John T. Hogg

Undesirable evolutionary consequences of trophy hunting.

Phenotype-based selective harvests, including trophy hunting, can have important implications for sustainable wildlife management if they target heritable traits. Here we show that in an evolutionary response to sport hunting of bighorn trophy rams (Ovis canadensis) body weight and horn size have declined significantly over time. We used quantitative genetic analyses, based on a partly genetically reconstructed pedigree from a 30-year study of a wild population in which trophy hunting targeted rams with rapidly growing horns, to explore the evolutionary response to hunter selection on ram weight and horn size. Both traits were highly heritable, and trophy-harvested rams were of significantly higher genetic ‘breeding value’ for weight and horn size than rams that were not harvested. Rams of high breeding value were also shot at an early age, and thus did not achieve high reproductive success. Declines in mean breeding values for weight and horn size therefore occurred in response to unrestricted trophy hunting, resulting in the production of smaller-horned, lighter rams, and fewer trophies.

Mating in bighorn sheep: frequent male reproduction via a high-risk “unconventional” tactic

Abstract Rocky Mountain bighorn rams use three distinct tactics in competition for mates. Two tactics (tending and blocking) feature defense and cooperative mating over a relatively prolonged consort period (up to 3 days). In the coursing tactic, subordinate rams fight dominants for temporary copulatory access (lasting seconds) to defended ewes. By combining population-wide genetic (microsatellite) exclusion of paternity, behavioral data and a model of bighorn reproductive competition, we estimated that coursing rams fathered 44% of 142 lambs assigned paternity in two natural populations. In one population, the probability of successful defense against coursing was lowest among rams that had many female consorts and held highest dominance rank. Even so, per capita annual male reproductive success was positively associated with social rank in both herds when measured in terms of fall conceptions. The proportion of coursing versus defending ram matings in each population (0.36 and 0.39) was similar to the corresponding fraction of lambs (0.43 and 0.47) fathered by coursing rams, suggesting that sperm competition approximated a fair lottery. Male traits important in gaining social status and obtaining cooperative consorts with ewes were different and potentially in conflict with those needed to defend against (and practise) coursing. Although the concussive weapons (horns) of rams are less dangerous than, for example, the piercing weapons of other bovids, injury from falls and horn blows during coursing brawls may cause death, handicap future mating competition or increase the risk of predation. Coursing is a rare example of an unconventional alternative mating tactic that is high-gain and high-risk.

Genetic rescue of an insular population of large mammals

Natural populations worldwide are increasingly fragmented by habitat loss. Isolation at small population size is thought to reduce individual and population fitness via inbreeding depression. However, little is known about the time-scale over which adverse genetic effects may develop in natural populations or the number and types of traits likely to be affected. The benefits of restoring gene flow to isolates are therefore also largely unknown. In contrast, the potential costs of migration (e.g. disease spread) are readily apparent. Management for ecological connectivity has therefore been controversial and sometimes avoided. Using pedigree and life-history data collected during 25 years of study, we evaluated genetic decline and rescue in a population of bighorn sheep founded by 12 individuals in 1922 and isolated at an average size of 42 animals for 10–12 generations. Immigration was restored experimentally, beginning in 1985. We detected marked improvements in reproduction, survival and five fitness-related traits among descendants of the 15 recent migrants. Trait values were increased by 23–257% in maximally outbred individuals. This is the first demonstration, to our knowledge, of increased male and female fitness attributable to outbreeding realized in a fully competitive natural setting. Our findings suggest that genetic principles deserve broader recognition as practical management tools with near-term consequences for large-mammal conservation.

SELECTION AND GENETIC (CO)VARIANCE IN BIGHORN SHEEP

Abstract Genetic theory predicts that directional selection should deplete additive genetic variance for traits closely related to fitness, and may favor the maintenance of alleles with antagonistically pleiotropic effects on fitness‐related traits. Trait heritability is therefore expected to decline with the degree of association with fitness, and some genetic correlations between selected traits are expected to be negative. Here we demonstrate a negative relationship between trait heritability and association with lifetime reproductive success in a wild population of bighorn sheep (Ovis canadensis) at Ram Mountain, Alberta, Canada. Lower heritability for fitness‐related traits, however, was not wholly a consequence of declining genetic variance, because those traits showed high levels of residual variance. Genetic correlations estimated between pairs of traits with significant heritability were positive. Principal component analyses suggest that positive relationships between morphometric traits constitute the main axis of genetic variation. Tradeoffs in the form of negative genetic or phenotypic correlations among the traits we have measured do not appear to constrain the potential for evolution in this population.

Stochastic predation events and population persistence in bighorn sheep

Many studies have reported temporal changes in the relative importance of density-dependence and environmental stochasticity in affecting population growth rates, but they typically assume that the predominant factor limiting growth remains constant over long periods of time. Stochastic switches in limiting factors that persist for multiple time-steps have received little attention, but most wild populations may periodically experience such switches. Here, we consider the dynamics of three populations of individually marked bighorn sheep (Ovis canadensis) monitored for 24–28 years. Each population experienced one or two distinct cougar (Puma concolor) predation events leading to population declines. The onset and duration of predation events were stochastic and consistent with predation by specialist individuals. A realistic Markov chain model confirms that predation by specialist cougars can cause extinction of isolated populations. We suggest that such processes may be common. In such cases, predator–prey equilibria may only occur at large geographical and temporal scales, and are unlikely with increasing habitat fragmentation.

Quantitative genetics and sex-specific selection on sexually dimorphic traits in bighorn sheep

Sexual conflict at loci influencing traits shared between the sexes occurs when sex-specific selection pressures are antagonistic relative to the genetic correlation between the sexes. To assess whether there is sexual conflict over shared traits, we estimated heritability and intersexual genetic correlations for highly sexually dimorphic traits (horn volume and body mass) in a wild population of bighorn sheep (Ovis canadensis) and quantified sex-specific selection using estimates of longevity and lifetime reproductive success. Body mass and horn volume showed significant additive genetic variance in both sexes, and intersexual genetic correlations were 0.24±0.28 for horn volume and 0.63±0.30 for body mass. For horn volume, selection coefficients did not significantly differ from zero in either sex. For body weight, selection coefficients were positive in females but did not differ from zero in males. The absence of detectable sexually antagonistic selection suggests that currently there are no sexual conflicts at loci influencing horn volume and body mass.

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.

Genetic linkage map of a wild genome: genomic structure, recombination and sexual dimorphism in bighorn sheep

BackgroundThe construction of genetic linkage maps in free-living populations is a promising tool for the study of evolution. However, such maps are rare because it is difficult to develop both wild pedigrees and corresponding sets of molecular markers that are sufficiently large. We took advantage of two long-term field studies of pedigreed individuals and genomic resources originally developed for domestic sheep (Ovis aries) to construct a linkage map for bighorn sheep, Ovis canadensis. We then assessed variability in genomic structure and recombination rates between bighorn sheep populations and sheep species.ResultsBighorn sheep population-specific maps differed slightly in contiguity but were otherwise very similar in terms of genomic structure and recombination rates. The joint analysis of the two pedigrees resulted in a highly contiguous map composed of 247 microsatellite markers distributed along all 26 autosomes and the X chromosome. The map is estimated to cover about 84% of the bighorn sheep genome and contains 240 unique positions spanning a sex-averaged distance of 3051 cM with an average inter-marker distance of 14.3 cM. Marker synteny, order, sex-averaged interval lengths and sex-averaged total map lengths were all very similar between sheep species. However, in contrast to domestic sheep, but consistent with the usual pattern for a placental mammal, recombination rates in bighorn sheep were significantly greater in females than in males (~12% difference), resulting in an autosomal female map of 3166 cM and an autosomal male map of 2831 cM. Despite differing genome-wide patterns of heterochiasmy between the sheep species, sexual dimorphism in recombination rates was correlated between orthologous intervals.ConclusionsWe have developed a first-generation bighorn sheep linkage map that will facilitate future studies of the genetic architecture of trait variation in this species. While domestication has been hypothesized to be responsible for the elevated mean recombination rate observed in domestic sheep, our results suggest that it is a characteristic of Ovis species. However, domestication may have played a role in altering patterns of heterochiasmy. Finally, we found that interval-specific patterns of sexual dimorphism were preserved among closely related Ovis species, possibly due to the conserved position of these intervals relative to the centromeres and telomeres. This study exemplifies how transferring genomic resources from domesticated species to close wild relative can benefit evolutionary ecologists while providing insights into the evolution of genomic structure and recombination rates of domesticated species.

Effect of chemical immobilization on social status of bighorn rams

M anagement programmes and research projects often require handling and marking of wild animals (Jorgenson et al. 1997; Gaillard et al. 2000). The consequences of capture on social behaviour, however, are often unknown, because they can only be determined through intensive monitoring of captured and control individuals (Berger & Kock 1988). Although a few studies have reported life history effects of chemical immobilization, for example, on female mountain goats, Oreamnos americanus (Côté et al. 1998), female moose, Alces alces (Ballard & Tobey 1981) and polar bears, Ursus maritimus (Ramsay & Stirling 1986), to our knowledge, no study has examined the impact of chemical immobilization on the behaviour and social organization ofwild animals.Here,we report the effects of chemical immobilization on intrasexual combat and social dominance among bighorn sheep rams, Ovis canadensis.

Genetic Characterization of Anaplasma ovis Strains from Bighorn Sheep in Montana

Wildlife reservoir species and genetic diversity of Anaplasma ovis (Rickettsiales: Anaplasmataceae) have been poorly characterized. Bighorn sheep (Ovis canadensis), captured in Montana from December 2004 to January 2005, were tested for antibodies to Anaplasma spp.; the presence of A. ovis was determined by the characterization of major surface protein msp4 sequences. Anaplasma antibodies were detected in 25/180 (14%) sampled bighorn sheep and A. ovis msp4 sequences were amplified by polymerase chain reaction (PCR) and sequenced from 9/23 (39%) of seropositive animals. All animals were negative by PCR for the related pathogens, Anaplasma phagocytophilum and Anaplasma marginale. All msp4 sequences identified in the bighorn sheep were identical and corresponded to a single A. ovis genotype that was identical to a sheep isolate reported previously from Idaho. The finding of a single genotype of A. ovis in this wild herd of bighorn sheep was in contrast to the genetic diversity reported for A. marginale in cattle herds in the western United States and worldwide. These results demonstrated that bighorn sheep may be a wildlife reservoir of A. ovis in Montana.