Domestication is associated with increased interspecific hybrid compatibility in landfowl (order: Galliformes).

Some species are able to hybridize despite being exceptionally diverged. The causes of this variation in accumulation of reproductive isolation remain poorly understood, and domestication as an impetus or hindrance to reproductive isolation remains to be characterized. In this study, we investigated the role of divergence time, domestication, and mismatches in morphology, habitat, and clutch size among hybridizing species on reproductive isolation in the bird order Galliformes. We compiled and analyzed hybridization occurrences from literature and recorded measures of postzygotic reproductive isolation. We used a text-mining approach leveraging a historical aviculture magazine to quantify the degree of domestication across species. We obtained divergence time, morphology, habitat, and clutch size data from open sources. We found 123 species pairs (involving 77 species) with known offspring fertility (sterile, only males fertile, or both sexes fertile). We found that divergence time and clutch size were significant predictors of reproductive isolation (McFadden's Pseudo-R2 = 0.59), but not habitat or morphological mismatch. Perhaps most interesting, we found a significant relationship between domestication and reproductive compatibility after correcting for phylogeny, removing extreme values, and addressing potential biases (F1,74 = 5.43, R2 = 0.06, P-value = 0.02). We speculate that the genetic architecture and disruption in selective reproductive regimes associated with domestication may impact reproductive isolation, causing domesticated species to be more reproductively labile.

Drift drives the evolution of chromosome number II: The impact of range size on genome evolution in Carnivora.

Chromosome number is a fundamental genomic trait that is often the first recorded characteristic of a genome. Across large clades, a common pattern emerges: many or even most lineages exhibit relative stasis, while a handful of lineages or species exhibit striking variation. Despite recent developments in comparative methods, most of this heterogeneity is still poorly understood. It is essential to understand why some lineages have rapid rates of chromosome number evolution, as it can impact a variety of other traits. Previous research suggests that biased female meiotic drive may shape rates of karyotype evolution in some mammals. However, Carnivora exhibits variation that this female meiotic drive model cannot explain. We hypothesize that variation in effective population size may underlie rate variation in Carnivora. To test this hypothesis, we estimated rates of fusions and fissions while accounting for range size, which we use as a proxy for effective population size. We reason fusions and fissions are deleterious or underdominant and that only in lineages with small range sizes will these changes be able to fix due to genetic drift. In this study, we find that the rates of fusions and fissions are elevated in taxa with small range sizes relative to those with large range sizes. Based on these findings, we conclude that 1) naturally occurring structural mutations that change chromosome number are underdominant or mildly deleterious, and 2) when population sizes are small, structural rearrangements may play an important role in speciation and reduction in gene flow among populations.

Drift drives the evolution of chromosome number I: The impact of trait transitions on genome evolution in Coleoptera.

Chromosomal mutations such as fusions and fissions are often thought to be deleterious, especially in heterozygotes (underdominant), and consequently are unlikely to become fixed. Yet, many models of chromosomal speciation ascribe an important role to chromosomal mutations. When the effective population size (Ne) is small, the efficacy of selection is weakened, and the likelihood of fixing underdominant mutations by genetic drift is greater. Thus, it is possible that ecological and phenotypic transitions that modulate Ne facilitate the fixation of chromosome changes, increasing the rate of karyotype evolution. We synthesize all available chromosome number data in Coleoptera and estimate the impact of traits expected to change Ne on the rate of karyotype evolution in the family Carabidae and 12 disparate clades from across Coleoptera. Our analysis indicates that in Carabidae, wingless clades have faster rates of chromosome number increase. Additionally, our analysis indicates clades exhibiting multiple traits expected to reduce Ne, including strict inbreeding, oligophagy, winglessness, and island endemism, have high rates of karyotype evolution. Our results suggest that chromosome number changes are likely fixed by genetic drift despite an initial fitness cost and that chromosomal speciation models may be important to consider in clades with very small Ne.

A pangenome graph reference of 30 chicken genomes allows genotyping of large and complex structural variants.

BACKGROUND: The red junglefowl, the wild outgroup of domestic chickens, has historically served as a reference for genomic studies of domestic chickens. These studies have provided insight into the etiology of traits of commercial importance. However, the use of a single reference genome does not capture diversity present among modern breeds, many of which have accumulated molecular changes due to drift and selection. While reference-based resequencing is well-suited to cataloging simple variants such as single-nucleotide changes and short insertions and deletions, it is mostly inadequate to discover more complex structural variation in the genome. METHODS: We present a pangenome for the domestic chicken consisting of thirty assemblies of chickens from different breeds and research lines. RESULTS: We demonstrate how this pangenome can be used to catalog structural variants present in modern breeds and untangle complex nested variation. We show that alignment of short reads from 100 diverse wild and domestic chickens to this pangenome reduces reference bias by 38%, which affects downstream genotyping results. This approach also allows for the accurate genotyping of a large and complex pair of structural variants at the K feathering locus using short reads, which would not be possible using a linear reference. CONCLUSIONS: We expect that this new paradigm of genomic reference will allow better pinpointing of exact mutations responsible for specific phenotypes, which will in turn be necessary for breeding chickens that meet new sustainability criteria and are resilient to quickly evolving pathogen threats.

Simulation Tests of Methods in Evolution, Ecology, and Systematics: Pitfalls, Progress, and Principles.

Complex statistical methods are continuously developed across the fields of ecology, evolution, and systematics (EES). These fields, however, lack standardized principles for evaluating methods, which has led to high variability in the rigor with which methods are tested, a lack of clarity regarding their limitations, and the potential for misapplication. In this review, we illustrate the common pitfalls of method evaluations in EES, the advantages of testing methods with simulated data, and best practices for method evaluations. We highlight the difference between method evaluation and validation and review how simulations, when appropriately designed, can refine the domain in which a method can be reliably applied. We also discuss the strengths and limitations of different evaluation metrics. The potential for misapplication of methods would be greatly reduced if funding agencies, reviewers, and journals required principled method evaluation.

Chromosome number evolves at equal rates in holocentric and monocentric clades.

Despite the fundamental role of centromeres two different types are observed across plants and animals. Monocentric chromosomes possess a single region that function as the centromere while in holocentric chromosomes centromere activity is spread across the entire chromosome. Proper segregation may fail in species with monocentric chromosomes after a fusion or fission, which may lead to chromosomes with no centromere or multiple centromeres. In contrast, species with holocentric chromosomes should still be able to safely segregate chromosomes after fusion or fission. This along with the observation of high chromosome number in some holocentric clades has led to the hypothesis that holocentricity leads to higher rates of chromosome number evolution. To test for differences in rates of chromosome number evolution between these systems, we analyzed data from 4,393 species of insects in a phylogenetic framework. We found that insect orders exhibit striking differences in rates of fissions, fusions, and polyploidy. However, across all insects we found no evidence that holocentric clades have higher rates of fissions, fusions, or polyploidy than monocentric clades. Our results suggest that holocentricity alone does not lead to higher rates of chromosome number changes. Instead, we suggest that other co-evolving traits must explain striking differences between clades.

The origins and evolution of chromosomes, dosage compensation, and mechanisms underlying venom regulation in snakes.

Here we use a chromosome-level genome assembly of a prairie rattlesnake (Crotalus viridis), together with Hi-C, RNA-seq, and whole-genome resequencing data, to study key features of genome biology and evolution in reptiles. We identify the rattlesnake Z Chromosome, including the recombining pseudoautosomal region, and find evidence for partial dosage compensation driven by an evolutionary accumulation of a female-biased up-regulation mechanism. Comparative analyses with other amniotes provide new insight into the origins, structure, and function of reptile microchromosomes, which we demonstrate have markedly different structure and function compared to macrochromosomes. Snake microchromosomes are also enriched for venom genes, which we show have evolved through multiple tandem duplication events in multiple gene families. By overlaying chromatin structure information and gene expression data, we find evidence for venom gene-specific chromatin contact domains and identify how chromatin structure guides precise expression of multiple venom gene families. Further, we find evidence for venom gland-specific transcription factor activity and characterize a complement of mechanisms underlying venom production and regulation. Our findings reveal novel and fundamental features of reptile genome biology, provide insight into the regulation of snake venom, and broadly highlight the biological insight enabled by chromosome-level genome assemblies.

Phylogenetics in space: How continuous spatial structure impacts tree inference.

The tendency to discretize biology permeates taxonomy and systematics, leading to models that simplify the often continuous nature of populations. Even when the assumption of panmixia is relaxed, most models still assume some degree of discrete structure. The multispecies coalescent has emerged as a powerful model in phylogenetics, but in its common implementation is entirely space-independent - what we call the "missing z-axis". In this article, we review the many lines of evidence for how continuous spatial structure can impact phylogenetic inference. We illustrate and expand on these by using complex continuous-space demographic models that include distinct modes of speciation. We find that the impact of spatial structure permeates all aspects of phylogenetic inference, including gene tree stoichiometry, topological and branch-length variance, network estimation, and species delimitation. We conclude by utilizing our results to suggest how researchers can identify spatial structure in phylogenetic datasets.

Of Traits and Trees: Probabilistic Distances under Continuous Trait Models for Dissecting the Interplay among Phylogeny, Model, and Data.

Stochastic models of character trait evolution have become a cornerstone of evolutionary biology in an array of contexts. While probabilistic models have been used extensively for statistical inference, they have largely been ignored for the purpose of measuring distances between phylogeny-aware models. Recent contributions to the problem of phylogenetic distance computation have highlighted the importance of explicitly considering evolutionary model parameters and their impacts on molecular sequence data when quantifying dissimilarity between trees. By comparing two phylogenies in terms of their induced probability distributions that are functions of many model parameters, these distances can be more informative than traditional approaches that rely strictly on differences in topology or branch lengths alone. Currently, however, these approaches are designed for comparing models of nucleotide substitution and gene tree distributions, and thus, are unable to address other classes of traits and associated models that may be of interest to evolutionary biologists. Here, we expand the principles of probabilistic phylogenetic distances to compute tree distances under models of continuous trait evolution along a phylogeny. By explicitly considering both the degree of relatedness among species and the evolutionary processes that collectively give rise to character traits, these distances provide a foundation for comparing models and their predictions, and for quantifying the impacts of assuming one phylogenetic background over another while studying the evolution of a particular trait. We demonstrate the properties of these approaches using theory, simulations, and several empirical data sets that highlight potential uses of probabilistic distances in many scenarios. We also introduce an open-source R package named PRDATR for easy application by the scientific community for computing phylogenetic distances under models of character trait evolution.[Brownian motion; comparative methods; phylogeny; quantitative traits.].

Lineage-specific patterns of chromosome evolution are the rule not the exception in Polyneoptera insects.

The structure of a genome can be described at its simplest by the number of chromosomes and the sex chromosome system it contains. Despite over a century of study, the evolution of genome structure on this scale remains recalcitrant to broad generalizations that can be applied across clades. To address this issue, we have assembled a dataset of 823 karyotypes from the insect group Polyneoptera. This group contains orders with a range of variations in chromosome number, and offer the opportunity to explore the possible causes of these differences. We have analysed these data using both phylogenetic and taxonomic approaches. Our analysis allows us to assess the importance of rates of evolution, phylogenetic history, sex chromosome systems, parthenogenesis and genome size on variation in chromosome number within clades. We find that fusions play a key role in the origin of new sex chromosomes, and that orders exhibit striking differences in rates of fusions, fissions and polyploidy. Our results suggest that the difficulty in finding consistent rules that govern evolution at this scale may be due to the presence of many interacting forces that can lead to variation among groups.

The probability of fusions joining sex chromosomes and autosomes.

Chromosome fusion and fission are primary mechanisms of karyotype evolution. In particular, the fusion of a sex chromosome and an autosome has been proposed as a mechanism to resolve intralocus sexual antagonism. If sexual antagonism is common throughout the genome, we should expect to see an excess of fusions that join sex chromosomes and autosomes. Here, we present a null model that provides the probability of a sex chromosome autosome fusion, assuming all chromosomes have an equal probability of being involved in a fusion. This closed-form expression is applicable to both male and female heterogametic sex chromosome systems and can accommodate unequal proportions of fusions originating in males and females. We find that over 25% of all chromosomal fusions are expected to join a sex chromosome and an autosome whenever the diploid autosome count is fewer than 16, regardless of the sex chromosome system. We also demonstrate the utility of our model by analysing two contrasting empirical datasets: one from Drosophila and one from the jumping spider genus Habronattus. We find that in the case of Habronattus, there is a significant excess of sex chromosome autosome fusions but that in Drosophila there are far fewer sex chromosome autosome fusions than would be expected under our null model.

A database of amphibian karyotypes.

One of the first characteristics that we learn about the genome of many species is the number of chromosomes it is divided among. Despite this, many questions regarding the evolution of chromosome number remain unanswered. Testing hypotheses of chromosome number evolution using comparative approaches requires trait data to be readily accessible and associated with currently accepted taxonomy. The lack of accessible karyotype data that can be linked to phylogenies has limited the application of comparative approaches that could help us understand the evolution of genome structure. Furthermore, for taxonomists, the significance of new karyotype data can only be determined with reference to records for other species. Here, we describe a curated database (karyotype.org) developed to facilitate access to chromosome number and sex chromosome system data for amphibians. The open web interface for this database allows users to generate customized exploratory plots and tables of selected clades, as well as downloading CSV files for offline analyses.

Ghosts of a Structured Past: Impacts of Ancestral Patterns of Isolation-by-Distance on Divergence-Time Estimation.

Isolation-by-distance is a widespread pattern in nature that describes the reduction of genetic correlation between subpopulations with increased geographic distance. In the population ancestral to modern sister species, this pattern may hypothetically inflate population divergence time estimation due to allele frequency differences in subpopulations at the ends of the ancestral population. In this study, we analyze the relationship between the time to the most recent common ancestor and the population divergence time when the ancestral population model is a linear stepping-stone. Using coalescent simulations, we compare the coalescent time to the population divergence time for various ratios of the divergence time over the population size. Next, we simulate whole genomes to obtain single nucleotide polymorphisms (SNPs), and use the Bayesian coalescent program SNAPP to estimate divergence times. We find that as the rate of migration between neighboring demes decreases, the coalescent time becomes significantly greater than the population divergence time when sampled from end demes. Divergence-time overestimation in SNAPP becomes severe when the divergence-to-population size ratio < 10 and migration is low. Finally, we demonstrate the impact of ancestral isolation-by-distance on divergence-time estimation using an empirical dataset of squamates (Tropidurus) endemic to Brazil. We conclude that studies estimating divergence times should be cognizant of the potential ancestral population structure in an explicitly spatial context or risk dramatically overestimating the timing of population splits.

The March of the Beetles: Epistatic Components Dominate Divergence in Dispersal Tendency in Tribolium castaneum.

The genetic underpinnings of traits are rarely simple. Most traits of interest are instead the product of multiple genes acting in concert to determine the phenotype. This is particularly true for behavioral traits, like dispersal. Our investigation focuses on the genetic architecture of dispersal tendency in the red flour beetle, Tribolium castaneum. We used artificial selection to generate lines with either high or low dispersal tendency. Our populations responded quickly in the first generations of selection and almost all replicates had higher dispersal tendency in males than in females. These selection lines were used to create a total of 6 additional lines: F1 and reciprocal F1, as well as 4 types of backcrosses. We estimated the composite genetic effects that contribute to divergence in dispersal tendency among lines using line cross-analysis. We found variation in the dispersal tendency of our lines was best explained by autosomal additive and 3 epistatic components. Our results indicate that dispersal tendency is heritable, but much of the divergence in our selection lines was due to epistatic effects. These results are consistent with other life-history traits that are predicted to maintain more epistatic variance than additive variance and highlight the potential for epistatic variation to act as an adaptive reserve that may become visible to selection when a population is subdivided.

Inferring the potentially complex genetic architectures of adaptation, sexual dimorphism and genotype by environment interactions by partitioning of mean phenotypes.

Genetic architecture fundamentally affects the way that traits evolve. However, the mapping of genotype to phenotype includes complex interactions with the environment or even the sex of an organism that can modulate the expressed phenotype. Line-cross analysis is a powerful quantitative genetics method to infer genetic architecture by analysing the mean phenotype value of two diverged strains and a series of subsequent crosses and backcrosses. However, it has been difficult to account for complex interactions with the environment or sex within this framework. We have developed extensions to line-cross analysis that allow for gene by environment and gene by sex interactions. Using extensive simulation studies and reanalysis of empirical data, we show that our approach can account for both unintended environmental variation when crosses cannot be reared in a common garden and can be used to test for the presence of gene by environment or gene by sex interactions. In analyses that fail to account for environmental variation between crosses, we find that line-cross analysis has low power and high false-positive rates. However, we illustrate that accounting for environmental variation allows for the inference of adaptive divergence, and that accounting for sex differences in phenotypes allows practitioners to infer the genetic architecture of sexual dimorphism.

GppFst: genomic posterior predictive simulations of FST and dXY for identifying outlier loci from population genomic data.

Summary: We introduce GppFst, an open source R package that generates posterior predictive distributions of FST and dx under a neutral coalescent model to identify putative targets of selection from genomic data. Availability and Implementation: GppFst is available at ( https://github.com/radamsRHA/GppFst ). Contact: todd.castoe@uta.edu. Supplementary information: Supplementary data are available at Bioinformatics online.

Sex Determination, Sex Chromosomes, and Karyotype Evolution in Insects.

Insects harbor a tremendous diversity of sex determining mechanisms both within and between groups. For example, in some orders such as Hymenoptera, all members are haplodiploid, whereas Diptera contain species with homomorphic as well as male and female heterogametic sex chromosome systems or paternal genome elimination. We have established a large database on karyotypes and sex chromosomes in insects, containing information on over 13000 species covering 29 orders of insects. This database constitutes a unique starting point to report phylogenetic patterns on the distribution of sex determination mechanisms, sex chromosomes, and karyotypes among insects and allows us to test general theories on the evolutionary dynamics of karyotypes, sex chromosomes, and sex determination systems in a comparative framework. Phylogenetic analysis reveals that male heterogamety is the ancestral mode of sex determination in insects, and transitions to female heterogamety are extremely rare. Many insect orders harbor species with complex sex chromosomes, and gains and losses of the sex-limited chromosome are frequent in some groups. Haplodiploidy originated several times within insects, and parthenogenesis is rare but evolves frequently. Providing a single source to electronically access data previously distributed among more than 500 articles and books will not only accelerate analyses of the assembled data, but also provide a unique resource to guide research on which taxa are likely to be informative to address specific questions, for example, for genome sequencing projects or large-scale comparative studies.

The fragile Y hypothesis: Y chromosome aneuploidy as a selective pressure in sex chromosome and meiotic mechanism evolution.

Loss of the Y-chromosome is a common feature of species with chromosomal sex determination. However, our understanding of why some lineages frequently lose Y-chromosomes while others do not is limited. The fragile Y hypothesis proposes that in species with chiasmatic meiosis the rate of Y-chromosome aneuploidy and the size of the recombining region have a negative correlation. The fragile Y hypothesis provides a number of novel insights not possible under traditional models. Specifically, increased rates of Y aneuploidy may impose positive selection for (i) gene movement off the Y; (ii) translocations and fusions which expand the recombining region; and (iii) alternative meiotic segregation mechanisms (achiasmatic or asynaptic). These insights as well as existing evidence for the frequency of Y-chromosome aneuploidy raise doubt about the prospects for long-term retention of the human Y-chromosome despite recent evidence for stable gene content in older non-recombining regions.