Abstract
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.
Abstract
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.
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.
Increasing turbidity in streams and rivers near human activity is cause for environmental concern, as the ability of aquatic organisms to use visual information declines. To investigate how some ...organisms might be able to developmentally compensate for increasing turbidity, we reared guppies (Poecilia reticulata) in either clear or turbid water. We assessed the effects of developmental treatments on adult behavior and aspects of the visual system by testing fish from both developmental treatments in turbid and clear water. We found a strong interactive effect of rearing and assay conditions: fish reared in clear water tended to decrease activity in turbid water, whereas fish reared in turbid water tended to increase activity in turbid water. Guppies from all treatments decreased activity when exposed to a predator. To measure plasticity in the visual system, we quantified treatment differences in opsin gene expression of individuals. We detected a shift from mid-wave-sensitive opsins to long wave-sensitive opsins for guppies reared in turbid water. Since long-wavelength sensitivity is important in motion detection, this shift likely allows guppies to salvage motion-detecting abilities when visual information is obscured in turbid water. Our results demonstrate the importance of developmental plasticity in responses of organisms to rapidly changing environments.
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.
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.
•Expression patterns of 22 neuroendocrine genes differ across brain regions.•Social relationships impact neuroendocrine state of NAc, TnA, POM and PAG.•Social relationships may have sex-specific effects in POM and PAG.•Opposite-sex pair bonds may have distinct neuroendocrine states in the NAc.•Different social relationships may utilize distinct brain networks.
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.
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.
Glucocorticoids (GCs) are produced by the adrenal glands and circulate in the blood to coordinate organismal physiology. In addition, different tissues may independently regulate their local GC ...levels via local GC synthesis. Here, we find that in the mouse, endogenous GCs show tissue-specific developmental patterns, rather than mirroring GCs in the blood. Using solid-phase extraction, HPLC, and specific immunoassays, we quantified endogenous steroids and found that in tissues of female and male mice, (1) local GC levels can be much higher than systemic GC levels, (2) local GCs follow age-related patterns different from those of systemic GCs, and (3) local GCs have identities different from those of systemic GCs. For example, whereas corticosterone is the predominant circulating adrenal GC in mice, high concentrations of cortisol were measured in neonatal thymus, bone marrow, and heart. The presence of cortisol was confirmed with liquid chromatography-tandem mass spectrometry. In addition, gene expression of steroidogenic enzymes was detected across multiple tissues, consistent with local GC production. Our results demonstrate that local GCs can differ from GCs in circulating blood. This finding suggests that steroids are widely used as local (paracrine or autocrine) signals, in addition to their classic role as systemic (endocrine) signals. Local GC regulation may even be the norm, rather than the exception, especially during development.
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
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
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
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.
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