Characterization of microsatellite DNA loci for the southern flying squirrel (Glaucomys volans)

Polymerase chain reaction primers for microsatellite DNA loci (one dinucleotide, four tetranucleotide and two compound) and the conditions necessary to amplify each are described for the southern flying squirrel (Glaucomys volans). These primers were tested on 22 or more individuals from a population at the Savannah River Site in South Carolina. These microsatellite primers yielded a high allelic diversity (6–22 alleles/locus), and moderate to high observed heterozygosities (0.318–0.826). Primers developed for the northern flying squirrel (Glaucomys sabrinus) were also tested for use on G. volans, with only two successful cross amplifications from the seven loci.     

Microsatellite loci for the Siberian flying squirrel,Pteromys volans

We report the isolation and characterization of polymorphic microsatellite loci for the Siberian flying squirrel Pteromys volans. The seven most useful loci had between six and 11 alleles and expected heterozygosities ranging from 0.477 to 0.866. We also tested the utility of these loci in other squirrel species, northern flying squirrels (Glaucomys sabrinus and G. volans) and the common red squirrel (Sciurus vulgaris). Three of the Siberian flying squirrel loci were polymorphic in other squirrel species, suggesting a limited potential for cross‐species use.     

Climate change induced hybridization in flying squirrels

There is now unequivocal evidence for global climate change; however, its potential impacts on evolutionary processes remain unclear. Many species have responded to contemporary climate change through shifts in their geographic range. This could lead to increased sympatry between recently diverged species; likely increasing the potential for hybridization. Recently, following a series of warm winters, southern flying squirrels ( Glaucomys volans ) in Ontario, Canada rapidly expanded their northern range limit resulting in increased sympatry with the closely related northern flying squirrel ( Glaucomys sabrinus ). This provided the opportunity to test the prediction that contemporary climate change can act as a catalyst creating conditions for the formation of hybrid zones. Following extensive sampling and molecular analyses (nuclear and mitochondrial DNA), we identified the occurrence of hybridization between sympatric G. sabrinus and G. volans . There was evidence of backcrossing but not of extensive introgession, consistent with the hypothesis of recent rather than historic hybridization. To our knowledge, this is the first report of hybrid zone formation following a range expansion induced by contemporary climate change. This is also the first report of hybridization between North American flying squirrel species.     

Patch occupancy by squirrels in fragmented deciduous forest: effects of behavior

We tested whether species-specific behavioral traits could explain patterns of habitat patch occupancy by five different squirrel species in Ontario, Canada: the northern and southern flying squirrel (Glaucomys sabrinus and Glaucomys volans), the North American red squirrel (Tamiasciurus hudsonicus), the eastern chipmunk (Tamias striatus), and the eastern gray squirrel (Sciurus carolinensis). Flying squirrel species exhibit group nesting in winter, which may put them at risk of extirpation in small patches with few individuals to contribute to group nests. Flying squirrels are also volant, potentially making non-treed matrix a barrier. Our surveys revealed that G. sabrinus was most likely to occur in large patches that were embedded in landscapes with low connectivity, and least likely to occur in small patches in highly connected landscapes. Conversely, G. volans was most likely to occur in large, well-connected patches and least likely to occur in small, unconnected patches. Patch occupancy by the cursorial squirrels was not strongly influenced by patch area or isolation. These findings reinforce previous studies suggesting that an understanding of species-specific traits such as behavior is an important consideration when interpreting habitat fragmentation effects.     

Signatures of selection in mammalian clock genes with coding trinucleotide repeats: Implications for studying the genomics of high‐pace adaptation

Climate change is predicted to affect the reproductive ecology of wildlife; however, we have yet to understand if and how species can adapt to the rapid pace of change. Clock genes are functional genes likely critical for adaptation to shifting seasonal conditions through shifts in timing cues. Many of these genes contain coding trinucleotide repeats, which offer the potential for higher rates of change than single nucleotide polymorphisms (SNPs) at coding sites, and, thus, may translate to faster rates of adaptation in changing environments. We characterized repeats in 22 clock genes across all annotated mammal species and evaluated the potential for selection on repeat motifs in three clock genes (NR1D1, CLOCK, and PER1) in three congeneric species pairs with different latitudinal range limits: Canada lynx and bobcat (Lynx canadensis and L. rufus), northern and southern flying squirrels (Glaucomys sabrinus and G. volans), and white‐footed and deer mouse (Peromyscus leucopus and P. maniculatus). Signatures of positive selection were found in both the interspecific comparison of Canada lynx and bobcat, and intraspecific analyses in Canada lynx. Northern and southern flying squirrels showed differing frequencies at common CLOCK alleles and a signature of balancing selection. Regional excess homozygosity was found in the deer mouse at PER1 suggesting disruptive selection, and further analyses suggested balancing selection in the white‐footed mouse. These preliminary signatures of selection and the presence of trinucleotide repeats within many clock genes warrant further consideration of the importance of candidate gene motifs for adaptation to climate change.     

A meta-analysis of forest age and structure effects on northern flying squirrel densities

Research on the impact of clearcut logging and partial harvesting practices on northern flying squirrels (Glaucomys sabrinus) has shown inconsistent and contrary results, limiting the use of this species as a management indicator species. Much of this variability in study results is due to the labor intensive nature of studying flying squirrels, resulting in small sampling sizes (average = 5.2 sites, n = 14) and high variation (CV = 0.59) across studies. We conducted a meta-analysis of relevant studies from North America to determine how forestry practices affect flying squirrel abundance. Mean effect size was −1.18 (P < 0.001; n = 14) for all studies, indicating a strong difference between control stands and those regenerating postclearcut or following partial harvesting. Our results support the association of northern flying squirrels with mature, uncut forest and their suitability as ecological indicators of these vegetation types. © 2011 The Wildlife Society.     

Seasonal energetics and torpor use in North American flying squirrels

Seasonal cold temperatures require mammals to use morphological, behavioural, or physiological traits to survive periods of extreme cold and food shortage. Torpor is a physiological state that minimizes energy requirements by decreasing resting metabolic rate (MR) and body temperature (T_b). Many rodent species are capable of torpor, however, evidence in northern and southern flying squirrels (Glaucomys sabrinus and Glaucomys volans, respectively) has remained anecdotal. We experimentally attempted to induce torpor in wild-caught flying squirrels by lowering ambient temperature (T_a) and measuring MR using open-flow respirometry. We also studied seasonal differences in MR and T_b at various T_a. Both MR and T_b provided evidence for torpor in flying squirrels, but only infrequent, shallow torpor. MR decreased infrequently and any decreases were rarely sustained for longer than one hour. We found a significant positive relationship between T_a and T_b only in G. volans, which suggests that G. volans is more susceptible to low T_a compared with G. sabrinus, possibly due to their small body size. We observed no substantive seasonal or interspecific differences in the relation between MR and T_a, with the exception that northern flying squirrels expended more energy at cold T_a during warm season trials than other species-season combinations. The infrequency of torpor use in our experiments suggests that other energy-saving strategies, such as social thermoregulation, may limit the reliance on torpor in this lineage.     

Genetic signature of the colonisation dynamics along a coastal expansion front in the damselfly Coenagrion scitulum

1. Many insects are expanding their distribution range polewards as a result of climate change, which has been shown to be associated with founder effects leading to a reduction in genetic diversity and an increase in genetic differentiation. These spatial genetic patterns may arise from colonisation from a broad expansion front or a limited neighbourhood after a stepping stone model of dispersal. The temporal persistence of such founder effects are poorly understood, mainly because studies looking at the fine‐scale initial temporal dynamics of the genetic signature of a range expansion are rare. 2. Using microsatellite markers, we performed a detailed spatiotemporal genetic analysis of the range expanding damselfly Coenagrion scitulum (Rambur) along a coastal axis during the first years after colonisation. 3. A decrease was in (private) allelic richness when going northwards along the coastline, which is consistent with a scenario of cumulative founder events. In spite of the spatiotemporal dynamics in the observation records of the species along the coastline, the spatial genetic data indicated a major contribution from the broad expansion front during the colonisation of the coastline rather than a stepping‐stone colonisation process. 4. The fine‐scale temporal dynamics of the range expansion indicated the absence of persistent founder effects and instead showed considerable temporal instability in genetic indices at the more northern edge populations. This may be explained by genetic immigration and admixture from the broad expansion front in this active disperser.     

Effects of Logging Pattern and Intensity on Squirrel Demography

ABSTRACT We examined the effect of harvesting intensity and pattern on red squirrels (Tamiasciurus hudsonicus), northern flying squirrels (Glaucomys sabrinus), and yellow-pine chipmunks (Tamias amoenus) in mature inland Douglas-fir (Pseudotsuga menziesii glauca) forests in south-central British Columbia, Canada. We sampled squirrels 1 year before harvesting through 4 years after harvesting and estimated population parameters using open-population models. Relative to unharvested stands, each of the 3 species showed a strong response to tree removal. From 2 years to 4 years after logging, red squirrel density was 40% (SE = 7.1) lower in stands with 50% basal-area tree removal. From 1 year and up to 4 years after logging, northern flying squirrel density averaged 60% (SE = 5.2) lower in harvested treatments regardless of intensity or pattern of logging. In contrast, density of yellow-pine chipmunks increased markedly with increased logging intensity. Beginning 3 years after logging, yellow-pine chipmunk density was 734% (SE = 269) greater in stands with 50% basal-area tree removal. In the short term, harvesting intensity was a more important determinant of squirrel density than harvesting pattern. Retaining >10 m² per ha of live residual stand structure in mature inland Douglas-fir forests maintained habitat for forest-dependent species such as red squirrels and northern flying squirrels, albeit at lower densities.     

A test of non‐kin social foraging in the southern flying squirrel (Glaucomys volans)

It can be challenging to understand the evolution of sociality, particularly the occurrence of co‐operation by non‐kin. Southern flying squirrels (Glaucomys volans) are an interesting example of non‐kin co‐operation because of the mutual benefits obtained by social thermoregulation during winter. Because group survival confers benefits to the entire group, flying squirrels may also follow an aggregation economy, whereby co‐operative foraging during winter is advantageous. However, the extent of such social foraging in flying squirrels is unknown. We tested for social foraging of southern flying squirrels, and also for relatedness among foraging groups. To determine the structure of foraging groups, we set up and remotely monitored feeding stations and nest cavities. All squirrels at the study site were tagged with passive integrated transponder (PIT) tags and nests and feeding stations were monitored with automated PIT‐tag recorders for a 24‐month period. Squirrels were found most often foraging alone. Squirrels that were recorded foraging together comprised unrelated individuals that were also found to share nest cavities. Squirrels were also recorded travelling farther distances between nest cavity and feeding station in the winter season than in the summer season, suggesting that, during winter, squirrels trade‐off proximity to food caches for membership in a nest group. Our data suggest that squirrels forage and cache alone in their summer home range and make solitary returns to this summer range to collect their cache during the winter months, despite exhibiting social winter nesting. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 1126–1135.     

Habitat and landscape correlates of southern flying squirrel use of red-cockaded woodpecker clusters

Southern flying squirrels (Glaucomys volans) can have significant negative impacts on red-cockaded woodpecker (Picoides borealis) reproductive success and group size. Although direct control of southern flying squirrels may be necessary in small red-cockaded woodpecker populations (<30 groups), creation of high quality habitat through landscape management is the preferred method for managing larger woodpecker populations. Thus, we determined the habitat and landscape factors within 100 m, 400 m, and 800 m of cluster centers that were related to southern flying squirrel use of red-cockaded woodpecker cavities at the Carolina Sandhills National Wildlife Refuge, South Carolina. At all spatial scales, the number of cavities in the cluster was the most influential variable determining use by southern flying squirrels. At the 400-m and 800-m scales, the amount of stream length was also positively associated with the presence of flying squirrels. The proximity and amount of hardwoods surrounding clusters were not related to southern flying squirrel use at any spatial scale; thus, removal or conversion of hardwood stands surrounding red-cockaded woodpeckers may not be necessary for reducing cavity kleptoparasitism by flying squirrels. However, when establishing recruitment clusters, areas with streams should be avoided and addition of artificial cavities to existing clusters should be done judiciously to minimize the number of excess cavities. Published 2012. This article is a U.S. Government work and is in the public domain in the USA.     

Long‐distance dispersal maximizes evolutionary potential during rapid geographic range expansion

Conventional wisdom predicts that sequential founder events will cause genetic diversity to erode in species with expanding geographic ranges, limiting evolutionary potential at the range margin. Here, we show that invasive European starlings (Sturnus vulgaris) in South Africa preserve genetic diversity during range expansion, possibly as a result of frequent long‐distance dispersal events. We further show that unfavourable environmental conditions trigger enhanced dispersal, as indicated by signatures of selection detected across the expanding range. This brings genetic variation to the expansion front, counterbalancing the cumulative effects of sequential founding events and optimizing standing genetic diversity and thus evolutionary potential at range margins during spread. Therefore, dispersal strategies should be highlighted as key determinants of the ecological and evolutionary performances of species in novel environments and in response to global environmental change.     

Evidence for evolutionary change associated with the recent range expansion of the British butterfly, Aricia agestis, in response to climate change

Poleward range expansions are widespread responses to recent climate change and are crucial for the future persistence of many species. However, evolutionary change in traits such as colonization history and habitat preference may also be necessary to track environmental change across a fragmented landscape. Understanding the likelihood and speed of such adaptive change is important in determining the rate of species extinction with ongoing climate change. We conducted an amplified fragment length polymorphism (AFLP)‐based genome scan across the recently expanded UK range of the Brown Argus butterfly, Aricia agestis, and used outlier‐based (DFDIST and BayeScan) and association‐based (Isolation‐By‐Adaptation) statistical approaches to identify signatures of evolutionary change associated with range expansion and habitat use. We present evidence for (i) limited effects of range expansion on population genetic structure and (ii) strong signatures of selection at approximately 5% AFLP loci associated with both the poleward range expansion of A. agestis and differences in habitat use across long‐established and recently colonized sites. Patterns of allele frequency variation at these candidate loci suggest that adaptation to new habitats at the range margin has involved selection on genetic variation in habitat use found across the long‐established part of the range. Our results suggest that evolutionary change is likely to affect species’ responses to climate change and that genetic variation in ecological traits across species’ distributions should be maximized to facilitate range shifts across a fragmented landscape, particularly in species that show strong associations with particular habitats.     

Population genetic structure and demographic history of the lone star tick,Amblyomma americanum (Ixodida: Ixodidae): New evidence supporting old records

Range expansions are a potential outcome of changes in habitat suitability, which commonly result as a consequence of climate change. Hypotheses on such changes in the geographic distribution of a certain species can be evaluated using population genetic structure and demography. In this study we explore the population genetic structure, genetic variability, demographic history of, and habitat suitability for Amblyomma americanum, a North American tick species that is a known vector of several pathogenic microorganisms. We used a double digestion restriction site‐associated DNA sequencing technique (dd‐RAD seq) and discovered 8,181 independent single nucleotide polymorphisms (SNPs) in 189 ticks from across the geographic range of the species. Genetic diversity was low, particularly when considering the broad geographic range of this species. The edge populations were less diverse than populations belonging to the historic range, possibly indicative of a range expansion, but this hypothesis was not statistically supported by a test based on genetic data. Nonetheless, moderate levels of population structure and substructure were detected between geographic regions. For New England, demographic and species distribution models support a scenario where A. americanum was present in more northern locations in the past, underwent a bottleneck, and subsequently recovered. These results are consistent with a hypothesis that this species is re‐establishing in this area, rather than one focused on range expansion from the south. This hypothesis is consistent with old records describing the presence of A. americanum in the northeastern US in the early colonial period.     

THE COALESCENT IN BOUNDARY‐LIMITED RANGE EXPANSIONS

Habitat ranges of most species shift over time, for instance due to climate change, human intervention, or adaptation. These demographic changes often have drastic population genetic effects, such as a stochastic resampling of the gene pool through the “surfing” phenomenon. Most models assume that the speed of range expansions is only limited by the dispersal ability of the colonizing species and its reproductive potential. While such models of “phenotype‐limited” expansions apply to species invasions, it is clear that many range expansions are limited rather by the slow motion of habitat boundaries, as driven for instance by global warming. Here, we develop a coalescent model to study the genetic impact of such “boundary‐limited” range expansions. Our simulations and analysis show that the resulting loss of genetic diversity is markedly lower than in species invasions if large carrying capacities can be maintained up to the habitat frontier. Counterintuitively, we find that the total loss of diversity does not depend on the speed of the range expansion: Slower expansions have a smaller rate of loss, but also last longer. Boundary‐limited range expansions exhibit a characteristic genetic footprint and should therefore be distinguished from range expansions limited only by intrinsic characteristics of the species.     

Ultrasonic Vocalizations Emitted by Flying Squirrels

Anecdotal reports of ultrasound use by flying squirrels have existed for decades, yet there has been little detailed analysis of their vocalizations. Here we demonstrate that two species of flying squirrel emit ultrasonic vocalizations. We recorded vocalizations from northern (Glaucomys sabrinus) and southern (G. volans) flying squirrels calling in both the laboratory and at a field site in central Ontario, Canada. We demonstrate that flying squirrels produce ultrasonic emissions through recorded bursts of broadband noise and time-frequency structured frequency modulated (FM) vocalizations, some of which were purely ultrasonic. Squirrels emitted three types of ultrasonic calls in laboratory recordings and one type in the field. The variety of signals that were recorded suggest that flying squirrels may use ultrasonic vocalizations to transfer information. Thus, vocalizations may be an important, although still poorly understood, aspect of flying squirrel social biology.     

Climate change is the primary driver of white‐tailed deer (Odocoileus virginianus) range expansion at the northern extent of its range; land use is secondary

Quantifying the relative influence of multiple mechanisms driving recent range expansion of non‐native species is essential for predicting future changes and for informing adaptation and management plans to protect native species. White‐tailed deer (Odocoileus virginianus) have been expanding their range into the North American boreal forest over the last half of the 20th century. This has already altered predator–prey dynamics in Alberta, Canada, where the distribution likely reaches the northern extent of its continuous range. Although current white‐tailed deer distribution is explained by both climate and human land use, the influence each factor had on the observed range expansion would depend on the spatial and temporal pattern of these changes. Our objective was to quantify the relative importance of land use and climate change as drivers of white‐tailed deer range expansion and to predict decadal changes in white‐tailed deer distribution in northern Alberta for the first half of the 21st century. An existing species distribution model was used to predict past decadal distributions of white‐tailed deer which were validated using independent data. The effects of climate and land use change were isolated by comparing predictions under theoretical “no‐change between decades” scenarios, for each factor, to predictions under observed climate and land use change. Climate changes led to more than 88%, by area, of the increases in probability of white‐tailed deer presence across all decades. The distribution is predicted to extend 100 km further north across the northeastern Alberta boreal forest as climate continues to change over the first half of the 21st century.     

Evolutionary response to Quaternary climate aridification and oscillations in north‐western China revealed by chloroplast phylogeography of the desert shrub Nitraria sphaerocarpa (Nitrariaceae)

To investigate the influence of climate aridification and oscillations on the genetic diversity and evolutionary processes of organisms in the Quaternary in north‐western China, we selected Nitraria sphaerocarpa and examined the phylogeographical structure and response to historical and environmental factors in populations of this species across most of its covered range. We found twelve haplotypes on the basis of two chloroplast DNA sequences (trnH‐psbA and rpl32‐trnL). The drying climate during the Quaternary is proposed to have been a driver for significant genetic isolation and divergence among populations in N. sphaerocarpa. Except for the sharing of haplotype D between the Hami Basin and Hexi Corridor, as well as of haplotype F between the Hexi Corridor and Alxa Desert, network analysis showed haplotypes to be almost completely different from region to region. Analysis of molecular variance indicated that genetic variation primarily occurred among populations and among nine geographical groups that were distinguished by spatial analysis of molecular variance, and a Mantel test showed that the correlation between genetic and geographical distances was significant. On the other hand, there was evidence for the occurrence of an episode of more favourable conditions in some regions. Geographical range expansion of two groups of N. sphaerocarpa populations was supported by significant values for Fu's F_S and unimodel mismatch distributions. During the last interglacial period, a warmer and wetter climate contributed to range expansion within portions of the Hexi Corridor. By contrast, based on ecological niche modelling, N. sphaerocarpa was indicated to have had a shrunken and more fragmented range during the Last Glacial Maximum. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 757–770.     

Experimental test of nest-site limitation in mature mixed forests of central British Columbia,Canada

Nest-site availability limits cavity-using populations in many harvested forests; however, little is known about the extent of nest-site limitation in mature forests with a full complement of excavator species and intact processes of cavity creation and loss. To examine the role of nest-site availability in limiting cavity-using populations in mature mixed conifer forests in central British Columbia, Canada, we conducted an 11-year before-after control-impact experiment in which we increased nest-site availability via nest box addition. Our 7 sites (3 treatments, 4 controls) had low cavity densities (<2/ha) prior to treatment and cavity occupation rates were also low (<10%/yr), which is a relationship often cited in the literature as evidence of non-limitation in cavity-nesting populations. Following nest box addition at our treatment sites, which tripled the availability of cavities, total density of bird and mammal nests more than tripled. Density of mountain chickadee (Poecile gambeli) nests increased 9-fold on treatment sites and returned to pre-treatment levels following box removal, suggesting that chickadee populations were limited by cavity availability at our study sites. Density of red squirrel (Tamiasciurus hudsonicus) and northern flying squirrel (Glaucomys sabrinus) nests and roosts also increased significantly at treatment sites following box addition and declined following box removal. We noted little change in chickadee or squirrel nest density at control sites monitored concurrently. Squirrels preferred large-sized over small-sized boxes, and significantly enlarged the entrance areas of small boxes by chewing, suggesting that there may have been a shortage of suitable nest and roost sites for them in our study area. We contend that low cavity occupancy rates may not accurately reflect nest-site availability for cavity nesters in mature forests, and that cavity size may influence the true availability of cavities on the landscape. © 2011 The Wildlife Society.     

GENETIC STRUCTURE OF THE FROGS GEOCRINIA LUTEA AND GEOCRINIA ROSEA REFLECTS EXTREME POPULATION DIVERGENCE AND RANGE CHANGES,NOT DISPERSAL BARRIERS

I describe the genetic structure of two frog species, Geocrinia rosea and Geocrinia lutea, using allozyme electrophoresis to understand population structure and thereby possible mechanisms of divergence and speciation. The sampling regimes represented the entire range of both species and provided replicated tests of the impact of ridges, rivers, and dry forest on gene flow. Geocrinia rosea and G. lutea were highly genetically subdivided (F_ST = 0.69, 0.64, respectively). In the extreme, there were fixed allelic differences between populations that were only 4 km (G. rosea) or 1.25 km (G. lutea) apart. In addition to localized divergence, two-dimensional scaling of genetic distance allowed the recognition of broad-scale genetic groups, each consisting of several sample sites. Patterns of divergence were unrelated to the presence of ridges, rivers, or dry forest. I argue that range contraction and expansion, combined with extreme genetic divergence in single, isolated populations, best accounts for the genetic structure of these species.