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Tiley, G. P.

Publications and source records attributed to Tiley, G. P..

13 recordsLinked to original sources

A simple and accurate method for inferring missing ploidy information from sequence data

Polyploidy can be a critical factor for explaining plant trait variation, niche diversification, or speciation. However, inferring ploidy from silica-dried or historical samples using chromosome counts or flow cytometry is not possible, and scaling up ploidy estimation to population-level fresh contemporary samples can be challenging as well. Thus, we present a new method for estimating ploidy levels directly from sequencing data using machine learning; the Polyploid Population Genomics Tool Kit (PPGTK). The machine-learning approach is advantageous as it relaxes the assumptions of previous probabilistic methods and provides per-sample probabilities, allowing investigators to evaluate uncertainty in their system of interest.. We demonstrate performance and accuracy of the method on simulated and empirical data. Simulations showed above 99% accuracy, even for low coverage data, as long reads were mappable to the reference genome. For empirical analyses, we used target enrichment data from blueberry wild relatives (Vaccinium sect. Cyanococcus) and whole-genome data from sweetpotato wild relatives (Ipomoea ser. Batatas). Ploidy was recovered with 99% accuracy across 70 Vaccinium individuals and 97% across 82 Ipomoea individuals. Analysis of many individuals is fast and requires only a multisample VCF, which is presumably generated for the research anyway, and some samples of known ploidy for training the classifier. The approach implemented in PPGTK is promising for collections-based research as well, enabling ploidy classification of historical specimens based on present-day observations. The method is implemented in a new Python package as a single command that can run on a conventional laptop.

evolutionary biology↗

SLEDGe: Inference of ancient whole genome duplications using machine learning

Ancient whole-genome duplication--previous genome duplication events that have since been eroded via diploidization, are increasingly identified throughout eukaryotes. One of the constraints against large-scale studies of ancient eukaryotic WGD is the relatively large, high-quality datasets often needed to definitively establish ancient WGD events; alternatively, the more low-input method interpretation of genome-wide synonymous substitution rates (Ks plots) is prone to bias and inconsistency. We improve upon the shortcomings of the current Ks plot method by building a Ks plot simulator. This data-agnostic approach simulates common distributions found in Ks plots in the presence or absence of ancient WGD signatures. In conjunction with a machine-learning classifier, this approach can quickly assess the likelihood that transcriptomic and genomic data bear WGD signatures. On independently-generated synthetic data and real plant transcriptomic data, SLEDGE is capable of correctly identifying ancient WGD in 93-100% of samples. This approach can serve as a quick classification step in large-scale genomic analyses, identifying putative ancient polyploids for further study.

bioinformatics↗

Extracting diamonds: Identifiability of 4-node cycles in level-1 phylogenetic networks under a pseudolikelihood coalescent model

Phylogenetic networks encode a broader picture of evolution by the inclusion of reticulate processes such as hybridization, introgression or horizontal gene transfer. Each reticulation event is represented by a "hybridization cycle". Here, we investigate the statistical identifiability of the position of the hybrid node in a 4-node hybridization cycle in a semi-directed level-1 phylogenetic network. That is, we investigate if our model is able to detect the correct placement of the hybrid node in the hybridization cycle from concordance factors as data. While generic identifiability is easily attained under non-restrictive assumptions such as t [isin] (0, {infty}) for all branches and{gamma} [isin] (0, 1) for the inheritance probability of the hybrid edges, simulations show that accurate detection of these cycles can be complicated by inadequate sampling, small sample size or gene tree estimation error. We identify practical advice for evolutionary biologists on best sampling strategies to improve the detection of this type of hybridization cycle.

evolutionary biology↗

The grass that built the Central Highland of Madagascar: environmental niches and morphological diversity of Loudetia simplex

1) Research Aims -- Loudetia simplex is a common and dominant species throughout grassland ecosystems in mainland Africa and Madagascar. It is highly polymorphic, often classified as two taxa endemic to Madagascar: L. simplex subsp. stipoides and L. madagascariensis. A better understanding of the inter- and intra-specific variation between these taxa and its contributing environmental factors could improve our understanding of the history of Madagascars grasslands. 2) Methods -- The taxonomic status of L. simplex subsp. stipoides and L. madagascariensis was evaluated by morphometric analyses of 119 herbarium specimens. Species distribution modelling was used to determine the most important environmental factors underlying the L. simplex distribution in Madagascar versus other African grasslands. We investigated if L. simplex in Madagascar could be predicted by distributions across mainland Africa with niche overlap analyses. 3) Key Result -- African and Malagasy species exhibited variation potentially associated with environment. Specimens from northern and western Madagascar were taller with smaller spikelets than those from Southern Africa and central Madagascar. Loudetia simplex typically occurred in cooler temperatures with high precipitation and pronounced seasonality, but taller populations were found in warmer conditions. Projecting ecological niches of Southern Africa and East Tropical Africa onto Madagascar demonstrates much of the present distribution in the Central Highlands is expected from other natural African grasslands. 4) Key Point -- Malagasy and African individuals represent a single species, and the Malagasy species can be considered as a synonym of L. simplex. Distribution models are congruent with pre-human presence of grasslands in Madagascar. SOCIETAL IMPACT STATEMENTUnderstanding dominant species like Loudetia simplex is necessary to understand the fire-driven grassy ecosystems they create. In Madagascar, grasslands are considered a low-value ecosystem despite their unique biodiversity and crucial importance as zebu rangeland. Only 1.8% of Madagascars grasslands are protected despite facing similar threats to forests and biodiversity loss. This study of common grasses will support the management of protected areas by providing information on resource management of vulnerable open ecosystems in Madagascar. Distribution models of common grass species and clear taxonomic classification can help land management stakeholders identify natural grasslands versus degraded forests.

ecology↗

Genetic variation in Loudetia simplex supports the presence of ancient grasslands in Madagascar

O_LIResearch Aims -- The extent of Madagascars grasslands prior to human colonization is unresolved. We used population genetic analyses of a broadly dominant C4 fire-adapted grass, Loudetia simplex, as a proxy for estimating grassland change through time. We carefully examined the utility of target-enrichment data for population genetics to make recommendations for conservation genetics. We explored the potential of estimating individual ploidy levels from target-enrichment data and how assumptions about ploidy could affect analyses. C_LIO_LIMethods -- We developed a novel bioinformatic pipeline to estimate ploidy and genotypes from target-enrichment data. We estimated standard population genetic summary statistics in addition to species trees and population structure. Extended Bayesian skyline plots provided estimates of population size through time for empirical and simulated data. C_LIO_LIKey Result -- All Malagasy Loudetia simplex individuals sampled in this study formed a clade and possibly indicated an ancestral Central Highland distribution of 800m in altitude and above. Demographic models suggested grassland expansions occurred prior to the Last Interglacial Period and supported extensive grasslands prior to human colonization. Though there are limitations to target-enrichment data for population genetic studies, we find that analyses of population structure are reliable. C_LIO_LIKey Point --Genetic variation in Loudetia simplex supports widespread grasslands in Madagascar prior to the more recent periods of notable paleoclimatic change. However, the methods explored here could not differentiate between paleoclimatic change near the Last Glacial Maximum and anthropogenic effects. Target-enrichment data can be a valuable tool for analyses of population structure in the absence a reference genome. C_LI Societal Impact StatementRecognizing Loudetia dominated grasslands were widespread prior to human colonization highlights that open ecosystems were and continue to be an important component of Madagascars biodiversity. Urgently required are biodiversity inventories and integrative taxonomic treatments of grassland flora and fauna to asses risks to understudied ecosystems historically regarded as wastelands. Substantial financial and logistical barriers exist to implementing conservation studies using contemporary genomic tools. We ameliorated some of the challenges for population genetic analyses of non-model polyploids lacking reference genomes by developing computational resources to leverage a cost-effective data generation strategy that requires no prior genetic knowledge of the target species. ResumeO_LILes objectifs de la recherche -- Letendue des ecosystemes ouverts de Madagascar avant la colonisation humaine reste a eclaircir. Nous avons utilise une analyse de la population genetique dune graminee C4 adaptee au feu, largement dominante, Loudetia simplex, comme reference pour estimer les changements au niveau de ces biomes au fil du temps. Nous avons examine attentivement lutilite des donnees denrichissement cible pour la genetique de population afin de formuler des recommandations pour la conservation genetique. Nous avons explore le potentiel de lestimation du niveau des ploidies individuelles a partir des donnees denrichissement cible et comment les hypotheses a propos de ces ploidies pourraient affecter les analyses. C_LIO_LILes methodes -- Nous avons developpe un nouveau canal bioinformatique pour estimer les ploidies et les genotypes a partir des donnees denrichissement cible. Nous avons estime les statistiques standard de la population genetique, en plus des arbres des especes et de la structure de la population. Lutilisation des traces etendus du ciel bayesien a fourni une estimation de la taille de la population au fil du temps pour des donnees empiriques et simulees. C_LIO_LIResultat cle -- Tous les individus Malagasy de Loudetia simplex echantillonnes dans cette etude ont forme un clade, indiquant une eventuelle ancienne distribution dans les hauts plateaux. Les modeles demographiques suggerent une expansion des prairies bien avant la derniere periode interglaciaire et soutiennent lexistence dune vaste distribution avant la colonisation humaine. Bien quil y ait des limites a lenrichissement des donnees cibles pour letude de la genetique des populations, nous constatons que lanalyse des structures des populations est fiable. C_LIO_LILes points cles -- La variation genetique de Loudetia simplex soutient lexistence de vastes prairies a Madagascar avant les periodes plus recentes de changements paleoclimatiques notables. Cependant, les methodes explorees ici nont pas permis de faire la difference entre les changements paleoclimatiques pres du dernier maximum glaciaire et les effets anthropogenes. Les donnees denrichissement cible peuvent etre un outil precieux pour les analyses de la structure des populations en labsence dun genome de reference. C_LI Declaration dimpact societalReconnaitre que les prairies dominees par Loudetia etaient repandues avant la colonisation humaine souligne que les ecosystemes ouverts etaient et continuent detre un composant important de la biodiversite de Madagascar. Il est urgent de realiser des inventaires de la biodiversite et une taxonomie integree pour le traitement de la flore et de la faune des ecosystemes ouverts afin devaluer les risques pour les ecosystemes sous-etudies consideres historiquement comme des terres en friches. Des barrieres financieres et logistiques existent pour mettre en uvre letude de la conservation en utilisant les outils genomiques contemporains. Nous avons ameliore certains des defis lies aux analyses genetiques de populations de polyploides non modeles, sans genomes de reference, en developpant des ressources informatiques pour exploiter une strategie pouvant generer des donnees rentables ne necessitant aucune connaissance genetique prealable de lespece cible. FamintinanaO_LINy tanjonny fikarohana -- Mbola tsy fantatra mazava tsara ny fivelaranny hivoka teto Madagasikara talohanny fahatongavany olombelona. Mba ahafantarana ny fihovana nitranga nandritra ny fotoana naharitra teo aminireo hivoka ireo dia nanao famakafakahana ara-genetika aminny ahitra C4 miompana aminny afo iray antsoina Loudetia simplex ara-tsiantifika na Berambo na Hara aminny teny malagasy izahay. Nandinika tsara ny maha-zava-dehibe ny fampitomboana ny antotan-kevitra mba ahafahana manolo-kevitra momba ny fiarovana ny fototarazo genetika. Nandinika ny mety mampiavaka ny fanombanana anny ploidy tsirairay aminny fampitomboana antotan-kevitra sy ny mety ho fiantraikanny fiheverana momba ireo ploidy ireo aminny fikarohana. C_LIO_LIFomba Fiasa -- Namorona fantsona bioinformatika vaovao mba ahafahana manombana ny ploidy sy ny << genotypes >> avy aminny antotan-kevitra nokendrena izahay. Notombanana ny antontanisa famintinana ny fototarazo ara-genetikanireo vondronahitra ireo, miampy ny karazana hazo sy ny firafitry ny vondrona na koa hoe mponina. Nanome tombantombana ny habenny mponina aminny alalanny fotoana ny antontan-kevitra voavinavina azo taminny fikarohana. Fikarohana izay azo taminny alalanny << Bayesina Skuline Plots >>. C_LIO_LIVokam-pikarohana fototra -- Ny vondrona Loudetia simplex eto Madagasikara izay niasana dia namorona << clade >> na fikambanana iray, izay manondro ny mety maha ela netezana sy tranainy anio ahitra io eny aminny faritra avo. Ny modely demografika dia manoro hevitra aminny naha be velarana ny hivoka izay efa ela talohanny vanim-potoana << interglacial >> farany ary manohana ny fivelarana midadasika anireo kijana ireo alohanny fonenanny olombelona. Na dia misy fetrany aza ny fampitomboana ny antotan-kevitra kendrena aminny fandalinana ny fototarazo genetika mombanny mponina, dia hita fa azo itokisana ny fikarohana natao mombanny firafitry ny mponina. C_LIO_LIHevi-dehibe -- Ny fahasamihafana ara-genetika ao aminny Loudetia simplex dia manohana ny fisianny hivoka na kijana midadasika eto Madagasikara talohanny vanim-potoananny fiovana paleoclimatika nisongadina. Na izany aza, ny fombam-pikarohana nampiasana teto dia tsy nahavita nanavaka ny fiovanny paleoclimatika akaikinny vanim-potoana lehibe nangatsiaka farany sy ny vokatry ny fitrandrahana nataonny olombelona. Mety ho fitaovana manan-danja aminny famakafakana ny firafitry ny mponina ny antotan-kevitra nampitombona na dia tsy misy fitaovana genomika iangaina aza. C_LI Fanambarana fiantraika ara-tsosialyNy fanekena fa niely patrana ny hivoka itoeranny Loudetia talohanny fanjanahanny olombelona dia manamarika fa ireo hivoka ireo dia singa manan-danja aminny zavamananaina eto Madagasikara. Ilaina maika ny fahafantarana ara biolojika sy taxononomique ny zavamaniry sy ny biby aminny hivoka mba hanombanana ny loza mety hitranga aminny hivoka izay tsy ananana fahalalana maro sady heverina ho tany maina. Misy sakana ara-bola sy ara-pitaovana aminny fampiharana ny fandalinana momba ny fiarovana izay nampiasana fitaovana genomika ankehitriny. Nohatsarainay ny sasany aminireo fanamby mifandraika aminny famakafakana ara-genetika ny mponina manana ploidy maro tsy modely, izay tsy misy fitaovana genomika iaingana, aminny alalanny fampivoarana loharanon-kevitra kajy mba hitrandrahana paikady izay mety hiteraka angon-drakitra mahomby tsy mitaky fahalalana mahakasika ny fototarazo ara-genetika ny zava-maniry izay tiana karohina.

evolutionary biology↗

Mutationathon: towards standardization in estimates of pedigree-based germline mutation rates

In the past decade, several studies have estimated the human per-generation germline mutation rate using large pedigrees. More recently, estimates for various non-human species have been published. However, methodological differences among studies in detecting germline mutations and estimating mutation rates make direct comparisons difficult. Here, we describe the many different steps involved in estimating pedigree-based mutation rates, including sampling, sequencing, mapping, variant calling, filtering, and how to appropriately account for false-positive and false-negative rates. For each step, we review the different methods and parameter choices that have been used in the recent literature. Additionally, we present the results from a "Mutationathon", a competition organized among five research labs to compare germline mutation rate estimates for a single pedigree of rhesus macaques. We report almost a two-fold variation in the final estimated rate among groups using different post-alignment processing, calling, and filtering criteria and provide details into the sources of variation across studies. Though the difference among estimates is not statistically significant, this discrepancy emphasizes the need for standardized methods in mutation rate estimations and the difficulty in comparing rates from different studies. Finally, this work aims to provide guidelines for computational and statistical benchmarks for future studies interested in identifying germline mutations from pedigrees.

evolutionary biology↗

Phasing Alleles Improves Network Inference with Allopolyploids

Accurately reconstructing the reticulate histories of polyploids remains a central challenge for understanding plant evolution. Although phylogenetic networks can provide insights into relationships among polyploid lineages, inferring networks may be hindered by the complexities of homology determination in polyploid taxa. We use simulations to show that phasing alleles from allopolyploid individuals can improve phylogenetic network inference under the multispecies coalescent by obtaining the true network with fewer loci compared to haplotype consensus sequences or sequences with heterozygous bases represented as ambiguity codes. Phased allelic data can also improve divergence time estimates for networks, which is helpful for evaluating allopolyploid speciation hypotheses and proposing mechanisms of speciation. To achieve these outcomes in empirical data, we present a novel pipeline that leverages a recently developed phasing algorithm to reliably phase alleles from polyploids. This pipeline is especially appropriate for target enrichment data, where depth of coverage is typically high enough to phase entire loci. We provide an empirical example in the North American Dryopteris fern complex that demonstrates insights from phased data as well as the challenges of network inference. We establish that our pipeline (PATE: Phased Alleles from Target Enrichment data) is capable of recovering a high proportion of phased loci from both diploids and polyploids. These data may improve network estimates compared to using haplotype consensus assemblies by accurately inferring the direction of gene flow, but statistical non-identifiability of phylogenetic networks poses a barrier to inferring the evolutionary history of reticulate complexes.

evolutionary biology↗

Chromosome fusions shape an ancient UV sex chromosome system

Non-recombining sex chromosomes, like the mammalian Y, often lose genes and accumulate transposable elements, a process termed degeneration1,2. The correlation between suppressed recombination and degeneration is clear in animal XY systems1,2, but the absence of recombination is confounded with other asymmetries between the X and Y. In contrast, UV sex chromosomes, like those found in bryophytes, experience symmetrical population genetic conditions3,4. Here we test for degeneration in the bryophyte UV sex chromosome system through genomic comparisons with new female and male chromosome-scale reference genomes of the moss Ceratodon purpureus. We show that the moss sex chromosomes evolved over 300 million years ago and expanded via two chromosomal fusions. Although the sex chromosomes show signs of weaker purifying selection than autosomes, we find suppressed recombination alone is insufficient to drive gene loss on sex-specific chromosomes. Instead, the U and V sex chromosomes harbor thousands of broadly-expressed genes, including numerous key regulators of sexual development across land plants.

evolutionary biology↗

A target enrichment probe set for resolving the flagellate plant tree of life

Premise of the studyNew sequencing technologies enable the possibility of generating large-scale molecular datasets for constructing the plant tree of life. We describe a new probe set for target enrichment sequencing to generate nuclear sequence data to build phylogenetic trees with any flagellate plants, comprising hornworts, liverworts, mosses, lycophytes, ferns, and gymnosperms. Methods and ResultsWe leveraged existing transcriptome and genome sequence data to design a set of 56,989 probes for target enrichment sequencing of 451 nuclear exons and non-coding flanking regions across flagellate plant lineages. We describe the performance of target enrichment using the probe set across flagellate plants and demonstrate the potential of the data to resolve relationships among both ancient and closely related taxa. ConclusionsA target enrichment approach using the new probe set provides a relatively low-cost solution to obtain large-scale nuclear sequence data for inferring phylogenetic relationships across flagellate plants.

evolutionary biology↗

Phylogeographic analysis of Goodman's mouse lemur reveals historical interconnectivity of Madagascar's Central Highlands and eastern rainforests

The Central Highland Plateau of Madagascar is largely composed of grassland savanna, interspersed with patches of closed-canopy forest. Conventional wisdom has it that these grasslands are anthropogenic in nature, having been created very recently via human agricultural practices. Yet, the ancient origins of the endemic grasses suggest that the extensive savannas are natural biomes, similar to others found around the globe. We use a phylogeographic approach to compare these two competing scenarios. By sampling multiple populations of Goodmans mouse lemur (Microcebus lehilahytsara), a small-bodied nocturnal primate, we reconstruct the phylogeographic and demographic history of these "environmental metronomes" to estimate the time at which their populations diverged, and thus proximally, when their habitats would have become fragmented. We applied coalescent methods to RADseq data to infer phylogenetic relationships, population structure, and migration corridors among sampling sites. These analyses indicate that forest fragmentation occurred rapidly during a period of decreased precipitation near the last glacial maximum and would have affected both the Central Highlands and eastern forests. Though there is clear genomic structure separating the populations of the Central Highland from those of the eastern rainforests, there is also evidence of historical migration between them. Findings support the hypothesis that the Central Highland savanna predates human arrival, indicating that it is a natural landscape that has long impacted the population dynamics of Goodmans mouse lemur, and by extension, other forest-dwelling organisms in Madagascar.

evolutionary biology↗

Complex processes of cryptic speciation in mouse lemurs from a micro-endemism hotspot in Madagascar

AO_SCPLOWBSTRACTC_SCPLOWMouse lemurs (Microcebus) are a radiation of morphologically cryptic primates distributed throughout Madagascar for which the number of recognized species has exploded in the past two decades. This taxonomic explosion has prompted understandable concern that there has been substantial oversplitting in the mouse lemur clade. Here, we take an integrative approach to investigate species diversity in two pairs of sister lineages that occur in a region in northeastern Madagascar with high levels of microendemism and predicted habitat loss. We analyzed RADseq data with multispecies coalescent (MSC) species delimitation methods for three named species and an undescribed lineage previously identified to have divergent mtDNA. Marked differences in effective population sizes, levels of gene flow, patterns of isolation-by-distance, and species delimitation results were found among them. Whereas all tests support the recognition of the presently undescribed lineage as a separate species, the species-level distinction of two previously described species, M. mittermeieri and M. lehilahytsara is not supported - a result that is particularly striking when using the genealogical discordance index (gdi). Non-sister lineages occur sympatrically in two of the localities sampled for this study, despite an estimated divergence time of less than 1 Ma. This suggests rapid evolution of reproductive isolation in the focal lineages, and in the mouse lemur clade generally. The divergence time estimates reported here are based on the MSC and calibrated with pedigree-based mutation rates and are considerably more recent than previously published fossil-calibrated concatenated likelihood estimates, however. We discuss the possible explanations for this discrepancy, noting that there are theoretical justifications for preferring the MSC estimates in this case.

evolutionary biology↗

Pedigree-based measurement of the de novo mutation rate in the gray mouse lemur reveals a high mutation rate, few mutations in CpG sites, and a weak sex bias

Spontaneous germline mutations are the raw material on which evolution acts, and knowledge of their frequency and genomic distribution is crucial for understanding how evolution operates at both long and short timescales. At present, the rate and spectrum of de novo mutations have been directly characterized in only a few lineages. It is therefore critical to expand the phylogenetic scope of these studies to gain a more general understanding of observed mutation rate patterns. Our study provides the first direct mutation rate estimate for a strepsirrhine (i.e., the lemurs and lorises), which comprise nearly half of the primate clade. Using high-coverage linked-read sequencing for a focal quartet of gray mouse lemurs (Microcebus murinus), we estimated the mutation rate to be 1.64 x 10-8 (95% credible interval: 1.41 x 10-8 to 1.98 x 10-8) mutations/site/generation. This estimate is higher than those measured for most previously characterized mammals. Further, we found an unexpectedly low count of paternal mutations, and only a modest overrepresentation of mutations at CpG-sites. Given the surprising nature of these observations, we conducted an independent analysis of context-dependent substitution types for gray mouse lemur and five additional primate species. This analysis yielded patterns consistent with the mutation spectrum from the pedigree mutation-rate analysis, which provides confidence in our ability to accurately identify de novo mutations with our data and bioinformatic filters.

evolutionary biology↗

Comparative genomic analysis of the pheromone receptor Class 1 family (V1R) reveals extreme complexity in mouse lemurs (genus, Microcebus) and chromosomal hotspots across mammals

Sensory gene families are of special interest, both for what they can tell us about molecular evolution, and for what they imply as mediators of social communication. The vomeronasal type-1 receptors (V1Rs) have often been hypothesized as playing a fundamental role in driving or maintaining species boundaries given their likely function as mediators of intraspecific mate choice, particularly in nocturnal mammals. Here, we employ a comparative genomic approach for revealing patterns of V1R evolution within primates, with a special focus on the small-bodied nocturnal mouse and dwarf lemurs of Madagascar (genera Microcebus and Cheirogaleus, respectively). By doubling the existing genomic resources for strepsirrhine primates (i.e., the lemurs and lorises), we find that the highly-speciose and morphologically-cryptic mouse lemurs have experienced an elaborate proliferation of V1Rs that we argue is functionally related to their capacity for rapid lineage diversification. Contrary to a previous study that found equivalent degrees of V1R diversity in diurnal and nocturnal lemurs, our study finds a strong correlation between nocturnality and V1R elaboration, with nocturnal lemurs showing elaborate V1R repertoires and diurnal lemurs showing less diverse repertoires. Recognized subfamilies among V1Rs show unique signatures of diversifying positive selection, as might be expected if they have each evolved to respond to specific stimuli. Further, a detailed syntenic comparison of mouse lemurs with mouse (genus Mus) and other mammalian outgroups shows that orthologous mammalian subfamilies, predicted to be of ancient origin, tend to cluster in a densely populated region across syntenic chromosomes that we refer to as V1R \"hotspots.\"

genomics↗