Allan D. McDevitt

Human selection of elk behavioural traits in a landscape of fear

Among agents of selection that shape phenotypic traits in animals, humans can cause more rapid changes than many natural factors. Studies have focused on human selection of morphological traits, but little is known about human selection of behavioural traits. By monitoring elk (Cervus elaphus) with satellite telemetry, we tested whether individuals harvested by hunters adopted less favourable behaviours than elk that survived the hunting season. Among 45 2-year-old males, harvested elk showed bolder behaviour, including higher movement rate and increased use of open areas, compared with surviving elk that showed less conspicuous behaviour. Personality clearly drove this pattern, given that inter-individual differences in movement rate were present before the onset of the hunting season. Elk that were harvested further increased their movement rate when the probability of encountering hunters was high (close to roads, flatter terrain, during the weekend), while elk that survived decreased movements and showed avoidance of open areas. Among 77 females (2–19 y.o.), personality traits were less evident and likely confounded by learning because females decreased their movement rate with increasing age. As with males, hunters typically harvested females with bold behavioural traits. Among less-experienced elk (2–9 y.o.), females that moved faster were harvested, while elk that moved slower and avoided open areas survived. Interestingly, movement rate decreased as age increased in those females that survived, but not in those that were eventually harvested. The latter clearly showed lower plasticity and adaptability to the local environment. All females older than 9 y.o. moved more slowly, avoided open areas and survived. Selection on behavioural traits is an important but often-ignored consequence of human exploitation of wild animals. Human hunting could evoke exploitation-induced evolutionary change, which, in turn, might oppose adaptive responses to natural and sexual selection.

Survival in the Rockies of an endangered hybrid swarm from diverged caribou (Rangifer tarandus) lineages

In North America, caribou (Rangifer tarandus) experienced diversification in separate refugia before the last glacial maximum. Geographical isolation produced the barren‐ground caribou (Rangifer tarandus groenlandicus) with its distinctive migratory habits, and the woodland caribou (Rangifer tarandus caribou), which has sedentary behaviour and is now in danger of extinction. Herein we report on the phylogenetics, population structure, and migratory habits of caribou in the Canadian Rockies, utilizing molecular and spatial data for 223 individuals. Mitochondrial DNA analyses show the occurrence of two highly diverged lineages; the Beringian–Eurasian and North American lineages, while microsatellite data reveal that present‐day Rockies’ caribou populations have resulted from interbreeding between these diverged lineages. An ice‐free corridor at the end of the last glaciation likely allowed, for the first time, for barren‐ground caribou to migrate from the North and overlap with woodland caribou expanding from the South. The lack of correlation between nuclear and mitochondrial data may indicate that different environmental forces, which might also include human‐caused habitat loss and fragmentation, are currently reshaping the population structure of this postglacial hybrid swarm. Furthermore, spatial ecological data show evidence of pronounced migratory behaviour within the study area, and suggest that the probability of being migratory may be higher in individual caribou carrying a Beringian–Eurasian haplotype which is mainly associated with the barren‐ground subspecies. Overall, our analyses reveal an intriguing example of postglacial mixing of diverged lineages. In a landscape that is changing due to climatic and human‐mediated factors, an understanding of these dynamics, both past and present, is essential for management and conservation of these populations.

The Celtic fringe of Britain: insights from small mammal phylogeography

Recent genetic studies have challenged the traditional view that the ancestors of British Celtic people spread from central Europe during the Iron Age and have suggested a much earlier origin for them as part of the human recolonization of Britain at the end of the last glaciation. Here we propose that small mammals provide an analogue to help resolve this controversy. Previous studies have shown that common shrews (Sorex araneus) with particular chromosomal characteristics and water voles (Arvicola terrestris) of a specific mitochondrial (mt) DNA lineage have peripheral western/northern distributions with striking similarities to that of Celtic people. We show that mtDNA lineages of three other small mammal species (bank vole Myodes glareolus, field vole Microtus agrestis and pygmy shrew Sorex minutus) also form a ‘Celtic fringe’. We argue that these small mammals most reasonably colonized Britain in a two-phase process following the last glacial maximum (LGM), with climatically driven partial replacement of the first colonists by the second colonists, leaving a peripheral geographical distribution for the first colonists. We suggest that these natural Celtic fringes provide insight into the same phenomenon in humans and support its origin in processes following the end of the LGM.

Preferred habitat and effective population size drive landscape genetic patterns in an endangered species

Landscape genetics provides a framework for pinpointing environmental features that determine the important exchange of migrants among populations. These studies usually test the significance of environmental variables on gene flow, yet ignore one fundamental driver of genetic variation in small populations, effective population size, Ne. We combined both approaches in evaluating genetic connectivity of a threatened ungulate, woodland caribou. We used least-cost paths to calculate matrices of resistance distance for landscape variables (preferred habitat, anthropogenic features and predation risk) and population-pairwise harmonic means of Ne, and correlated them with genetic distances, FST and Dc. Results showed that spatial configuration of preferred habitat and Ne were the two best predictors of genetic relationships. Additionally, controlling for the effect of Ne increased the strength of correlations of environmental variables with genetic distance, highlighting the significant underlying effect of Ne in modulating genetic drift and perceived spatial connectivity. We therefore have provided empirical support to emphasize preventing increased habitat loss and promoting population growth to ensure metapopulation viability.

Reconstruction of caribou evolutionary history in Western North America and its implications for conservation

The role of Beringia as a refugium and route for trans‐continental exchange of fauna during glacial cycles of the past 2 million years are well documented; less apparent is its contribution as a significant reservoir of genetic diversity. Using mitochondrial DNA sequences and 14 microsatellite loci, we investigate the phylogeographic history of caribou (Rangifer tarandus) in western North America. Patterns of genetic diversity reveal two distinct groups of caribou. Caribou classified as a Northern group, of Beringian origin, exhibited greater number and variability in mtDNA haplotypes compared to a Southern group originating from refugia south of glacial ice. Results indicate that subspecies R. t. granti of Alaska and R. t. groenlandicus of northern Canada do not constitute distinguishable units at mtDNA or microsatellites, belying their current status as separate subspecies. Additionally, the Northern Mountain ecotype of woodland caribou (presently R. t. caribou) has closer kinship to caribou classified as granti or groenlandicus. Comparisons of mtDNA and microsatellite data suggest that behavioural and ecological specialization is a more recently derived life history characteristic. Notably, microsatellite differentiation among Southern herds is significantly greater, most likely as a result of human‐induced landscape fragmentation and genetic drift due to smaller population sizes. These results not only provide important insight into the evolutionary history of northern species such as caribou, but also are important indicators for managers evaluating conservation measures for this threatened species.

Colonization of Ireland: revisiting ‘the pygmy shrew syndrome’ using mitochondrial, Y chromosomal and microsatellite markers

There is great uncertainty about how Ireland attained its current fauna and flora. Long-distance human-mediated colonization from southwestern Europe has been seen as a possible way that Ireland obtained many of its species; however, Britain has (surprisingly) been neglected as a source area for Ireland. The pygmy shrew has long been considered an illustrative model species, such that the uncertainty of the Irish colonization process has been dubbed ‘the pygmy shrew syndrome’. Here, we used new genetic data consisting of 218 cytochrome (cyt) b sequences, 153 control region sequences, 17 Y-intron sequences and 335 microsatellite multilocus genotypes to distinguish between four possible hypotheses for the colonization of the British Isles, formulated in the context of previously published data. Cyt b sequences from western Europe were basal to those found in Ireland, but also to those found in the periphery of Britain and several offshore islands. Although the central cyt b haplotype in Ireland was found in northern Spain, we argue that it most likely occurred in Britain also, from where the pygmy shrew colonized Ireland as a human introduction during the Holocene. Y-intron and microsatellite data are consistent with this hypothesis, and the biological traits and distributional data of pygmy shrews argue against long-distance colonization from Spain. The compact starburst of the Irish cyt b expansion and the low genetic diversity across all markers strongly suggests a recent colonization. This detailed molecular study of the pygmy shrew provides a new perspective on an old colonization question.

Land-Bridge Calibration of Molecular Clocks and the Post-Glacial Colonization of Scandinavia by the Eurasian Field Vole Microtus agrestis

Phylogeography interprets molecular genetic variation in a spatial and temporal context. Molecular clocks are frequently used to calibrate phylogeographic analyses, however there is mounting evidence that molecular rates decay over the relevant timescales. It is therefore essential that an appropriate rate is determined, consistent with the temporal scale of the specific analysis. This can be achieved by using temporally spaced data such as ancient DNA or by relating the divergence of lineages directly to contemporaneous external events of known time. Here we calibrate a Eurasian field vole (Microtus agrestis) mitochondrial genealogy from the well-established series of post-glacial geophysical changes that led to the formation of the Baltic Sea and the separation of the Scandinavian peninsula from the central European mainland. The field vole exhibits the common phylogeographic pattern of Scandinavian colonization from both the north and the south, however the southernmost of the two relevant lineages appears to have originated in situ on the Scandinavian peninsula, or possibly in the adjacent island of Zealand, around the close of the Younger Dryas. The mitochondrial substitution rate and the timescale for the genealogy are closely consistent with those obtained with a previous calibration, based on the separation of the British Isles from mainland Europe. However the result here is arguably more certain, given the level of confidence that can be placed in one of the central assumptions of the calibration, that field voles could not survive the last glaciation of the southern part of the Scandinavian peninsula. Furthermore, the similarity between the molecular clock rate estimated here and those obtained by sampling heterochronous (ancient) DNA (including that of a congeneric species) suggest that there is little disparity between the measured genetic divergence and the population divergence that is implicit in our land-bridge calibration.

Revisiting the phylogeography and demography of European badgers (Meles meles) based on broad sampling, multiple markers and simulations

Although the phylogeography of European mammals has been extensively investigated since the 1990s, many studies were limited in terms of sampling distribution, the number of molecular markers used and the analytical techniques employed, frequently leading to incomplete postglacial recolonisation scenarios. The broad-scale genetic structure of the European badger (Meles meles) is of interest as it may result from historic restriction to glacial refugia and/or recent anthropogenic impact. However, previous studies were based mostly on samples from western Europe, making it difficult to draw robust conclusions about the location of refugia, patterns of postglacial expansion and recent demography. In the present study, continent-wide sampling and analyses with multiple markers provided evidence for two glacial refugia (Iberia and southeast Europe) that contributed to the genetic variation observed in badgers in Europe today. Approximate Bayesian computation provided support for a colonisation of Scandinavia from both Iberian and southeastern refugia. In the whole of Europe, we observed a decline in genetic diversity with increasing latitude, suggesting that the reduced diversity in the peripheral populations resulted from a postglacial expansion processes. Although MSVAR v.1.3 also provided evidence for recent genetic bottlenecks in some of these peripheral populations, the simulations performed to estimate the method’s power to correctly infer the past demography of our empirical populations suggested that the timing and severity of bottlenecks could not be established with certainty. We urge caution against trying to relate demographic declines inferred using MSVAR with particular historic or climatological events.

Landscape genetic approaches in conservation biology and management

Landscape genetics is an integrative field of research that combines approaches from population genetics, landscape ecology, and spatial statistics (Manel et al. 2003; Storfer et al. 2007). It seeks to understand the influence of ecological and environmental constraints on genetic variation by quantifying the relationship between landscape features, genetic diversity and spatial genetic structure. The field is developing rapidly due to recent advances in molecular laboratory technologies, environmental data acquisition, and spatial analytical methods that can relate landscape and genetic data in meaningful ways (Storfer et al. 2010). The integrated approach allows an assessment of the impact of landscape composition, configuration, and matrix quality on the spatial distribution of neutral and adaptive genetic variation and associated microevolutionary processes across natural populations (Holderegger and Wagner 2008; Balkenhol et al. 2009; Manel et al. 2010; Segelbacher et al. 2010; Epperson et al. 2010). This understanding is crucial in order to promote research in evolutionary ecology and genetics, but also has tremendous potential for applied management and conservation of threatened or endangered plant and animal species (Sork and Waits 2010). It allows us to identify the effects of anthropogenic barriers that reduce gene flow or genetic diversity, and to predict the long-term effects of proposed management alternatives and specific reserve and corridor designs on genetic variation and population connectivity (Storfer et al. 2007). This special issue includes 23 contributions spanning different aspects of landscape genetic research. It covers recent conceptual developments, study design and sampling considerations, and illustrates the usefulness and importance of integrated landscape genetic approaches in empirical applications to different taxonomic levels in plants, invertebrates and vertebrates.

Invading and expanding : range dynamics and ecological consequences of the Greater White-Toothed Shrew (Crocidura russula) invasion in Ireland

Establishing how invasive species impact upon pre-existing species is a fundamental question in ecology and conservation biology. The greater white-toothed shrew (Crocidura russula) is an invasive species in Ireland that was first recorded in 2007 and which, according to initial data, may be limiting the abundance/distribution of the pygmy shrew (Sorex minutus), previously Irelands only shrew species. Because of these concerns, we undertook an intensive live-trapping survey (and used other data from live-trapping, sightings and bird of prey pellets/nest inspections collected between 2006 and 2013) to model the distribution and expansion of C. russula in Ireland and its impacts on Irelands small mammal community. The main distribution range of C. russula was found to be approximately 7,600 km2 in 2013, with established outlier populations suggesting that the species is dispersing with human assistance within the island. The species is expanding rapidly for a small mammal, with a radial expansion rate of 5.5 km/yr overall (2008–2013), and independent estimates from live-trapping in 2012–2013 showing rates of 2.4–14.1 km/yr, 0.5–7.1 km/yr and 0–5.6 km/yr depending on the landscape features present. S. minutus is negatively associated with C. russula. S. minutus is completely absent at sites where C. russula is established and is only present at sites at the edge of and beyond the invasion range of C. russula. The speed of this invasion and the homogenous nature of the Irish landscape may mean that S. minutus has not had sufficient time to adapt to the sudden appearance of C. russula. This may mean the continued decline/disappearance of S. minutus as C. russula spreads throughout the island.