Allopolyploidization from two dioecious ancestors leads to recurrent evolution of sex chromosomes.

Polyploidization presents an unusual challenge for species with sex chromosomes, as it can lead to complex combinations of sex chromosomes that disrupt reproductive development. This is particularly true for allopolyploidization between species with different sex chromosome systems. Here, we assemble haplotype-resolved chromosome-level genomes of a female allotetraploid weeping willow (Salix babylonica) and a male diploid S. dunnii. We show that weeping willow arose from crosses between a female ancestor from the Salix-clade, which has XY sex chromosomes on chromosome 7, and a male ancestor from the Vetrix-clade, which has ancestral XY sex chromosomes on chromosome 15. We find that weeping willow has one pair of sex chromosomes, ZW on chromosome 15, that derived from the ancestral XY sex chromosomes in the male ancestor of the Vetrix-clade. Moreover, the ancestral 7X chromosomes from the female ancestor of the Salix-clade have reverted to autosomal inheritance. Duplicated intact ARR17-like genes on the four homologous chromosomes 19 likely have contributed to the maintenance of dioecy during polyploidization and sex chromosome turnover. Taken together, our results suggest the rapid evolution and reversion of sex chromosomes following allopolyploidization in weeping willow.

The grasshopper genome reveals long-term gene content conservation of the X Chromosome and temporal variation in X Chromosome evolution.

We present the first chromosome-level genome assembly of the grasshopper, Locusta migratoria, one of the largest insect genomes. We use coverage differences between females (XX) and males (X0) to identify the X Chromosome gene content, and find that the X Chromosome shows both complete dosage compensation in somatic tissues and an underrepresentation of testis-expressed genes. X-linked gene content from L. migratoria is highly conserved across seven insect orders, namely Orthoptera, Odonata, Phasmatodea, Hemiptera, Neuroptera, Coleoptera, and Diptera, and the 800 Mb grasshopper X Chromosome is homologous to the fly ancestral X Chromosome despite 400 million years of divergence, suggesting either repeated origin of sex chromosomes with highly similar gene content, or long-term conservation of the X Chromosome. We use this broad conservation of the X Chromosome to test for temporal dynamics to Fast-X evolution, and find evidence of a recent burst evolution for new X-linked genes in contrast to slow evolution of X-conserved genes.

On the resolution of sexual conflict over shared traits.

Anisogamy, different-sized male and female gametes, sits at the heart of sexual selection and conflict between the sexes. Sperm producers (males) and egg producers (females) of the same species generally share most, if not all, of the same genome, but selection frequently favours different trait values in each sex for traits common to both. The extent to which this conflict might be resolved, and the potential mechanisms by which this can occur, have been widely debated. Here, we summarize recent findings and emphasize that once the sexes evolve, sexual selection is ongoing, and therefore new conflict is always possible. In addition, sexual conflict is largely a multivariate problem, involving trait combinations underpinned by networks of interconnected genes. Although these complexities can hinder conflict resolution, they also provide multiple possible routes to decouple male and female phenotypes and permit sex-specific evolution. Finally, we highlight difficulty in the study of sexual conflict over shared traits and promising directions for future research.

Molecular Mechanisms of Temperature Tolerance Plasticity in an Arthropod.

How species thrive in a wide range of environments is a major focus of evolutionary biology. For many species, limited genetic diversity or gene flow among habitats means that phenotypic plasticity must play an important role in their capacity to tolerate environmental heterogeneity and to colonize new habitats. However, we have a limited understanding of the molecular components that govern plasticity in ecologically relevant phenotypes. We examined this hypothesis in a spider species (Stegodyphus dumicola) with extremely low species-wide genetic diversity that nevertheless occupies a broad range of thermal environments. We determined phenotypic responses to temperature stress in individuals from four climatic zones using common garden acclimation experiments to disentangle phenotypic plasticity from genetic adaptations. Simultaneously, we created data sets on multiple molecular modalities: the genome, the transcriptome, the methylome, the metabolome, and the bacterial microbiome to determine associations with phenotypic responses. Analyses of phenotypic and molecular associations reveal that acclimation responses in the transcriptome and metabolome correlate with patterns of phenotypic plasticity in temperature tolerance. Surprisingly, genes whose expression seemed to be involved in plasticity in temperature tolerance were generally highly methylated contradicting the idea that DNA methylation stabilizes gene expression. This suggests that the function of DNA methylation in invertebrates varies not only among species but also among genes. The bacterial microbiome was stable across the acclimation period; combined with our previous demonstrations that the microbiome is temporally stable in wild populations, this is convincing evidence that the microbiome does not facilitate plasticity in temperature tolerance. Our results suggest that population-specific variation in temperature tolerance among acclimation temperatures appears to result from the evolution of plasticity in mainly gene expression.

Gene gain and loss from the Asian corn borer W chromosome.

BACKGROUND: Sex-limited chromosomes Y and W share some characteristics, including the degeneration of protein-coding genes, enrichment of repetitive elements, and heterochromatin. However, although many studies have suggested that Y chromosomes retain genes related to male function, far less is known about W chromosomes and whether they retain genes related to female-specific function. RESULTS: Here, we built a chromosome-level genome assembly of the Asian corn borer, Ostrinia furnacalis Guenée (Lepidoptera: Crambidae, Pyraloidea), an economically important pest in corn, from a female, including both the Z and W chromosome. Despite deep conservation of the Z chromosome across Lepidoptera, our chromosome-level W assembly reveals little conservation with available W chromosome sequence in related species or with the Z chromosome, consistent with a non-canonical origin of the W chromosome. The W chromosome has accumulated significant repetitive elements and experienced rapid gene gain from the remainder of the genome, with most genes exhibiting pseudogenization after duplication to the W. The genes that retain significant expression are largely enriched for functions in DNA recombination, the nucleosome, chromatin, and DNA binding, likely related to meiotic and mitotic processes within the female gonad. CONCLUSIONS: Overall, our chromosome-level genome assembly supports the non-canonical origin of the W chromosome in O. furnacalis, which experienced rapid gene gain and loss, with the retention of genes related to female-specific function.

Functional convergence of genomic and transcriptomic architecture underlies schooling behaviour in a live-bearing fish.

The organization and coordination of fish schools provide a valuable model to investigate the genetic architecture of affiliative behaviours and dissect the mechanisms underlying social behaviours and personalities. Here we used replicate guppy selection lines that vary in schooling propensity and combine quantitative genetics with genomic and transcriptomic analyses to investigate the genetic basis of sociability phenotypes. We show that consistent with findings in collective motion patterns, experimental evolution of schooling propensity increased the sociability of female, but not male, guppies when swimming with unfamiliar conspecifics. This finding highlights a relevant link between coordinated motion and sociability for species forming fission-fusion societies in which both group size and the type of social interactions are dynamic across space and time. We further show that alignment and attraction, the two major traits forming the sociability personality axis in this species, showed heritability estimates at the upper end of the range previously described for social behaviours, with important variation across sexes. The results from both Pool-seq and RNA-seq data indicated that genes involved in neuron migration and synaptic function were instrumental in the evolution of sociability, highlighting a crucial role of glutamatergic synaptic function and calcium-dependent signalling processes in the evolution of schooling.

Transposon wave remodeled the epigenomic landscape in the rapid evolution of X-Chromosome dosage compensation.

Sex chromosome dosage compensation is a model to understand the coordinated evolution of transcription; however, the advanced age of the sex chromosomes in model systems makes it difficult to study how the complex regulatory mechanisms underlying chromosome-wide dosage compensation can evolve. The sex chromosomes of Poecilia picta have undergone recent and rapid divergence, resulting in widespread gene loss on the male Y, coupled with complete X Chromosome dosage compensation, the first case reported in a fish. The recent de novo origin of dosage compensation presents a unique opportunity to understand the genetic and evolutionary basis of coordinated chromosomal gene regulation. By combining a new chromosome-level assembly of P. picta with whole-genome bisulfite sequencing and RNA-seq data, we determine that the YY1 transcription factor (YY1) DNA binding motif is associated with male-specific hypomethylated regions on the X, but not the autosomes. These YY1 motifs are the result of a recent and rapid repetitive element expansion on the P. picta X Chromosome, which is absent in closely related species that lack dosage compensation. Taken together, our results present compelling support that a disruptive wave of repetitive element insertions carrying YY1 motifs resulted in the remodeling of the X Chromosome epigenomic landscape and the rapid de novo origin of a dosage compensation system.

Evolution of schooling drives changes in neuroanatomy and motion characteristics across predation contexts in guppies.

One of the most spectacular displays of social behavior is the synchronized movements that many animal groups perform to travel, forage and escape from predators. However, elucidating the neural mechanisms underlying the evolution of collective behaviors, as well as their fitness effects, remains challenging. Here, we study collective motion patterns with and without predation threat and predator inspection behavior in guppies experimentally selected for divergence in polarization, an important ecological driver of coordinated movement in fish. We find that groups from artificially selected lines remain more polarized than control groups in the presence of a threat. Neuroanatomical measurements of polarization-selected individuals indicate changes in brain regions previously suggested to be important regulators of perception, fear and attention, and motor response. Additional visual acuity and temporal resolution tests performed in polarization-selected and control individuals indicate that observed differences in predator inspection and schooling behavior should not be attributable to changes in visual perception, but rather are more likely the result of the more efficient relay of sensory input in the brain of polarization-selected fish. Our findings highlight that brain morphology may play a fundamental role in the evolution of coordinated movement and anti-predator behavior.

Extensive variation in germline de novo mutations in Poecilia reticulata.

The rate of germline mutation is fundamental to evolutionary processes, as it generates the variation upon which selection acts. The guppy, Poecilia reticulata, is a model of rapid adaptation, however the relative contribution of standing genetic variation versus de novo mutation (DNM) to evolution in this species remains unclear. Here, we use pedigree-based approaches to quantify and characterize germline DNMs in three large guppy families. Our results suggest germline mutation rate in the guppy varies substantially across individuals and families. Most DNMs are shared across multiple siblings, suggesting they arose during early embryonic development. DNMs are randomly distributed throughout the genome, and male-biased mutation rate is low, as would be expected from the short guppy generation time. Overall, our study shows remarkable variation in germline mutation rate and provides insights into rapid evolution of guppies.

Conceptual and empirical bridges between micro- and macroevolution.

Explaining broad molecular, phenotypic and species biodiversity patterns necessitates a unifying framework spanning multiple evolutionary scales. Here we argue that although substantial effort has been made to reconcile microevolution and macroevolution, much work remains to identify the links between biological processes at play. We highlight four major questions of evolutionary biology whose solutions require conceptual bridges between micro and macroevolution. We review potential avenues for future research to establish how mechanisms at one scale (drift, mutation, migration, selection) translate to processes at the other scale (speciation, extinction, biogeographic dispersal) and vice versa. We propose ways in which current comparative methods to infer molecular evolution, phenotypic evolution and species diversification could be improved to specifically address these questions. We conclude that researchers are in a better position than ever before to build a synthesis to understand how microevolutionary dynamics unfold over millions of years.

Sex chromosome heteromorphism and the Fast-X effect in poeciliids.

Fast-X evolution has been observed in a range of heteromorphic sex chromosomes. However, it remains unclear how early in the process of sex chromosome differentiation the Fast-X effect becomes detectible. Recently, we uncovered an extreme variation in sex chromosome heteromorphism across poeciliid fish species. The common guppy, Poecilia reticulata, Endler's guppy, P. wingei, swamp guppy, P. picta and para guppy, P. parae, appear to share the same XY system and exhibit a remarkable range of heteromorphism. Species outside this group lack this sex chromosome system. We combined analyses of sequence divergence and polymorphism data across poeciliids to investigate X chromosome evolution as a function of hemizygosity and reveal the causes for Fast-X effects. Consistent with the extent of Y degeneration in each species, we detect higher rates of divergence on the X relative to autosomes, a signal of Fast-X evolution, in P. picta and P. parae, species with high levels of X hemizygosity in males. In P. reticulata, which exhibits largely homomorphic sex chromosomes and little evidence of hemizygosity, we observe no change in the rate of evolution of X-linked relative to autosomal genes. In P. wingei, the species with intermediate sex chromosome differentiation, we see an increase in the rate of nonsynonymous substitutions on the older stratum of divergence only. We also use our comparative approach to test for the time of origin of the sex chromosomes in this clade. Taken together, our study reveals an important role of hemizygosity in Fast-X evolution.

Sex-biased gene expression at single-cell resolution: cause and consequence of sexual dimorphism.

Gene expression differences between males and females are thought to be key for the evolution of sexual dimorphism, and sex-biased genes are often used to study the molecular footprint of sex-specific selection. However, gene expression is often measured from complex aggregations of diverse cell types, making it difficult to distinguish between sex differences in expression that are due to regulatory rewiring within similar cell types and those that are simply a consequence of developmental differences in cell-type abundance. To determine the role of regulatory versus developmental differences underlying sex-biased gene expression, we use single-cell transcriptomic data from multiple somatic and reproductive tissues of male and female guppies, a species that exhibits extensive phenotypic sexual dimorphism. Our analysis of gene expression at single-cell resolution demonstrates that nonisometric scaling between the cell populations within each tissue and heterogeneity in cell-type abundance between the sexes can influence inferred patterns of sex-biased gene expression by increasing both the false-positive and false-negative rates. Moreover, we show that, at the bulk level, the subset of sex-biased genes that are the product of sex differences in cell-type abundance can significantly confound patterns of coding-sequence evolution. Taken together, our results offer a unique insight into the effects of allometry and cellular heterogeneity on perceived patterns of sex-biased gene expression and highlight the power of single-cell RNA-sequencing in distinguishing between sex-biased genes that are the result of regulatory change and those that stem from sex differences in cell-type abundance, and hence are a consequence rather than a cause of sexual dimorphism.

Sexual selection: Changing the definition of the fittest.

Sexual selection has long been known to produce rapid evolution of spectacular traits. A new study reveals how sexual selection can also rapidly reshape the genome.

The roles of sexual selection and sexual conflict in shaping patterns of genome and transcriptome variation.

Sexual dimorphism is one of the most prevalent, and often the most extreme, examples of phenotypic variation within species, and arises primarily from genomic variation that is shared between females and males. Many sexual dimorphisms arise through sex differences in gene expression, and sex-biased expression is one way that a single, shared genome can generate multiple, distinct phenotypes. Although many sexual dimorphisms are expected to result from sexual selection, and many studies have invoked the possible role of sexual selection to explain sex-specific traits, the role of sexual selection in the evolution of sexually dimorphic gene expression remains difficult to differentiate from other forms of sex-specific selection. In this Review, we propose a holistic framework for the study of sex-specific selection and transcriptome evolution. We advocate for a comparative approach, across tissues, developmental stages and species, which incorporates an understanding of the molecular mechanisms, including genomic variation and structure, governing gene expression. Such an approach is expected to yield substantial insights into the evolution of genetic variation and have important applications in a variety of fields, including ecology, evolution and behaviour.

Evolutionary History of the Poecilia picta Sex Chromosomes.

The degree of divergence between the sex chromosomes is not always proportional to their age. In poeciliids, four closely related species all exhibit a male heterogametic sex chromosome system on the same linkage group, yet show a remarkable diversity in X and Y divergence. In Poecilia reticulata and P. wingei, the sex chromosomes remain homomorphic, yet P. picta and P. parae have a highly degraded Y chromosome. To test alternative theories about the origin of their sex chromosomes, we used a combination of pedigrees and RNA-seq data from P. picta families in conjunction with DNA-seq data collected from P. reticulata, P. wingei, P. parae, and P. picta. Phylogenetic clustering analysis of X and Y orthologs, identified through segregation patterns, and their orthologous sequences in closely related species demonstrates a similar time of origin for both the P. picta and P. reticulata sex chromosomes. We next used k-mer analysis to identify shared ancestral Y sequence across all four species, suggesting a single origin to the sex chromosome system in this group. Together, our results provide key insights into the origin and evolution of the poeciliid Y chromosome and illustrate that the rate of sex chromosome divergence is often highly heterogenous, even over relatively short evolutionary time frames.

Sexual selection and the evolution of condition-dependence: an experimental test at two resource levels.

Stronger condition-dependence in sexually selected traits is well-documented, but how this relationship is established remains unknown. Moreover, resource availability can shape responses to sexual selection, but resource effects on the relationship between sexual selection and condition-dependence are also unknown. In this study, we directly test the hypotheses that sexual selection drives the evolution of stronger-condition-dependence and that resource availability affects the outcome, by evolving fruit flies (Drosophila melanogaster) under relatively strong or weak sexual selection (through varied sex ratios) and at resource-poor or resource-rich adult diets. We then experimentally manipulated condition via developmental diet and assessed condition-dependence in adult morphology, behavior, and reproduction. We observed stronger condition-dependence in female size in male-biased populations and in female ovariole production in resource-limited populations. However, we found no evidence that male condition-dependence increased in response to sexual selection, or that responses depended on resource levels. These results offer no support for the hypotheses that sexual selection increases male condition-dependence or that sexual selection's influence on condition-dependence is influenced by resource availability. Our study is, to our knowledge, the first experimental test of these hypotheses. If the results we report are general, then sexual selection's influence on the evolution of condition-dependence may be less important than predicted.

Sex-specific morphs: the genetics and evolution of intra-sexual variation.

Sex-specific morphs exhibit discrete phenotypes, often including many disparate traits, that are observed in only one sex. These morphs have evolved independently in many different animals and are often associated with alternative mating strategies. The remarkable diversity of sex-specific morphs offers unique opportunities to understand the genetic basis of complex phenotypes, as the distinct nature of many morphs makes it easier to both categorize and compare genomes than for continuous traits. Sex-specific morphs also expand the study of sexual dimorphism beyond traditional bimodal comparisons of male and female averages, as they allow for a more expansive range of sexualization. Although ecological and endocrinological studies of sex-specific morphs have been advancing for some time, genomic and transcriptomic studies of morphs are far more recent. These studies reveal not only many different paths to the evolution of sex-specific morphs but also many commonalities, such as the role of sex-determining genes and hormone signalling in morph development, and the mixing of male and female traits within some morphs.