locus selection
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The position of some taxa on the Tree of Life remains controversial despite the increase in genomic data used to infer phylogenies. While analyzing large datasets alleviates stochastic errors, it does not prevent systematic errors in inference, caused by both biological (e.g., incomplete lineage sorting, hybridization) and methodological (e.g., incorrect modeling, erroneous orthology assessments) factors. In our study, we systematically investigated factors that could result in these controversies, using the treeshrew (Scandentia, Mammalia) as a study case. Recent studies have narrowed the phylogenetic position of treeshrews to three competing hypotheses: sister to primates and flying lemurs (Primatomorpha), sister to rodents and lagomorphs (Glires), or sister to a clade comprising all of these. We sampled 50 mammal species including three treeshrews, a selection of taxa from the potential sister groups, and outgroups. Using a large diverse set of loci, we assessed support for the alternative phylogenetic position of treeshrews. A plurality of loci support treeshrews as sister to rodents and lagomorphs; however, only a few loci exhibit strong support for any hypothesis. Surprisingly, we found that a subset of loci that strongly support the monophyly of Primates, support treeshrews as sister to primates and flying lemurs. The overall small magnitude of differences in phylogenetic signal among the alternative hypotheses suggests that these three groups diversified nearly simultaneously. However, with our large dataset and approach to examining support, we provide evidence for the hypothesis of treeshrews as sister to rodents and lagomorphs, while demonstrating why support for alternate hypotheses has been seen in prior work. We also suggest that locus selection can unwittingly bias results.

AbstractThe coupled Wright–Fisher diffusion is a multi-dimensional Wright–Fisher diffusion for multi-locus and multi-allelic genetic frequencies, expressed as the strong solution to a system of stochastic differential equations that are coupled in the drift, where the pairwise interaction among loci is modelled by an inter-locus selection. In this paper, an ancestral process, which is dual to the coupled Wright–Fisher diffusion, is derived. The dual process corresponds to the block counting process of coupled ancestral selection graphs, one for each locus. Jumps of the dual process arise from coalescence, mutation, single-branching, which occur at one locus at the time, and double-branching, which occur simultaneously at two loci. The coalescence and mutation rates have the typical structure of the transition rates of the Kingman coalescent process. The single-branching rate not only contains the one-locus selection parameters in a form that generalises the rates of an ancestral selection graph, but it also contains the two-locus selection parameters to include the effect of the pairwise interaction on the single loci. The double-branching rate reflects the particular structure of pairwise selection interactions of the coupled Wright–Fisher diffusion. Moreover, in the special case of two loci, two alleles, with selection and parent independent mutation, the stationary density for the coupled Wright–Fisher diffusion and the transition rates of the dual process are obtained in an explicit form.

The cumulative reproductive cost of multi-locus selection has been considered to be a potentially limiting factor on the rate of adaptive evolution. In this paper, we show that Haldane’s arguments for the accumulation of reproductive costs over multiple loci are valid only for a clonally reproducing population of asexual genotypes. We show that a sexually reproducing population avoids this accumulation of costs. Thus, sex removes a perceived reproductive constraint on the rate of adaptive evolution. The significance of our results is twofold. First, the results demonstrate that adaptation based on multiple genes—such as selection acting on the standing genetic variation—does not entail a huge reproductive cost as suggested by Haldane, provided of course that the population is reproducing sexually. Second, this reduction in the cost of natural selection provides a simple biological explanation for the advantage of sex. Specifically, Haldane’s calculations illustrate the evolutionary disadvantage of asexuality; sexual reproduction frees the population from this disadvantage.

AbstractThe cumulative reproductive cost of multi-locus selection has been seen as a potentially limiting factor on the rate of adaptive evolution. In this paper, we show that Haldane’s arguments for the accumulation of reproductive costs over multiple loci are valid only for a clonally reproducing population of asexual genotypes. We show that a sexually reproducing population avoids this accumulation of costs. Thus, sex removes a perceived reproductive constraint on the rate of adaptive evolution. The significance of our results is twofold. First, the results demonstrate that adaptation based on multiple genes – such as selection acting on the standing genetic variation - does not entail a huge reproductive cost as suggested by Haldane, provided of course that the population is reproducing sexually. Secondly, this reduction in the cost of natural selection provides a simple biological explanation for the advantage of sex. Specifically, Haldane’s calculations illustrate the evolutionary disadvantage of asexuality; sexual reproduction frees the population from this disadvantage.

This chapter examines models of one- and two-locus selection in the absence of drift and mutation. Expressions for the per-generation rate of allele-frequency change and the expected time for a specified amount of change are developed for single-locus models, and their equilibrium structure is examined for those settings where selection retains more than one allele. The presence of selection-generated linkage disequilibrium greatly complicates the extension of single-locus results to two loci, and the chapter examines some of the resulting complications. Finally, it examines the nature of selection on a locus that underlies a trait under selection, and then uses this to develop the breeder's equation for the single-generation response in a trait under selection. One important result is that the loci for a trait under stabilizing selection experience fitness underdominance, and thus trait selection removes, rather than retains, genetic variation.

ABSTRACTHigh-throughput sequencing has fundamentally changed how molecular phylogenetic datasets are assembled, and phylogenomic datasets commonly contain 50-100-fold more loci than those generated using traditional Sanger-based approaches. Here, we demonstrate a new approach for building phylogenomic datasets using single tube, highly multiplexed amplicon sequencing, which we name HiMAP (Highly Multiplexed Amplicon-based Phylogenomics), and present bioinformatic pipelines for locus selection based on genomic and transcriptomic data resources and post-sequencing consensus calling and alignment. This method is inexpensive and amenable to sequencing a large number (hundreds) of taxa simultaneously, requires minimal hands-on time at the bench (<1/2 day), and data analysis can be accomplished without the need for read mapping or assembly. We demonstrate this approach by sequencing 878 amplicons in single reactions for 82 species of tephritid fruit flies across seven genera (384 individuals), including some of the most economically-important agricultural insect pests. The resulting dataset (>150,000 bp concatenated alignment) contained >40,000 phylogenetically informative characters, and although some discordance was observed between analyses, it provided unparalleled resolution of many phylogenetic relationships in this group. Most notably, we found high support for the generic status ofZeugodacusand the sister relationship betweenDacusandZeugodacus. We discuss HiMAP, with regard to its molecular and bioinformatic strengths, and the insight the resulting dataset provides into relationships of this diverse insect group.

AbstractThe advent of next-generation sequencing allows researchers to use large-scale datasets for species delimitation analyses, yet one can envision an inflection point where the added accuracy of including more loci does not offset the increased computational burden. One alternative to including all loci could be to prioritize the analysis of loci for which there is an expectation of high informativeness, such as those with higher numbers of parsimony-informative sites. Here, we explore the issue of species delimitation and locus selection with species from two anuran genera: Melanophryniscus (Bufonidae) and Brachycephalus (Brachycephalidae). Montane species in these genera have been isolated in sky islands across the southern Brazilian Atlantic Forest, which led to the formation of a number of microendemic species. To delimit species, we obtained genetic data using target enrichment of ultraconserved elements from 32 populations (13 for Melanophryniscus and 19 for Brachycephalus), and we were able to create datasets that included over 800 loci with no missing data. We ranked loci according to their corresponding number of parsimony-informative sites, and we performed species delimitation analyses using BPP in each genus based on the top 10, 20, 40, 80, 160, 320, and 640 loci. We also conducted several additional analyses using 10 randomly sampled datasets containing the same numbers of loci to discriminate the relative contribution of increasing the number of loci from prioritizing those with higher informativeness. We identified three types of node: nodes with either consistently high or low support regardless of the number of loci or their informativeness, and nodes that were initially poorly supported, but their support became stronger with more data. Adding more loci had a stronger impact on model support than prioritizing loci for their informativeness, but this effect was less apparent in datasets with more than 160 loci. When viewed across all sensitivity analyses, our results suggest that the current species richness in both genera might have been underestimated. In addition, our results provide useful guidelines to the use of different sampling strategies to carry out species delimitation with phylogenomic datasets.

Abstract We surveyed sequence variation and divergence for the entire 5972-bp transcriptional unit of the white gene in 15 lines of Drosophila melanogaster and one line of D. simulans. We found a very high degree of haplotypic structuring for the polymorphisms in the 3′ half of the gene, as opposed to the polymorphisms in the 5′ half. To determine the evolutionary mechanisms responsible for this pattern, we sequenced a 1612-bp segment of the white gene from an additional 33 lines of D. melanogaster from a European and a North American population. This 1612-bp segment encompasses an 834bp region of the white gene in which the polymorphisms form high frequency haplotypes that cannot be explained by a neutral equilibrium model of molecular evolution. The small number of recombinants in the 834bp region suggests epistatic selection as the cause of the haplotypic structuring, while an investigation of nucleotide diversity supports a directional selection hypothesis. A multi-locus selection model that combines features from both-hypotheses and takes the recent history of D. melanogaster into account may be the best explanation for these data.