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

What Have Long-Term Field Studies Taught Us About Population Dynamics?

Long-term studies have been crucial to the advancement of population biology, especially our understanding of population dynamics. We argue that this progress arises from three key characteristics of long-term research. First, long-term data are necessary to observe the heterogeneity that drives most population processes. Second, long-term studies often inherently lead to novel insights. Finally, long-term field studies can serve as model systems for population biology, allowing for theory and methods to be tested under well-characterized conditions. We illustrate these ideas in three long-term field systems that have made outsized contributions to our understanding of population ecology, evolution, and conservation biology. We then highlight three emerging areas to which long-term field studies are well positioned to contribute in the future: ecological forecasting, genomics, and macrosystems ecology. Overcoming the obstacles associated with maintaining long-term studies requires continued emphasis on recognizing the benefits of such studies to ensure that long-term research continues to have a substantial impact on elucidating population biology

Direct and indirect causal effects of heterozygosity on fitness-related traits in Alpine ibex

Heterozygosity–fitness correlations (HFCs) are a useful tool to investigate the effects of inbreeding in wild populations, but are not informative in distinguishing between direct and indirect effects of heterozygosity on fitness-related traits. We tested HFCs in male Alpine ibex (Capra ibex) in a free-ranging population (which suffered a severe bottleneck at the end of the eighteenth century) and used confirmatory path analysis to disentangle the causal relationships between heterozygosity and fitness-related traits. We tested HFCs in 149 male individuals born between 1985 and 2009. We found that standardized multi-locus heterozygosity (MLH), calculated from 37 microsatellite loci, was related to body mass and horn growth, which are known to be important fitness-related traits, and to faecal egg counts (FECs) of nematode eggs, a proxy of parasite resistance. Then, using confirmatory path analysis, we were able to show that the effect of MLH on horn growth was not direct but mediated by body mass and FEC. HFCs do not necessarily imply direct genetic effects on fitness-related traits, which instead can be mediated by other traits in complex and unexpected ways

Transmission Heterogeneity and Control Strategies for Infectious Disease Emergence

The control of emergence and spread of infectious diseases depends critically on the details of the genetic makeup of pathogens and hosts, their immunological, behavioral and ecological traits, and the pattern of temporal and spatial contacts among the age/stage-classes of susceptible and infectious host individuals.We show that failing to acknowledge the existence of heterogeneities in the transmission rate among age/stage-classes can make traditional eradication and control strategies ineffective, and in some cases, policies aimed at controlling pathogen emergence can even increase disease incidence in the host. When control strategies target for reduction in numbers those subsets of the population that effectively limit the production of new susceptible individuals, then control can produce a flush of new susceptibles entering the population. The availability of a new cohort of susceptibles may actually increase disease incidence. We illustrate these general points using Classical Swine Fever as a reference disease.Negative effects of culling are robust to alternative formulations of epidemiological processes and underline the importance of better assessing transmission structure in the design of wildlife disease control strategies

Postcopulatory sexual selection

The female reproductive tract is where competition between the sperm of different males takes place, aided and abetted by the female herself. Intense postcopulatory sexual selection fosters inter-sexual conflict and drives rapid evolutionary change to generate a startling diversity of morphological, behavioural and physiological adaptations. We identify three main issues that should be resolved to advance our understanding of postcopulatory sexual selection. We need to determine the genetic basis of different male fertility traits and female traits that mediate sperm selection; identify the genes or genomic regions that control these traits; and establish the coevolutionary trajectory of sexes

The genetic mating system of a sea spider with male-biased sexual size dimorphism: evidence for paternity skew despite random mating success

Male-biased size dimorphism is usually expected to evolve in taxa with intense male–male competition for mates, and it is hence associated with high variances in male mating success. Most species of pycnogonid sea spiders exhibit female-biased size dimorphism, and are notable among arthropods for having exclusive male parental care of embryos. Relatively little, however, is known about their natural history, breeding ecology, and mating systems. Here we first show that Ammothella biunguiculata, a small intertidal sea spider, exhibits male-biased size dimorphism. Moreover, we combine genetic parentage analysis with quantitative measures of sexual selection to show that male body size does not appear to be under directional selection. Simulations of random mating revealed that mate acquisition in this species is largely driven by chance factors, although actual paternity success is likely non-randomly distributed. Finally, the opportunity for sexual selection (Is), an indirect metric for the potential strength of sexual selection, in A. biunguiculata males was less than half of that estimated in a sea spider with female-biased size dimorphism, suggesting the direction of size dimorphism may not be a reliable predictor of the intensity of sexual selection in this group. We highlight the suitability of pycnogonids as model systems for addressing questions relating parental investment and sexual selection, as well as the current lack of basic information on their natural history and breeding ecology

Does Genetic Diversity Predict Health in Humans?

Genetic diversity, especially at genes important for immune functioning within the Major Histocompatibility Complex (MHC), has been associated with fitness-related traits, including disease resistance, in many species. Recently, genetic diversity has been associated with mate preferences in humans. Here we asked whether these preferences are adaptive in terms of obtaining healthier mates. We investigated whether genetic diversity (heterozygosity and standardized mean d2) at MHC and nonMHC microsatellite loci, predicted health in 153 individuals. Individuals with greater allelic diversity (d2) at nonMHC loci and at one MHC locus, linked to HLA-DRB1, reported fewer symptoms over a four-month period than individuals with lower d2. In contrast, there were no associations between MHC or nonMHC heterozygosity and health. NonMHC-d2 has previously been found to predict male preferences for female faces. Thus, the current findings suggest that nonMHC diversity may play a role in both natural and sexual selection acting on human populations

Developmental Stability Covaries with Genome-Wide and Single-Locus Heterozygosity in House Sparrows

Fluctuating asymmetry (FA), a measure of developmental instability, has been hypothesized to increase with genetic stress. Despite numerous studies providing empirical evidence for associations between FA and genome-wide properties such as multi-locus heterozygosity, support for single-locus effects remains scant. Here we test if, and to what extent, FA co-varies with single- and multilocus markers of genetic diversity in house sparrow (Passer domesticus) populations along an urban gradient. In line with theoretical expectations, FA was inversely correlated with genetic diversity estimated at genome level. However, this relationship was largely driven by variation at a single key locus. Contrary to our expectations, relationships between FA and genetic diversity were not stronger in individuals from urban populations that experience higher nutritional stress. We conclude that loss of genetic diversity adversely affects developmental stability in P. domesticus, and more generally, that the molecular basis of developmental stability may involve complex interactions between local and genome-wide effects. Further study on the relative effects of single-locus and genome-wide effects on the developmental stability of populations with different genetic properties is therefore needed

Estimating Heritabilities and Genetic Correlations: Comparing the ‘Animal Model’ with Parent-Offspring Regression Using Data from a Natural Population

Quantitative genetic parameters are nowadays more frequently estimated with restricted maximum likelihood using the ‘animal model’ than with traditional methods such as parent-offspring regressions. These methods have however rarely been evaluated using equivalent data sets. We compare heritabilities and genetic correlations from animal model and parent-offspring analyses, respectively, using data on eight morphological traits in the great reed warbler (Acrocephalus arundinaceus). Animal models were run using either mean trait values or individual repeated measurements to be able to separate between effects of including more extended pedigree information and effects of replicated sampling from the same individuals. We show that the inclusion of more pedigree information by the use of mean traits animal models had limited effect on the standard error and magnitude of heritabilities. In contrast, the use of repeated measures animal model generally had a positive effect on the sampling accuracy and resulted in lower heritabilities; the latter due to lower additive variance and higher phenotypic variance. For most trait combinations, both animal model methods gave genetic correlations that were lower than the parent-offspring estimates, whereas the standard errors were lower only for the mean traits animal model. We conclude that differences in heritabilities between the animal model and parent-offspring regressions were mostly due to the inclusion of individual replicates to the animal model rather than the inclusion of more extended pedigree information. Genetic correlations were, on the other hand, primarily affected by the inclusion of more pedigree information. This study is to our knowledge the most comprehensive empirical evaluation of the performance of the animal model in relation to parent-offspring regressions in a wild population. Our conclusions should be valuable for reconciliation of data obtained in earlier studies as well as for future meta-analyses utilizing estimates from both traditional methods and the animal model