Sexually-antagonistic effects in red deer

We will investigate the phenomenon of sexually-antagonistic selection as a force maintaining genetic variation in natural populations in a sexually-dimorphic species, the red deer. We will use a unique set of records available on the individual life-histories and pedigree of both sexes of deer collected over the last 34 years on the island of Rum, Scotland. Specifically, we will address the following questions:

1. What is the prevalence and the genetic basis of sexually-antagonistic effects in red deer?

2. Does selection favour relatively 'masculine' versus relatively 'feminine' phenotypes differently within either sex?

3. What is the impact of environmental variation on the genetic basis of sexually-antagonistic effects, and on the selection pressures generating them?

4. Is intrasexual variation in fitness and morphology in both males and females associated with individual variation in testosterone levels?

Evolutionary biologists are continually puzzled by the following problem: natural selection should remove genetic variation that affects the fitness of individuals, yet, when measured, there is often quite a lot of genetic variation for fitness. One
possible explanation for the persistence of genetic variation in a population is that, in those species which have two sexes, the genes (alleles) that make a successful male are different from those that make a successful female. These 'sexually-antagonistic' effects are likely to be especially important in a species experiencing extensive sexual selection, in which one sex (usually males) is bigger than females, and has developed weaponry such as antlers or horns or spectacular colouration, characteristics which enhance mating success. Sexually-antagonistic effects have been well explored using theoretical models, and there is empirical support for their existence from laboratory studies of fruit flies, but they have rarely been investigated in nature.
In this study we investigated sexually-antagonistic selection in a wild population of a sexually-dimorphic mammal, red deer. Doing so required construction of a multigenerational pedigree (or family tree) of individuals can be constructed, stretching for up to ten generations of deer. This pedigree revealed instances of inbreeding, and therefore allowed us to also investigate levels of inbreeding depression. We have also been investigating variation in sex hormone levels and the extent to which this may be associated with sexually antagonistic selection pressures.

Several hypotheses have been proposed to explain the maintenance of genetic variation in the face of the eroding effects of selection, of which one of the most prominent is the concept of trade-offs between different components of fitness, whereby high performance for one trait is associated with low performance for another, and vice versa; the net effect is that no single genotype is optimal, and genetic variation may persist in the population. One particular form in which such trade-offs may manifest themselves is between the sexes: the genes (alleles) that make a successful male may be different from those that make a successful female. We had initial evidence for this observation for the Rum red deer (Foerster et al. 2007), and the aim of the grant was to explore it further.
Investigating these issues requires quantitative genetic models based on pedigree information. The first stage of the project was therefore to determine an up-to-date pedigree with as comprehensive information about individual parentage as possible. To this end, we undertook a comparison of different parentage software programmes; this turned out to be an extensive (and important) exercise in its own right and generated a Molecular Ecology publication: our final pedigree was an amalgamation of relationships determined using two different software programmes (Walling et al. 2010).
Our analyses of multiple components of life history required complex multivariate models of the genetic variance-covariance (G) matrix, for up to eight traits when considering male- and female-specific values. Because of this high dimensionality, estimating the full G matrix for all traits was not possible for our data. We therefore used factor analysis to identify the factors (combinations of traits) with most genetic variation; this approach generated a tractable analysis and also indicated constraints in the form of no genetic variation for some combinations of traits. Most interestingly in relation to the original hypotheses, it indicated a potential trade-off between aspects of female fecundity on the one hand, and female longevity and male performance (both fecundity and longevity) on the other. Following referees’ comments on a manuscript submitted in 2011, we are currently revising this work for Evolution (Walling et al, in prep). At the same time, we also undertook a detailed analysis of female life-history traits, again with the aim of identifying evolutionary constraints, but also incorporating a novel combination of quantitative genetic analyses with methods for estimating selection via a demographic model. This work also indicated an important trade-off between female fecundity and longevity, to the extent that the overall rate of adaptation would be reduced to 60% of the value that it would have been had each trait been independent of all others (Morrissey et al. 2012). To date, our results therefore indicate less support for sexually-antagonistic variation than we anticipated, but still indicate the presence of evolutionary constraints via multivariate associations; we note that these analyses have also gone substantially further than any other work on a natural system in investigating genetic associations between multiple aspects of fitness.
This work also laid the foundation for several other analyses of selection and multivariate genetic architectture of the deer population. We investigated the role of genetic variation in determining the social dominance amongst individuals, demonstrating an important role both of the genotype of an individual in predicting whether or not it wins a contest, and of the genotype of its opponent (Wilson et al. 2011). We also investigated the genetic basis of variation in timing of key events in both males and females, finding substantial heritability of different phenological traits, but little in the way of significant cross-sex correlations, either positive or antagonistic (Clements et al. 2011). We analysed the timing of male antler growth in detail, finding large variation due to effects of age and of environmental conditions (phenotypic plasticity) in addition to the genetic variation, and associations between antler growth timing and male breeding success (Clements et al. 2010). Further quantitative genetic analyses have also revealed the importance of considering shared environmental effects when partitioning covariance in phenotypic traits between relatives (Stopher et al. 2012). Finally, the new pedigree also allowed an investigation of inbreeding and inbreeding depression, revealing that whilst the occurrence of inbreeding is low, its effects on fitness are substantial, for example reducing juvenile survival of calves born to father-daughter matings by 70% (Walling et al. 2011).
As part of the grant proposal, we had proposed an investigation of sex hormone variation, with the hypothesis that high levels of testosterone might be associated with higher breeding success in males but lower in females. These assays have taken longer to run than initially planned, but we now have data for 808 calf plasma levels, and are in the process of using these to test for sex-specific associations with different components of fitness (part of A. Pavitt’s PhD studentship). Analyses of adult testosterone levels will be based on fecal samples, and undertaken later this year in collaboration with Prof. E. Moestl (Univ. Vienna). This part of the project has therefore not been completed, but we hope that it may be finished within 12 months.