Estimating genome-wide heterozygosity: effects of demographic history and marker type

Heterozygosity–fitness correlations (HFCs) are often used to link individual genetic variation to differences in fitness. However, most studies examining HFCs find weak or no correlations. Here, we derive broad theoretical predictions about how many loci are needed to adequately measure genomic heterozygosity assuming different levels of identity disequilibrium (ID), a proxy for inbreeding. We then evaluate the expected ability to detect HFCs using an empirical data set of 200 microsatellites and 412 single nucleotide polymorphisms (SNPs) genotyped in two populations of bighorn sheep (Ovis canadensis), with different demographic histories. In both populations, heterozygosity was significantly correlated across marker types, although the strength of the correlation was weaker in a native population compared with one founded via translocation and later supplemented with additional individuals. Despite being bi-allelic, SNPs had similar correlations to genome-wide heterozygosity as microsatellites in both populations. For both marker types, this association became stronger and less variable as more markers were considered. Both populations had significant levels of ID; however, estimates were an order of magnitude lower in the native population. As with heterozygosity, SNPs performed similarly to microsatellites, and precision and accuracy of the estimates of ID increased as more loci were considered. Although dependent on the demographic history of the population considered, these results illustrate that genome-wide heterozygosity, and therefore HFCs, are best measured by a large number of markers, a feat now more realistically accomplished with SNPs than microsatellites.     

Environmental coupling of selection and heritability limits evolution

There has recently been great interest in applying theoretical quantitative genetic models to empirical studies of evolution in wild populations. However, while classical models assume environmental constancy, most natural populations exist in variable environments. Here, we applied a novel analytical technique to a long-term study of birthweight in wild sheep and examined, for the first time, how variation in environmental quality simultaneously influences the strength of natural selection and the genetic basis of trait variability. In addition to demonstrating that selection and genetic variance vary dramatically across environments, our results show that environmental heterogeneity induces a negative correlation between these two parameters. Harsh environmental conditions were associated with strong selection for increased birthweight but low genetic variance, and vice versa. Consequently, the potential for microevolution in this population is constrained by either a lack of heritable variation (in poor environments) or by a reduced strength of selection (in good environments). More generally, environmental dependence of this nature may act to limit rates of evolution, maintain genetic variance, and favour phenotypic stasis in many natural systems. Assumptions of environmental constancy are likely to be violated in natural systems, and failure to acknowledge this may generate highly misleading expectations for phenotypic microevolution.     

Evidence for cryptic glacial refugia from North American mountain sheep mitochondrial DNA

The separation of populations by ice sheets into large refugia can account for much of the genetic diversity found in present day populations. The evolutionary implications of small glacial refugia have not been as thoroughly explored. To examine refugial origins of North American mountain sheep Ovis spp., we analyzed a 604 bp portion of the mitochondrial DNA (mtDNA) control region from 223 O. dalli and O. canadensis. Major refugia were identified in eastern Beringia and southern North America, and we found evidence for two smaller refugia situated between the Laurentide and Cordilleran glaciers. Our results are the first to demonstrate support for survival of any organism in the latter two refugia. These refugia also appear to have conserved a genetic signal that confirms past hybridization of O. dalli and O. canadensis.     

Something Darwin didn't know about barnacles: spermcast mating in a common stalked species

Most free-living barnacles are hermaphroditic, and eggs are presumed to be fertilized either by pseudo-copulation or self-fertilization. Although the common northeast Pacific intertidal gooseneck barnacle, Pollicipes polymerus, is believed only to cross-fertilize, some isolated individuals well outside penis range nonetheless bear fertilized eggs. They must therefore either self-fertilize or—contrary to all prior expectations about barnacle mating—obtain sperm from the water. To test these alternative hypotheses, we collected isolated individuals bearing egg masses, as well as isolated pairs where at least one parent carried egg masses. Using 16 single nucleotide polymorphism markers, we confirmed that a high percentage of eggs were fertilized with sperm captured from the water. Sperm capture occurred in 100 per cent of isolated individuals and, remarkably, even in 24 per cent of individuals that had an adjacent partner. Replicate subsamples of individual egg masses confirmed that eggs fertilized by captured sperm occurred throughout the egg mass. Sperm capture may therefore be a common supplement to pseudo-copulation in this species. These observations (i) overturn over a century of beliefs about what barnacles can (or cannot) do in terms of sperm transfer, (ii) raise doubts about prior claims of self-fertilization in barnacles, (iii) raise interesting questions about the capacity for sperm capture in other species (particularly those with short penises), and (iv) show, we believe for the first time, that spermcast mating can occur in an aquatic arthropod.     

Mountain pine beetle host-range expansion threatens the boreal forest

The current epidemic of the mountain pine beetle (MPB), an indigenous pest of western North American pine, has resulted in significant losses of lodgepole pine. The leading edge has reached Alberta where forest composition shifts from lodgepole to jack pine through a hybrid zone. The susceptibility of jack pine to MPB is a major concern, but there has been no evidence of host-range expansion, in part due to the difficulty in distinguishing the parentals and their hybrids. We tested the utility of a panel of microsatellite loci optimized for both species to classify lodgepole pine, jack pine and their hybrids using simulated data. We were able to accurately classify simulated individuals, and hence applied these markers to identify the ancestry of attacked trees. Here we show for the first time successful MPB attack in natural jack pine stands at the leading edge of the epidemic. This once unsuitable habitat is now a novel environment for MPB to exploit, a potential risk which could be exacerbated by further climate change. The consequences of host-range expansion for the vast boreal ecosystem could be significant.     

A quantitative trait locus analysis of personality in wild bighorn sheep

Personality, the presence of persistent behav105 ioral differences among individuals over time or contexts, potentially has important ecological and evolutionary consequences. However, a lack of knowledge about its genetic architecture limits our ability to understand its origin, evolution, and maintenance. Here, we report on a genome‐wide quantitative trait locus (QTL) analysis for two personality traits, docility and boldness, in free‐living female bighorn sheep from Ram Mountain, Alberta, Canada. Our variance component linkage analysis based on 238 microsatellite loci genotyped in 310 pedigreed individuals identified suggestive docility and boldness QTL on sheep chromosome 2 and 6, respectively. A lack of QTL overlap indicated that genetic covariance between traits was not modulated by pleiotropic effects at a major locus and may instead result from linkage disequilibrium or pleiotropic effects at QTL of small effects. To our knowledge, this study represents the first attempt to dissect the genetic architecture of personality in a free‐living wildlife population, an important step toward understanding the link between molecular genetic variation in personality and fitness and the evolutionary processes maintaining this variation.     

Spatial genetic structure of a symbiotic beetle-fungal system: toward multi-taxa integrated landscape genetics

Spatial patterns of genetic variation in interacting species can identify shared features that are important to gene flow and can elucidate co-evolutionary relationships. We assessed concordance in spatial genetic variation between the mountain pine beetle (Dendroctonus ponderosae) and one of its fungal symbionts, Grosmanniaclavigera, in western Canada using neutral genetic markers. We examined how spatial heterogeneity affects genetic variation within beetles and fungi and developed a novel integrated landscape genetics approach to assess reciprocal genetic influences between species using constrained ordination. We also compared landscape genetic models built using Euclidean distances based on allele frequencies to traditional pair-wise Fst. Both beetles and fungi exhibited moderate levels of genetic structure over the total study area, low levels of structure in the south, and more pronounced fungal structure in the north. Beetle genetic variation was associated with geographic location while that of the fungus was not. Pinevolume and climate explained beetle genetic variation in the northern region of recent outbreak expansion. Reciprocal genetic relationships were only detectedin the south where there has been alonger history of beetle infestations. The Euclidean distance and Fst-based analyses resulted in similar models in the north and over the entire study area, but differences between methods in the south suggest that genetic distances measures should be selected based on ecological and evolutionary contexts. The integrated landscape genetics framework we present is powerful, general, and can be applied to other systems to quantify the biotic and abiotic determinants of spatial genetic variation within and among taxa.     

Spatial genetic structure of the mountain pine beetle (Dendroctonus ponderosae) outbreak in western Canada: historical patterns and contemporary dispersal

Environmental change has a wide range of ecological consequences, including species extinction and range expansion. Many studies have shown that insect species respond rapidly to climatic change. A mountain pine beetle epidemic of record size in North America has led to unprecedented mortality of lodgepole pine, and a significant range expansion to the northeast of its historic range. Our goal was to determine the spatial genetic variation found among outbreak population from which genetic structure, and dispersal patterns may be inferred. Beetles from 49 sampling locations throughout the outbreak area in western Canada were analysed at 13 microsatellite loci. We found significant north-south population structure as evidenced by: (i) Bayesian-based analyses, (ii) north-south genetic relationships and diversity gradients; and (iii) a lack of isolation-by-distance in the northernmost cluster. The north-south structure is proposed to have arisen from the processes of postglacial colonization as well as recent climate-driven changes in population dynamics. Our data support the hypothesis of multiple sources of origin for the outbreak and point to the need for population specific information to improve our understanding and management of outbreaks. The recent range expansion across the Rocky Mountains into the jack/lodgepole hybrid and pure jack pine zones of northern Alberta is consistent with a northern British Columbia origin. We detected no loss of genetic variability in these populations, indicating that the evolutionary potential of mountain pine beetle to adapt has not been reduced by founder events. This study illustrates a rapid range-wide response to the removal of climatic constraints, and the potential for range expansion of a regional population.     

Sexing the Sciuridae: a simple and accurate set of molecular methods to determine sex in tree squirrels, ground squirrels and marmots

We determined the sequence of the male-specific minor histocompatibility complex antigen (Smcy) from the Y chromosome of seven squirrel species (Sciuridae, Rodentia). Based on conserved regions inside the Smcy intron sequence, we designed PCR primers for sex determination in these species that can be co-amplified with nuclear loci as controls. PCR co-amplification yields two products for males and one for females that are easily visualized as bands by agarose gel electrophoresis. Our method provides simple and reliable sex determination across a wide range of squirrel species.