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bioRxiv2021

The role of genus and life span in predicting seed and vegetative trait variation and correlation in Lathyrus, Phaseolus, and Vicia (Fabaceae)

PREMISE OF THE STUDYAnnual and perennial life history transitions are abundant among angiosperms, and understanding the phenotypic variation underlying life span shifts is a key endeavor of plant evolutionary biology. Comparative analyses of trait variation and correlation networks among annual and perennial plants is increasingly important as new perennial crops are being developed in a predominately annual-based agricultural setting. However, it remains unclear how seed to vegetative growth trait relationships may correlate with life span. METHODSWe measured 29 annual and perennial congeneric species of three herbaceous legume genera (Lathyrus, Phaseolus, and Vicia) for seed size and shape, germination proportion, and early vegetative height and leaf growth over three months in order to assess relative roles of genus and life span in predicting phenotypic variation and correlation. KEY RESULTSGenus was the greatest predictor of seed size and shape variation, while life span consistently predicted static vegetative growth traits. Correlation networks revealed that annual species had significant associations between seed traits and vegetative traits, while perennials had no significant seed-vegetative associations. Each genus also differed in the extent of integration between seed and vegetative traits, as well as within-vegetative trait correlation patterns. CONCLUSIONSGenus and life span were important for predicting aspects of early life stage phenotypic variation and trait relationships. Differences in phenotypic correlation may indicate selection on seed size traits will impact vegetative growth differently depending on life span, which has important implications for nascent perennial breeding programs.

plant biology↗

bioRxiv2021

Underground Heterosis for Melons Yield

Heterosis, the superiority of hybrids over their parents, is a major genetic force associated with plant fitness and crop yield enhancement. Understanding and predicting heterosis is crucial for evolutionary biology, as well as for plant and animal breeding. We investigated root-mediated yield heterosis in melons (Cucumis melo) by characterizing common variety grafted onto 190 hybrid rootstocks resulting from crossing 20 diverse inbreds in a diallel-mating scheme. Hybrid rootstocks improved yield by more than 40% compared to their parents and the best hybrid outperformed the reference commercial variety by 65% under both optimal and minimal irrigation treatments. To characterize the genetics of the underground heterosis we conducted whole-genome re-sequencing of the 20 founder lines, and showed that parental genetic distance was no predictor for the level of heterosis. Through inference of the 190 hybrids genotypes from their parental genomes, followed by genome-wide association analysis, we mapped multiple root-mediated yield QTLs. The yield enhancement of the four best-performing hybrid rootstocks was validated in multiple experiments with four different scion varieties. While root biology is receiving increased attention, most of the research is conducted using plants not amenable to grafting and, as a result, it is difficult to separate root and shoot effects. Here, we use the rich genetic and genomic resources of Cucumis melo, where grafting is a common practice, to dissect a unique phenomenon of root-mediated yield heterosis, by directly evaluating in the field the contribution of the roots to fruit yield. Our grafting approach is inverted to the common roots genetics research path that focuses mainly on variation in root system architecture rather than the ultimate root-mediated whole-plant performance, and is a step towards discovery of candidate genes involved in root function and yield enhancement. HighlightWe show that yield heterosis is significant in melon and controlled independently above and underground. Using common-scion grafting approach, we find that heritable rootstock-mediated variation in a diallel population is associated with substantial fruit yield heterosis.

plant biology↗

bioRxiv2021

Developmental innovations promote species diversification in mushroom-forming fungi

Fungi evolved complex fruiting body ( mushroom) morphologies as adaptations to efficient spore dispersal in terrestrial habitats. Mushroom-forming fungi (Agaricomycetes) display a graded series of developmental innovations related to fruiting body morphology, however, how these evolved is largely unknown, leaving the functional biology and evolutionary principles of complex multicellularity in the third largest multicellular kingdom poorly known. Here, we show that developmental innovations of mushroom-forming fungi that enclose the spore-producing surface (hymenophore) in a protected environment display significant asymmetry in their evolution and are associated with increased diversification rates. Enclosed development and related tissues (partial and universal veils) evolved convergently and became a widespread developmental type in clades in which it emerged. This probably mirrors increased fitness for protected fruiting body initials in terrestrial habitats, by better coping with environmental factors such as desiccation or predators, among others. We observed similar patterns in the evolution of complex hymenophore architectures, such as gills, pores or teeth, which optimize biomass-to-propagule number ratios and were found to spur diversification in mushrooms. Taken together, our results highlight new morphological traits associated with the adaptive radiation of mushroom-forming fungi and present formal phylogenetic testing of hypotheses on the reproductive ecology of a poorly known but hyperdiverse clade.

evolutionary biology↗

bioRxiv2021

Chromosome-level genome assembly of Acanthopagrus latus using PacBio and Hi-C technologies

The yellowfin seabream, Acanthopagrus latus, is widely distributed throughout the Indo-West Pacific. This fish is an ideal model species in which to study the mechanism of sex reversal since it exhibits a specific feature: sequential hermaphrodite. Here, we report a chromosome-scale assembly of the A. latus based on PacBio and Hi-C data. 22,485 protein-coding genes were annotated in whole genome level using transcriptome data. Taken together, this highly accurate, chromosome-level reference genome can provide a valuable resource to elucidate the mechanism of sex reversal for A. latus. Background & SummaryEvolution of sex, especially the evolution of different sexual systems, is a fascinating subject in evolutionary biology. The Sparidae, commonly known as seabreams or progies, is a family of fishes of the order Perciformes. And this family consist about 150 species in the world, which are mainly coastal fish1. Previous researchers mentioned that Sparidae is an ideal taxon to study the evolution history and adaptive significance of sexual systems, particularly for both types of sequential hermaphroditism, given that this group contains many protogyny, protandry and genochorist species2. The yellowfin seabream, Acanthopagrus latus is a protandry species which belongs to the Sparidae family. It is widely distributed in Indo-West Pacific area3. It has a great relevance for marine aquaculture and its biology is well focused on reproductive physiology and nutrition4. Interestingly, A. latus has a special gender feature is that it belongs to protandrous sexual system (initially as male and change later to female)5. Most of the past studies of A. latus mainly focused on the reproductive biology, population structure, aquaculture and taxonomy3,4,6-8. Although some sex reversal related genes were found in A. latus, the lack of genomic resources still limit us to elucidate the mechanism of sex reversal for this species.9,10. In addition, this lack was also limited the studies of evolution of sexual systems for Sparidae. In this study, long-read (PacBio SMRT) sequencing and Hi-C sequencing technologies were applied to construct a high quality reference genome for yellowfin seabream. This high-quality genome can provide a valuable resource to elucidate the mechanism of sex reversal for A. latus. Furthermore, this genome can also facilitate the studies of evolution of sexual systems for Sparidae.

genomics↗

bioRxiv2021

Fauxcurrence: simulating multi-species occurrences for null models in species distribution modelling and biogeography

Defining appropriate null expectations for species distribution hypotheses is important because sampling bias and spatial autocorrelation can produce realistic, but ecologically meaningless, geographic patterns. Generating null species occurrences with similar spatial structure to observed data can help overcome these problems, but existing methods focus on single or pairs of species and do not incorporate between-species spatial structure that may occlude comparative biogeographic analyses. Here, we describe an algorithm for generating randomised species occurrence points that mimic the within- and between-species spatial structure of real datasets and implement it in a new R package - fauxcurrence. The algorithm can be implemented on any geographic domain for any number of species, limited only by computing power. To demonstrate its utility, we apply the algorithm to two common analysis-types: testing the fit of species distribution models (SDMs) and evaluating niche-overlap. The method works well on all tested datasets within reasonable timescales. We found that many SDMs, despite a good fit to the data, were not significantly better than null expectations and identified only two cases (out of a possible 32) of significantly higher niche divergence than expected by chance. The package is user-friendly, flexible and has many potential applications beyond those tested here, such as joint SDM evaluation and species co-occurrence analysis, spanning the areas of ecology, evolutionary biology and biogeography.

ecology↗

bioRxiv2021

Natural selection does not affect the estimates of effective population size based on linkage disequilibrium

The effective population size (Ne) is a key parameter to quantify the magnitude of genetic drift and inbreeding, with important implications in human evolution. The increasing availability of high-density genetic markers allows the estimation of historical changes in Ne across time using measures of genome diversity or linkage disequilibrium between markers. Selection is expected to reduce diversity and Ne, and this reduction is modulated by the heterogeneity of the genome in terms of recombination rate. Here we investigate by computer simulations the consequences of selection (both positive and negative) and of recombination rate heterogeneity in the estimation of historical Ne. We also investigate the relationship between diversity parameters and Ne across the different regions of the genome using human marker data. We show that the estimates of historical Ne obtained from linkage disequilibrium between markers (NeLD) are virtually unaffected by selection. In contrast, those estimates obtained by coalescence mutation-recombination-based methods can be strongly affected by it, what could have important consequences for the estimation of human demography. The simulation results are supported by the analysis of human data. The estimates of NeLD obtained for particular genomic regions do not correlate with recombination rate, nucleotide diversity, polymorphism, background selection statistic, minor allele frequency of SNPs, loss of function and missense variants and gene density. This suggests that NeLD measures are merely indicative of demographic changes in population size across generations. Author summaryThe inference of the demographic history of populations is of great relevance in evolutionary biology. This inference can be made from genomic data using coalescence methods or linkage disequilibrium methods. However, the assessment of these methods is usually made assuming neutrality (absence of selection). Here we show by computer simulations and analyses of human data that the estimates of historical effective population size obtained from linkage disequilibrium between markers are unaffected by natural selection, either positive or negative. In contrast, estimates obtained by coalescence mutation-recombination-based methods can be strongly affected by it, which could have important consequences for recent estimations of human demography. Thus, only linkage disequilibrium methods appear to provide unbiased estimates of the population census size.

genetics↗

bioRxiv2021

Learning the local landscape of protein structures with convolutional neural networks

The fundamental problem of protein biochemistry is to predict protein structure from amino acid sequence. The inverse problem, predicting either entire sequences or individual mutations that are consistent with a given protein structure, has received much less attention even though it has important applications in both protein engineering and evolutionary biology. Here, we ask whether 3D convolutional neural networks (3D CNNs) can learn the local fitness landscape of protein structure to reliably predict either the wild-type amino acid or the consensus in a multiple sequence alignment from the local structural context surrounding a site of interest. We find that the network can predict wild type with good accuracy, and that network confidence is a reliable measure of whether a given prediction is likely going to be correct or not. Predictions of consensus are less accurate, and are primarily driven by whether or not the consensus matches the wild type. Our work suggests that high-confidence mis-predictions of the wild type may identify sites that are primed for mutation and likely targets for protein engineering.

bioinformatics↗

bioRxiv2021

phylogatR: Phylogeographic data aggregation and repurposing

Patterns of genetic diversity within species contain information about the history of that species, including how they have responded to historical climate change and how easily the organism is able to disperse across its habitat. More than 40,000 phylogeographic and population genetic investigations have been published to date, each collecting genetic data from hundreds of samples. Despite these millions of data points, meta-analyses are challenging because the synthesis of results across hundreds of studies, each using different methods and forms of analysis, is a daunting and time-consuming task. It is more efficient to proceed by repurposing existing data and using automated data analysis. To facilitate data repurposing, we created a database (phylogatR) that aggregates data from different sources and conducts automated multiple sequence alignments and data curation to provide users with nearly ready-to-analyze sets of data for thousands of species. Two types of scientific research will be made easier by phylogatR, large meta-analyses of thousands of species that can address classic questions in evolutionary biology and ecology and student- or citizen-science based investigations that will introduce a broad range of people to the analysis of genetic data. phylogatR enhances the value of existing data via the creation of software and web-based tools that enable these data to be recycled and reanalyzed and increase accessibility to big data for research labs and classroom instructors with limited computational expertise and resources.

bioinformatics↗

bioRxiv2021

Molecular mechanisms governing circulating immune cell heterogeneity across different species revealed by single cell sequencing

BackgroundImmune cells play important roles in mediating immune response and host defense against invading pathogens. However, insights into the molecular mechanisms governing circulating immune cell diversity among multiple species are limited. MethodsIn this study, we compared the single-cell transcriptomes of 77{square}957 immune cells from 12 species using single-cell RNA-sequencing (scRNA-seq). Distinct molecular profiles were characterized for different immune cell types, including T cells, B cells, natural killer cells, monocytes, and dendritic cells. ResultsResults revealed the heterogeneity and compositions of circulating immune cells among 12 different species. Additionally, we explored the conserved and divergent cellular crosstalk and genetic regulatory networks among vertebrate immune cells. Notably, the ligand and receptor pair VIM-CD44 was highly conserved among the immune cells. ConclusionsThis study is the first to provide a comprehensive analysis of the cross-species single-cell atlas for peripheral blood mononuclear cells (PBMCs). This research should advance our understanding of the cellular taxonomy and fundamental functions of PBMCs, with important implications in evolutionary biology, developmental biology, and immune system disorders.

cell biology↗

bioRxiv2022

The First High-Quality Genome Assembly and Data Analysis of the Malaysian mahseer (Tor tambroides)

The Malaysian mahseer (Tor tambroides), one of the most valuable freshwater fish in the world, is mainly targeted for human consumption. The mitogenomic data of this species is available to date, but the genomic information is still lacking. For the first time, we sequenced the whole genome of an adult fish on both Illumina and Nanopore platforms. The hybrid genome assembly had resulted in a sum of 1.5 Gb genomic sequence from the 44,726 contigs found with 44 kb N50 length and BUSCO genome completeness of 84.3%. Four types of SSRs had been detected and identified within the genome with a greater AT abundance than that of GC. Predicted protein sequences had been functionally annotated to public databases, namely GO, KEGG and COG. A maximum likelihood phylogenomic tree containing 53 Actinopterygii species and two outgroups was constructed, providing first insights into the genome-based evolutionary relationship of T. tambroides with other ray-finned fish. These data are crucial in facilitating the study of population genomics, species identification, morphological variations, and evolutionary biology, which are helpful in the conservation of this species.

genomics↗

bioRxiv2022

NGSEP 4: Efficient and Accurate Identification of Orthogroups and Whole Genome Alignment

Whole-genome alignment allows researchers to understand the genomic structure and variations among the genomes. Approaches based on direct pairwise comparisons of DNA sequences require large computational capacities. As a consequence, pipelines combining tools for orthologous gene identification and synteny have been developed. In this manuscript, we present the latest functionalities implemented in NGSEP 4, to identify orthogroups and perform whole genome alignments. NGSEP implements functionalities for identification of clusters of homologus genes, synteny analysis and whole genome alignment, and visualization. Our results showed that the NGSEP algorithm for ortholog identification has competitive accuracy and better efficiency in comparison to commonly used tools. The implementation also includes a visualization of the whole genome alignment based on synteny of the orthogroups that were identified, and a reconstruction of the pangenome based on frequencies of the orthogroups among the genomes. Finally, our software includes a new graphical user interface. We expect that these new developments will be very useful for several studies in evolutionary biology and population genomics.

bioinformatics↗

bioRxiv2022

Mineralized coleoid cranial cartilage from the Late Triassic Polzberg Konservat-Lagerstätte (Austria)

Although hyaline cartilage is widely distributed in various invertebrate groups such as sabellid polychaetes, molluscs (cephalopods, gastropods) and a chelicerate arthropod group (horseshoe crabs), the enigmatic relationship and distribution of cartilage in taxonomic groups remains to be explained. It can be interpreted as a convergent trait in animal evolution and thus does not seem to be a vertebrate invention. Due to the poor fossil record of cartilaginous structures, occurrences of mineralized fossil cartilages are important for evolutionary biology and paleontology. Although the biochemical composition of recent cephalopod cartilage differs from vertebrate cartilage, histologically the cartilages of these animal groups resemble one another remarkably. In this study we present fossil material from the late Triassic Polzberg Konservat-Lagerstatte near Lunz am See (Lower Austria, Northern Calcareous Alps). A rich Carnian fauna is preserved here, whereby a morphogroup (often associated with coleoid remains) of black, amorphous appearing fossils still remained undetermined. These multi-elemental, mirroring fossils show remarkable similarities to recent cephalopod cartilage. We examined the conspicuous micro- and ultrastructure of these enigmatic fossils by thin-sectioning and Scanning Electron Microscopy (SEM). The geochemical composition analyzed by Microprobe and Energy Dispersive X-ray Spectroscopy (SEM-EDX) revealed carbonisation as the taphonomic pathway for this fossil group. 3D preservation of this otherwise degradable soft tissue can be explained by the mineralization processes that may take place in particular environments. Fifty-nine specimens from the Polzberg locality and five specimens from Cave del Predil (formerly Raibl, Julian Alps, Italy) underwent extensive studies. The detected grooves are interpreted to be muscular attachment areas, and the preserved branched system of canaliculi is comparable to a channel system that is also present in recent coleoid cartilage. The new findings on these long-known enigmatic structures strongly point to the preservation of cranial cartilage belonging to the belemnoid Phragmoteuthis bisinuata.

paleontology↗

bioRxiv2022

Population structure and inbreeding in wild house mice (Mus musculus) at different geographic scales

House mice (Mus musculus) have spread globally as a result of their commensal relationship with humans. In the form of laboratory strains, both inbred and outbred, they are also among the most widely-used model organisms in biomedical research. Although the general outlines of house mouse dispersal and population structure are well known, details have been obscured by either limited sample size or small numbers of markers. Here we examine ancestry, population structure and inbreeding using SNP microarray genotypes in a cohort of 814 wild mice spanning five continents and all major subspecies of Mus, with a focus on M. m. domesticus. We find that the major axis of genetic variation in M. m. domesticus is a south-to-north gradient within Europe and the Mediterranean. The dominant ancestry component in North America, Australia, New Zealand and various small offshore islands is of northern European origin. Next we show that inbreeding is surprisingly pervasive and highly variable, even between nearby populations. By inspecting the length distribution of homozygous segments in individual genomes, we find that inbreeding in commensal populations is mostly due to consanguinity. Our results offer new insight into the natural history of an important model organism for medicine and evolutionary biology.

genetics↗

bioRxiv2022

Rpadrino: an R package to access and use PADRINO, an open access database of Integral Projection Models

O_LIDiscrete time structured population projection models are an important tool for studying population dynamics. Within this field, Integral Projection Models (IPMs) have become a popular method for studying populations structured by continuously distributed traits (e.g. height, weight). Databases of discrete time, discrete state structured population models, for example DATLife (life tables) and COMPADRE & COMADRE (matrix population models), have made quantitative syntheses straightforward to implement. These efforts allow researchers to address questions in both basic and applied ecology and evolutionary biology. There are now over 300 peer-reviewed publications containing IPMs. We describe a novel framework to quickly reconstruct these models for subsequent analyses using Rpadrino R package, which serves as an interface to PADRINO, a new database of structured population models. C_LIO_LIWe introduce an R package, Rpadrino, which enables users to download, subset, reconstruct, and extend published IPMs. Rpadrino makes use of recently created software, ipmr, to provide an engine to reconstruct a wide array of IPMs from their symbolic representations and conduct subsequent analyses. Rpadrino and ipmr are extensively documented to help users learn their usage. C_LIO_LIRpadrino currently enables users to reconstruct 280 IPMs from 40 publications that describe the demography of 14 animal and 26 plant species. All of these IPMs are tested to ensure they reproduce published estimates. Rpadrino provides an interface to augment PADRINO with external data and modify parameter values, creating a platform to extend models beyond their original purpose while retaining full reproducibility. C_LIO_LIPADRINO and Rpadrino provide a toolbox for asking new questions and conducting syntheses with peer-reviewed published IPMs. Rpadrino provides a user-friendly interface so researchers do not need to worry about the database structure or syntax, and can focus on their research questions and analyses. Additionally, Rpadrino is thoroughly documented, and provides numerous examples of how to perform analyses which are not included in the packages functionality. C_LI

ecology↗

bioRxiv2022

Web-based Histology Reference Atlas for the Freshwater Crustacean Daphnia magna

Daphnia are keystone species of freshwater habitats used as model organisms in ecology and evolutionary biology. Their small size, wide geographic distribution, and sensitivity to chemicals make them useful as environmental sentinels in regulatory toxicology and chemical risk assessment. Biomolecular (-omic) assessments of responses to chemical toxicity, which reveal detailed molecular signatures, become more powerful when correlated with other phenotypic outcomes (such as behavioral, physiological, or histopathological) for comparative validation and regulatory relevance. However, the lack of histopathology or tissue phenotype characterization of this species presently limits our ability to access cellular mechanisms of toxicity. Here, we address the central concept that interpreting aberrant tissue phenotypes requires a basic understanding of species normal microanatomy. We introduce the female and male Daphnia Histology Reference Atlas (DaHRA) for the baseline knowledge of Daphnia magna microanatomy. Additionally, we also included developmental stages of female Daphnia in this current atlas. This interactive web-based resource of adult Daphnia features overlaid vectorized demarcation of anatomical structures whose labels comply with an anatomical ontology created for this atlas. We demonstrate the potential utility of DaHRA for toxicological investigations by presenting aberrant phenotypes of acetaminophen-exposed D. magna. We envision DaHRA to facilitate the effort of integrating molecular and phenotypic data from the scientific community as we seek to understand how genes, chemicals, and environment interactions determine organismal phenotype.

zoology↗

bioRxiv2022

Dominance vs. epistasis: the biophysical origins and plasticity of genetic interactions within and between alleles

A central challenge in genetics, evolutionary biology and biotechnology is to understand and predict how mutations combine to alter phenotypes, including molecular activities, fitness and disease. In diploid organisms, two mutations in the same gene can either combine on the same chromosome or on different chromosomes, with interactions between the mutations quantified as epistasis and dominance, respectively. However, a direct comparison of the extent, sign and stability of interactions within and between alleles is lacking. Here we show that, even in the simplest biophysical systems, interactions between mutations are frequent, context-dependent and different when variants are combined within and between alleles. Whereas protein folding alone generates epistasis, the addition of a single molecular interaction is sufficient to cause dominance. Epistasis and dominance interactions change quantitatively, qualitatively and differently as a system becomes more complicated or the conditions change. Altering the concentration of a ligand can, for example, switch an allele from dominant to recessive. Our results show that epistasis and dominance should be widely expected in even the simplest biological systems but also reinforce the view that they are plastic system properties and so a formidable challenge to predict. Accurate prediction of epistasis and dominance will require either detailed mechanistic understanding and experimental parameterization or brute-force measurement and learning.

genetics↗

bioRxiv2022

The history and organization of the Workshop on Population and Speciation Genomics

With the advent of high-throughput genome sequencing, bioinformatics training has become essential for research in evolutionary biology and related fields. However, individual research groups are often not in the position to teach students about the most up-to-date methodology in the field. To fill this gap, extended bioinformatics courses have been developed by various institutions and provide intense training over the course of two or more weeks. Here, we describe our experience with the organization of a course in one of the longest-running extended bioinformatics series of work-shops, the Evomics Workshop on Population and Speciation Genomics that takes place biennially in the UNESCO world heritage town of [C]esky Krumlov, Czech Republic. We list the key ingredients that make this workshop successful in our view, and describe the routine for workshop organization that we have optimized over the years. We report the results of a survey conducted among past workshop participants that quantifies measures of effective teaching and provide examples of how the workshop setting has led to the cross-fertilisation of ideas and ultimately scientific progress. We expect that our account may be useful for other groups aiming to set up their own extended bioinformatics courses.

scientific communication and education↗

bioRxiv2022

Genome dynamics in mosses: Extensive synteny coexists with a highly dynamic gene space

BackgroundWhile genome evolutionary processes of seed plants are intensively investigated, very little is known about seed-free plants in this respect. Here, we use one of the largest groups of seed-free plants, the mosses, and newly generated chromosome-scale genome assemblies to investigate three poorly known aspects of genome dynamics and their underlying processes in seed-free plants: (i) genome size variation, (ii) genomic collinearity/synteny, and (iii) gene set differentiation. ResultsComparative genomic analyses on the model moss Physcomitrium (Physcomitrella) patens and two genomes of Funaria hygrometrica reveal that, like in seed plants, genome size change (approx. 140 Mbp) is primarily due to transposable element expansion/contraction. Despite 60 million years of divergence, the genomes of P. patens and F. hygrometrica show remarkable chromosomal stability with the majority of homologous genes located in conserved collinear blocks. In addition, both genomes contain a relatively large set of lineage-specific genes with no detectible homologs in the other species genome, suggesting a highly dynamic gene space fueled by the process of de novo gene birth and loss rather than by gene family diversification/duplication. ConclusionsThese, combined with previous observations suggest that genome dynamics in mosses involves the coexistence of a collinear homologous and a highly dynamic species-specific gene sets. Besides its significance for understanding genome evolution, the presented chromosome-scale genome assemblies will provide a foundation for comparative genomic and functional studies in the Funariaceae, a family holding historical and contemporary model taxa in the evolutionary biology of mosses.

genomics↗