The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine

The geographic mosaic theory of coevolution posits that the form of selection between interacting species varies across a landscape with coevolution important and active in some locations (i.e., coevolutionary hotspots) but not in others (i.e., coevolutionary coldspots). We tested the hypothesis that the presence of red squirrels (Tamiasciurus hudsonicus) affects the occurrence of coevolution between red crossbills (Loxia curvirostra complex) and Rocky Mountain lodgepole pine (Pinus contorta ssp. latifolia) and thereby provides a mechanism giving rise to a geographic mosaic of selection. Red squirrels are the predominant predispersal seed predator and selective agent on lodgepole pine cones. However, in four isolated mountain ranges east and west of the Rocky Mountains, red squirrels are absent and red crossbills are the main predispersal seed predator. These isolated populations of pine have apparently evolved without Tamiasciurus for about 10,000 to 12,000 years. Based on published morphological, genetic, and paleobotanical studies, we infer that cone traits in these isolated populations that show parallel differences from cones in the Rocky Mountains have changed in parallel. We used data on crossbill and conifer cone morphology and feeding preferences and efficiency to detect whether red crossbills and lodgepole pine exhibit reciprocal adaptations, which would imply coevolution. Cone traits that act to deter Tamiasciurus and result in high ratios of cone mass to seed mass were less developed in the isolated populations. Cone traits that act to deter crossbills include larger and thicker scales and perhaps increased overlap between successive scales and were enhanced in the isolated populations. In the larger, isolated mountain ranges crossbills have evolved deeper, shorter, and therefore more decurved bills to exploit these cones. This provides crossbills with higher feeding rates, and the change in bill shape has improved efficiency by reducing the concomitant increases in body mass and daily energy expenditures that would have resulted if only bill size had increased. These parallel adaptations and counter adaptations in red crossbills and lodgepole pine are interpreted as reciprocal adaptations and imply that these crossbills and pine are in coevolutionary arms races where red squirrels are absent (i.e., coevolutionary hotspots) but not where red squirrels are present (i.e., coevolutionary cold-spots).     

Genetic assessment of the red squirrel in Illinois: Immigrants or Exotics?

Novel populations pose unusual challenges for wildlife managers because knowledge regarding the source of these populations is essential to develop sound management approaches. One example that illustrates the complexity of this issue is the small population of red squirrels (Tamiasciurus hudsonicus) identified in northeastern Illinois in the 1970s. To elucidate the source of the red squirrel population in Illinois, we examined both contemporary and less recent patterns of genetic structure using nuclear microsatellite loci and mitochondrial DNA. Analyses revealed the Illinois subpopulation was primarily comprised of descendents of immigrants from Indiana, but there was also evidence of a translocation of squirrels from Minnesota. We recommend continued protection for the red squirrel in Illinois due to its restricted geographic range, small population size, and status as a native population. © 2011 The Wildlife Society.     

Optimisation of energetic and reproductive gains explains behavioural responses to environmental variation across seasons and years

Animals switch between inactive and active states, simultaneously impacting their energy intake, energy expenditure and predation risk, and collectively defining how they engage with environmental variation and trophic interactions. We assess daily activity responses to long‐term variation in temperature, resources and mating opportunities to examine whether individuals choose to be active or inactive according to an optimisation of the relative energetic and reproductive gains each state offers. We show that this simplified behavioural decision approach predicts most activity variation (R² = 0.83) expressed by free‐ranging red squirrels over 4 years, as quantified through accelerometer recordings (489 deployments; 5066 squirrel‐days). Recognising activity as a determinant of energetic status, the predictability of activity variation aggregated at a daily scale, and the clear signal that behaviour is environmentally forced through optimisation of gain, provides an integrated approach to examine behavioural variation as an intermediary between environmental variation and energetic, life‐history and ecological outcomes.     

DIVERSIFICATION AND GENE FLOW IN NASCENT LINEAGES OF ISLAND AND MAINLAND NORTH AMERICAN TREE SQUIRRELS (TAMIASCIURUS)

Pleistocene climate cycles and glaciations had profound impacts on taxon diversification in the Boreal Forest Biome. Using population genetic analyses with multilocus data, we examined diversification, isolation, and hybridization in two sibling species of tree squirrels (Tamiasciurus douglasii and Tamiasciurus hudsonicus) with special attention to the geographically and genetically enigmatic population of T. hudsonicus on Vancouver Island, Canada. The two species differentiated only about 500,000 years ago, in the Late Pleistocene. The island population is phylogenetically nested within T. hudsonicus according to our nuclear analysis but within T. douglasii according to mitochondrial DNA. This conflict is more likely due to historical hybridization than to incomplete lineage sorting, and it appears that bidirectional gene flow occurred between the island population and both species on the mainland. This interpretation of our genetic analyses is consistent with our bioclimatic modeling, which demonstrates that both species were able to occupy this region throughout the Late Pleistocene. The divergence of the island population 40,000 years ago suggests that tree squirrels persisted in a refugium on Vancouver Island at the last glacial maximum, 20,000 years ago. Our observations demonstrate how Pleistocene climate change and habitat shifts have created incipient divergence in the presence of gene flow.     

Cohort effects in red squirrels: the influence of density, food abundance and temperature on future survival and reproductive success

1. Environmental conditions experienced early in life may have long-lasting effects on individual performance, thereby creating 'silver-spoon effects'. 2. We used 15 years of data from a North American red squirrel (Tamiasciurus hudsonicus Erxleben) population to investigate influences of food availability, density and spring temperature experienced early in life on reproduction and survival of female squirrels during adulthood. 3. We found that spring temperature and food availability did not affect female survival after 1 year of age, whereas higher squirrel densities led to lower survival, thereby affecting longevity and lifetime fitness. 4. In addition, both food availability experienced between birth and weaning, and spring temperature in the year of birth, had long-lasting positive effects on female reproductive success. These results emphasize the critical effect environmental conditions during the early life stages can have on the lifetime performance of small mammals. 5. These long-term effects of early food and temperature were apparent only once we controlled for conditions experienced during adulthood. This suggests that silver-spoon effects can be masked when conditions experienced early in life are correlated to some environmental conditions experienced later in life. 6. The general importance of silver-spoon effects for adult demographic performance might therefore be underestimated, and taking adult environment into account appears to be necessary when studying long-term cohort effects.     

Lifetime selection on heritable life-history traits in a natural population of red squirrels

Abstract Despite their importance in evolutionary biology, heritability and the strength of natural selection have rarely been estimated in wild populations of iteroparous species or have usually been limited to one particular event during an organism's lifetime. Using an animal-model restricted maximum likelihood and phenotypic selection models, we estimated quantitative genetic parameters and the strength of lifetime selection on parturition date and litter size at birth in a natural population of North American red squirrels, Tamiasciurus hudsonicus. Litter size at birth and parturition date had low heritabilities ( h² = 0.15 and 0.16, respectively). We considered potential effects of temporal environmental covariances between phenotypes and fitness and of spatial environmental heterogeneity in estimates of selection. Selection favored early breeders and females that produced litter sizes close to the population average. Stabilizing selection on litter size at birth may occur because of a trade-off between number of offspring produced per litter and offspring survival or a trade-off between a female's fecundity and her future reproductive success and survival.     

Diets of native and introduced tree squirrels in Washington

Competition for food resources can be a primary mechanism for displacement of native species by introduced species. Investigation of dietary partitioning between potential competitors and spatiotemporal variability in food resources can reveal contested food items and intensity of competition. Introduced eastern gray squirrels (Sciurus carolinensis) have been implicated as competitors with western gray squirrels (S. griseus) and Douglas’ squirrels (Tamiasciurus douglasii), but little is known about interactions among these species. We collected foraging observations and fecal pellets of sympatric gray and Douglas’ squirrels trapped and radio-tracked in western Washington, USA, from 2007 to 2012. We compared food resources consumed across species, seasons, and years to evaluate dietary overlap and the potential for competitive interactions. All squirrel species ate hypogeous fungi throughout all seasons; spores of several genera were present in 272 of 275 fecal samples and observed in all months. Rhizopogon, Geopora, and Melanogaster spp. occurred in most fecal pellets for all squirrels, but the diet of the Douglas’ squirrels had slightly lower richness of hypogeous fungi than gray squirrels. Although foraging observations suggest that eastern and western gray squirrels shared important dietary items such as acorns, strong differences in consumption of seeds of a common conifer may facilitate their coexistence. Our results suggest that dietary overlap among arboreal squirrels could lead to competitive interactions during periods of food scarcity, but subtle differences may be sufficient to permit long-term coexistence. Tree squirrels in Washington would likely benefit from forest management practices that promote or sustain robust crops of hypogeous fungi. © 2019 The Wildlife Society.     

Maternal effects and the potential for evolution in a natural population of animals

Maternal effects are widespread and can have dramatic influences on evolutionary dynamics, but their genetic basis has been measured rarely in natural populations. We used cross-fostering techniques and a long-term study of a natural population of red squirrels, Tamiasciurus hudsonicus, to estimate both direct (heritability) and indirect (maternal) influences on the potential for evolution. Juvenile growth in both body mass and size had significant amounts of genetic variation (mass h(2) = 0.10; size h(2) = 0.33), but experienced large, heritable maternal effects. Growth in body mass also had a large positive covariance between direct and maternal genetic effects. The consideration of these indirect genetic effects revealed a greater than three-fold increase in the potential for evolution of growth in body mass (h(2)t = 0.36) relative to that predicted by heritability alone. Simple heritabilities, therefore, may severely underestimate or overestimate the potential for evolution in natural populations of animals.     

Territorial bequeathal by red squirrel mothers

Red squirrels (Tamiasciurus hudsonicus) defend individual, food-basedterritories year round. These territories are crucial for overwintersurvival, yet some female red squirrels in northern populationsbequeath their territories to offspring and search for a newone. Bequeathal involves active, strategic dispersal by breedingfemales. Our study documents this unusual behavior and investigatesits correlates in two red squirrel populations in northern Canada.Thirty percent of breeding females dispersed. Bequeathal wasrelated to breeding date, with late-breeding females more oftendispersing, but was not related detectably to female conditionor territory quality. As an underlying trade-off, early-bornjuveniles more likely acquired a territory independently, butearly-breeding females lost mass and may have increased theirrisk of territory loss. We suggest that bequeathal has evolvedas a consequence of condition dependence in breeding date coupledwith limited resources.