Evolution of life cycles and reproductive traits: Insights from the brown algae.

A vast diversity of types of life cycles exists in nature, and several theories have been advanced to explain how this diversity has evolved and how each type of life cycle is retained over evolutionary time. Here, we exploited the diversity of life cycles and reproductive traits of the brown algae (Phaeophyceae) to test several hypotheses on the evolution of life cycles. We investigated the evolutionary dynamics of four life-history traits: life cycle, sexual system, level of gamete dimorphism and gamete parthenogenetic capacity. We assigned states to up to 77 representative species of the taxonomic diversity of the brown algal group, in a multi-gene phylogeny. We used maximum likelihood and Bayesian analyses of correlated evolution, while taking the phylogeny into account, to test for correlations between traits and to investigate the chronological sequence of trait acquisition. Our analyses are consistent with the prediction that diploid growth evolves when sexual reproduction is preferred over asexual reproduction, possibly because it allows the complementation of deleterious mutations. We also found that haploid sex determination is ancestral in relation to diploid sex determination. However, our results could not address whether increased zygotic and diploid growth are associated with increased sexual dimorphism. Our analyses suggest that in the brown algae, isogamous species evolved from anisogamous ancestors, contrary to the commonly reported pattern where evolution proceeds from isogamy to anisogamy.

Population genomics of Vibrionaceae isolated from an endangered oasis reveals local adaptation after an environmental perturbation.

BACKGROUND: In bacteria, pan-genomes are the result of an evolutionary "tug of war" between selection and horizontal gene transfer (HGT). High rates of HGT increase the genetic pool and the effective population size (Ne), resulting in open pan-genomes. In contrast, selective pressures can lead to local adaptation by purging the variation introduced by HGT and mutation, resulting in closed pan-genomes and clonal lineages. In this study, we explored both hypotheses, elucidating the pan-genome of Vibrionaceae isolates after a perturbation event in the endangered oasis of Cuatro Ciénegas Basin (CCB), Mexico, and looking for signals of adaptation to the environments in their genomes. RESULTS: We obtained 42 genomes of Vibrionaceae distributed in six lineages, two of them did not showed any close reference strain in databases. Five of the lineages showed closed pan-genomes and were associated to either water or sediment environment; their high Ne estimates suggest that these lineages are not from a recent origin. The only clade with an open pan-genome was found in both environments and was formed by ten genetic groups with low Ne, suggesting a recent origin. The recombination and mutation estimators (r/m) ranged from 0.005 to 2.725, which are similar to oceanic Vibrionaceae estimations. However, we identified 367 gene families with signals of positive selection, most of them found in the core genome; suggesting that despite recombination, natural selection moves the Vibrionaceae CCB lineages to local adaptation, purging the genomes and keeping closed pan-genome patterns. Moreover, we identify 598 SNPs associated with an unstructured environment; some of the genes associated with these SNPs were related to sodium transport. CONCLUSIONS: Different lines of evidence suggest that the sampled Vibrionaceae, are part of the rare biosphere usually living under famine conditions. Two of these lineages were reported for the first time. Most Vibrionaceae lineages of CCB are adapted to their micro-habitats rather than to the sampled environments. This pattern of adaptation is concordant with the association of closed pan-genomes and local adaptation.

Evolutionary Dynamics of Transferred Sequences Between Organellar Genomes in Cucurbita.

Twenty-nine DNA regions of plastid origin have been previously identified in the mitochondrial genome of Cucurbita pepo (pumpkin; Cucurbitaceae). Four of these regions harbor homolog sequences of rbcL, matK, rpl20-rps12 and trnL-trnF, which are widely used as molecular markers for phylogenetic and phylogeographic studies. We extracted the mitochondrial copies of these regions based on the mitochondrial genome of C. pepo and, along with published sequences for these plastome markers from 13 Cucurbita taxa, we performed phylogenetic molecular analyses to identify inter-organellar transfer events in the Cucurbita phylogeny and changes in their nucleotide substitution rates. Phylogenetic reconstruction and tree selection tests suggest that rpl20 and rbcL mitochondrial paralogs arose before Cucurbita diversification whereas the mitochondrial matK and trnL-trnF paralogs emerged most probably later, in the mesophytic Cucurbita clade. Nucleotide substitution rates increased one order of magnitude in all the mitochondrial paralogs compared to their original plastid sequences. Additionally, mitochondrial trnL-trnF sequences obtained by PCR from nine Cucurbita taxa revealed higher nucleotide diversity in the mitochondrial than in the plastid copies, likely related to the higher nucleotide substitution rates in the mitochondrial region and loss of functional constraints in its tRNA genes.

Historical biogeography and phylogeny of Cucurbita: Insights from ancestral area reconstruction and niche evolution.

Knowledge of the role of geographical and ecological events associated to the divergence process of wild progenitors is important to understand the process of domestication. We analysed the temporal, spatial and ecological patterns of the diversification of Cucurbita, an American genus of worldwide economic importance. We conducted a phylogenetic analysis based on six chloroplast regions (5907 bp) to estimate diversification rates and dates of divergence between taxa. This is the first phylogenetic study to include C. radicans, a wild species that is endemic to the Trans Mexican Volcanic Belt. We performed analysis of ancestral area reconstruction and paleoreconstructions of species distribution models to understand shifts in wild species ranges. We used principal component analysis (PCA) and multivariate analysis of variance (MANOVA) to evaluate the environmental differentiation among taxa within each clade. The phylogenetic analyses showed good support for at least six independent domestication events in Cucurbita. The genus Cucurbita showed a time of divergence of 11.24 Ma (6.88-17 Ma 95% HDP), and the dates of divergence between taxa within each group ranged from 0.35 to 6.58 Ma, being the divergence between C. lundelliana and C. okeechobeensis subsp. martinezii the most recent. The diversification rate of the genus was constant through time. The diversification of most wild taxa occurred during the Pleistocene, and its date of divergence is concordant with the dates of divergence reported for specialized bees of the genera Xenoglossa and Peponapis, suggesting a process of coevolution between Cucurbita and their main pollinators that should be further investigated. Tests of environmental differentiation together with ancestral area reconstruction and species distribution models past projections suggest that divergence was promoted by the onset of geographic barriers and secondary range contraction and by expansion related to glacial-interglacial cycles.

Rates of ecological divergence and body size evolution are correlated with species diversification in scaly tree ferns.

Variation in species richness across regions and between different groups of organisms is a major feature of evolution. Several factors have been proposed to explain these differences, including heterogeneity in the rates of species diversification and the age of clades. It has been frequently assumed that rapid rates of diversification are coupled to high rates of ecological and morphological evolution, leading to a prediction that remains poorly explored for most species: the positive association between ecological niche divergence, morphological evolution and species diversification. We combined a time-calibrated phylogeny with distribution, ecological and body size data for scaly tree ferns (Cyatheaceae) to test whether rates of species diversification are predicted by the rates at which clades have evolved distinct ecological niches and body sizes. We found that rates of species diversification are positively correlated with rates of ecological and morphological evolution, with rapidly diversifying clades also showing rapidly evolving ecological niches and body sizes. Our results show that rapid diversification of scaly tree ferns is associated with the evolution of species with comparable morphologies that diversified into similar, yet distinct, environments. This suggests parallel evolutionary pathways opening in different tropical regions whenever ecological and geographical opportunities arise. Accordingly, rates of ecological niche and body size evolution are relevant to explain the current patterns of species richness in this 'ancient' fern lineage across the tropics.

Repeated co-option of HMG-box genes for sex determination in brown algae and animals.

In many eukaryotes, genetic sex determination is not governed by XX/XY or ZW/ZZ systems but by a specialized region on the poorly studied U (female) or V (male) sex chromosomes. Previous studies have hinted at the existence of a dominant male-sex factor on the V chromosome in brown algae, a group of multicellular eukaryotes distantly related to animals and plants. The nature of this factor has remained elusive. Here, we demonstrate that an HMG-box gene acts as the male-determining factor in brown algae, mirroring the role HMG-box genes play in sex determination in animals. Over a billion-year evolutionary timeline, these lineages have independently co-opted the HMG box for male determination, representing a paradigm for evolution's ability to recurrently use the same genetic "toolkit" to accomplish similar tasks.

Uncovering gene-family founder events during major evolutionary transitions in animals, plants and fungi using GenEra.

We present GenEra ( https://github.com/josuebarrera/GenEra ), a DIAMOND-fueled gene-family founder inference framework that addresses previously raised limitations and biases in genomic phylostratigraphy, such as homology detection failure. GenEra also reduces computational time from several months to a few days for any genome of interest. We analyze the emergence of taxonomically restricted gene families during major evolutionary transitions in plants, animals, and fungi. Our results indicate that the impact of homology detection failure on inferred patterns of gene emergence is lineage-dependent, suggesting that plants are more prone to evolve novelty through the emergence of new genes compared to animals and fungi.

A highly contiguous genome assembly reveals sources of genomic novelty in the symbiotic fungus Rhizophagus irregularis.

The root systems of most plant species are aided by the soil-foraging capacities of symbiotic arbuscular mycorrhizal (AM) fungi of the Glomeromycotina subphylum. Despite recent advances in our knowledge of the ecology and molecular biology of this mutualistic symbiosis, our understanding of the AM fungi genome biology is just emerging. Presented here is a close to T2T genome assembly of the model AM fungus Rhizophagus irregularis DAOM197198, achieved through Nanopore long-read DNA sequencing and Hi-C data. This haploid genome assembly of R. irregularis, alongside short- and long-read RNA-Sequencing data, was used to produce a comprehensive annotation catalog of gene models, repetitive elements, small RNA loci, and DNA cytosine methylome. A phylostratigraphic gene age inference framework revealed that the birth of genes associated with nutrient transporter activity and transmembrane ion transport systems predates the emergence of Glomeromycotina. While nutrient cycling in AM fungi relies on genes that existed in ancestor lineages, a burst of Glomeromycotina-restricted genetic innovation is also detected. Analysis of the chromosomal distribution of genetic and epigenetic features highlights evolutionarily young genomic regions that produce abundant small RNAs, suggesting active RNA-based monitoring of genetic sequences surrounding recently evolved genes. This chromosome-scale view of the genome of an AM fungus genome reveals previously unexplored sources of genomic novelty in an organism evolving under an obligate symbiotic life cycle.

Population Genomics of Domesticated Cucurbita ficifolia Reveals a Recent Bottleneck and Low Gene Flow with Wild Relatives.

Cucurbita ficifolia is a squash grown from Mexico to Bolivia. Its ancestor is unknown, but it has limited compatibility with wild xerophytic Cucurbita from Mexico's highlands. We assembled the reference genome of C. ficifolia and assessed the genetic diversity and historical demography of the crop in Mexico with 2524 nuclear single nucleotide polymorphisms (SNPs). We also evaluated the gene flow between C. ficifolia and xerophytic taxa with 6292 nuclear and 440 plastome SNPs from 142 individuals sampled in 58 sites across their area of sympatry. Demographic modelling of C. ficifolia supports an eight-fold decrease in effective population size at about 2409 generations ago (95% CI = 464-12,393), whereas plastome SNPs support the expansion of maternal lineages ca. 1906-3635 years ago. Our results suggest a recent spread of C. ficifolia in Mexico, with high genetic diversity (π = 0.225, FST = 0.074) and inbreeding (FIS = 0.233). Coalescent models suggest low rates of gene flow with C. radicans and C. pedatifolia, whereas ABBA-BABA tests did not detect significant gene flow with wild taxa. Despite the ecogeographic proximity of C. ficifolia and its relatives, this crop persists as a highly isolated lineage of puzzling origin.

The domestication of Cucurbita argyrosperma as revealed by the genome of its wild relative.

Despite their economic importance and well-characterized domestication syndrome, the genomic impact of domestication and the identification of variants underlying the domestication traits in Cucurbita species (pumpkins and squashes) is currently lacking. Cucurbita argyrosperma, also known as cushaw pumpkin or silver-seed gourd, is a Mexican crop consumed primarily for its seeds rather than fruit flesh. This makes it a good model to study Cucurbita domestication, as seeds were an essential component of early Mesoamerican diet and likely the first targets of human-guided selection in pumpkins and squashes. We obtained population-level data using tunable Genotype by Sequencing libraries for 192 individuals of the wild and domesticated subspecies of C. argyrosperma across Mexico. We also assembled the first high-quality wild Cucurbita genome. Comparative genomic analyses revealed several structural variants and presence/absence of genes related to domestication. Our results indicate a monophyletic origin of this domesticated crop in the lowlands of Jalisco. We found evidence of gene flow between the domesticated and wild subspecies, which likely alleviated the effects of the domestication bottleneck. We uncovered candidate domestication genes that are involved in the regulation of growth hormones, plant defense mechanisms, seed development, and germination. The presence of shared selected alleles with the closely related species Cucurbita moschata suggests domestication-related introgression between both taxa.

Genomic, Transcriptomic and Epigenomic Tools to Study the Domestication of Plants and Animals: A Field Guide for Beginners.

In the last decade, genomics and the related fields of transcriptomics and epigenomics have revolutionized the study of the domestication process in plants and animals, leading to new discoveries and new unresolved questions. Given that some domesticated taxa have been more studied than others, the extent of genomic data can range from vast to nonexistent, depending on the domesticated taxon of interest. This review is meant as a rough guide for students and academics that want to start a domestication research project using modern genomic tools, as well as for researchers already conducting domestication studies that are interested in following a genomic approach and looking for alternate strategies (cheaper or more efficient) and future directions. We summarize the theoretical and technical background needed to carry out domestication genomics, starting from the acquisition of a reference genome and genome assembly, to the sampling design for population genomics, paleogenomics, transcriptomics, epigenomics and experimental validation of domestication-related genes. We also describe some examples of the aforementioned approaches and the relevant discoveries they made to understand the domestication of the studied taxa.

Genomic consequences of dietary diversification and parallel evolution due to nectarivory in leaf-nosed bats.

BACKGROUND: The New World leaf-nosed bats (Phyllostomids) exhibit a diverse spectrum of feeding habits and innovations in their nutrient acquisition and foraging mechanisms. However, the genomic signatures associated with their distinct diets are unknown. RESULTS: We conducted a genomic comparative analysis to study the evolutionary dynamics related to dietary diversification and specialization. We sequenced, assembled, and annotated the genomes of five Phyllostomid species: one insect feeder (Macrotus waterhousii), one fruit feeder (Artibeus jamaicensis), and three nectar feeders from the Glossophaginae subfamily (Leptonycteris yerbabuenae, Leptonycteris nivalis, and Musonycteris harrisoni), also including the previously sequenced vampire Desmodus rotundus. Our phylogenomic analysis based on 22,388 gene families displayed differences in expansion and contraction events across the Phyllostomid lineages. Independently of diet, genes relevant for feeding strategies and food intake experienced multiple expansions and signatures of positive selection. We also found adaptation signatures associated with specialized diets: the vampire exhibited traits associated with a blood diet (i.e., coagulation mechanisms), whereas the nectarivore clade shares a group of positively selected genes involved in sugar, lipid, and iron metabolism. Interestingly, in fruit-nectar-feeding Phyllostomid and Pteropodids bats, we detected positive selection in two genes: AACS and ALKBH7, which are crucial in sugar and fat metabolism. Moreover, in these two proteins we found parallel amino acid substitutions in conserved positions exclusive to the tribe Glossophagini and to Pteropodids. CONCLUSIONS: Our findings illuminate the genomic and molecular shifts associated with the evolution of nectarivory and shed light on how nectar-feeding bats can avoid the adverse effects of diets with high glucose content.

The Genome of Cucurbita argyrosperma (Silver-Seed Gourd) Reveals Faster Rates of Protein-Coding Gene and Long Noncoding RNA Turnover and Neofunctionalization within Cucurbita.

Whole-genome duplications are an important source of evolutionary novelties that change the mode and tempo at which genetic elements evolve within a genome. The Cucurbita genus experienced a whole-genome duplication around 30 million years ago, although the evolutionary dynamics of the coding and noncoding genes in this genus have not yet been scrutinized. Here, we analyzed the genomes of four Cucurbita species, including a newly assembled genome of Cucurbita argyrosperma, and compared the gene contents of these species with those of five other members of the Cucurbitaceae family to assess the evolutionary dynamics of protein-coding and long intergenic noncoding RNA (lincRNA) genes after the genome duplication. We report that Cucurbita genomes have a higher protein-coding gene birth-death rate compared with the genomes of the other members of the Cucurbitaceae family. C. argyrosperma gene families associated with pollination and transmembrane transport had significantly faster evolutionary rates. lincRNA families showed high levels of gene turnover throughout the phylogeny, and 67.7% of the lincRNA families in Cucurbita showed evidence of birth from the neofunctionalization of previously existing protein-coding genes. Collectively, our results suggest that the whole-genome duplication in Cucurbita resulted in faster rates of gene family evolution through the neofunctionalization of duplicated genes.

Rates of molecular evolution in tree ferns are associated with body size, environmental temperature, and biological productivity.

Variation in rates of molecular evolution (heterotachy) is a common phenomenon among plants. Although multiple theoretical models have been proposed, fundamental questions remain regarding the combined effects of ecological and morphological traits on rate heterogeneity. Here, we used tree ferns to explore the correlation between rates of molecular evolution in chloroplast DNA sequences and several morphological and environmental factors within a Bayesian framework. We revealed direct and indirect effects of body size, biological productivity, and temperature on substitution rates, where smaller tree ferns living in warmer and less productive environments tend to have faster rates of molecular evolution. In addition, we found that variation in the ratio of nonsynonymous to synonymous substitution rates (dN/dS) in the chloroplast rbcL gene was significantly correlated with ecological and morphological variables. Heterotachy in tree ferns may be influenced by effective population size associated with variation in body size and productivity. Macroevolutionary hypotheses should go beyond explaining heterotachy in terms of mutation rates and instead, should integrate population-level factors to better understand the processes affecting the tempo of evolution at the molecular level.

Genomic Signals of Adaptation towards Mutualism and Sociality in Two Ambrosia Beetle Complexes.

Mutualistic symbiosis and eusociality have developed through gradual evolutionary processes at different times in specific lineages. Like some species of termites and ants, ambrosia beetles have independently evolved a mutualistic nutritional symbiosis with fungi, which has been associated with the evolution of complex social behaviors in some members of this group. We sequenced the transcriptomes of two ambrosia complexes (Euwallacea sp. near fornicatus⁻Fusarium euwallaceae and Xyleborus glabratus⁻Raffaelea lauricola) to find evolutionary signatures associated with mutualism and behavior evolution. We identified signatures of positive selection in genes related to nutrient homeostasis; regulation of gene expression; development and function of the nervous system, which may be involved in diet specialization; behavioral changes; and social evolution in this lineage. Finally, we found convergent changes in evolutionary rates of proteins across lineages with phylogenetically independent origins of sociality and mutualism, suggesting a constrained evolution of conserved genes in social species, and an evolutionary rate acceleration related to changes in selective pressures in mutualistic lineages.