ABSTRACT
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.
ABSTRACT
Social relationships, affiliative social attachments, are important for many species. The best studied types of relationships are monogamous pair bonds. However, it remains unclear how generalizable models of pair bonding are across types of social attachments. Zebra finches are a fascinating system to explore the neurobiology of social relationships because they form various adult bonds with both same- and opposite-sex partners. To test whether different bonds are supported by a single brain network, we quantified individuals' neuroendocrine state after either 24 h or 2 weeks of co-housing with a novel same- or opposite-sex partner. We defined neuroendocrine state by the expression of 22 genes related to 4 major signaling pathways (dopamine, steroid, nonapeptide, and opioid) in six brain regions associated with affiliation or communication [nucleus accumbens (NAc), nucleus taeniae of the amygdala (TnA), medial preoptic area (POM), and periaqueductal gray (PAG), ventral tegmental area, and auditory cortex]. Overall, we found dissociable effects of social contexts (same- or opposite-sex partnerships) and duration of co-housing. Social bonding impacted the neuroendocrine state of four regions in males (NAc, TnA, POM, and PAG) and three regions in females (NAc, TnA, and POM). Monogamous pair bonding specifically appeared to impact male NAc. However, the patterns of gene expression in zebra finches were different than has previously been reported in mammals. Together, our results support the view that there are numerous mechanisms regulating social relationships and highlight the need to further our understanding of how social interactions shape social bonds.
ABSTRACT
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.
Subject(s)
Poecilia , Sex Chromosomes , Male , Animals , Sex Chromosomes/genetics , X Chromosome/genetics , Polymorphism, Genetic , Genes, X-Linked , Poecilia/genetics , Evolution, MolecularABSTRACT
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.
Subject(s)
Poecilia , Humans , Animals , Male , Poecilia/genetics , Phylogeny , Sex Chromosomes , Y Chromosome , DNAABSTRACT
The presence of stable color polymorphisms within populations begs the question of how genetic variation is maintained. Consistent variation among populations in coloration, especially when correlated with environmental variation, raises questions about whether environmental conditions affect either the fulcrum of those balanced polymorphisms, the plastic expression of coloration, or both. Color patterns in male bluefin killifish provoke both types of questions. Red and yellow morphs are common in all populations. Blue males are more common in tannin-stained swamps relative to clear springs. Here, we combined crosses with a manipulation of light to explore how genetic variation and phenotypic plasticity shape these patterns. We found that the variation in coloration is attributable mainly to two axes of variation: (1) a red-yellow axis with yellow being dominant to red, and (2) a blue axis that can override red-yellow and is controlled by genetics, phenotypic plasticity, and genetic variation for phenotypic plasticity. The variation among populations in plasticity suggests it is adaptive in some populations but not others. The variation among sires in plasticity within the swamp population suggests balancing selection may be acting not only on the red-yellow polymorphism but also on plasticity for blue coloration.
Subject(s)
Fundulidae , Killifishes , Adaptation, Physiological , Animals , Color , Fundulidae/genetics , Genetic Variation , Male , Polymorphism, GeneticABSTRACT
Differences in allele frequencies at autosomal genes between males and females in a population can result from two scenarios. First, unresolved sexual conflict over survival can produce allelic differentiation between the sexes. However, given the substantial mortality costs required to produce allelic differences between males and females at each generation, it remains unclear how many loci within the genome experience significant sexual conflict over survival. Alternatively, recent studies have shown that similarity between autosomal and Y sequences can create perceived allelic differences between the sexes. However, Y duplications are most likely in species with large nonrecombining regions, in part because they simply represent larger targets for duplications. We assessed the genomes of 120 wild-caught guppies, which experience extensive predation- and pathogen-induced mortality and have a relatively small ancestral Y chromosome. We identified seven autosomal genes that show allelic differences between male and female adults. Five of these genes show clear evidence of whole or partial gene duplication between the Y chromosome and the autosomes. The remaining two genes show evidence of partial homology to the Y. Overall, our findings suggest that the guppy genome experiences a very low level of unresolved sexual conflict over survival, and instead the Y chromosome, despite its small ancestral size and recent origin, may nonetheless accumulate genes with male-specific functions.
Subject(s)
Poecilia , Animals , Female , Gene Duplication , Genome , Male , Poecilia/genetics , Predatory Behavior , Y Chromosome/geneticsABSTRACT
Dosage compensation balances gene expression between the sexes in systems with diverged heterogametic sex chromosomes. Theory predicts that dosage compensation should rapidly evolve in tandem with the divergence of sex chromosomes to prevent the deleterious effects of dosage imbalances that occur as a result of sex chromosome divergence. Examples of complete dosage compensation, where gene expression of the entire sex chromosome is compensated, are rare, and have only been found in relatively ancient sex chromosome systems. Consequently, very little is known about the evolutionary dynamics of complete dosage compensation systems. Within the family Poeciliidae the subgenus Lebistes share the same sex chromosome system which originated 18.48-26.08 Ma. In Poecilia reticulata and P. wingei, the Y chromosome has been largely maintained, whereas the Y in the closely related species P. picta and P. parae has rapidly degraded. We recently found P. picta to be the first example of complete dosage compensation in a fish. Here, we show that P. parae also has complete dosage compensation, thus complete dosage compensation likely evolved in the short (â¼3.7 Myr) interval after the split of the ancestor of these two species from P. reticulata, but before they diverged from each other. These data suggest that novel dosage compensation mechanisms can evolve rapidly, thus supporting the longstanding theoretical prediction that such mechanisms arise in tandem with rapidly diverging sex chromosomes.
Subject(s)
Poecilia , Animals , Dosage Compensation, Genetic , Poecilia/genetics , Sex Chromosomes/genetics , Y ChromosomeABSTRACT
Loss of recombination between sex chromosomes often depletes Y chromosomes of functional content and genetic variation, which might limit their potential to generate adaptive diversity. Males of the freshwater fish Poecilia parae occur as one of five discrete morphs, all of which shoal together in natural populations where morph frequency has been stable for over 50 years. Each morph uses a different complex reproductive strategy and morphs differ dramatically in colour, body size and mating behaviour. Morph phenotype is passed perfectly from father to son, indicating there are five Y haplotypes segregating in the species, which encode the complex male morph characteristics. Here, we examine Y diversity in natural populations of P. parae. Using linked-read sequencing on multiple P. parae females and males of all five morphs, we find that the genetic architecture of the male morphs evolved on the Y chromosome after recombination suppression had occurred with the X. Comparing Y chromosomes between each of the morphs, we show that, although the Ys of the three minor morphs that differ in colour are highly similar, there are substantial amounts of unique genetic material and divergence between the Ys of the three major morphs that differ in reproductive strategy, body size and mating behaviour. Altogether, our results suggest that the Y chromosome is able to overcome the constraints of recombination loss to generate extreme diversity, resulting in five discrete Y chromosomes that control complex reproductive strategies.
Subject(s)
Poecilia , Animals , Female , Fresh Water , Male , Poecilia/genetics , Polymorphism, Genetic , Reproduction/genetics , Y Chromosome/geneticsABSTRACT
The guppy sex chromosomes show an extraordinary diversity in divergence across populations and closely related species. In order to understand the dynamics of the guppy Y chromosome, we used linked-read sequencing to assess Y chromosome evolution and diversity across upstream and downstream population pairs that vary in predator and food abundance in three replicate watersheds. Based on our population-specific genome assemblies, we first confirmed and extended earlier reports of two strata on the guppy sex chromosomes. Stratum I shows significant accumulation of male-specific sequence, consistent with Y divergence, and predates the colonization of Trinidad. In contrast, Stratum II shows divergence from the X, but no Y-specific sequence, and this divergence is greater in three replicate upstream populations compared with their downstream pair. Despite longstanding assumptions that sex chromosome recombination suppression is achieved through inversions, we find no evidence of inversions associated with either Stratum I or Stratum II. Instead, we observe a remarkable diversity in Y chromosome haplotypes within each population, even in the ancestral Stratum I. This diversity is likely due to gradual mechanisms of recombination suppression, which, unlike an inversion, allow for the maintenance of multiple haplotypes. In addition, we show that this Y diversity is dominated by low-frequency haplotypes segregating in the population, suggesting a link between haplotype diversity and female preference for rare Y-linked color variation. Our results reveal the complex interplay between recombination suppression and Y chromosome divergence at the earliest stages of sex chromosome divergence.
Subject(s)
Biological Evolution , Poecilia/genetics , Y Chromosome , Animals , Female , Haplotypes , Male , Polymorphism, GeneticABSTRACT
African cichlid fishes are a prime model for studying speciation mechanisms. Despite the development of extensive genomic resources, it has been difficult to determine which sources of genetic variation are responsible for cichlid phenotypic variation. One of their most variable phenotypes is visual sensitivity, with some of the largest spectral shifts among vertebrates. These shifts arise primarily from differential expression of seven cone opsin genes. By mapping expression quantitative trait loci (eQTL) in intergeneric crosses of Lake Malawi cichlids, we previously identified four causative genetic variants that correspond to indels in the promoters of either key transcription factors or an opsin gene. In this comprehensive study, we show that these indels are the result of the movement of transposable elements (TEs) that correlate with opsin expression variation across the Malawi flock. In tracking the evolutionary history of these particular indels, we found they are endemic to Lake Malawi, suggesting that these TEs are recently active and are segregating within the Malawi cichlid lineage. However, an independent indel has arisen at a similar genomic location in one locus outside of the Malawi flock. The convergence in TE movement suggests these loci are primed for TE insertion and subsequent deletions. Increased TE mobility may be associated with interspecific hybridization, which disrupts mechanisms of TE suppression. This might provide a link between cichlid hybridization and accelerated regulatory variation. Overall, our study suggests that TEs may be an important driver of key regulatory changes, facilitating rapid phenotypic change and possibly speciation in African cichlids.
Subject(s)
Cichlids , Cone Opsins , Animals , Cichlids/genetics , Cone Opsins/genetics , DNA Transposable Elements/genetics , Malawi , Opsins/genetics , PhylogenyABSTRACT
Genomic analysis of many nonmodel species has uncovered an incredible diversity of sex chromosome systems, making it possible to empirically test the rich body of evolutionary theory that describes each stage of sex chromosome evolution. Classic theory predicts that sex chromosomes originate from a pair of homologous autosomes and recombination between them is suppressed via inversions to resolve sexual conflict. The resulting degradation of the Y chromosome gene content creates the need for dosage compensation in the heterogametic sex. Sex chromosome theory also implies a linear process, starting from sex chromosome origin and progressing to heteromorphism. Despite many convergent genomic patterns exhibited by independently evolved sex chromosome systems, and many case studies supporting these theoretical predictions, emerging data provide numerous interesting exceptions to these long-standing theories, and suggest that the remarkable diversity of sex chromosomes is matched by a similar diversity in their evolution. For example, it is clear that sex chromosome pairs are not always derived from homologous autosomes. In addition, both the cause and the mechanism of recombination suppression between sex chromosome pairs remain unclear, and it may be that the spread of recombination suppression is a more gradual process than previously thought. It is also clear that dosage compensation can be achieved in many ways, and displays a range of efficacy in different systems. Finally, the remarkable turnover of sex chromosomes in many systems, as well as variation in the rate of sex chromosome divergence, suggest that assumptions about the inevitable linearity of sex chromosome evolution are not always empirically supported, and the drivers of the birth-death cycle of sex chromosome evolution remain to be elucidated. Here, we concentrate on how the diversity in sex chromosomes across taxa highlights an equal diversity in each stage of sex chromosome evolution.
Subject(s)
Biological Evolution , Sex Chromosomes , Animals , Chromosomes, Plant , Dosage Compensation, Genetic , Genetic Variation , Recombination, Genetic , Selection, GeneticABSTRACT
Sensory systems are tuned by selection to maximize organismal fitness in particular environments. This tuning has implications for intraspecies communication, the maintenance of species boundaries, and speciation. Tuning of color vision largely depends on the sequence of the expressed opsin proteins. To improve tuning of visual sensitivities to shifts in habitat or foraging ecology over the course of development, many organisms change which opsins are expressed. Changes in this developmental sequence (heterochronic shifts) can create differences in visual sensitivity among closely related species. The genetic mechanisms by which these developmental shifts occur are poorly understood. Here, we use quantitative trait locus analyses, genome sequencing, and gene expression studies in African cichlid fishes to identify a role for the transcription factor Tbx2a in driving a switch between long wavelength sensitive (LWS) and Rhodopsin-like (RH2) opsin expression. We identify binding sites for Tbx2a in the LWS promoter and the highly conserved locus control region of RH2 which concurrently promote LWS expression while repressing RH2 expression. We also present evidence that a single change in Tbx2a regulatory sequence has led to a species difference in visual tuning, providing the first mechanistic model for the evolution of rapid switches in sensory tuning. This difference in visual tuning likely has important roles in evolution as it corresponds to differences in diet, microhabitat choice, and male nuptial coloration.
Subject(s)
Cichlids/metabolism , Evolution, Molecular , Opsins/metabolism , T-Box Domain Proteins/metabolism , Animals , HEK293 Cells , Humans , Quantitative Trait LociABSTRACT
Once recombination is halted between the X and Y chromosomes, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about the variation in sex chromosome differentiation within clades. Here, we combined whole-genome and transcriptome sequencing data to characterize the structure and conservation of sex chromosome systems across Poeciliidae, the livebearing clade that includes guppies. We found that the Poecilia reticulata XY system is much older than previously thought, being shared not only with its sister species, Poecilia wingei, but also with Poecilia picta, which diverged roughly 20 million years ago. Despite the shared ancestry, we uncovered an extreme heterogeneity across these species in the proportion of the sex chromosome with suppressed recombination, and the degree of Y chromosome decay. The sex chromosomes in P. reticulata and P. wingei are largely homomorphic, with recombination in the former persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely nonrecombining and strikingly heteromorphic. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of functional chromosome-wide dosage compensation in this species, which has not been previously observed in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation.
Subject(s)
Dosage Compensation, Genetic , Genes, X-Linked , Genetic Variation , Genome , Poecilia/genetics , Sex Chromosomes/genetics , Sex Differentiation , Animals , Evolution, Molecular , Female , Male , Poecilia/classification , TranscriptomeABSTRACT
To determine the visual sensitivities of an organism of interest, quantitative reverse transcription-polymerase chain reaction (qRT-PCR) is often used to quantify expression of the light-sensitive opsins in the retina. While qRT-PCR is an affordable, high-throughput method for measuring expression, it comes with inherent normalization issues that affect the interpretation of results, especially as opsin expression can vary greatly based on developmental stage, light environment or diurnal cycles. We tested for diurnal cycles of opsin expression over a period of 24 hr at 1-hr increments and examined how normalization affects a data set with fluctuating expression levels using qRT-PCR and transcriptome data from the retinae of the cichlid Pelmatolapia mariae. We compared five methods of normalizing opsin expression relative to (a) the average of three stably expressed housekeeping genes (Ube2z, EF1-α and ß-actin), (b) total RNA concentration, (c) GNAT2, (the cone-specific subunit of transducin), (d) total opsin expression and (e) only opsins expressed in the same cone type. Normalizing by proportion of cone type produced the least variation and would be best for removing time-of-day variation. In contrast, normalizing by housekeeping genes produced the highest daily variation in expression and demonstrated that the peak of cone opsin expression was in the late afternoon. A weighted correlation network analysis showed that the expression of different cone opsins follows a very similar daily cycle. With the knowledge of how these normalization methods affect opsin expression data, we make recommendations for designing sampling approaches and quantification methods based upon the scientific question being examined.
Subject(s)
Genes, Essential/genetics , Opsins/genetics , Animals , Cichlids/genetics , Real-Time Polymerase Chain Reaction/methods , Retina/metabolism , Retinal Cone Photoreceptor Cells/physiology , Rod Opsins/genetics , Transcriptome/geneticsSubject(s)
Models, Genetic , Recombination, Genetic , Animals , Fishes , Male , Polymorphism, GeneticABSTRACT
The African cichlid radiations have created thousands of new cichlid species with a wide diversity of trophic morphologies, behaviors, sensory systems and pigment patterns. In addition, recent research has uncovered a surprising number of young sex chromosome systems within African cichlids. Here we refine methods to describe the differentiation of young sex chromosomes from whole genome comparisons. We identified a novel XY sex chromosome system on linkage group 14 in Oreochromis mossambicus, confirmed a linkage group 1 XY system in Coptodon zillii and also defined the limits of our methodology by examining a ZW system on linkage group 3 in Pelmatolapia mariae. These data further demonstrate that cichlids are an excellent model system for understanding the early stages of sex chromosome evolution.
ABSTRACT
Sensory drive predicts coevolution of mate choice signals with the sensory systems detecting those signals. Guppies are a classic model for sensory drive as mate preferences based on coloration differ across individuals and populations. A large body of work has identified variation in color vision, yet we lack a direct tie between how such variation in color vision influences variation in color preference. Here we bring together studies that have investigated guppy vision over the past 40 years to: (1) highlight our current understanding of where variation occurs in the guppy color vision pathway and (2) suggest future avenues of research into sources of visual system variation that could influence guppy color preference. This will allow researchers to design careful studies that couple measures of color preference with measures of visual system variation from the same individual or population. Such studies will finally provide important answers as to what sets the direction and speed of mate preference evolution via sensory drive.
ABSTRACT
African cichlids are well known for their adaptive radiations, but it is now apparent that they also harbor an extraordinary diversity of sex chromosome systems. In this study, we sequenced pools of males and females from species in 3 different genera of cichlids from Lake Tanganyika. We then searched for regions that were differentiated following the patterns expected for sex chromosomes. We report 2 novel sex chromosomes systems, an XY system on LG19 in Tropheus sp. "black" and a ZW system on LG7 in Hemibates stenosoma. We also identify a ZW system on LG5 in Cyprichromis leptosoma that may be convergent with a system previously described in Lake Malawi cichlids. Our data also identify candidate single nucleotide polymorphisms for the blue/yellow tail color polymorphism observed among male C. leptosoma.
Subject(s)
Cichlids/genetics , Sex Chromosomes , Africa , Alleles , Animals , Cichlids/classification , Female , Lakes , Male , Phylogeny , Polymorphism, Single Nucleotide , Species SpecificityABSTRACT
Many models of evolution by sexual selection predict a coevolution of sensory systems and mate preferences, but the genomic architecture (number and arrangement of contributing loci) underlying these characters could constrain this coevolution. Here, we examine how the genomic organization and evolution of the opsin genes (responsible for tuning color vision) can influence the evolutionary trajectory of sexually selected traits across 15 species in the family Poeciliidae, which includes classic systems for studies of color-mediated sexual selection such as guppies, swordtails, and mollies. Although male coloration patterns and the importance of this coloration in female mate choice vary widely within and among genera, sequencing revealed low variability at amino acid sites that tune Long Wavelength-Sensitive (LWS) opsins in this speciose family. Although most opsin genes in these species appear to have evolved along traditional mutation-selection dynamics, we identified high rates of gene conversion between two of the LWS loci (LWS-1 and LWS-3), likely due to the inverted tandem repeat nature of these genes. Yet members of the subgenus Lebistes appear to resist LWS gene conversion. The LWS opsins are responsible for detecting and discriminating red and orange coloration-a key sexually selected trait in members of the subgenus Lebistes. Taken together these results suggest selection is acting against the homogenizing effects of gene conversion to maintain LWS-1/LWS-3 differences within this subgenus.