Patterns Of Incomplete Lineage Sorting Research Articles

Phylogenomics of the extinct Heath Hen provides support for sex-biased introgression among extant prairie grouse

Rapid divergence and subsequent reoccurring patterns of gene flow can complicate our ability to discern phylogenetic relationships among closely related species. To what degree such patterns may differ across the genome can provide an opportunity to extrapolate better how life history constraints may influence species boundaries. By exploring differences between autosomal and Z (or X) chromosomal-derived phylogenetic patterns, we can better identify factors that may limit introgression despite patterns of incomplete lineage sorting among closely related taxa. Here, using a whole-genome resequencing approach coupled with an exhaustive sampling of subspecies within the recently divergent prairie grouse complex (genus: Tympanuchus), including the extinct Heath Hen (T. cupido cupido), we show that their phylogenomic history differs depending on autosomal or Z-chromosome partitioned SNPs. Because the Heath Hen was allopatric relative to the other prairie grouse taxa, its phylogenetic signature should not be influenced by gene flow. In contrast, all the other extant prairie grouse taxa, except Attwater’s Prairie-chicken (T. c. attwateri), possess overlapping contemporary geographic distributions and have been known to hybridize. After excluding samples that were likely translocated prairie grouse from the Midwest to the eastern coastal states or their resulting hybrids with mainland Heath Hens, species tree analyses based on autosomal SNPs consistently identified a paraphyletic relationship with regard to the Heath Hen with Lesser Prairie-chicken (T. pallidicinctus) sister to Greater Prairie-chicken (T. c. pinnatus) regardless of genic or intergenic partitions. In contrast, species trees based on the Z-chromosome were consistent with Heath Hen sister to a clade that included its conspecifics, Greater and Attwater’s Prairie-chickens (T. c. attwateri). These results were further explained by historic gene flow, as shown with an excess of autosomal SNPs shared between Lesser and Greater Prairie-chickens but not with the Z-chromosome. Phylogenetic placement of Sharp-tailed Grouse (T. phasianellus), however, did not differ among analyses and was sister to a clade that included all other prairie grouse despite low levels of autosomal gene flow with Greater Prairie-chicken. These results, along with strong sexual selection (i.e., male hybrid behavioral isolation) and a lek breeding system (i.e., high variance in male mating success), are consistent with a pattern of female-biased introgression between prairie grouse taxa with overlapping geographic distributions. Additional study is warranted to explore how genomic components associated with the Z-chromosome influence the phenotype and thereby impact species limits among prairie grouse taxa despite ongoing contemporary gene flow.

Phylotranscriptomics reveals the reticulate evolutionary history of a widespread diatom species complex.

In contrast to surveys based on a few genes that often provide limited taxonomic resolution, transcriptomes provide a wealth of genomic loci that can resolve relationships among taxonomically challenging lineages. Diatoms are a diverse group of aquatic microalgae that includes important bioindicator species and many such lineages. One example is Nitzschia palea, a widespread species complex with several morphologically defined taxonomic varieties, some of which are critical pollution indicators. Morphological differences among the varieties are subtle and phylogenetic studies based on a few genes fail to resolve their evolutionary relationships. We conducted morphometric and transcriptome analyses of 10 Nitzschia palea strains to resolve the relationships among strains and taxonomic varieties. Nitzschia palea was resolved into three clades, one of which corresponds to a group of strains with narrow linear-lanceolate valves. The other morphological group recovered in the shape outline analysis was not monophyletic and consisted of two clades. Gene-tree concordance analyses and phylogenetic network estimations revealed patterns of incomplete lineage sorting and gene flow between intraspecific lineages. We detected reticulated evolutionary patterns among lineages with different morphologies, resulting in a putative recent hybrid. Our study shows that phylogenomic analyses of unlinked nuclear loci, complemented with morphometrics, can resolve complex evolutionary histories of recently diverged species complexes.

Selective Sweeps across Twenty Millions Years of Primate Evolution.

The contribution from selective sweeps to variation in genetic diversity has proven notoriously difficult to assess, in part because polymorphism data only allows detection of sweeps in the most recent few hundred thousand years. Here, we show how linked selection in ancestral species can be quantified across evolutionary timescales by analyzing patterns of incomplete lineage sorting (ILS) along the genomes of closely related species. We show that sweeps in the human-chimpanzee and human-orangutan ancestors can be identified as depletions of ILS in regions in excess of 100 kb in length. Sweeps predicted in each ancestral species, as well as recurrent sweeps predicted in both species, often overlap sweeps predicted in humans. This suggests that many genomic regions experience recurrent selective sweeps. By comparing the ILS patterns along the genomes of the closely related human-chimpanzee and human-orangutan ancestors, we are further able to quantify the impact of selective sweeps relative to that of background selection. Compared with the human-orangutan ancestor, the human-chimpanzee ancestor shows a strong excess of regions depleted of ILS as well as a stronger reduction in ILS around genes. We conclude that sweeps play a strong role in reducing diversity along the genome and that sweeps have reduced diversity in the human-chimpanzee ancestor much more than in the human-orangutan ancestor.

BioEssays 8∕2014

BioEssaysVolume 36, Issue 9 Cover PictureFree Access BioEssays 8∕2014 First published: 13 August 2014 https://doi.org/10.1002/bies.201470091AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Graphical Abstract Mapping recombination rates. Recombination and its control can not only be studied within an individual species but can also be analyzed between species. On pages 892–900 Munch et al. discuss a method by which recombination maps for ancestral species can be constructed from patterns of incomplete lineage sorting along the genomes of closely related species. Such ancestral recombination maps identify how recombination rate has changed along individual branches in a phylogeny. The cover shows a cladogram of old-world monkeys, the colored dots marking the ancestral species. Furthermore, the authors review what is known about the cause and effect of recombination on the evolution of genomes. Volume36, Issue9September 2014 RelatedInformation

Genetic delineation between and within the widespread coccolithophore morpho-species Emiliania huxleyi and Gephyrocapsa oceanica (Haptophyta).

Emiliania huxleyi and Gephyrocapsa oceanica are abundant coccolithophore morpho-species that play key roles in ocean carbon cycling due to their importance as both primary producers and cal-cifiers. Global change processes such as ocean acidification impact these key calcifying species. The physiology of E.huxleyi, a developing model species, has been widely studied, but its genetic delineation from G.oceanica remains unclear due to a lack of resolution in classical genetic markers. Using nuclear (18S rDNA and 28S rDNA), mitochondrial (cox1, cox2, cox3, rpl16, and dam), and plastidial (16S rDNA, rbcL, tufA, and petA) DNA markers from 99 E.huxleyi and 44 G.oceanica strains, we conducted a multigene/multistrain survey to compare the suitability of different markers for resolving phylogenetic patterns within and between these two morpho-species. The nuclear genes tested did not provide sufficient resolution to discriminate between the two morpho-species that diverged only 291Kya. Typical patterns of incomplete lineage sorting were generated in phylogenetic analyses using plastidial genes. In contrast, full morpho-species delineation was achieved with mitochondrial markers and common intra-morpho-species phylogenetic patterns were observed despite differing rates of DNA substitution. Mitochondrial genes are thus promising barcodes for distinguishing these coccolithophore morpho-species, in particular in the context of environmental monitoring.

Incomplete lineage sorting patterns among human, chimpanzee, and orangutan suggest recent orangutan speciation and widespread selection

We search the complete orangutan genome for regions where humans are more closely related to orangutans than to chimpanzees due to incomplete lineage sorting (ILS) in the ancestor of human and chimpanzees. The search uses our recently developed coalescent hidden Markov model (HMM) framework. We find ILS present in ∼1% of the genome, and that the ancestral species of human and chimpanzees never experienced a severe population bottleneck. The existence of ILS is validated with simulations, site pattern analysis, and analysis of rare genomic events. The existence of ILS allows us to disentangle the time of isolation of humans and orangutans (the speciation time) from the genetic divergence time, and we find speciation to be as recent as 9-13 million years ago (Mya; contingent on the calibration point). The analyses provide further support for a recent speciation of human and chimpanzee at ∼4 Mya and a diverse ancestor of human and chimpanzee with an effective population size of about 50,000 individuals. Posterior decoding infers ILS for each nucleotide in the genome, and we use this to deduce patterns of selection in the ancestral species. We demonstrate the effect of background selection in the common ancestor of humans and chimpanzees. In agreement with predictions from population genetics, ILS was found to be reduced in exons and gene-dense regions when we control for confounding factors such as GC content and recombination rate. Finally, we find the broad-scale recombination rate to be conserved through the complete ape phylogeny.

Ancestral Population Genomics: The Coalescent Hidden Markov Model Approach

With incomplete lineage sorting (ILS), the genealogy of closely related species differs along their genomes. The amount of ILS depends on population parameters such as the ancestral effective population sizes and the recombination rate, but also on the number of generations between speciation events. We use a hidden Markov model parameterized according to coalescent theory to infer the genealogy along a four-species genome alignment of closely related species and estimate population parameters. We analyze a basic, panmictic demographic model and study its properties using an extensive set of coalescent simulations. We assess the effect of the model assumptions and demonstrate that the Markov property provides a good approximation to the ancestral recombination graph. Using a too restricted set of possible genealogies, necessary to reduce the computational load, can bias parameter estimates. We propose a simple correction for this bias and suggest directions for future extensions of the model. We show that the patterns of ILS along a sequence alignment can be recovered efficiently together with the ancestral recombination rate. Finally, we introduce an extension of the basic model that allows for mutation rate heterogeneity and reanalyze human-chimpanzee-gorilla-orangutan alignments, using the new models. We expect that this framework will prove useful for population genomics and provide exciting insights into genome evolution.

Multiple nuclear loci reveal patterns of incomplete lineage sorting and complex species history within western mouse lemurs ( Microcebus)

Mouse lemurs (genus Microcebus) are nocturnal primates endemic to the island of Madagascar. Until recently, they were classified as two species, one from eastern and one from western Madagascar. Previously published analyses of morphometric and mitochondrial DNA data show strong support for the recognition of more than eight species, however. Here, we test the eight-species hypothesis with DNA data derived from four independently segregating nuclear loci. We find many areas of congruence between the mitochondrial and nuclear data, but incomplete lineage sorting and low mutation rates limit the phylogenetic resolution of the nuclear data. Even so, the nuclear loci unanimously find evidence for three deeply diverged lineages within the mouse lemur radiation: one that is congruent with the mtDNA “southern clade”, another that is congruent with the mtDNA “northern clade”, and one monospecific branch comprised of the species Microcebus ravelobensis. The latter result in particular emphasizes the need for careful biological study of this species.

Shifting distributions and speciation: species divergence during rapid climate change

Questions about how shifting distributions contribute to species diversification remain virtually without answer, even though rapid climate change during the Pleistocene clearly impacted genetic variation within many species. One factor that has prevented this question from being adequately addressed is the lack of precision associated with estimates of species divergence made from a single genetic locus and without incorporating processes that are biologically important as populations diverge. Analysis of DNA sequences from multiple variable loci in a coalescent framework that (i) corrects for gene divergence pre-dating speciation, and (ii) derives divergence-time estimates without making a priori assumptions about the processes underlying patterns of incomplete lineage sorting between species (i.e. allows for the possibility of gene flow during speciation), is critical to overcoming the inherent logistical and analytical difficulties of inferring the timing and mode of speciation during the dynamic Pleistocene. Estimates of species divergence that ignore these processes, use single locus data, or do both can dramatically overestimate species divergence. For example, using a coalescent approach with data from six loci, the divergence between two species of montane Melanoplus grasshoppers is estimated at between 200,000 and 300,000 years before present, far more recently than divergence estimates made using single-locus data or without the incorporation of population-level processes. Melanoplus grasshoppers radiated in the sky islands of the Rocky Mountains, and the analysis of divergence between these species suggests that the isolation of populations in multiple glacial refugia was an important factor in promoting speciation. Furthermore, the low estimates of gene flow between the species indicate that reproductive isolation must have evolved rapidly for the incipient species boundaries to be maintained through the subsequent glacial periods and shifts in species distributions.