Variable social organization is ubiquitous in Artiodactyla and probably evolved from pair-living ancestors.

Previous studies to understand the evolution of interspecific variation in mammalian social organization (SO; composition of social units) produced inconsistent results, possibly by ignoring intraspecific variation. Here we present systematic data on SO in artiodactyl populations, coding SO as solitary, pair-living, group-living, sex-specific or variable (different kinds of SOs in the same population). We found that 62% of 245 populations and 83% of species (83/100) exhibited variable SO. Using Bayesian phylogenetic mixed-effects models, we simultaneously tested whether research effort, habitat, sexual dimorphism, breeding seasonality or body size predicted the likelihood of different SOs and inferred the ancestral SO. Body size and sexual dimorphism were strongly associated with different SOs. Contingent on the small body size (737 g) and putative sexual monomorphism of the earliest fossil artiodactyl, the ancestral SO was most likely to be pair-living (probability = 0.76, 95% CI = 0-1), followed by variable (p = 0.19, 95% CI = 0-0.99). However, at body size values typical of extant species, variable SO becomes the dominant form (p = 0.74, 95% CI = 0.18-1.00). Distinguishing different kinds of 'variable' highlights transitions from SOs involving pair-living to SOs involving solitary and/or group-living with increasing body size and dimorphism. Our results support the assumption that ancestral artiodactyl was pair-living and highlight the ubiquity of intraspecific variation in SO.

Towards robust evolutionary inference with integral projection models.

Integral projection models (IPMs) are extremely flexible tools for ecological and evolutionary inference. IPMs track the distribution of phenotype in populations through time, using functions describing phenotype-dependent development, inheritance, survival and fecundity. For evolutionary inference, two important features of any model are the ability to (i) characterize relationships among traits (including values of the same traits across ages) within individuals, and (ii) characterize similarity between individuals and their descendants. In IPM analyses, the former depends on regressions of observed trait values at each age on values at the previous age (development functions), and the latter on regressions of offspring values at birth on parent values as adults (inheritance functions). We show analytically that development functions, characterized this way, will typically underestimate covariances of trait values across ages, due to compounding of regression to the mean across projection steps. Similarly, we show that inheritance, characterized this way, is inconsistent with a modern understanding of inheritance, and underestimates the degree to which relatives are phenotypically similar. Additionally, we show that the use of a constant biometric inheritance function, particularly with a constant intercept, is incompatible with evolution. Consequently, current implementations of IPMs will predict little or no phenotypic evolution, purely as artefacts of their construction. We present alternative approaches to constructing development and inheritance functions, based on a quantitative genetic approach, and show analytically and through an empirical example on a population of bighorn sheep how they can potentially recover patterns that are critical to evolutionary inference.

Demographic drivers of age-dependent sexual selection.

Sexual selection has a critical role in evolution, and it is fundamental to identify what ecological factors drive its variation. Disentangling the ecological correlates of sexual selection over the long term, however, is challenging and has rarely been done in nature. We sought to assess how demographic changes influenced the intensity, direction and form of sexual selection and whether selective pressures varied with age. We tested whether breeder sex ratio, number of competitors and age structure influenced selection differentials on horn length of wild bighorn rams (Ovis canadensis) of different age classes on Ram Mountain, Alberta. We used 21 years of data including a detailed pedigree, demographic parameters and repeated morphological measurements. Sexual selection on horn length of males of all ages was directional and positive. Selection intensity increased with the number of competitors, reflecting male-male encounter rate during the rut, but was independent of breeder sex ratio or age structure. This result can also be linked to changes in population size because the number of competitors was highly correlated to total number of sheep. This demographic effect likely arises from age-dependent mating tactics. Males aged 2-4 years are weakly competitive and experienced stronger sexual selection as they accounted for a greater proportion of all males. Selection experienced by mature males appeared independent of demography. Our study provides a rare description of the demographic determinants of sexual selection in nature.

Sex-based differences in the adaptive value of social behavior contrasted against morphology and environment.

The adaptive nature of sociality has long been a central question in ecology and evolution. However, the relative importance of social behavior for fitness, compared to morphology and environment, remains largely unknown. We assessed the importance of sociality for fitness (lamb production and survival) in a population of mark6d bighorn sheep (Ovis canadensis) over 16 years (n = 1022 sheep-years). We constructed social networks from observations (n = 38,350) of group membership (n = 3150 groups). We then tested whether consistent individual differences in social behavior (centrality) exist and evaluated their relative importance compared to factors known to affect fitness: mass, age, parental effects, and population density. Sheep exhibited consistent individual differences in social centrality. Controlling for maternal carryover effects and age, the positive effect of centrality in a social network on adult female lamb production and survival was equal or greater than the effect of body mass or population density. Social centrality had less effect on male survival and no effect on adult male lamb production or lamb survival. Through its effect on lamb production and survival, sociality in fission-fusion animal societies may ultimately influence population dynamics equally or more than morphological or environmental effects.

Comparing measures of breeding inequality and opportunity for selection with sexual selection on a quantitative character in bighorn rams.

The reliability and consistency of the many measures proposed to quantify sexual selection have been questioned for decades. Realized selection on quantitative characters measured by the selection differential i was approximated by metrics based on variance in breeding success, using either the opportunity for sexual selection Is or indices of inequality. There is no consensus about which metric best approximates realized selection on sexual characters. Recently, the opportunity for selection on character mean OSM was proposed to quantify the maximum potential selection on characters. Using 21 years of data on bighorn sheep (Ovis canadensis), we investigated the correlations between seven indices of inequality, Is , OSM and i on horn length of males. Bighorn sheep are ideal for this comparison because they are highly polygynous and sexually dimorphic, ram horn length is under strong sexual selection, and we have detailed knowledge of individual breeding success. Different metrics provided conflicting information, potentially leading to spurious conclusions about selection patterns. Iδ, an index of breeding inequality, and, to a lesser extent, Is showed the highest correlation with i on horn length, suggesting that these indices document breeding inequality in a selection context. OSM on horn length was strongly correlated with i, Is and indices of inequality. By integrating information on both realized sexual selection and breeding inequality, OSM appeared to be the best proxy of sexual selection and may be best suited to explore its ecological bases.

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.

A quantitative trait locus analysis of personality in wild bighorn sheep.

Personality, the presence of persistent behav105ioral 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.

Evolutionary rescue in vertebrates: evidence, applications and uncertainty.

The current rapid rate of human-driven environmental change presents wild populations with novel conditions and stresses. Theory and experimental evidence for evolutionary rescue present a promising case for species facing environmental change persisting via adaptation. Here, we assess the potential for evolutionary rescue in wild vertebrates. Available information on evolutionary rescue was rare and restricted to abundant and highly fecund species that faced severe intentional anthropogenic selective pressures. However, examples from adaptive tracking in common species and genetic rescues in species of conservation concern provide convincing evidence in favour of the mechanisms of evolutionary rescue. We conclude that low population size, long generation times and limited genetic variability will result in evolutionary rescue occurring rarely for endangered species without intervention. Owing to the risks presented by current environmental change and the possibility of evolutionary rescue in nature, we suggest means to study evolutionary rescue by mapping genotype → phenotype → demography → fitness relationships, and priorities for applying evolutionary rescue to wild populations.

Sex-differential effects of inbreeding on overwinter survival, birth date and mass of bighorn lambs.

Although it is generally expected that inbreeding would lower fitness, few studies have directly quantified the effects of inbreeding in wild mammals. We investigated the effects of inbreeding using long-term data from bighorn sheep on Ram Mountain, Alberta, Canada, over 20 years. This population underwent a drastic decline from 1992 to 2002 and has since failed to recover. We used a pedigree to calculate inbreeding coefficients and examined their impact on lamb growth, birth date and survival. Inbreeding had a substantial effect on female survival: for a given mass in September, the probability of overwinter survival for inbred female lambs was about 40% lower than that of noninbred ones. Contrary to our expectations, inbred female lambs were born earlier than noninbred ones. Earlier birth led to inbred female lambs being heavier by mid-September than noninbred ones. There was a nonsignificant trend for inbred female yearlings to weigh more than noninbred ones. A stronger mass-dependent viability selection for inbred compared to noninbred female lambs may explain why surviving inbred females were heavier than noninbred ones. Survival of male lambs was not affected by inbreeding. Sex-differential effects of inbreeding may be a general pattern in sexually dimorphic mammals, because of sex-biased maternal care or sexual differences in early development strategies.

Male personality, life-history strategies and reproductive success in a promiscuous mammal.

Recent theoretical work suggests that personality is a component of life history, but links between personality and either age-dependent reproductive success or life-history strategy are yet to be established. Using quantitative genetic analyses on a long-term pedigree we estimated indices of boldness and docility for 105 bighorn sheep rams (Ovis canadensis), born between 1983 and 1999, and compared these indices to their reproductive history from 2 years of age until death. Docility and boldness were highly heritable and negatively genetically correlated. Docile and bold rams survived longer than indocile and shy rams. Docility and boldness had a weak negative effect on reproductive success early in life, but a strong positive effect on older rams. Our findings highlight an important role of personality on reproductive success and suggest that personality could be an important component of life-history strategy.

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.

Consistency of temperament in bighorn ewes and correlates with behaviour and life history.

Individual differences in temperament may affect how animals react to novel situations, avoid predation, invest in reproduction and behave in a variety of social contexts. Little information is available, however, about individual differences in temperament for wild animals. For bighorn sheep, Ovis canadensis, ewes captured as part of a long-term study, we compared behaviour during handling to behaviour in the field and reproductive history. We considered 'bold' ewes those that were frequently trapped during the summer, and assigned to each ewe a docility index based on her behaviour during handling. Measurements of temperament for the same individual at different captures were highly consistent. Temperament was not affected by reproductive status or age, nor was it related to body mass. Correlations between behaviour at the trap and in the field were weak and mostly nonsignificant, suggesting that temperament is domain specific rather than domain general. Bold ewes tended to start reproducing earlier and have higher weaning success than shy ewes. Variability in temperamental traits in the study population could be maintained by life-history trade-offs and by yearly changes in selective pressures. Copyright 2000 The Association for the Study of Animal Behaviour.

Body mass and individual fitness in female ungulates: bigger is not always better.

In female vertebrates, differences in fitness often correspond to differences in phenotypic quality, suggesting that larger females have greater fitness. Variation in individual fitness can result from variation in life span and/or variation in yearly reproductive success, but no study has yet assessed the relationships between the components of fitness and phenotypic quality while controlling for life span. We tried to fill this gap using data from long-term monitoring (23 years) of marked roe deer and bighorn sheep, two ungulates with very different life histories. In both species, we found a strong positive relationship between an adult female's mass and her probability of reaching old age: over the long term, bigger is indeed better for ungulate females. On the other hand, we found no evidence in either species that heavier females had higher fitness when differences in life span were accounted for: over the short term, bigger is not necessarily better. Our results indicate that, while broad differences in phenotypic quality affect individual fitness, when differences in life span are accounted for phenotypic quality has no residual effect on fitness. Therefore, within a given range of phenotypic quality, bigger is not always better, for reasons which may differ between species.

Quantitative genetics of life-history traits in a long-lived wild mammal.

Quantitative genetic studies of life-history traits in wild populations are very rare, yet variance/covariance estimates of these traits are crucial to understanding the evolution of reproductive strategies. We estimated heritabilities (h2) of several life-history traits (longevity, age and mass at primiparity, and reproductive traits) in two bighorn sheep (Ovis canadensis) populations, and both phenotypic (rP) and genetic (rA) correlations between life-history traits in one population. We included adult mass in our analyses because it is related to several life-history traits. We used the mother-daughter regression method and resampling tests based on data from long-term monitoring of marked females. Contrary to the theoretical prediction of low heritability for fitness-related traits, heritability estimates in the Ram Mountain population ranged from 0.02 to 0.81 (mean of 0.52), and several were different from zero. Coefficients of variation tend to support the hypothesis of a higher environmental influence on life-history traits. In contrast, at Sheep River we found low heritabilities of life-history traits. Phenotypic correlations varied between -0.09 and 0.95. Several genetic correlations were strong, particularly for different reproductive traits that are functionally related, and ranged from -0.34 to 1.71. Overall, genetic and phenotypic correlations between the same variables were similar in magnitude and direction. We found no phenotypic or genetic correlations suggesting trade-offs among life-history traits. Bighorn sheep may not form the large, outbred populations at equilibrium that are assumed by both Fisher's fundamental theorem and by theories predicting antagonistic pleiotropy between life-history traits. Alternatively, the absence of negative genetic correlations may result from genetic variation in ability to acquire resources or from novel environmental conditions existing during the study period.

Heritability of body mass varies with age and season in wild bighorn sheep

Heritabilities (h2) of body mass at different ages and seasons were estimated using offspring-mother regression and restricted maximum likelihood (REML) methods for bighorn sheep on Ram Mountain, Alberta. Both methods resulted in similar estimates of h2 for adults, but for lambs and yearlings heritability was underestimated by offspring-mother regression relative to REML, possibly because of higher maternal-effects bias for offspring-mother regression. Heritabilities of body mass in bighorn were similar to published estimates for domestic sheep. Heritability estimated by offspring-mother regression increased after 2 years of age. The REML method suggested that heritability was moderate for lambs and yearlings, very low at 2 years of age, and increased afterwards. The increase in heritability with age was attributed to declining negative maternal effects. Very low h2 estimates at 2 years of age, obtained with both methods, appeared to be caused by a combination of high environmental variance and very low genetic variance. Body mass of bighorn sheep has a pronounced seasonal cycle, and h2 was lower in June than in September for 2-year-olds and older sheep, and associated with both lower VA and higher VE in spring.

Immobilization of mountain goats with xylazine and reversal with idazoxan.

Mountain goats (Oreamnos americanus) were captured in traps and immobilized with xylazine, later reversed with idazoxan. One hundred and forty-one goats were immobilized, 94 with a single injection and 47 with multiple injections. Dosage (mg/kg of body weight) of xylazine received, induction time, and recovery time after handling did not differ among sex-age classes. Increasing the dosage did not shorten induction time. The first injection of xylazine in multiple-injection captures was lower than the dose given in single-injection captures, suggesting that insufficient initial doses of xylazine made multiple injections necessary. Xylazine is an effective drug for immobilization of mountain goats captured in traps, at dosages of about 4.9 mg/kg. The dosage of xylazine required to immobilize mountain goats is higher than that reported for bighorn sheep and white-tailed deer.

Mass- and density-dependent reproductive success and reproductive costs in a capital breeder.

For capital breeders, mass may affect reproductive potential. Reproductive expenditure may reduce future reproductive potential, particularly when resources are scarce. To test the hypothesis that reproductive success and the costs of reproduction vary according to mass and population density, we analyzed 25 yr of data on bighorn ewes (Ovis canadensis). The number of adult females was first limited by yearly removals, then allowed to triple. We found no survival costs of reproduction for ewes aged 4-7 yr. For ewes aged 8-14 yr, survival was density dependent for barren ewes but not for ewes that weaned lambs. Failure to lamb was rare and negatively correlated with fertility the following year. At low population density, lactation had a negative effect on mass gain but had a limited reproductive cost. At high density, heavy ewes had higher reproductive success than light ewes, and the reproductive cost and somatic costs of reproduction increased. The cost of reproduction was greater for light than for heavy ewes. Survival of weaned lambs to 1 yr was affected by population density but not by maternal mass or previous reproductive success. In large mammals, manipulations of reproductive effort are problematic, but long-term monitoring of individual mass and reproductive success under varying conditions of resource availability can provide insights into the evolution of life histories.

Population dynamics of large herbivores: variable recruitment with constant adult survival.

Recent long-term studies of population ecology of large herbivorous mammals suggest that survival of prime-aged females varies little from year to year and across populations. Juvenile survival, on the other hand, varies considerably from year to year. The pattern of high and stable adult survival and variable juvenile survival is observed in contrasting environments, independently of the main proximal sources of mortality and regardless of whether mortality is stochastic or density-dependent. High yearly variability in juvenile survival may play a predominant role in population dynamics.