakes are present in all areas, population density of pygmy shrews during autumn in concluded to be regulated primarly by competition with common shrews in areas of sympatry.     

The distribution and status of the adder (Vipera berus L) in Scotland determined from questionnaire surveys

Abstract. During 1992 two questionnaire surveys, aimed at farmers and sections of the general public, were conducted to determine the distribution and status of the adder ( Vipera berus L.) in Scotland. In total, 94% of the Scottish mainland and inner isles were covered by the two surveys. The adder appears to be widespread throughout Scotland, although it is absent from much of the Central Valley, the Outer Hebrides and Northern Isles, and from much of the mountainous region between Inverness and Glasgow.
The distribution of the adder in Scotland was compared with the distributions of different habitat types defined in the ITE Land Class survey. Adders were strongly associated with areas of heterogeneous land use and negatively associated with intensively arable areas and rugged mountainous areas. Strong evidence was found to suggest that perceived adder abundance had declined during the last 10 years. Although the evidence suggesting that the distribution of adders in Scotland had changed was less strong, the results of the Farm Survey did indicate that it had contracted. The perceived change in status of the adder in Scotland during the last 10 years was compared with the observed changes in land use over the same period.     

Genetic signatures of population change in the British golden eagle (<Emphasis Type="Italic">Aquila chrysaetos</Emphasis>)

The golden eagle (Aquila chrysaetos) was once widely distributed in the uplands of the British Isles, but is now extinct in Ireland, and largely confined to the highlands and islands of Scotland. As the precise extent and severity of the reduction in population size are unclear, it is important to understand how the population was affected by the decline. We therefore genotyped 13 polymorphic microsatellite loci in 172 individuals from the contemporary British population and compared their genetic diversity to 70 British and 9 Irish museum specimens. Despite the recent population decline, there is only slight evidence for a concomitant loss of genetic variation. Instead, two likelihood-based Bayesian methods provided evidence for a severe ancient genetic bottleneck, possibly caused by the fragmentation of a large mainland European population and/or the founding effects of colonising the British Isles. As the population persisted despite this ancient bottleneck, our conclusion is that there is limited need for intervention to augment the present-day genetic diversity. The main short-term objective of conservation measures should be to increase population sizes by continuous safeguarding of individuals and habitat management. Finally, we also confirmed that, for management purposes, the species should be considered a single population unit and that the extinct Irish population was not differentiated from the British one.     

Island Populations, Human Introductions and the Limitations of Genetic Analyses: the Case of the Sardinian Red Deer (Cervus elaphus corsicanus)

The Corsican red deer (Cervus elaphus corsicanus) is endemic to the Tyrrhenian islands of Corsica and Sardinia. It has been regarded as an introduced species and has allegedly been present on the islands since the beginning of the Neolithic culture some 8,000 years ago. In this review, we present the results of relevant genetic analyses and discuss their implications for the origin of C. e. corsicanus. Different genetic studies hypothesize that the most probable ancestral populations for Sardianian red deer were alternatively, the Near East, North Africa, or mainland Italy. These respective scenarios are evaluated and it is concluded that geneticists have not yet been unable to definitively solve the problem. However, a natural colonization of the Tyrrhenian islands from mainland Italy via the Tuscan archipelago is not only in accordance with palaeontological findings but also with at least some of the genetic data.     

Variation in coat colour gene frequencies and selection in the cats of Scotland

Estimates of Felis catus coat colour gene frequencies were obtained from samples in 27 Scottish localities. These areas ranged from island samples in Shetland, Orkney and the Outer Hebrides to remote highland areas on the Scottish mainland. Animals from several towns and cities were also sampled. The results reveal considerable heterogeneity in the frequencies of the O, a, t ^b, l, S and W alleles. The frequencies of d were relatively homogeneous throughout Scotland. There were indications that island and mainland cat populations may have been derived from separate ancestral gene pools. Much of the observed gene frequency heterogeneity in rural areas could be attributed to differential migration or lack of penetrance. Geographical isolation and possible hybridization with F. sylvestris may explain the high frequency of wild-type alleles in mainland rural areas. A correlation between cat population coefficient of darkness and human population was observed. Such an observation supports the concept of cumulative urban pressure and indicates that a process analogous to industrial melanism is occurring in urban cat populations. The darkening of phenotype appears to be acting through the t, a and O loci and may be the result of pleiotropic effects of alleles at these loci.     

The colonization of Scottish islands by the common shrew, Sorex araneus (Eulipotyphla: Soricidae)

In this paper we apply molecular methods to study the colonization of islands off the west coast of Scotland by the common shrew ( Sorex araneus L.), and current gene flow. We collected 497 individuals from 13 islands of the Inner Hebrides and Clyde Island groups and six mainland regions. Individuals were genotyped at eight microsatellite loci, and the mitochondrial cytochrome b sequence (1140 base pairs) was obtained for five individuals from each island/mainland region. Based on these molecular data, island colonization apparently proceeded directly from the mainland, except for Islay, for which Jura was the most likely source population. Raasay may also have been colonized by island hopping. Most island populations are genetically very distinct from the mainland populations, suggesting long periods of isolation. Two exceptions to this are the islands of Skye and Seil, which are geographically and genetically close to the mainland, suggesting in each case that there has been long-term gene flow between these islands and the mainland. We consider possible methods of island colonization, including human-mediated movement, swimming, and land and ice bridges.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 797–808.     

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.     

THE RACES OF TURDUS ERICETORUM INDIGENOUS TO THE BRITISH ISLES

The diagnostic criteria, ranges, hybrid zones, and migrations of the three indigenous British races of Turdus ericetorum are defined. The migratory dispersal of T. e. catherinœ is traced, and its identity as the innominate "small, dark migrant Song-thrush" of workers is established. An explanation of the distributions of T. ericetorum races in the British Isles is advanced. T. e. ericetorum and T. e. hebridensis are ascertained to be moderately migratory, T. e. catherinœ strongly so. The findings on early records of T. e. hebridensis on passage evidence confusion between that form and T. e. catherinœ. Irish, Stornoway (Lewis, Outer Hebrides), and Orkney and Shetland breeding populations require further racial study.     

Elytral polymorphism in spittlebugs: Philaenus spumarius (L.) from the Inner Hebrides

The frequencies of colour and pattern morphs of the elytra of Philaenus spumarius are similar on three of the Small Isles of the Inner Hebrides (Eigg, Canna and Muck); the population on the fourth island (Rhum: is somewhat distinct but is like that at sea level on the nearby mountainous mainland. These similarities and differences suggest that these morph frequencies are regulated by natural selection.     

Chance and change in British Long-tailed field mice: (Apodemus sylvaticus)

The Long-tailed field mouse ( Apodemus sylvaticus (L.)) has undergone a marked degree of racial differentiation on the islands of the north-west Atlantic (Iceland, Shetland, and the Hebrides). The differences have arisen as a result of the colonization of these islands after the Pleistocene by small numbers of animals carrying alleles in different proportions to those in the parental population. In contrast, the populations on some islands to the south of Britain (Jersey and Guernsey in the Channel Isles, and St. Mary's in the Isles of Scilly) are similar to A. sylvaticus from the mainland of Britain, and are likely to represent the descendants of mice which survived the Ice Ages ( A. sylvaticus populations on the smaller islands–Alderney, Sark, Herm and Tresco–differ markedly from their closest relatives, and probably represent the results of recolonization following extinction in the same way as on the glaciated islands to the north).
On the mainland of Britain there is a fairly clear distinction between two groups: western and central populations, and eastern ones (which have closer affinities to French mice than western British ones). It is suggested that the two mainland British "races" may have diverged in Pleistocene refuges. Since no pelage or size genes are involved in the divergence, it would not be expected that they would be taxonomically distinct.
The data on which these conclusions are based derive from the incidence of 20 nonmetrical variants in the skulls of 1096 mice from 22 series.     

Genetic diversity in the Eurasian otter, Lutra lutra, in Scotland. Evidence from microsatellite polymorphism

The relationship between microsatellite diversity and geographical fragmentation and isolation was studied in Scottish populations of the Eurasian otter, Lutra lutra. The geographic range of the study encompassed isolated archipelagos, islands adjacent to the Scottish mainland and both fragmented and continuous mainland populations. Tissue samples of 496 individuals from across Scotland were assayed for polymorphism at ten microsatellites. The isolation of populations on Shetland, and to a lesser degree on Orkney, was associated with reduced levels of microsatellite diversity. Most of the remaining island and fragmented mainland populations contained levels of microsatellite diversity similar to the high levels observed in die continuous mainland populations. Unexpectedly, both island and continuous mainland populations showed similar rates of departures from mutation-drift equilibrium. Such departures could have arisen from a variety of local demographic processes besides population bottlenecks. Gene flow appeared to be a major factor maintaining microsatellite diversity in all of these populations except the one on Shedand.     

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.     

mtDna and the islands of the North Atlantic: estimating the proportions of Norse and Gaelic ancestry

A total of 1,664 new mtDNA control-region sequences were analyzed in order to estimate Gaelic and Scandinavian matrilineal ancestry in the populations of Iceland, Orkney, the Western Isles, and the Isle of Skye and to investigate other aspects of their genetic history. A relative excess of private lineages in the Icelanders is indicative of isolation, whereas the scarcity of private lineages in Scottish island populations may be explained by recent gene flow and population decline. Differences in the frequencies of lineage clusters are observed between the Scandinavian and the Gaelic source mtDNA pools, and, on a continent-wide basis, such differences between populations seem to be associated with geography. A multidimensional scaling analysis of genetic distances, based on mtDNA lineage-cluster frequencies, groups the North Atlantic islanders with the Gaelic and the Scandinavian populations, whereas populations from the central, southern, and Baltic regions of Europe are arranged in clusters in broad agreement with their geographic locations. This pattern is highly significant, according to a Mantel correlation between genetic and geographic distances (r=.716). Admixture analyses indicate that the ancestral contributions of mtDNA lineages from Scandinavia to the populations of Iceland, Orkney, the Western Isles, and the Isle of Skye are 37.5%, 35.5%, 11.5%, and 12.5%, respectively.     

Genetic structure of,and hybridisation between,red (Cervus elaphus) and sika (Cervus nippon) deer in Ireland

This study investigated the levels of genetic diversity and variation exhibited by red and sika deer in Ireland, along with the extent and regional location of hybridisation between these two species. Bi-parental (microsatellites) and maternally-inherited (mitochondrial DNA) genetic markers were utilised that allowed comparisons between 85 red deer from six localities and 47 sika deer from 3 localities in Ireland. Population genetic structure was assessed using Bayesian analysis, indicating the existence of two genetic clusters in sika deer and three clusters in red deer. Levels of genetic diversity were low in both red and sika deer. These genetic data presented herein indicate a recent introduction of sika deer and subsequent translocations in agreement with historical data. The origins of the current red deer populations found in Ireland, based on genetic data presented in this study, still remain obscure. All hybrid deer (red/sika) found in this study were found in Wicklow, Galway and Mayo where the ‘red-like’ deer exhibited sika deer alleles/haplotypes, and vice versa in the case of Wicklow. Molecular methods proved invaluable in the identification of the hybrid deer because identification of hybrids based on phenotypic external appearances (pelage and body proportions) can be misleading. Areas where red and sika deer are sympatric need to be assessed for the level and extent of hybridisation occurring and thus need to be managed in order to protect the genetic integrity of ‘pure’ red deer populations.     

Breeding Population of the Ringed Plover in Britain

A census of Ringed Plovers in Britain in 1973–74 revealed a total of over 5,700 pairs, with the best concentrations in eastern England (particularly in Norfolk and Essex), the Outer Hebrides, Orkney and Shetland. Some interesting recent changes in habitat are chronicled.     

Divergent evolutionary processes associated with colonization of offshore islands

Oceanic islands have been a test ground for evolutionary theory, but here, we focus on the possibilities for evolutionary study created by offshore islands. These can be colonized through various means and by a wide range of species, including those with low dispersal capabilities. We use morphology, modern and ancient sequences of cytochrome b (cytb) and microsatellite genotypes to examine colonization history and evolutionary change associated with occupation of the Orkney archipelago by the common vole (Microtus arvalis), a species found in continental Europe but not in Britain. Among possible colonization scenarios, our results are most consistent with human introduction at least 5100 bp (confirmed by radiocarbon dating). We used approximate Bayesian computation of population history to infer the coast of Belgium as the possible source and estimated the evolutionary timescale using a Bayesian coalescent approach. We showed substantial morphological divergence of the island populations, including a size increase presumably driven by selection and reduced microsatellite variation likely reflecting founder events and genetic drift. More surprisingly, our results suggest that a recent and widespread cytb replacement event in the continental source area purged cytb variation there, whereas the ancestral diversity is largely retained in the colonized islands as a genetic ‘ark’. The replacement event in the continental M. arvalis was probably triggered by anthropogenic causes (land‐use change). Our studies illustrate that small offshore islands can act as field laboratories for studying various evolutionary processes over relatively short timescales, informing about the mainland source area as well as the island.     

A new method of salt pan formation in intertidal marshes

Summary

Records of fungi occurring in the Hebrides are extended, particularly for Jura and Islay where, respectively, 40 and 47 taxa are recorded for the first time. Twenty taxa are added to the list for Rhum and 89 to that for Colonsay. Additional fungi are also reported for Hirta (St. Kilda) , Bernary, Mingulay, Barra and South Uist in the Outer Hebrides, and Eigg and Canna in the Inner Hebrides.     

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.