Abstract
Introgression is increasingly recognized as a source of genetic diversity that fuels adaptation. Its role in the evolution of sex chromosomes, however, is not well known. Here, we confirm ...the hypothesis that the Y chromosome in the ninespine stickleback, Pungitius pungitius, was established by introgression from the Amur stickleback, P. sinensis. Using whole genome resequencing, we identified a large region of Chr 12 in P. pungitius that is diverged between males and females. Within but not outside of this region, several lines of evidence show that the Y chromosome of P. pungitius shares a most recent common ancestor not with the X chromosome, but with the homologous chromosome in P. sinensis. Accumulation of repetitive elements and gene expression changes on the new Y are consistent with a young sex chromosome in early stages of degeneration, but other hallmarks of Y chromosomes have not yet appeared. Our findings indicate that porous species boundaries can trigger rapid sex chromosome evolution.
Speciation is a continuous process and analysis of species pairs at different stages of divergence provides insight into how it unfolds. Previous genomic studies on young species pairs have revealed ...peaks of divergence and heterogeneous genomic differentiation. Yet less known is how localised peaks of differentiation progress to genome-wide divergence during the later stages of speciation in the presence of persistent gene flow. Spanning the speciation continuum, stickleback species pairs are ideal for investigating how genomic divergence builds up during speciation. However, attention has largely focused on young postglacial species pairs, with little knowledge of the genomic signatures of divergence and introgression in older stickleback systems. The Japanese stickleback species pair, composed of the Pacific Ocean three-spined stickleback (Gasterosteus aculeatus) and the Japan Sea stickleback (G. nipponicus), which co-occur in the Japanese islands, is at a late stage of speciation. Divergence likely started well before the end of the last glacial period and crosses between Japan Sea females and Pacific Ocean males result in hybrid male sterility. Here we use coalescent analyses and Approximate Bayesian Computation to show that the two species split approximately 0.68-1 million years ago but that they have continued to exchange genes at a low rate throughout divergence. Population genomic data revealed that, despite gene flow, a high level of genomic differentiation is maintained across the majority of the genome. However, we identified multiple, small regions of introgression, occurring mainly in areas of low recombination rate. Our results demonstrate that a high level of genome-wide divergence can establish in the face of persistent introgression and that gene flow can be localized to small genomic regions at the later stages of speciation with gene flow.
Sexual reproduction is an ancient feature of life on earth, and the familiar X and Y chromosomes in humans and other model species have led to the impression that sex determination mechanisms are old ...and conserved. In fact, males and females are determined by diverse mechanisms that evolve rapidly in many taxa. Yet this diversity in primary sex-determining signals is coupled with conserved molecular pathways that trigger male or female development. Conflicting selection on different parts of the genome and on the two sexes may drive many of these transitions, but few systems with rapid turnover of sex determination mechanisms have been rigorously studied. Here we survey our current understanding of how and why sex determination evolves in animals and plants and identify important gaps in our knowledge that present exciting research opportunities to characterize the evolutionary forces and molecular pathways underlying the evolution of sex determination.
Karyotype, including the chromosome and arm numbers, is a fundamental genetic characteristic of all organisms and has long been used as a species-diagnostic character. Additionally, karyotype ...evolution plays an important role in divergent adaptation and speciation. Centric fusion and fission change chromosome numbers, whereas the intra-chromosomal movement of the centromere, such as pericentric inversion, changes arm numbers. A probabilistic model simultaneously incorporating both chromosome and arm numbers has not been established. Here, we built a probabilistic model of karyotype evolution based on the "karyograph", which treats karyotype evolution as a walk on the two-dimensional space representing the chromosome and arm numbers. This model enables analysis of the stationary distribution with a stable karyotype for any given parameter. After evaluating their performance using simulated data, we applied our model to two large taxonomic groups of fish, Eurypterygii and series Otophysi, to perform maximum likelihood estimation of the transition rates and reconstruct the evolutionary history of karyotypes. The two taxa significantly differed in the evolution of arm number. The inclusion of speciation and extinction rates demonstrated possibly high extinction rates in species with karyotypes other than the most typical karyotype in both groups. Finally, we made a model including polyploidization rates and applied it to a small plant group. Thus, the use of this probabilistic model can contribute to a better understanding of tempo and mode in karyotype evolution and its possible role in speciation and extinction.
It is generally accepted that taxa exhibit genetic variation in phenotypic plasticity, but many questions remain unan- swered about how divergent plastic responses evolve under dissimilar ecological ...conditions. Hormones are signaling molecules that act as proximate mediators of phenotype expression by regulating a variety of cellular, physiological, and behavioral re- sponses. Hormones not only change cellular and physiological states but also influence gene expression directly or indirectly, thereby linking environmental conditions to phenotypic development. Studying how hormonal pathways respond to environ- mental variation and how those responses differ between individuals, populations, and species can expand our understanding of the evolution of phenotypic plasticity. Here, we explore the ways that the study of hormone signaling is providing new insights into the underlying proximate bases for individual, population or species variation in plasticity. Using several studies as exem- plars, we examine how a ＇norm of reaction＇ approach can be used in investigations of hormone-mediated plasticity to inform the following： 1） how environmental cues affect the component hormones, receptors and enzymes that comprise any endocrine sig- naling pathway, 2） how genetic and epigenetic variation in endocrine-associated genes can generate variation in plasticity among these diverse components, and 3） how phenotypes mediated by the same hormone can be coupled and decoupled via independent plastic responses of signaling components across target tissues. Future studies that apply approaches such as reaction norms and network modeling to questions concerning how hormones link environmental stimuli to ecologically-relevant phenotypic re- sponses should help unravel how phenotypic plasticity evolves
Elucidation of the genetic mechanisms of convergent evolution, the evolution of similar or the same phenotypes in phylogenetically independent lineages, helps predict how populations will respond to ...the same selective pressures. Convergent evolution can be caused by either the fixation of identical‐by‐descent alleles, independent mutations at the same gene, or mutations in different genes controlling the same trait. To what extent does the fixation of identical‐by‐descent alleles lead to convergent evolution in isolated populations where inflow of adaptive alleles from other populations is limited? In a From the Cover article in this issue of Molecular Ecology, Kemppainen et al. (2021) compared the genetic basis for the reduction of pelvic structures in three isolated freshwater populations of nine‐spined stickleback (Pungitius pungitius) from Northern Europe. The authors used quantitative trait loci (QTL) mapping to reveal that the pelvic reduction in these three populations was caused by mutations at different genetic loci. In contrast to studies in three‐spined stickleback (Gasterosteus aculeatus), where independently derived Pitx1 mutations were shown to be responsible for plate reduction across multiple freshwater populations, Kemppainen et al. (2021) found Pitx1 to be the candidate causative gene for only one population of P. pungitius. This study highlights the importance of genetic studies of convergent evolution, not only in the presence of gene flow but also in its absence for a better understanding of the genetic architecture of convergent evolution.
Sex chromosomes are among the most evolutionarily labile features in some groups of animals. One of the mechanisms causing structural changes of sex chromosomes is fusion with an autosome. A recent ...study showed that the establishment rates of Y chromosome–autosome fusions are much higher than those of other fusions (i.e., X-autosome, W-autosome, and Z-autosome fusions) in fishes and reptiles. Although sexually antagonistic selection may be one of the most important driving forces of sex chromosome–autosome fusions, a previous theoretical analysis showed that sexually antagonistic selection alone cannot explain the excess of Y-autosome fusions in these taxa. This previous analysis, however, is based on the assumption that sexually antagonistic selection is symmetric, sexually antagonistic alleles are maintained only by selection-drift balance (i.e., no supply of mutation), and only one type of fusion arises within a population. Here, we removed these assumptions and made an individual-based model to simulate the establishment of sex chromosome–autosome fusions. Our simulations showed that the highest establishment rate of Y-autosome fusion can be achieved when the fusion captures a rare male-beneficial allele, if the recurrent mutation rates are high enough to maintain the polymorphism of alleles with asymmetric, sexually antagonistic effects. Our results demonstrate that sexually antagonistic selection can influence the dynamics of sex chromosome structural changes, but the type of fusion that becomes the most common depends on fusion rates, recurrent mutation rates, and selection regimes. Because the evolutionary fate of sex chromosome–autosome fusions is highly parameter-sensitive, further attempts to empirically measure these parameters in natural populations are essential for a better understanding of the roles of sexually antagonistic selection in sex chromosome evolution.
•We studied the evolutionary mechanisms of sex chromosome fusions theoretically.•We focused on the effect of sexually antagonistic alleles on autosomes.•We generated a simple one-locus model and conducted individual based simulations.•Our results show that the evolutionary fate of the fusions is parameter sensitive.•Stronger selection in females can cause the predominance of Y-autosome fusions.
Cis-regulatory mutations often underlie phenotypic evolution. However, because identifying the locations of promoters and enhancers in non-coding regions is challenging, we have fewer examples of ...identified causative cis-regulatory mutations that underlie naturally occurring phenotypic variations than of causative amino acid-altering mutations. Because cis-regulatory elements have epigenetic marks of specific histone modifications, we can detect cis-regulatory elements by mapping and analyzing them. Here, we investigated histone modifications and chromatin accessibility with cleavage under targets and tagmentation (CUT&Tag) and assay for transposase-accessible chromatin-sequencing (ATAC-seq). Using the threespine stickleback (Gasterosteus aculeatus) as a model, we confirmed that the genes for which nearby regions showed active marks, such as H3K4me1, H3K4me3, and high chromatin accessibility, were highly expressed. In contrast, the expression levels of genes for which nearby regions showed repressive marks, such as H3K27me3, were reduced, suggesting that our chromatin analysis protocols overall worked well. Genomic regions with peaks of histone modifications showed higher nucleotide diversity within and between populations. By comparing gene expression in the gills of the marine and stream ecotypes, we identified several insertions and deletions (indels) with transposable element fragments in the candidate cis-regulatory regions. Thus, mapping and analyzing histone modifications can help identify cis-regulatory elements and accelerate the identification of causative mutations in the non-coding regions underlying naturally occurring phenotypic variations.
Colonization of new ecological niches has triggered large adaptive radiations. Although some lineages have made use of such opportunities, not all do so. The factors causing this variation among ...lineages are largely unknown. Here, we show that deficiency in docosahexaenoic acid (DHA), an essential ω-3 fatty acid, can constrain freshwater colonization by marine fishes. Our genomic analyses revealed multiple independent duplications of the fatty acid desaturase gene
in stickleback lineages that subsequently colonized and radiated in freshwater habitats, but not in close relatives that failed to colonize. Transgenic manipulation of
in marine stickleback increased their ability to synthesize DHA and survive on DHA-deficient diets. Multiple freshwater ray-finned fishes also show a convergent increase in
copies, indicating its key role in freshwater colonization.
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