Andrés Pérez-Figueroa

Comparing three different methods to detect selective loci using dominant markers

We carried out a simulation study to compare the efficiency of three alternative programs (dfdist, detseld and bayescan) to detect loci under directional selection from genome‐wide scans using dominant markers. We also evaluated the efficiency of correcting for multiple testing those methods that use a classical probability approach. Under a wide range of scenarios, we conclude that bayescan appears to be more efficient than the other methods, detecting a usually high percentage of true selective loci as well as less than 1% of outliers (false positives) under a fully neutral model. In addition, the percentage of outliers detected by this software is always correlated with the true percentage of selective loci in the genome. Our results show, nevertheless, that false positives are common even with a combination of methods and multitest correction, suggesting that conclusions obtained from this approach should be taken with extreme caution.

Early detection of population declines: high power of genetic monitoring using effective population size estimators

Early detection of population declines is essential to prevent extinctions and to ensure sustainable harvest. We evaluated the performance of two Ne estimators to detect population declines: the two‐sample temporal method and a one‐sample method based on linkage disequilibrium (LD). We used simulated data representing a wide range of population sizes, sample sizes and number of loci. Both methods usually detect a population decline only one generation after it occurs if Ne drops to less than approximately 100, and 40 microsatellite loci and 50 individuals are sampled. However, the LD method often out performed the temporal method by allowing earlier detection of less severe population declines (Ne approximately 200). Power for early detection increased more rapidly with the number of individuals sampled than with the number of loci genotyped, primarily for the LD method. The number of samples available is therefore an important criterion when choosing between the LD and temporal methods. We provide guidelines regarding design of studies targeted at monitoring for population declines. We also report that 40 single nucleotide polymorphism (SNP) markers give slightly lower precision than 10 microsatellite markers. Our results suggest that conservation management and monitoring strategies can reliably use genetic based methods for early detection of population declines.

A simulation study on the performance of differentiation-based methods to detect selected loci using linked neutral markers.

We investigated the performance of two of the most popular differentiation‐based methods to detect loci under selection (dfdist/fdist and bayescan) in order to ascertain the average chromosome map distance between the detected outlier markers and the nearest loci under selection. We used a model of neutral markers genetically linked to selected loci (QTL) controlling a quantitative trait subject to divergent selection in two subpopulations connected by migration. The results are not particularly encouraging because for chromosome lengths above 0.5 morgan, at least 30% of outliers detected were positioned in chromosomes where QTL were absent, clearly denoting false positives. Outliers linked to QTL were on average closer to the nearest QTL than randomly chosen markers, but the methods showed a substantial uncertainty about the genetic association between markers and selected loci, as this association could be shown significantly only in a moderate number of replicates for most scenarios. At equal conditions, bayescan seemed to perform somewhat more efficiently than dfdist/fdist, with little difference between results for dominant and codominant markers.

Preserving Population Allele Frequencies in Ex Situ Conservation Programs

Optimization of contributions of parents to progeny by minimizing the average coancestry of the progeny is an effective strategy for maintaining genetic diversity in ex situ conservation programs, but its application on the basis of molecular markers has the negative collateral effect of homogenizing the allelic frequencies at each locus. Because one of the objectives of a conservation program is to preserve the genetic composition of the original endangered population, we devised a method in which markers are used to maintain the allele frequency distribution at each locus as closely as possible to that of the native population. Contributions of parents were obtained so as to minimize changes in allele frequency for a set of molecular markers in a population of reduced size. We used computer simulations, under a range of scenarios, to assess the effectiveness of the method in comparison with methods in which contributions of minimum coancestry are sought, either making use of molecular markers or genealogical information. Our simulations indicated that the proposed method effectively maintained the original distribution of allele frequencies, particularly under strong linkage, and maintained acceptable levels of genetic diversity in the population. Nevertheless, contributions of minimum coancestry determined from pedigree information but ignoring the genealogy previous to the conservation program, was the most effective method for maintaining allelic frequencies in realistic situations.

METAPOP—A software for the management and analysis of subdivided populations in conservation programs

We introduce a computer program for the dynamic and flexible management of conserved subdivided populations. Using molecular marker data or pedigree information, the software determines the optimal contributions (i.e., number of offspring) of each individual, the number of migrants, and the particular subpopulations involved in the exchange of individuals in order to maintain the largest level of gene diversity in the whole population with a desired control in the rate of inbreeding. Restrictions can be introduced for the total number of migrants, and the mating of particular pairs and their contribution. A full genetic diversity analysis of the population is carried out. The optimal contribution from each subpopulation to a pool of maximal gene diversity is also provided by the program.

The evolutionary forces maintaining a wild polymorphism of Littorina saxatilis: model selection by computer simulations

Two rocky shore ecotypes of Littorina saxatilis from north‐west Spain live at different shore levels and habitats and have developed an incomplete reproductive isolation through size assortative mating. The system is regarded as an example of sympatric ecological speciation. Several experiments have indicated that different evolutionary forces (migration, assortative mating and habitat‐dependent selection) play a role in maintaining the polymorphism. However, an assessment of the combined contributions of these forces supporting the observed pattern in the wild is absent. A model selection procedure using computer simulations was used to investigate the contribution of the different evolutionary forces towards the maintenance of the polymorphism. The agreement between alternative models and experimental estimates for a number of parameters was quantified by a least square method. The results of the analysis show that the fittest evolutionary model for the observed polymorphism is characterized by a high gene flow, intermediate‐high reproductive isolation between ecotypes, and a moderate to strong selection against the nonresident ecotypes on each shore level. In addition, a substantial number of additive loci contributing to the selected trait and a narrow hybrid definition with respect to the phenotype are scenarios that better explain the polymorphism, whereas the ecotype fitnesses at the mid‐shore, the level of phenotypic plasticity, and environmental effects are not key parameters.

Mutation-selection balance accounting for genetic variation for viability in Drosophila melanogaster as deduced from an inbreeding and artificial selection experiment.

We carried out an experiment of inbreeding and upward artificial selection for egg‐to‐adult viability in a recently captured population of Drosophila melanogaster, as well as computer simulations of the experimental design, in order to obtain information on the nature of genetic variation for this important fitness component. The inbreeding depression was linear with a rate of 0.70 ± 0.11% of the initial mean per 1% increase in inbreeding coefficient, and the realized heritability was 0.06 ± 0.07. We compared the empirical observations of inbreeding depression and selection response with computer simulations assuming a balance between the occurrence of partially recessive deleterious mutations and their elimination by selection. Our results suggest that a model assuming mutation‐selection balance with realistic mutational parameters can explain the genetic variation for viability in the natural population studied. Several mutational models are incompatible with some observations and can be discarded. Mutational models assuming a low rate of mutations of large average effect and highly recessive gene action, and others assuming a high rate of mutations of small average effect and close to additive gene action, are compatible with all the observations.

Allelic diversity for neutral markers retains a higher adaptive potential for quantitative traits than expected heterozygosity

The adaptive potential of a population depends on the amount of additive genetic variance for quantitative traits of evolutionary importance. This variance is a direct function of the expected frequency of heterozygotes for the loci which affect the trait (QTL). It has been argued, but not demonstrated experimentally, that long‐term response to selection is more dependent on QTL allelic diversity than on QTL heterozygosity. Conservation programmes, aimed at preserving this variation, usually rely on neutral markers rather than on quantitative traits for making decisions on management. Here, we address, both through simulation analyses and experimental studies with Drosophila melanogaster, the question of whether allelic diversity for neutral markers is a better indicator of a high adaptive potential than expected heterozygosity. In both experimental and simulation studies, we established synthetic populations for which either heterozygosity or allelic diversity was maximized using information from QTL (simulations) or unlinked neutral markers (simulations and experiment). The synthetic populations were selected for the quantitative trait to evaluate the evolutionary potential provided by the two optimization methods. Our results show that maximizing the number of alleles of a low number of markers implies higher responses to selection than maximizing their heterozygosity.

LACK OF NONADDITIVE GENETIC EFFECTS ON EARLY FECUNDITY IN DROSOPHILA MELANOGASTER

Abstract Fecundity is usually considered as a trait closely connected to fitness and is expected to exhibit substantial nonadditive genetic variation and inbreeding depression. However, two independent experiments, using populations of different geographical origin, indicate that early fecundity inDrosophila melanogaster behaves as a typical additive trait of low heritability. The first experiment involved artificial selection in inbred and non‐inbred lines, all of them started from a common base population previously maintained in the laboratory for about 35 generations. The realized heritability estimate was 0.151 ± 0.075 and the inbreeding depression was very small and nonsignificant (0.09 ± 0.09% of the non‐inbred mean per 1% increase in inbreeding coefficient). With inbreeding, the observed decrease in the within‐line additive genetic variance and the corresponding increase of the between‐line variance were very close to their expected values for pure additive gene action. This result is at odds with previous studies showing inbreeding depression and, therefore, directional dominance for the same trait and species. All experiments, however, used laboratory populations, and it is possible that the original genetic architecture of the trait in nature was subsequently altered by the joint action of random drift and adaptation to captivity. Thus, we carried out a second experiment, involving inbreeding without artificial selection in a population recently collected from the wild. In this case we obtained, again, a maximum‐likelihood heritability estimate of 0.210 ± 0.027 and very little nonsignificant inbreeding depression (0.06 ± 0.12%). The results suggest that, for fitness‐component traits, low levels of additive genetic variance are not necessarily associated with large inbreeding depression or high levels of nonadditive genetic variance.

The action of purifying selection, mutation and drift on fitness epistatic systems.

For different fitness mutational models, with epistasis introduced, we simulated the consequences of drift (D scenario) or mutation, selection, and drift (MSD scenario) in populations at the MSD balance subsequently subjected to bottlenecks of size N = 2, 10, 50 during 100 generations. No “conversion” of nonadditive into additive variance was observed, all components of the fitness genetic variance initially increasing with the inbreeding coefficient F and subsequently decreasing to zero (D) or to an equilibrium value (MSD). In the D scenario, epistasis had no appreciable effect on inbreeding depression and that on the temporal change of variance components was relevant only for high rates of strong epistatic mutation. In parallel, between-line differentiation in mean fitness accelerated with F and that in additive variance reached a maximum at F ∼ 0.6–0.7, both processes being intensified by strong epistasis. In the MSD scenario, however, the increase in additive variance was smaller, as it was used by selection to purge inbreeding depression (N ≥ 10), and selection prevented between-line differentiation. Epistasis, either synergistic or antagonistic (this leading to multiple adaptive peaks), had no appreciable effect on MSD results nor, therefore, on the evolutionary rate of fitness change.