Craig A. Walling

An ecologist's guide to the animal model.

1. Efforts to understand the links between evolutionary and ecological dynamics hinge on our ability to measure and understand how genes influence phenotypes, fitness and population dynamics. Quantitative genetics provides a range of theoretical and empirical tools with which to achieve this when the relatedness between individuals within a population is known. 2. A number of recent studies have used a type of mixed-effects model, known as the animal model, to estimate the genetic component of phenotypic variation using data collected in the field. Here, we provide a practical guide for ecologists interested in exploring the potential to apply this quantitative genetic method in their research. 3. We begin by outlining, in simple terms, key concepts in quantitative genetics and how an animal model estimates relevant quantitative genetic parameters, such as heritabilities or genetic correlations. 4. We then provide three detailed example tutorials, for implementation in a variety of software packages, for some basic applications of the animal model. We discuss several important statistical issues relating to best practice when fitting different kinds of mixed models. 5. We conclude by briefly summarizing more complex applications of the animal model, and by highlighting key pitfalls and dangers for the researcher wanting to begin using quantitative genetic tools to address ecological and evolutionary questions.

Natural and Sexual Selection in a Wild Insect Population

Insects in the Wild Insects are of fundamental importance to terrestrial ecosystems and provide laboratory model systems for the study of physiology and genetics. Studies examining how natural and sexual selection operate to drive evolution in wild populations have often neglected invertebrates, resulting in a chasm between our understandings of how things work in the lab versus the natural environment. Rodríguez-Muñoz et al. (p. 1269; see the Perspective by Zuk) bridge this gap by comprehensively monitoring the life histories, behavior, and reproductive success of an entire population of field crickets. Adding genetic data allowed evaluation of how behavior impacts reproductive success and confirmed that male reproductive success varies more than that of females. Monitoring reproduction in wild crickets confirms that male success varies more than female success. The understanding of natural and sexual selection requires both field and laboratory studies to exploit the advantages and avoid the disadvantages of each approach. However, studies have tended to be polarized among the types of organisms studied, with vertebrates studied in the field and invertebrates in the lab. We used video monitoring combined with DNA profiling of all of the members of a wild population of field crickets across two generations to capture the factors predicting the reproductive success of males and females. The factors that predict a male’s success in gaining mates differ from those that predict how many offspring he has. We confirm the fundamental prediction that males vary more in their reproductive success than females, and we find that females as well as males leave more offspring when they mate with more partners.

Comparing parentage inference software: reanalysis of a red deer pedigree.

Knowledge of the parentage of individuals is required to address a variety of questions concerning the evolutionary dynamics of wild populations. A major advance in parentage inference in natural populations has been the use of molecular markers and the development of statistical methods to analyse these data. Cervus, one of the most widely used parentage inference programs, uses molecular data to determine parent–offspring relationships. However, Cervus does not make use of all available information: additional phenotypic information may exist predicting parent–offspring relationships, and additional genetic information may be exploited by simultaneously considering multiple types of relationships rather than just pairwise or just parent–offspring relationships. Here we reanalyse data from a wild red deer population using two programs capable of using this additional information, MasterBayes and COLONY2, and quantify the impact of these alternative approaches by comparison with a ‘known pedigree’ estimated using a larger suite of microsatellite makers for a subset of the population. The use of phenotypic information and multiple relationships increased the number of correct assignments. We highlight the differences between programs, particularly the use of population‐ rather than individual‐level statistical confidence in Cervus. We conclude that the use of additional information allows MasterBayes and COLONY2 to assign more correct paternities, whereas their use of individual‐ rather than population‐level confidence generates fewer erroneous assignments. We suggest that maximal information may be gained by combining outputs from different programs. Higher accuracy and completeness of pedigree information will improve parameters estimated from pedigree information in studies of natural populations.

Indirect genetics effects and evolutionary constraint: an analysis of social dominance in red deer, Cervus elaphus.

By determining access to limited resources, social dominance is often an important determinant of fitness. Thus, if heritable, standard theory predicts mean dominance should evolve. However, dominance is usually inferred from the tendency to win contests, and given one winner and one loser in any dyadic contest, the mean proportion won will always equal 0.5. Here, we argue that the apparent conflict between quantitative genetic theory and common sense is resolved by recognition of indirect genetic effects (IGEs). We estimate selection on, and genetic (co)variance structures for, social dominance, in a wild population of red deer Cervus elaphus, on the Scottish island of Rum. While dominance is heritable and positively correlated with lifetime fitness, contest outcomes depend as much on the genes carried by an opponent as on the genotype of a focal individual. We show how this dependency imposes an absolute evolutionary constraint on the phenotypic mean, thus reconciling theoretical predictions with common sense. More generally, we argue that IGEs likely provide a widespread but poorly recognized source of evolutionary constraint for traits influenced by competition.

Do female association preferences predict the likelihood of reproduction

Sexual selection acting on male traits through female mate choice is commonly inferred from female association preferences in dichotomous mate choice experiments. However, there are surprisingly few empirical demonstrations that such association preferences predict the likelihood of females reproducing with a particular male. This information is essential to confirm association preferences as good predictors of mate choice. We used green swordtails (Xiphophorus helleri) to test whether association preferences predict the likelihood of a female reproducing with a male. Females were tested for a preference for long- or short-sworded males in a standard dichotomous choice experiment and then allowed free access to either their preferred or non-preferred male. If females subsequently failed to produce fry, they were provided a second unfamiliar male with similar sword length to the first male. Females were more likely to reproduce with preferred than non-preferred males, but for those that reproduced, neither the status (preferred/non-preferred) nor the sword length (long/short) of the male had an effect on brood size or relative investment in growth by the female. There was no overall preference based on sword length in this study, but male sword length did affect likelihood of reproduction, with females more likely to reproduce with long- than short-sworded males (independent of preference for such males in earlier choice tests). These results suggest that female association preferences are good indicators of female mate choice but that ornament characteristics of the male are also important.

The quantitative genetics of sex differences in parenting

Sex differences in parenting are common in species where both males and females provide care. Although there is a considerable body of game and optimality theory for why the sexes should differ in parental care, genetics can also play a role, and no study has examined how genetic influences might influence differences in parenting. We investigated the extent that genetic variation influenced differences in parenting, whether the evolution of differences could be constrained by shared genetic influences, and how sex-specific patterns of genetic variation underlying parental care might dictate which behaviors are free to evolve in the burying beetle Nicrophorus vespilloides. Females provided more direct care than males but did not differ in levels of indirect care or the number of offspring they were willing to rear. We found low to moderate levels of heritability and evolvability for all 3 parenting traits in both sexes. Intralocus sexual conflict was indicated by moderately strong intersex genetic correlations, but these were not so strong as to represent an absolute constraint to the evolution of sexual dimorphism in care behavior. Instead, the pattern of genetic correlations between parental behaviors showed sex-specific tradeoffs. Thus, differences in the genetic correlations between parental traits within a sex create sex-specific lines of least evolutionary resistance, which in turn produce the specific patterns of sex differences in parental care. Our results therefore suggest a mechanism for the evolution of behavioral specialization during biparental care if uniparental and biparental care behaviors share the same genetic influences.

Inbreeding and inbreeding depression of early life traits in a cooperative mammal.

Mating between relatives often results in negative fitness consequences or inbreeding depression. However, the expression of inbreeding in populations of wild cooperative mammals and the effects of environmental, maternal and social factors on inbreeding depression in these systems are currently not well understood. This study uses pedigree‐based inbreeding coefficients from a long‐term study of meerkats (Suricata suricatta) in South Africa to reveal that 44% of the population have detectably non‐zero (F > 0) inbreeding coefficients. 15% of these inbred individuals were the result of moderate inbreeding (F ≥ 0.125), although such inbreeding events almost solely occurred when mating individuals had no prior experience of each other. Inbreeding depression was evident for a range of traits: pup mass at emergence from the natal burrow, hind‐foot length, growth until independence and juvenile survival. However, we found no evidence of significant inbreeding depression for skull and forearm length or for pup survival. This research provides a rare investigation into inbreeding in a cooperative mammal, revealing high levels of inbreeding, considerable negative consequences and complex interactions with the social environment.

Inbreeding depression in red deer calves

BackgroundUnderstanding the fitness consequences of inbreeding is of major importance for evolutionary and conservation biology. However, there are few studies using pedigree-based estimates of inbreeding or investigating the influence of environment and age variation on inbreeding depression in natural populations. Here we investigated the consequences of variation in inbreeding coefficient for three juvenile traits, birth date, birth weight and first year survival, in a wild population of red deer, considering both calf and mothers inbreeding coefficient. We also tested whether inbreeding depression varied with environmental conditions and maternal age.ResultsWe detected non-zero inbreeding coefficients for 22% of individuals with both parents and at least one grandparent known (increasing to 42% if the dataset was restricted to those with four known grandparents). Inbreeding depression was evident for birth weight and first year survival but not for birth date: the first year survival of offspring with an inbreeding coefficient of 0.25 was reduced by 77% compared to offspring with an inbreeding coefficient of zero. However, it was independent of measures of environmental variation and maternal age. The effect of inbreeding on birth weight appeared to be driven by highly inbred individuals (F = 0.25). On the other hand first year survival showed strong inbreeding depression that was not solely driven by individuals with the highest inbreeding coefficients, corresponding to an estimate of 4.35 lethal equivalents.ConclusionsThese results represent a rare demonstration of inbreeding depression using pedigree-based estimates in a wild mammal population and highlight the potential strength of effects on key components of fitness.

The evolution of repeated mating in the burying beetle, Nicrophorus vespilloides

Abstract Animals of many species accept or solicit recurring copulations with the same partner; i.e., show repeated mating. An evolutionary explanation for this excess requires that the advantages of repeated mating outweigh the costs, and that behavioral components of repeated mating are genetically influenced. There can be benefits of repeated mating for males when there is competition for fertilizations or where the opportunities for inseminating additional mates are rare or unpredictable. The benefits to females are less obvious and, depending on underlying genetic architecture, repeated mating may have evolved as a correlated response to selection on males. We investigated the evolution of repeated mating with the same partner in the burying beetle Nicrophorus vespilloides by estimating the direct and indirect fitness benefits for females and the genetics of behavior underlying repeated mating. The number of times a female mated had minimal direct and no indirect fitness benefits for females. The behavioral components of repeated mating (mating frequency and mating speed) were moderately negatively genetically correlated in males and uncorrelated in females. However, mating frequency and mating speed were strongly positively genetically correlated between males and females. Our data suggest that repeated mating by female N. vespilloides may have evolved as a correlated response to selection on male behavior rather than in response to benefits of repeated mating for females.

Genetic Analysis of Life-History Constraint and Evolution in a Wild Ungulate Population

Trade-offs among life-history traits are central to evolutionary theory. In quantitative genetic terms, trade-offs may be manifested as negative genetic covariances relative to the direction of selection on phenotypic traits. Although the expression and selection of ecologically important phenotypic variation are fundamentally multivariate phenomena, the in situ quantification of genetic covariances is challenging. Even for life-history traits, where well-developed theory exists with which to relate phenotypic variation to fitness variation, little evidence exists from in situ studies that negative genetic covariances are an important aspect of the genetic architecture of life-history traits. In fact, the majority of reported estimates of genetic covariances among life-history traits are positive. Here we apply theory of the genetics and selection of life histories in organisms with complex life cycles to provide a framework for quantifying the contribution of multivariate genetically based relationships among traits to evolutionary constraint. We use a Bayesian framework to link pedigree-based inference of the genetic basis of variation in life-history traits to evolutionary demography theory regarding how life histories are selected. Our results suggest that genetic covariances may be acting to constrain the evolution of female life-history traits in a wild population of red deer Cervus elaphus: genetic covariances are estimated to reduce the rate of adaptation by about 40%, relative to predicted evolutionary change in the absence of genetic covariances. Furthermore, multivariate phenotypic (rather than genetic) relationships among female life-history traits do not reveal this constraint.