An empirical test of the estimation of historical effective population size using Drosophila melanogaster.

The availability of a large number of high-density markers (SNPs) allows the estimation of historical effective population size (Ne ) from linkage disequilibrium between loci. A recent refinement of methods to estimate historical Ne from the recent past has been shown to be rather accurate with simulation data. The method has also been applied to real data for numerous species. However, the simulation data cannot encompass all the complexities of real genomes, and the performance of any estimation method with real data is always uncertain, as the true demography of the populations is not known. Here, we carried out an experimental design with Drosophila melanogaster to test the method with real data following a known demographic history. We used a population maintained in the laboratory with a constant census size of about 2800 individuals and subjected the population to a drastic decline to a size of 100 individuals. After a few generations, the population was expanded back to the previous size and after a few further generations again expanded to twice the initial size. Estimates of historical Ne were obtained with the software GONE both for autosomal and X chromosomes from samples of 17 individuals sequenced for the whole genome. Estimates of the historical effective size were able to infer the patterns of changes that occurred in the populations showing generally good performance of the method. We discuss the limitations of the method and the application of the software carried out so far.

An empirical evaluation of the estimation of inbreeding depression from molecular markers under suboptimal conditions.

Inbreeding depression (ID), the reduction in fitness due to inbreeding, is typically measured by the regression of the phenotypic values of individuals for a particular trait on their corresponding inbreeding coefficients (F). While genealogical records can provide these coefficients, they may be unavailable or incomplete, making molecular markers a useful alternative. The power to detect ID and its accuracy depend on the variation of F values of individuals, the sample sizes available, and the accuracy in the estimation of individual fitness traits and F values. In this study, we used Drosophila melanogaster to evaluate the effectiveness of molecular markers in estimating ID under suboptimal conditions. We generated two sets of 100 pairs of unrelated individuals from a large panmictic population and mated them for two generations to produce non-inbred and unrelated individuals (F = 0) and inbred individuals (full-sib progeny; F = 0.25). Using these expected genealogical F values, we calculated inbreeding depression for two fitness-related traits, pupae productivity and competitive fitness. We then sequenced the males from 17 non-inbred pairs and 17 inbred pairs to obtain their genomic inbreeding coefficients and estimate ID for the two traits. The scenario assumed was rather restrictive in terms of estimation of ID because: (1) the individuals belonged to the same generation of a large panmictic population, leading to low variation in individual F coefficients; (2) the sample sizes were small; and (3) the traits measured depended on both males and females while only males were sequenced. Despite the challenging conditions of our study, we found that molecular markers provided estimates of ID that were comparable to those obtained from simple pedigree estimations with larger sample sizes. The results therefore suggest that genomic measures of inbreeding are useful to provide estimates of inbreeding depression even under very challenging scenarios.

Long-term exhaustion of the inbreeding load in Drosophila melanogaster.

Inbreeding depression, the decline in fitness of inbred individuals, is a ubiquitous phenomenon of great relevance in evolutionary biology and in the fields of animal and plant breeding and conservation. Inbreeding depression is due to the expression of recessive deleterious alleles that are concealed in heterozygous state in noninbred individuals, the so-called inbreeding load. Genetic purging reduces inbreeding depression by removing these alleles when expressed in homozygosis due to inbreeding. It is generally thought that fast inbreeding (such as that generated by full-sib mating lines) removes only highly deleterious recessive alleles, while slow inbreeding can also remove mildly deleterious ones. However, a question remains regarding which proportion of the inbreeding load can be removed by purging under slow inbreeding in moderately large populations. We report results of two long-term slow inbreeding Drosophila experiments (125-234 generations), each using a large population and a number of derived lines with effective sizes about 1000 and 50, respectively. The inbreeding load was virtually exhausted after more than one hundred generations in large populations and between a few tens and over one hundred generations in the lines. This result is not expected from genetic drift alone, and is in agreement with the theoretical purging predictions. Computer simulations suggest that these results are consistent with a model of relatively few deleterious mutations of large homozygous effects and partially recessive gene action.

Can parallel ecological speciation be detected with phylogenetic analyses?

Distinguishing parallel divergence from vicariance scenarios is crucial to establish the determinism of natural selection in the formation of new species. It has been proposed that phylogenetic methods can be used to disentangle a single origin in allopatry and multiple origins in sympatry for ecological speciation. However, a key issue is to what extent introgression in a patchy environment may complicate the distinction between both origins through the analysis of variation at neutral markers. While divergence at environmentally-based selected loci retains the initial correlation with ecological variables, such association may be lost at neutral loci unlinked to any selected locus. Thus, neutral divergence might reflect in the long-term the molecular fingerprint of isolation by distance regardless of the model of speciation considered, and a question arises as to whether phylogenetic analyses of neutral markers are able or not to retrieve the signals acquired in the ancestral populations. Here, we use computer simulations to show that the detection of the original signal using a phylogenetic method strongly depends on the migration rates among populations. Recombination accelerates the loss of the initial phylogenetic signal, but this effect is rather small compared with the effect of migration, and only substantial when recombination is very large. For model species with reduced gene flow between distant populations and between populations adapted to different habitats, the phylogenetic approach is able to distinguish a single origin in allopatry from multiple origins in sympatry.