Primate phylogenomics uncovers multiple rapid radiations and ancient interspecific introgression.

Our understanding of the evolutionary history of primates is undergoing continual revision due to ongoing genome sequencing efforts. Bolstered by growing fossil evidence, these data have led to increased acceptance of once controversial hypotheses regarding phylogenetic relationships, hybridization and introgression, and the biogeographical history of primate groups. Among these findings is a pattern of recent introgression between species within all major primate groups examined to date, though little is known about introgression deeper in time. To address this and other phylogenetic questions, here, we present new reference genome assemblies for 3 Old World monkey (OWM) species: Colobus angolensis ssp. palliatus (the black and white colobus), Macaca nemestrina (southern pig-tailed macaque), and Mandrillus leucophaeus (the drill). We combine these data with 23 additional primate genomes to estimate both the species tree and individual gene trees using thousands of loci. While our species tree is largely consistent with previous phylogenetic hypotheses, the gene trees reveal high levels of genealogical discordance associated with multiple primate radiations. We use strongly asymmetric patterns of gene tree discordance around specific branches to identify multiple instances of introgression between ancestral primate lineages. In addition, we exploit recent fossil evidence to perform fossil-calibrated molecular dating analyses across the tree. Taken together, our genome-wide data help to resolve multiple contentious sets of relationships among primates, while also providing insight into the biological processes and technical artifacts that led to the disagreements in the first place.

Males optimally balance selfish and kin-selected strategies of sexual competition in the guppy.

Resolving the strategies by which organisms compete for limited resources is key to understanding behavioural and social evolution. When competing for matings, males in many species allocate mating effort preferentially towards higher-quality females. How males balance this against avoiding competition with rival males, who should also prefer high-quality females, is poorly understood. Kin selection theory further complicates these dynamics: males should avoid competition with close relatives especially because of added, indirect fitness costs. However, whether between-male relatedness modulates the intensity of intrasexual competition is equivocal. Here, we develop and test an analytical model describing how males should optimally allocate their mating efforts in response to information about differences in female quality, competitor presence/absence and competitor relatedness. Using freely interacting groups of Trinidadian guppies (Poecilia reticulata), we show concordance between observed and predicted mating effort allocation across all combinations of these factors. Thus, male mating effort is sensitive to variation in female quality, competitor presence and competitor relatedness, which is consistent with a kin-selected strategy of male-male competition. The fit of our model's predictions demonstrates that males integrate assessments of female quality and competitive context in a quantitatively meaningful way, implicating a competitive strategy that has been fine-tuned to maximize inclusive fitness gains.

Mutation Accumulation in an Asexual Relative of Arabidopsis.

Asexual populations experience weaker responses to natural selection, which causes deleterious mutations to accumulate over time. Additionally, stochastic loss of individuals free of deleterious mutations can lead to an irreversible increase in mutational load in asexuals (the "click" in Muller's Ratchet). Here we report on the genomic divergence and distribution of mutations across eight sympatric pairs of sexual and apomictic (asexual) Boechera (Brassicaceae) genotypes. We show that apomicts harbor a greater number of derived mutations than sympatric sexual genotypes. Furthermore, in phylogenetically constrained sites that are subject to contemporary purifying selection, the ancestral, conserved allele is more likely to be retained in sexuals than apomicts. These results indicate that apomictic lineages accumulate mutations at otherwise conserved sites more often than sexuals, and support the conclusion that deleterious mutation accumulation can be a powerful force in the evolution of asexual higher plants.

Hybrid origins and the earliest stages of diploidization in the highly successful recent polyploid Capsella bursa-pastoris.

Whole-genome duplication (WGD) events have occurred repeatedly during flowering plant evolution, and there is growing evidence for predictable patterns of gene retention and loss following polyploidization. Despite these important insights, the rate and processes governing the earliest stages of diploidization remain poorly understood, and the relative importance of genetic drift, positive selection, and relaxed purifying selection in the process of gene degeneration and loss is unclear. Here, we conduct whole-genome resequencing in Capsella bursa-pastoris, a recently formed tetraploid with one of the most widespread species distributions of any angiosperm. Whole-genome data provide strong support for recent hybrid origins of the tetraploid species within the past 100,000-300,000 y from two diploid progenitors in the Capsella genus. Major-effect inactivating mutations are frequent, but many were inherited from the parental species and show no evidence of being fixed by positive selection. Despite a lack of large-scale gene loss, we observe a decrease in the efficacy of natural selection genome-wide due to the combined effects of demography, selfing, and genome redundancy from WGD. Our results suggest that the earliest stages of diploidization are associated with quantitative genome-wide decreases in the strength and efficacy of selection rather than rapid gene loss, and that nonfunctionalization can receive a "head start" through a legacy of deleterious variants and differential expression originating in parental diploid populations.

Evidence for widespread positive and negative selection in coding and conserved noncoding regions of Capsella grandiflora.

The extent that both positive and negative selection vary across different portions of plant genomes remains poorly understood. Here, we sequence whole genomes of 13 Capsella grandiflora individuals and quantify the amount of selection across the genome. Using an estimate of the distribution of fitness effects, we show that selection is strong in coding regions, but weak in most noncoding regions, with the exception of 5' and 3' untranslated regions (UTRs). However, estimates of selection on noncoding regions conserved across the Brassicaceae family show strong signals of selection. Additionally, we see reductions in neutral diversity around functional substitutions in both coding and conserved noncoding regions, indicating recent selective sweeps at these sites. Finally, using expression data from leaf tissue we show that genes that are more highly expressed experience stronger negative selection but comparable levels of positive selection to lowly expressed genes. Overall, we observe widespread positive and negative selection in coding and regulatory regions, but our results also suggest that both positive and negative selection on plant noncoding sequence are considerably rarer than in animal genomes.

Pollen-specific, but not sperm-specific, genes show stronger purifying selection and higher rates of positive selection than sporophytic genes in Capsella grandiflora.

Selection on the gametophyte can be a major force shaping plant genomes as 7-11% of genes are expressed only in that phase and 60% of genes are expressed in both the gametophytic and sporophytic phases. The efficacy of selection on gametophytic tissues is likely to be influenced by sexual selection acting on male and female functions of hermaphroditic plants. Moreover, the haploid nature of the gametophytic phase allows selection to be efficient in removing recessive deleterious mutations and fixing recessive beneficial mutations. To assess the importance of gametophytic selection, we compared the strength of purifying selection and extent of positive selection on gametophyte- and sporophyte-specific genes in the highly outcrossing plant Capsella grandiflora. We found that pollen-exclusive genes had a larger fraction of sites under strong purifying selection, a greater proportion of adaptive substitutions, and faster protein evolution compared with seedling-exclusive genes. In contrast, sperm cell-exclusive genes had a smaller fraction of sites under strong purifying selection, a lower proportion of adaptive substitutions, and slower protein evolution compared with seedling-exclusive genes. Observations of strong selection acting on pollen-expressed genes are likely explained by sexual selection resulting from pollen competition aided by the haploid nature of that tissue. The relaxation of selection in sperm might be due to the reduced influence of intrasexual competition, but reduced gene expression may also be playing an important role.

An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions.

Despite the central importance of noncoding DNA to gene regulation and evolution, understanding of the extent of selection on plant noncoding DNA remains limited compared to that of other organisms. Here we report sequencing of genomes from three Brassicaceae species (Leavenworthia alabamica, Sisymbrium irio and Aethionema arabicum) and their joint analysis with six previously sequenced crucifer genomes. Conservation across orthologous bases suggests that at least 17% of the Arabidopsis thaliana genome is under selection, with nearly one-quarter of the sequence under selection lying outside of coding regions. Much of this sequence can be localized to approximately 90,000 conserved noncoding sequences (CNSs) that show evidence of transcriptional and post-transcriptional regulation. Population genomics analyses of two crucifer species, A. thaliana and Capsella grandiflora, confirm that most of the identified CNSs are evolving under medium to strong purifying selection. Overall, these CNSs highlight both similarities and several key differences between the regulatory DNA of plants and other species.

Bayesian analysis of molecular variance in pyrosequences quantifies population genetic structure across the genome of Lycaeides butterflies.

The distribution of genetic variation within and among populations is commonly used to infer their demographic and evolutionary histories. This endeavour has the potential to benefit substantially from high-throughput next-generation sequencing technologies through a rapid increase in the amount of data available and a corresponding increase in the precision of parameter estimation. Here we report the results of a phylogeographic study of the North American butterfly genus Lycaeides using 454 sequence data. This study serves the dual purpose of demonstrating novel molecular and analytical methods for population genetic analyses with 454 sequence data and expanding our knowledge of the phylogeographic history of Lycaeides. We obtained 341,045 sequence reads from 12 populations that we were able to assemble into 15,262 contigs (most of which were variable), representing one of the largest population genetic data sets for a non-model organism to date. We examined patterns of genetic variation using a hierarchical Bayesian analysis of molecular variance model, which provides precise estimates of genome-level phi(ST) while appropriately modelling uncertainty in locus-specific phi(ST). We found that approximately 36% of sequence variation was partitioned among populations, suggesting historical or current isolation among the sampled populations. Estimates of pairwise genome-level phi(ST) were largely consistent with a previous phylogeographic model for Lycaeides, suggesting fragmentation into two to three refugia during Pleistocene glacial cycles followed by post-Pleistocene range expansion and secondary contact leading to introgressive hybridization. This study demonstrates the potential of using genome-level data to better understand the phylogeographic history of populations.