Rapidly declining fine-scale spatial genetic structure in female red deer

A growing literature now documents the presence of fine-scale genetic structure in wild vertebrate populations. Breeding population size, levels of dispersal and polygyny--all hypothesized to affect population genetic structure--are known to be influenced by ecological conditions experienced by populations. However the possibility of temporal or spatial variation in fine-scale genetic structure as a result of ecological change is rarely considered or explored. Here we investigate temporal variation in fine-scale genetic structure in a red deer population on the Isle or Rum, Scotland. We document extremely fine-scale spatial genetic structure (< 100 m) amongst females but not males across a 24-year study period during which resource competition has intensified and the population has reached habitat carrying capacity. Based on census data, adult deer were allocated to one of three subpopulations in each year of the study. Global F(ST) estimates for females generated using these subpopulations decreased over the study period, indicating a rapid decline in fine-scale genetic structure of the population. Global F(ST) estimates for males were not different from zero across the study period. Using census and genetic data, we illustrate that, as a consequence of a release from culling early in the study period, the number of breeding females has increased while levels of polygyny have decreased in this population. We found little evidence for increasing dispersal between subpopulations over time in either sex. We argue that both increasing female population size and decreasing polygyny could explain the decline in female population genetic structure.     

Polygamy and an absence of fine-scale structure in Dendroctonus ponderosae (Hopk.) (Coleoptera: Curcilionidae) confirmed using molecular markers

An understanding of mating systems and fine-scale spatial genetic structure is required to effectively manage forest pest species such as Dendroctonus ponderosae (mountain pine beetle). Here we used genome-wide single-nucleotide polymorphisms to assess the fine-scale genetic structure and mating system of D. ponderosae collected from a single stand in Alberta, Canada. Fine-scale spatial genetic structure was absent within the stand and the majority of genetic variation was best explained at the individual level. Relatedness estimates support previous reports of pre-emergence mating. Parentage assignment tests indicate that a polygamous mating system better explains the relationships among individuals within a gallery than the previously reported female monogamous/male polygynous system. Furthermore, there is some evidence to suggest that females may exploit the galleries of other females, at least under epidemic conditions. Our results suggest that current management models are likely to be effective across large geographic areas based on the absence of fine-scale genetic structure.     

Post‐weaning parental care increases fitness but is not heritable in North American red squirrels

Most empirical attempts to explain the evolution of parental care have focused on its costs and benefits (i.e. fitness consequences). In contrast, few investigations have been made of the other necessary prerequisite for evolutionary change, inheritance. Here, we examine the fitness consequences and heritability (h²) of a post‐weaning parental care behaviour (territory bequeathal) in a wild population of North American red squirrels. Each year, a subset (average across all years = 19%) of reproductive females bequeathed their territory to a dependent offspring. Bequeathing females experienced higher annual reproductive success and did not suffer a survival cost to themselves relative to those females retaining their territory. Bequeathing females thus realized higher relative annual fitness [ω = 1.18 ± 0.03 (SE)] than nonbequeathing females [ω = 0.96 ± 0.02 (SE)]. Additive genetic influences on bequeathal behaviour, however, were not significantly different from 0 (h² = 1.9 × 10^?3; 95% highest posterior density interval = 3.04 × 10^?8 to 0.37) and, in fact, bequeathal behaviour was not significantly repeatable (R = 2.0 × 10^?3; 95% HPD interval =0–0.27). In contrast, directional environmental influences were apparent. Females were more likely to bequeath in years following low food abundance and when food availability in the upcoming autumn was high. Despite an evident fitness benefit, a lack of heritable genetic variance will constrain evolution of this trait.     

Harnessing cross-species alignment to discover SNPs and generate a draft genome sequence of a bighorn sheep (Ovis canadensis)

Background

Whole genome sequences (WGS) have proliferated as sequencing technology continues to improve and costs decline. While many WGS of model or domestic organisms have been produced, a growing number of non-model species are also being sequenced. In the absence of a reference, construction of a genome sequence necessitates de novo assembly which may be beyond the ability of many labs due to the large volumes of raw sequence data and extensive bioinformatics required. In contrast, the presence of a reference WGS allows for alignment which is more tractable than assembly. Recent work has highlighted that the reference need not come from the same species, potentially enabling a wide array of species WGS to be constructed using cross-species alignment. Here we report on the creation a draft WGS from a single bighorn sheep (Ovis canadensis) using alignment to the closely related domestic sheep (Ovis aries).

Results

Two sequencing libraries on SOLiD platforms yielded over 865 million reads, and combined alignment to the domestic sheep reference resulted in a nearly complete sequence (95% coverage of the reference) at an average of 12x read depth (104 SD). From this we discovered over 15 million variants and annotated them relative to the domestic sheep reference. We then conducted an enrichment analysis of those SNPs showing fixed differences between the reference and sequenced individual and found significant differences in a number of gene ontology (GO) terms, including those associated with reproduction, muscle properties, and bone deposition.

Conclusion

Our results demonstrate that cross-species alignment enables the creation of novel WGS for non-model organisms. The bighorn sheep WGS will provide a resource for future resequencing studies or comparative genomics.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1618-x) contains supplementary material, which is available to authorized users.     

The nature of nurture in a wild mammal's fitness

Genetic variation in fitness is required for the adaptive evolution of any trait but natural selection is thought to erode genetic variance in fitness. This paradox has motivated the search for mechanisms that might maintain a population''s adaptive potential. Mothers make many contributions to the attributes of their developing offspring and these maternal effects can influence responses to natural selection if maternal effects are themselves heritable. Maternal genetic effects (MGEs) on fitness might, therefore, represent an underappreciated source of adaptive potential in wild populations. Here we used two decades of data from a pedigreed wild population of North American red squirrels to show that MGEs on offspring fitness increased the population''s evolvability by over two orders of magnitude relative to expectations from direct genetic effects alone. MGEs are predicted to maintain more variation than direct genetic effects in the face of selection, but we also found evidence of maternal effect trade-offs. Mothers that raised high-fitness offspring in one environment raised low-fitness offspring in another environment. Such a fitness trade-off is expected to maintain maternal genetic variation in fitness, which provided additional capacity for adaptive evolution beyond that provided by direct genetic effects on fitness.     

Sexually antagonistic association between paternal phenotype and offspring viability reinforces total selection on a sexually selected trait

The evolution of conspicuous sexually selected traits, such as horns or antlers, has fascinated biologists for more than a century. Elaborate traits can only evolve if they substantially increase reproduction, because they probably incur survival costs to the bearer. Total selection on these traits, however, includes sexual selection on sires and viability selection on offspring and can be influenced by changes in each of these components. Non-random associations between paternal phenotype and offspring viability may thus affect total selection on sexually selected traits. Long-term data on wild bighorn sheep (Ovis canadensis) provide the first evidence in nature that association between paternal phenotype and lamb viability strengthens total selection on horn size of adult rams, a sexually selected trait. The association of paternal horn length and offspring viability was sexually antagonistic: long-horned males sired sons with high viability but daughters of low viability. These results shed new light on the evolutionary dynamics of an iconic sexually selected trait and have important implications for sustainable wildlife management.     

The regulation of mitochondrial DNA copy number in glioblastoma cells

As stem cells undergo differentiation, mitochondrial DNA (mtDNA) copy number is strictly regulated in order that specialized cells can generate appropriate levels of adenosine triphosphate (ATP) through oxidative phosphorylation (OXPHOS) to undertake their specific functions. It is not understood whether tumor-initiating cells regulate their mtDNA in a similar manner or whether mtDNA is essential for tumorigenesis. We show that human neural stem cells (hNSCs) increased their mtDNA content during differentiation in a process that was mediated by a synergistic relationship between the nuclear and mitochondrial genomes and results in increased respiratory capacity. Differentiating multipotent glioblastoma cells failed to match the expansion in mtDNA copy number, patterns of gene expression and increased respiratory capacity observed in hNSCs. Partial depletion of glioblastoma cell mtDNA rescued mtDNA replication events and enhanced cell differentiation. However, prolonged depletion resulted in impaired mtDNA replication, reduced proliferation and induced the expression of early developmental and pro-survival markers including POU class 5 homeobox 1 (OCT4) and sonic hedgehog (SHH). The transfer of glioblastoma cells depleted to varying degrees of their mtDNA content into immunocompromised mice resulted in tumors requiring significantly longer to form compared with non-depleted cells. The number of tumors formed and the time to tumor formation was relative to the degree of mtDNA depletion. The tumors derived from mtDNA depleted glioblastoma cells recovered their mtDNA copy number as part of the tumor formation process. These outcomes demonstrate the importance of mtDNA to the initiation and maintenance of tumorigenesis in glioblastoma multiforme.     

A quantitative genetic analysis of hibernation emergence date in a wild population of Columbian ground squirrels

The life history schedules of wild organisms have long attracted scientific interest, and, in light of ongoing climate change, an understanding of their genetic and environmental underpinnings is increasingly becoming of applied concern. We used a multi-generation pedigree and detailed phenotypic records, spanning 18 years, to estimate the quantitative genetic influences on the timing of hibernation emergence in a wild population of Columbian ground squirrels (Urocitellus columbianus). Emergence date was significantly heritable [h(2) = 0.22 ± 0.05 (in females) and 0.34 ± 0.14 (in males)], and there was a positive genetic correlation (r(G) = 0.76 ± 0.22) between male and female emergence dates. In adult females, the heritabilities of body mass at emergence and oestrous date were h(2) = 0.23 ± 0.09 and h(2) = 0.18 ± 0.12, respectively. The date of hibernation emergence has been hypothesized to have evolved so as to synchronize subsequent reproduction with upcoming peaks in vegetation abundance. In support of this hypothesis, although levels of phenotypic variance in emergence date were higher than oestrous date, there was a highly significant genetic correlation between the two (r(G) = 0.98 ± 0.01). Hibernation is a prominent feature in the annual cycle of many small mammals, but our understanding of its influences lags behind that for phenological traits in many other taxa. Our results provide the first insight into its quantitative genetic influences and thus help contribute to a more general understanding of its evolutionary significance.