Variation in the response of an Arctic top predator experiencing habitat loss: feeding and reproductive ecology of two polar bear populations

Polar bears (Ursus maritimus) have experienced substantial changes in the seasonal availability of sea ice habitat in parts of their range, including the Beaufort, Chukchi, and Bering Seas. In this study, we compared the body size, condition, and recruitment of polar bears captured in the Chukchi and Bering Seas (CS) between two periods (1986–1994 and 2008–2011) when declines in sea ice habitat occurred. In addition, we compared metrics for the CS population 2008–2011 with those of the adjacent southern Beaufort Sea (SB) population where loss in sea ice habitat has been associated with declines in body condition, size, recruitment, and survival. We evaluated how variation in body condition and recruitment were related to feeding ecology. Comparing habitat conditions between populations, there were twice as many reduced ice days over continental shelf waters per year during 2008–2011 in the SB than in the CS. CS polar bears were larger and in better condition, and appeared to have higher reproduction than SB bears. Although SB and CS bears had similar diets, twice as many bears were fasting in spring in the SB than in the CS. Between 1986–1994 and 2008–2011, body size, condition, and recruitment indices in the CS were not reduced despite a 44‐day increase in the number of reduced ice days. Bears in the CS exhibited large body size, good body condition, and high indices of recruitment compared to most other populations measured to date. Higher biological productivity and prey availability in the CS relative to the SB, and a shorter recent history of reduced sea ice habitat, may explain the maintenance of condition and recruitment of CS bears. Geographic differences in the response of polar bears to climate change are relevant to range‐wide forecasts for this and other ice‐dependent species.     

Natural selection on the genetical component of variance in body condition in a wild bird population

Although there is substantial evidence that skeletal measures of body size are heritable in wild animal populations, it is frequently assumed that the nonskeletal component of body weight (or ‘condition’) is determined primarily by environmental factors, in particular nutritional state. We tested this assumption by quantifying the genetic and environmental components of variance in fledgling body condition index (=relative body weight) in a natural population of collared flycatchers (Ficedula albicollis), and compared the strength of natural selection on individual breeding values with that on phenotypic values. A mixed model analysis of the components of variance, based on an ‘animal model’ and using 18 years of data on 17 717 nestlings, revealed a significant additive genetic component of variance in body condition, which corresponded to a narrow sense heritability (h²) of 0.30 (SE=0.03). Nongenetic contributions to variation in body condition were large, but there was no evidence of dominance variance nor of contributions from early maternal or common environment effects (pre‐manipulation environment) in condition at fledging. Comparison of pre‐ and post‐selection samples revealed virtually identical h² of body condition index, despite the fact that there was a significant decrease (35%) in the levels of additive genetic variance from fledging to breeding. The similar h² in the two samples occurred because the environmental component of variance was also reduced by selection, suggesting that natural selection was acting on both genotypic and environmental variation. The effects of selection on genetic variance were confirmed by calculation of the selection differentials for both phenotypic values and best linear unbiased predictor (BLUP) estimates of breeding values: there was positive directional selection on condition index both at the phenotypic and the genotypic level. The significant h² of body condition index is consistent with data from human and rodent populations showing significant additive genetic variance in relative body mass and adiposity, but contrasts with the common assumption in ecology that body condition reflects an individual’s nongenetic nutritional state. Furthermore, the substantial reduction in the additive genetic component of variance in body condition index suggests that selection on environmental deviations cannot alone explain the maintenance of additive genetic variation in heritable traits, but that other mechanisms are needed to explain the moderate to high heritabilities of traits under consistent and strong directional selection.     

SEX CHROMOSOME LINKED GENETIC VARIANCE AND THE EVOLUTION OF SEXUAL DIMORPHISM OF QUANTITATIVE TRAITS

Theory predicts that sex chromsome linkage should reduce intersexual genetic correlations thereby allowing the evolution of sexual dimorphism. Empirical evidence for sex linkage has come largely from crosses and few studies have examined how sexual dimorphism and sex linkage are related within outbred populations. Here, we use data on an array of different traits measured on over 10,000 individuals from two pedigreed populations of birds (collared flycatcher and zebra finch) to estimate the amount of sex‐linked genetic variance (h²_z). Of 17 traits examined, eight showed a nonzero h²_Z estimate but only four were significantly different from zero (wing patch size and tarsus length in collared flycatchers, wing length and beak color in zebra finches). We further tested how sexual dimorphism and the mode of selection operating on the trait relate to the proportion of sex‐linked genetic variance. Sexually selected traits did not show higher h²_Z than morphological traits and there was only a weak positive relationship between h²_Z and sexual dimorphism. However, given the relative scarcity of empirical studies, it is premature to make conclusions about the role of sex chromosome linkage in the evolution of sexual dimorphism.     

Canadian polar bear population structure using genome‐wide markers

Predicting the consequences of environmental changes, including human‐mediated climate change on species, requires that we quantify range‐wide patterns of genetic diversity and identify the ecological, environmental, and historical factors that have contributed to it. Here, we generate baseline data on polar bear population structure across most Canadian subpopulations (n = 358) using 13,488 genome‐wide single nucleotide polymorphisms (SNPs) identified with double‐digest restriction site‐associated DNA sequencing (ddRAD). Our ddRAD dataset showed three genetic clusters in the sampled Canadian range, congruent with previous studies based on microsatellites across the same regions; however, due to a lack of sampling in Norwegian Bay, we were unable to confirm the existence of a unique cluster in that subpopulation. These data on the genetic structure of polar bears using SNPs provide a detailed baseline against which future shifts in population structure can be assessed, and opportunities to develop new noninvasive tools for monitoring polar bears across their range.     

Estimating the energy expenditure of free‐ranging polar bears using tri‐axial accelerometers: A validation with doubly labeled water

Measures of energy expenditure can be used to inform animal conservation and management, but methods for measuring the energy expenditure of free‐ranging animals have a variety of limitations. Advancements in biologging technologies have enabled the use of dynamic body acceleration derived from accelerometers as a proxy for energy expenditure. Although dynamic body acceleration has been shown to strongly correlate with oxygen consumption in captive animals, it has been validated in only a few studies on free‐ranging animals. Here, we use relationships between oxygen consumption and overall dynamic body acceleration in resting and walking polar bears Ursus maritimus and published values for the costs of swimming in polar bears to estimate the total energy expenditure of 6 free‐ranging polar bears that were primarily using the sea ice of the Beaufort Sea. Energetic models based on accelerometry were compared to models of energy expenditure on the same individuals derived from doubly labeled water methods. Accelerometer‐based estimates of energy expenditure on average predicted total energy expenditure to be 30% less than estimates derived from doubly labeled water. Nevertheless, accelerometer‐based measures of energy expenditure strongly correlated (r² = 0.70) with measures derived from doubly labeled water. Our findings highlight the strengths and limitations in dynamic body acceleration as a measure of total energy expenditure while also further supporting its use as a proxy for instantaneous, detailed energy expenditure in free‐ranging animals.     

What to eat now? Shifts in polar bear diet during the ice-free season in western Hudson Bay

Under current climate trends, spring ice breakup in Hudson Bay is advancing rapidly, leaving polar bears (Ursus maritimus) less time to hunt seals during the spring when they accumulate the majority of their annual fat reserves. For this reason, foods that polar bears consume during the ice‐free season may become increasingly important in alleviating nutritional stress from lost seal hunting opportunities. Defining how the terrestrial diet might have changed since the onset of rapid climate change is an important step in understanding how polar bears may be reacting to climate change. We characterized the current terrestrial diet of polar bears in western Hudson Bay by evaluating the contents of passively sampled scat and comparing it to a similar study conducted 40 years ago. While the two terrestrial diets broadly overlap, polar bears currently appear to be exploiting increasingly abundant resources such as caribou (Rangifer tarandus) and snow geese (Chen caerulescens caerulescens) and newly available resources such as eggs. This opportunistic shift is similar to the diet mixing strategy common among other Arctic predators and bear species. We discuss whether the observed diet shift is solely a response to a nutritional stress or is an expression of plastic foraging behavior.     

Environmental and genetic influences on body mass and resting metabolic rates (RMR) in a natural population of weasel Mustela nivalis

Body mass (BM) and resting metabolic rates (RMR) are two inexorably linked traits strongly related to mammalian life histories. Yet, there have been no studies attempting to estimate heritable variation and covariation of BM and RMR in natural populations. We used a marker‐based approach to construct a pedigree and then the ‘animal model’ to estimate narrow sense heritability (h²) of these traits in a free‐living population of weasels Mustela nivalis—a small carnivore characterised by a wide range of BM and extremely high RMR. The most important factors affecting BM of weasels were sex and habitat type, whereas RMR was significantly affected only by seasonal variation of this trait. All environmental factors had only small effect on estimates of additive genetic variance of both BM and RMR. The amount of additive genetic variance associated with BM and estimates of heritability were high and significant in males (h² = 0.61), but low and not significant in females (h² = 0.32), probably due to small sample size for the latter sex. The results from the two‐trait model revealed significant phenotypic (r_P = 0.62) and genetic correlation (r_A = 0.89) between BM and whole body RMR. The estimate of heritability of whole body RMR (0.54) and BM corrected RMR (0.45) were lower than estimates of heritability for BM. Both phenotypic and genetic correlations between BM corrected RMR and BM had negative signals (r_P = ?0.42 and r_A = ?0.58). Our results indicate that total energy expenditures of individuals can quickly evolve through concerted changes in BM and RMR.     

Genome‐wide screening for DNA variants associated with reading and language traits

Reading and language abilities are heritable traits that are likely to share some genetic influences with each other. To identify pleiotropic genetic variants affecting these traits, we first performed a genome‐wide association scan (GWAS) meta‐analysis using three richly characterized datasets comprising individuals with histories of reading or language problems, and their siblings. GWAS was performed in a total of 1862 participants using the first principal component computed from several quantitative measures of reading‐ and language‐related abilities, both before and after adjustment for performance IQ. We identified novel suggestive associations at the SNPs rs59197085 and rs5995177 (uncorrected P ≈ 10^–7 for each SNP), located respectively at the CCDC136/FLNC and RBFOX2 genes. Each of these SNPs then showed evidence for effects across multiple reading and language traits in univariate association testing against the individual traits. FLNC encodes a structural protein involved in cytoskeleton remodelling, while RBFOX2 is an important regulator of alternative splicing in neurons. The CCDC136/FLNC locus showed association with a comparable reading/language measure in an independent sample of 6434 participants from the general population, although involving distinct alleles of the associated SNP. Our datasets will form an important part of on‐going international efforts to identify genes contributing to reading and language skills.     

Development of an integrated 200K SNP genotyping array and application for genetic mapping,genome assembly improvement and genome wide association studies in pear (Pyrus)

Pear (Pyrus; 2n = 34), the third most important temperate fruit crop, has great nutritional and economic value. Despite the availability of many genomic resources in pear, it is challenging to genotype novel germplasm resources and breeding progeny in a timely and cost‐effective manner. Genotyping arrays can provide fast, efficient and high‐throughput genetic characterization of diverse germplasm, genetic mapping and breeding populations. We present here 200K AXIOM^® PyrSNP, a large‐scale single nucleotide polymorphism (SNP) genotyping array to facilitate genotyping of Pyrus species. A diverse panel of 113 re‐sequenced pear genotypes was used to discover SNPs to promote increased adoption of the array. A set of 188 diverse accessions and an F₁ population of 98 individuals from ‘Cuiguan’ × ‘Starkrimson’ was genotyped with the array to assess its effectiveness. A large majority of SNPs (166 335 or 83%) are of high quality. The high density and uniform distribution of the array SNPs facilitated prediction of centromeric regions on 17 pear chromosomes, and significantly improved the genome assembly from 75.5% to 81.4% based on genetic mapping. Identification of a gene associated with flowering time and candidate genes linked to size of fruit core via genome wide association studies showed the usefulness of the array in pear genetic research. The newly developed high‐density SNP array presents an important tool for rapid and high‐throughput genotyping in pear for genetic map construction, QTL identification and genomic selection.     

A trait‐based approach to predict population genetic structure in bees

Understanding population genetic structure is key to developing predictions about species susceptibility to environmental change, such as habitat fragmentation and climate change. It has been theorized that life‐history traits may constrain some species in their dispersal and lead to greater signatures of population genetic structure. In this study, we use a quantitative comparative approach to assess if patterns of population genetic structure in bees are driven by three key species‐level life‐history traits: body size, sociality, and diet breadth. Specifically, we reviewed the current literature on bee population genetic structure, as measured by the differentiation indices Nei's G_ST, Hedrick's G′_ST, and Jost's D. We then used phylogenetic generalised linear models to estimate the correlation between the evolution of these traits and patterns of genetic differentiation. Our analyses revealed a negative and significant effect of body size on genetic structure, regardless of differentiation index utilized. For Hedrick's G′_ST and Jost's D, we also found a significant impact of sociality, where social species exhibited lower levels of differentiation than solitary species. We did not find an effect of diet specialization on population genetic structure. Overall, our results suggest that physical dispersal or other functions related to body size are among the most critical for mediating population structure for bees. We further highlight the importance of standardizing population genetic measures to more easily compare studies and to identify the most susceptible species to landscape and climatic changes.     

Shifts in frog size and phenology: Testing predictions of climate change on a widespread anuran using data from prior to rapid climate warming

Changes in body size and breeding phenology have been identified as two major ecological consequences of climate change, yet it remains unclear whether climate acts directly or indirectly on these variables. To better understand the relationship between climate and ecological changes, it is necessary to determine environmental predictors of both size and phenology using data from prior to the onset of rapid climate warming, and then to examine spatially explicit changes in climate, size, and phenology, not just general spatial and temporal trends. We used 100 years of natural history collection data for the wood frog, Lithobates sylvaticus with a range >9 million km², and spatially explicit environmental data to determine the best predictors of size and phenology prior to rapid climate warming (1901–1960). We then tested how closely size and phenology changes predicted by those environmental variables reflected actual changes from 1961 to 2000. Size, phenology, and climate all changed as expected (smaller, earlier, and warmer, respectively) at broad spatial scales across the entire study range. However, while spatially explicit changes in climate variables accurately predicted changes in phenology, they did not accurately predict size changes during recent climate change (1961–2000), contrary to expectations from numerous recent studies. Our results suggest that changes in climate are directly linked to observed phenological shifts. However, the mechanisms driving observed body size changes are yet to be determined, given the less straightforward relationship between size and climate factors examined in this study. We recommend that caution be used in “space‐for‐time” studies where measures of a species’ traits at lower latitudes or elevations are considered representative of those under future projected climate conditions. Future studies should aim to determine mechanisms driving trends in phenology and body size, as well as the impact of climate on population density, which may influence body size.     

Development of on‐shore behavior among polar bears (Ursus maritimus) in the southern Beaufort Sea: inherited or learned?

Polar bears (Ursus maritimus) are experiencing rapid and substantial changes to their environment due to global climate change. Polar bears of the southern Beaufort Sea (SB) have historically spent most of the year on the sea ice. However, recent reports from Alaska indicate that the proportion of the SB subpopulation observed on‐shore during late summer and early fall has increased. Our objective was to investigate whether this on‐shore behavior has developed through genetic inheritance, asocial learning, or through social learning. From 2010 to 2013, genetic data were collected from SB polar bears in the fall via hair snags and remote biopsy darting on‐shore and in the spring from captures and remote biopsy darting on the sea ice. Bears were categorized as either on‐shore or off‐shore individuals based on their presence on‐shore during the fall. Levels of genetic relatedness, first‐order relatives, mother–offspring pairs, and father–offspring pairs were determined and compared within and between the two categories: on‐shore versus off‐shore. Results suggested transmission of on‐shore behavior through either genetic inheritance or social learning as there was a higher than expected number of first‐order relatives exhibiting on‐shore behavior. Genetic relatedness and parentage data analyses were in concurrence with this finding, but further revealed mother–offspring social learning as the primary mechanism responsible for the development of on‐shore behavior. Recognizing that on‐shore behavior among polar bears was predominantly transmitted via social learning from mothers to their offspring has implications for future management and conservation as sea ice continues to decline.     

Quantitative trait loci for magnitude of the plasma cortisol response to confinement in rainbow trout

Better understanding of the mechanisms underlying interindividual variation in stress responses and their links with production traits is a key issue for sustainable animal breeding. In this study, we searched for quantitative trait loci (QTL) controlling the magnitude of the plasma cortisol stress response and compared them to body size traits in five F2 full‐sib families issued from two rainbow trout lines divergently selected for high or low post‐confinement plasma cortisol level. Approximately 1000 F2 individuals were individually tagged and exposed to two successive acute confinement challenges (1 month interval). Post‐stress plasma cortisol concentrations were determined for each fish. A medium density genome scan was carried out (268 markers, overall marker spacing less than 10 cM). QTL detection was performed using qtlmap software, based on an interval mapping method ( http://www.inra.fr/qtlmap ). Overall, QTL of medium individual effects on cortisol responsiveness (<10% of phenotypic variance) were detected on 18 chromosomes, strongly supporting the hypothesis that control of the trait is polygenic. Although a core array of QTL controlled cortisol concentrations at both challenges, several QTL seemed challenge specific, suggesting that responses to the first and to a subsequent exposure to the confinement stressor are distinct traits sharing only part of their genetic control. Chromosomal location of the steroidogenic acute regulatory protein (STAR) makes it a good potential candidate gene for one of the QTL. Finally, comparison of body size traits QTL (weight, length and body conformation) with cortisol‐associated QTL did not support evidence for negative genetic relationships between the two types of traits.     

Room without a view—Den excavation in relation to body size in brown bears

Hibernation is an adaptive strategy to survive harsh winter conditions and food shortage. The use of well‐insulated winter dens helps animals minimize energy loss during hibernation. Brown bears (Ursus arctos) commonly use excavated dens for hibernation. Physical attributes of excavated dens are expected to impact the bear's heat retention and energy conservation. The objective of this study was to examine the determinants of cavity size of excavated dens and the impact of physical attributes of excavated dens on energy conservation in hibernating bears, hypothesizing that bears excavate dens in a way to minimize heat loss and optimize energy conservation during hibernation. We predicted that den cavity size would be determined by the bear's body size and that older bears would excavate better‐fitting cavities to minimize heat loss, due to their previous experience. We further predicted that physical attributes of excavated dens would affect the bears’ posthibernation body condition. Our results revealed that bears excavated a den cavity in relation to their body size, regardless of sex, and that older bears tended to excavate better‐fitting den cavities compared to young bears, as we expected. Older bears excavated better‐fitting den cavities, suggesting a potentially experience‐based shift with age in den‐excavation behavior and an optimum cavity size relative to a bear's body size. Our key finding is that insulation of excavated dens provided by wall/rood thickness and bedding materials had a significant positive effect on bears’ posthibernation body condition. We believe that our study provides new insight into how not only the quality of denning habitat, but also the quality of dens may affect hibernating animals, by presenting a potential adaptive aspect of den preparation (age effect on efficiency in den excavation) and effect of den attributes on the posthibernation body condition of brown bears.     

Inheritance of vertebral number in the three-spined stickleback (Gasterosteus aculeatus)

Intraspecific variation in the number of vertebrae is taxonomically widespread, and both genetic and environmental factors are known to contribute to this variation. However, the relative importance of genetic versus environmental influences on variation in vertebral number has seldom been investigated with study designs that minimize bias due to non-additive genetic and maternal influences. We used a paternal half-sib design and animal model analysis to estimate heritability and causal components of variance in vertebral number in three-spined sticklebacks (Gasterosteus aculeatus). We found that both the number of vertebrae (h² = 0.36) and body size (h² = 0.42) were moderately heritable, whereas the influence of maternal effects was estimated to be negligible. While the number of vertebrae had a positive effect on body size, no evidence for a genetic correlation between body size and vertebral number was detected. However, there was a significant positive environmental correlation between these two traits. Our results support the generalization-in accordance with results from a review of heritability estimates for vertebral number in fish, reptiles and mammals-that the number of vertebrae appears to be moderately to highly heritable in a wide array of species. In the case of the three-spined stickleback, independent evolution of body size and number of vertebrae should be possible given the low genetic correlation between the two traits.     

Heritability of male mandible length in the stag beetle Cyclommatus metallifer

Numerous coleopteran species express male‐specific “weapon traits” that often show size variations among males, even within a single population. Many empirical studies have demonstrated that environmental conditions during development affect absolute weapon size. However, relatively few studies in horned beetles support the hypothesis that the relationship between weapon size and body size, also referred to as a “scaling relationship” or “static allometry”, is largely determined by genetic factors. In this study, the heritability of absolute mandible length and static allometry between mandible length and body size were estimated in the stag beetle Cyclommatus metallifer. While no significant heritable variation was observed in absolute mandible length, high heritability (h² = 0.57 ± 0.25) was detected in the static allometry between mandible length and body size. This is the first report on the genetic effect on male mandible size in Lucanidae, suggesting that absolute mandible size is largely determined by environmental conditions while the static allometry between weapon size and body size is primarily determined by genetic factors.     

Temporal change in the morphometry–body mass relationship of polar bears

Accurate information on animal body mass is often an essential component of wildlife research and management. However, for many large-bodied species, obtaining direct scale weights from individuals may be difficult. In these cases, morphometric equations (e.g., based on girth or length) may provide accurate and precise estimates of body mass. We developed predictive equations to estimate the body mass of free-ranging polar bears (Ursus maritimus) in western Hudson Bay, Canada. Using multiple linear and non-linear regression, we identified a strong relationship between polar bear body weight and linear measures of straight line length and axillary girth. The mass–morphometry relationship appeared to change over time and we developed separate equations for polar bears measured during 2 time periods, 1980–1996 and 2007–2009. Non-linear models were more accurate and provided body mass estimates within 5.8% (R² = 0.98) and 6.1% (R² = 0.98) of scale weight in the earlier and later time periods, respectively. Earlier equations developed for polar bears in this subpopulation performed poorly when applied to recently sampled individuals. In contrast, some contemporary equations from other regions performed reasonably well, suggesting that temporal changes within a subpopulation may be more pronounced than regional differences and can render earlier predictive equations obsolete. Our results have important implications for current and future studies of polar bear body condition and the effects of ongoing climate warming. © 2011 The Wildlife Society.     

Effects of climate warming on polar bears: a review of the evidence

Climate warming is causing unidirectional changes to annual patterns of sea ice distribution, structure, and freeze‐up. We summarize evidence that documents how loss of sea ice, the primary habitat of polar bears (Ursus maritimus), negatively affects their long‐term survival. To maintain viable subpopulations, polar bears depend on sea ice as a platform from which to hunt seals for long enough each year to accumulate sufficient energy (fat) to survive periods when seals are unavailable. Less time to access to prey, because of progressively earlier breakup in spring, when newly weaned ringed seal (Pusa hispida) young are available, results in longer periods of fasting, lower body condition, decreased access to denning areas, fewer and smaller cubs, lower survival of cubs as well as bears of other age classes and, finally, subpopulation decline toward eventual extirpation. The chronology of climate‐driven changes will vary between subpopulations, with quantifiable negative effects being documented first in the more southerly subpopulations, such as those in Hudson Bay or the southern Beaufort Sea. As the bears' body condition declines, more seek alternate food resources so the frequency of conflicts between bears and humans increases. In the most northerly areas, thick multiyear ice, through which little light penetrates to stimulate biological growth on the underside, will be replaced by annual ice, which facilitates greater productivity and may create habitat more favorable to polar bears over continental shelf areas in the short term. If the climate continues to warm and eliminate sea ice as predicted, polar bears will largely disappear from the southern portions of their range by mid‐century. They may persist in the northern Canadian Arctic Islands and northern Greenland for the foreseeable future, but their long‐term viability, with a much reduced global population size in a remnant of their former range, is uncertain.