Biomedical subjects

D W Coltman

Publications and source records attributed to D W Coltman.

At least 19 recordsLinked to original sources

PubMed2006

Detecting the signature of selection on immune genes in highly structured populations of wild sheep (Ovis dalli).

The confounding effects of population structure complicate efforts to identify regions of the genome under the influence of selection in natural populations. Here we test for evidence of selection in three genes involved in vertebrate immune function - the major histocompatibility complex (MHC), interferon gamma (IFNG) and natural resistance associated macrophage polymorphism (NRAMP) - in highly structured populations of wild thinhorn sheep (Ovis dalli). We examined patterns of variation at microsatellite loci linked to these gene regions and at the DNA sequence level. Simple Watterson's tests indicated balancing selection at all three gene regions. However, evidence for selection was confounded by population structure, as the Watterson's test statistics from linked markers were not outside of the range of values from unlinked and presumably neutral microsatellites. The translated coding sequences of thinhorn IFNG and NRAMP are fixed and identical to those of domestic sheep (Ovis aries). In contrast, the thinhorn MHC DRB locus shows significant evidence of overdominance through both an excess of nonsynonymous substitution and trans-species polymorphism. The failure to detect balancing selection at microsatellite loci linked to the MHC is likely the result of recombination between the markers and expressed gene regions.

Animals↗

PubMed2006

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.

Altitude↗

PubMed2006

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.

Animals↗

PubMed2005

Male mate choice influences female promiscuity in Soay sheep.

In most animal species, males are predicted to compete for reproductive opportunities, while females are expected to choose between potential mates. However, when males' rate of reproduction is constrained, or females vary widely in 'quality', male mate choice is also predicted to occur. Such conditions exist in the promiscuous mating system of feral Soay sheep on St Kilda, Scotland, where a highly synchronized mating season, intense sperm competition and limitations on sperm production constrain males' potential reproductive rate, and females vary substantially in their ability to produce successful offspring. We show that, consistent with predictions, competitive rams focus their mating activity and siring success towards heavier females with higher inclusive fitness. To our knowledge, this is the first time that male mate choice has been identified and shown to lead to assortative patterns of parentage in a natural mammalian system, and occurs despite fierce male-male competition for mates. An additional consequence of assortative mating in this population is that lighter females experience a series of unstable consorts with less adept rams, and hence are mated by a greater number of males during their oestrus. We have thus also identified a novel male-driven mechanism that generates variation in female promiscuity, which suggests that the high levels of female promiscuity in this system are not part of an adaptive female tactic to intensify post-copulatory competition between males.

Animals↗

PubMed2005

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.

Animals↗

PubMed2005

Maternal genetic effects set the potential for evolution in a free-living vertebrate population.

Heritable maternal effects have important consequences for the evolutionary dynamics of phenotypic traits under selection, but have only rarely been tested for or quantified in evolutionary studies. Here we estimate maternal effects on early-life traits in a feral population of Soay sheep (Ovis aries) from St Kilda, Scotland. We then partition the maternal effects into genetic and environmental components to obtain the first direct estimates of maternal genetic effects in a free-living population, and furthermore test for covariance between direct and maternal genetic effects. Using an animal model approach, direct heritabilities (h2) were low but maternal genetic effects (m2) represented a relatively large proportion of the total phenotypic variance for each trait (birth weight m2=0.119, birth date m2=0.197, natal litter size m2=0.211). A negative correlation between direct and maternal genetic effects was estimated for each trait, but was only statistically significant for natal litter size (ram= -0.714). Total heritabilities (incorporating variance from heritable maternal effects and the direct-maternal genetic covariance) were significant for birth weight and birth date but not for natal litter size. Inadequately specified models greatly overestimated additive genetic variance and hence direct h2 (by a factor of up to 6.45 in the case of birth date). We conclude that failure to model heritable maternal variance can result in over- or under-estimation of the potential for traits to respond to selection, and advocate an increased effort to explicitly measure maternal genetic effects in evolutionary studies.

Analysis of Variance↗

PubMed2004

Population genetic structure of North American thinhorn sheep (Ovis dalli).

The thinhorn sheep (Ovis dalli ssp.) provides a rare example of a North American large mammal that occupies most of its native range and maintains close to ancestral population size. There are currently two recognized subspecies, Dall's sheep (O. d. dalli) and Stone's sheep (O. d. stonei), the validity of which remains uncertain. We investigated the spatial genetic structure of thinhorn sheep populations representing both subspecies by genotyping individuals (n = 919) from across the species range at 12 variable microsatellite loci. We found high levels of genetic diversity within (HE = 0.722) and significant genetic structure among the 24 sampled areas (FST = 0.160). Genetic distance measures and Bayesian clustering analyses revealed the presence of at least eight subpopulations that are delineated by mountain range topology. A strong overall pattern of isolation-by-distance is evident across the sampling range (r = 0.75, P < 0.001) suggesting limited dispersal and extensive philopatry. Partial Mantel tests of this relationship showed mountain range distinctions represent significant barriers to gene flow (P = 0.0001), supporting the Bayesian analyses. Genetic structure was more strongly pronounced in southern Yukon and Alaska than elsewhere. We also show evidence for genetic differences between the two currently recognized thinhorn subspecies.

Alaska↗

PubMed2003

Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success.

Male contests for access to receptive females are thought to have selected for the larger male body size and conspicuous weaponry frequently observed in mammalian species. However, when females copulate with multiple males within an oestrus, male reproductive success is a function of both pre- and postcopulatory strategies. The relative importance of these overt and covert forms of sexual competition has rarely been assessed in wild populations. The Soay sheep mating system is characterized by male contests for mating opportunities and high female promiscuity. We find that greater horn length, body size and good condition each independently influence a male's ability to monopolize receptive females. For males with large horns at least, this behavioural success translates into greater siring success. Consistent with sperm-competition theory, we also find that larger testes are independently associated with both higher copulation rates and increased siring success. This advantage of larger testes emerges, and strengthens, as the number of oestrous females increases, as dominant males can no longer control access to them all. Our results thus provide direct quantitative evidence that male reproductive success in wild populations of mammals is dependent upon the relative magnitude of both overt contest competition and covert sperm competition.

Animals↗

PubMed2003

Fine-scale genetic structure in a free-living ungulate population.

The fine-scale genetic structure of wild animal populations has rarely been analysed, yet is potentially important as a confounding factor in quantitative genetic and allelic association studies, as well as having implications for population dynamics, inbreeding and kin selection. In this study, we examined the extent to which the three spatial subunits, or hefts, of the Village Bay population of Soay sheep (Ovis aries) on St Kilda, Scotland, are genetically structured using data from 20 microsatellite and protein loci. Allele frequencies differed significantly among three hefts in all the study years we considered (1987-2000 inclusive). Small but significantly positive F(ST) and negative F(IS) values were observed in most years, indicating that the hefts are genetically differentiated, and that within each heft there is more observed heterozygosity than would be expected if each were an isolated breeding population. Males showed less fidelity to their natal heft, and as a consequence higher levels of relatedness within hefts were observed among females than among males. There was a significant negative relationship between geographical proximity and relatedness in pairwise comparisons involving females, and on average pairs of females located within 50 m of each other were related at the equivalent level of second cousins. Structure is therefore largely driven by incomplete postnatal dispersal by females. Mating appears to be random with respect to the spatial-genetic substructure of the hefts, and therefore genetic structure does not contribute to the overall rate of inbreeding in the population. However, genetic substructure can lead to allelic associations and generate environmental effects within lineages that have the potential to confound heritability analyses and allelic association studies.

Adenosine Deaminase↗

PubMed2003

Microsatellite measures of inbreeding: a meta-analysis.

Meta-analyses of published and unpublished correlations between phenotypic variation and two measures of genetic variation at microsatellite loci, multilocus heterozygosity (MLH) and mean d2, revealed that the strength of these associations are generally weak (mean r < 0.10). Effects on life-history trait variation were significantly greater than zero for both measures over all reported effect sizes (r = 0.0856 and 0.0479 for MLH and mean d2, respectively), whereas effects on morphometric traits were not (r = 0.0052 and r = 0.0038), which is consistent with the prediction that life-history traits exhibit greater inbreeding depression than morphometric traits. Effect sizes reported using mean d2 were smaller and more variable than those reported using MLH, suggesting that MLH may be a better metric for capturing inbreeding depression most of the time. However, analyses of paired effect sizes reported using both measures from the same data did not differ significantly. Several lines of evidence suggest that published effects sizes are upwardly biased. First, effect sizes from published studies were significantly higher than those reported in unpublished studies. Second, fail-safe numbers for reported effect sizes were generally quite low, with the exception of correlations between MLH and life-history traits. Finally, the slope of the regression of effect size on sample size was negative for most sets of traits. Taken together, these results suggest that studies designed to detect inbreeding depression on a life-history trait using microsatellites will need to sample in excess of 600 individuals to detect an average effect size (r = 0.10) with reasonable statistical power (0.80). Very few published studies have used samples sizes approaching this value.

Body Weights and Measures↗

PubMed2002

Estimating the prevalence of inbreeding from incomplete pedigrees.

A previous review of inbreeding in natural populations suggested that close inbreeding (inbreeding coefficient f = 0.25) is generally rare in wild birds and mammals. However, the review did not assess rates of moderate inbreeding (f = 0.125), which may make a rather larger contribution to overall inbreeding in a population. Furthermore, previous studies may have underestimated the prevalence of inbreeding in wild populations with incomplete pedigrees. By categorizing inbreeding events by the relationship of the parental pair, we suggest a simple method for estimating rates of close and moderate inbreeding from incomplete pedigree data. We applied this method to three wild populations of ruminants: red deer on Rum, Scotland, Soay sheep on Hirta, Scotland and reintroduced Arabian oryx on the Jiddat-al-Harasis, Oman. Although paternal half-sib pairs were the most common category of inbreeding in all three populations, there was considerable variation among populations in the frequencies of the various categories of inbreeding. This variation may be largely explained by differences in population size and dynamics, in maternal and paternal sibship size and in the overlap of reproductive lifespan of consecutive generations. Close and moderate inbreeding appear to be a routine part of breeding behaviour in these ruminant populations.

Animals↗

PubMed2002

Age-dependent sexual selection in bighorn rams.

Although mating systems and sexual selection have been intensively studied in ungulate model systems, very few studies have combined genetic paternity analysis with individual phenotypic data over several breeding seasons. We used microsatellite paternity analysis to determine the parentage of 83 bighorn sheep (Ovis canadensis) born between 1995 and 2000 at Ram Mountain, Alberta, Canada. We could assign the paternity of 64 lambs at a high level of statistical confidence (95%). Within each season, the most successful ram sired an average of 35.5% of the lambs with assigned paternity, and a single ram sired 26.1% of all lambs over the six mating seasons. Although a few large-horned, mature (age 8+ years) rams had very high reproductive success, younger rams sired ca. 50% of the lambs. Mixed-effects models indicated that mating success increases as a nonlinear function of age, with horn length increasingly positive in correlation with mating success in older rams. These results indicate that young or small rams possibly achieve mating success through alternative mating tactics that are less dependent on body and weapon size, such as coursing and blocking. Sexual selection is therefore likely to have age-dependent effects on traits such as agility, body and horn size.

Age Factors↗

PubMed2001

A microsatellite polymorphism in the gamma interferon gene is associated with resistance to gastrointestinal nematodes in a naturally-parasitized population of Soay sheep.

Free-living Soay sheep (Ovis aries) on the island of Hirta, St Kilda, Scotland, are naturally parasitized by gastrointestinal nematodes, predominantly Teladorsagia circumcincta. In this paper we show that reduced faecal egg counts (FEC) are associated with an allele at a microsatellite locus located in the first intron of the interferon gamma gene (o(IFN)-gamma) in Soay sheep lambs and yearlings, measured at approximately 4 and 16 months of age, respectively. The same allele was also associated with increased T. circumcincta-specific antibody (IgA) in lambs, but not associated significantly in yearlings. Flanking control markers failed to show a significant association with either FEC or IgA. These results suggest that a polymorphic gene conferring increased resistance to gastrointestinal nematode parasites is located at or near the interferon gamma gene, and support previous reports which have mapped a quantitative trait locus (QTL) for resistance to this region in domestic sheep. Our data are consistent with the idea that a functional polymorphism leading to reduced expression or efficacy of (IFN)-gamma could enhance the immune response to gastrointestinal nematodes by favouring the activity of the Th2 cell subset and antibody associated immune mechanisms.

Animals↗

PubMed2001

Positive genetic correlation between parasite resistance and body size in a free-living ungulate population.

Parasite resistance and body size are subject to directional natural selection in a population of feral Soay sheep (Ovis aries) on the island of St. Kilda, Scotland. Classical evolutionary theory predicts that directional selection should erode additive genetic variation and favor the maintenance of alleles that have negative pleiotropic effects on other traits associated with fitness. Contrary to these predictions, in this study we show that there is considerable additive genetic variation for both parasite resistance, measured as fecal egg count (FEC), and body size, measured as weight and hindleg length, and that there are positive genetic correlations between parasite resistance and body size in both sexes. Body size traits had higher heritabilities than parasite resistance. This was not due to low levels of additive genetic variation for parasite resistance, but was a consequence of high levels of residual variance in FEC. Measured as coefficients of variation, levels of additive genetic variation for FEC were actually higher than for weight or hindleg length. High levels of additive genetic variation for parasite resistance may be maintained by a number of mechanisms including high mutational input, balancing selection, antagonistic pleiotropy, and host-parasite coevolution. The positive genetic correlation between parasite resistance and body size, a trait also subject to sexual selection in males, suggests that parasite resistance and growth are not traded off in Soay sheep, but rather that genetically resistant individuals also experience superior growth.

Alleles↗

PubMed1999

Male reproductive success in a promiscuous mammal: behavioural estimates compared with genetic paternity.

Molecular techniques have enabled behavioural ecologists to reassess mating systems from a genetic perspective. Studies of paternity frequently reveal that mating behaviour does not always reflect parentage, and may bring to light alternative mating tactics. Here we present a comparison of behavioural and genetic measures of male reproductive success in a mammalian mating system in which both sexes are highly promiscuous. Rather than having a stable harem social structure, Soay rams (Ovis aries) on the island of Hirta, St Kilda, UK usually consort with individual oestrous ewes sequentially. Not all matings occur between consort pairs, however, and ewes have been seen to mate with up to 10 different rams on the same day. Using locus-specific polymorphism at five protein and 10 microsatellite DNA loci, we determined paternity for 236 lambs born into three cohorts, and compared paternity with estimates of mating success derived from more than one census of rutting behaviour. The correlation between the number of ewes with which each ram was witnessed in consort and the number of paternities assigned was positive and statistically significant, and rams that were observed in consort with a ewe were 18 times more likely to have sired her offspring than other candidate rams. However, most lambs (73%) were not sired by a ram seen in consort with the oestrous mother. Many juveniles, yearlings and some adult rams were rarely seen in consort with ewes, yet were assigned a significant number of paternities. These results suggest that mating tactics differ between age groups, and that alternative mating strategies among adults that do not involve forming consorts with many females also confer mating success. For these reasons, census-based observations of consort associations between individuals cannot be used to accurately estimate individual male reproductive success in this population.

Animals↗

PubMed1999

Density-dependent variation in lifetime breeding success and natural and sexual selection in Soay rams.

Variation in male lifetime breeding success (LBS) is central to understanding selection, yet it has rarely been measured in natural populations of large mammals. Here, we first describe variation in the opportunity for selection in cohorts of Soay rams (Ovis aries) on the archipelago of St. Kilda, Scotland, that were born during years of varying population density. Variation in LBS is closely coupled with demography, as rams born in years of low density following population crashes enjoy greater LBS than do those born in high-density years. Paradoxically, the opportunity for selection was greatest in the largest cohorts, those born in years of high population density, owing to low juvenile breeding success and overwinter survival. Variation in longevity and the contribution of nonbreeders were the most important components of the total variance in LBS in cohorts born in years of high density, while variation in fecundity was more important in cohorts born in low-density years. The opportunity for sexual selection is thus stronger in cohorts born in low-density years, as many rams in these cohorts survive to compete for mates as adults in subsequent ruts. Variation in population density in the year of birth also influenced the intensity of selection. Individuals born in years of high population density underwent strong natural selection in favor of longer hindlimbs over their first winter. In contrast, in cohorts born in low-density years, there was no natural selection on hindlimb in the first year of life. Longer hindlimbs were associated with increased fecundity over the entire lifetime of individuals born in low-density years. Natural and sexual selection thus act on the same trait in the same direction at different life-history stages in Soay rams, depending on the population density experienced in the year of birth.

Journal Article↗

PubMed1998

Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites.

We examined the relations between fitness-related traits of wild harbour seal (Phoca vitulina) pups with microsatellite heterozygosity, and with a measure of genomic diversity based on the mean squared distance between microsatellite alleles within an individual, mean d2. Birth weight was positively influenced by maternal age, pup sex, and either mean d2 or individual heterozygosity in separate multiple regression models. The association of birth weight with mean d2 was stronger than that with heterozygosity, however. The factors maternal age, pup sex, and mean d2 combined to account for 36.8% of the variation in birth weight, with mean d2 accounting for the greatest explanatory power (52.3% of the variance explained). Pups which survived until weaning had significantly higher mean d2 than pups which died, independent of birth weight. These effects are consistent with heterosis resulting from recent population mixing, and/or inbreeding depression in this population. Mean d2 thus provides (i) a better measure of individual genetic variability than heterozygosity for microsatellite data; and (ii) a convenient tool for assessing the effects of inbreeding and outbreeding in natural populations.

Animals↗

PubMed1998

Bovine microsatellite loci are highly conserved in red deer (Cervus elaphus), sika deer (Cervus nippon) and Soay sheep (Ovis aries).

We tested 174 bovine microsatellite primer pairs for use in a primitive breed of sheep and two species of deer. Of 173 markers, 127 (73.4%) gave a product in Soay sheep (Ovis aries) of which 54 (42.5%) were polymorphic. One hundred and twenty-nine of 174 (74.1%) markers gave a product in red deer (Cervus elaphus) of which 72 (55.8%) were polymorphic. In sika deer (Cervus nippon) 126 of 171 (73.7%) microsatellite primers gave a product with 47 (37.3%) polymorphic. The proportion of bovine microsatellite loci conserved across artiodactyl species was significantly greater in this study than previously reported. Reasons for this high degree of microsatellite conservation are discussed. We suggest that a high resolution comparative map of the artiodactyls can be constructed using microsatellites.

Alleles↗