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How consistent are the evolutionary trajectories of sex chromosomes shortly after they form? Insights into the evolution of recombination, differentiation, and degeneration can be provided by comparing closely related species with homologous sex chromosomes. The sex chromosomes of the threespine stickleback (Gasterosteus aculeatus) and its sister species, the Japan Sea stickleback (G. nipponicus), have been well characterized. Little is known, however, about the sex chromosomes of their congener, the blackspotted stickleback (G. wheatlandi). We used pedigrees to obtain experimentally phased whole genome sequences from blackspotted stickleback X and Y chromosomes. Using multispecies gene trees and analysis of shared duplications, we demonstrate that Chromosome 19 is the ancestral sex chromosome and that its oldest stratum evolved in the common ancestor of the genus. After the blackspotted lineage diverged, its sex chromosomes experienced independent and more extensive recombination suppression, greater X–Y differentiation, and a much higher rate of Y degeneration than the other two species. These patterns may result from a smaller effective population size in the blackspotted stickleback. A recent fusion between the ancestral blackspotted stickleback Y chromosome and Chromosome 12, which produced a neo-X and neo-Y, may have been favored by the very small size of the recombining region on the ancestral sex chromosome. We identify six strata on the ancestral and neo-sex chromosomes where recombination between the X and Y ceased at different times. These results confirm that sex chromosomes can evolve large differences within and between species over short evolutionary timescales.

Single nucleotide polymorphism (SNP) discovery and genotyping are essential to genetic mapping. There remains a need for a simple, inexpensive platform that allows high-density SNP discovery and genotyping in large populations. Here we describe the sequencing of restriction-site associated DNA (RAD) tags, which identified more than 13,000 SNPs, and mapped three traits in two model organisms, using less than half the capacity of one Illumina sequencing run. We demonstrated that different marker densities can be attained by choice of restriction enzyme. Furthermore, we developed a barcoding system for sample multiplexing and fine mapped the genetic basis of lateral plate armor loss in threespine stickleback by identifying recombinant breakpoints in F(2) individuals. Barcoding also facilitated mapping of a second trait, a reduction of pelvic structure, by in silico re-sorting of individuals. To further demonstrate the ease of the RAD sequencing approach we identified polymorphic markers and mapped an induced mutation in Neurospora crassa. Sequencing of RAD markers is an integrated platform for SNP discovery and genotyping. This approach should be widely applicable to genetic mapping in a variety of organisms.

Parasitic infections are a global occurrence and impact the health of many species. Coinfections, where two or more species of parasite are present in a host, are a common phenomenon across species. Coinfecting parasites can interact directly or indirectly via their manipulation of (and susceptibility to) the immune system of their shared host. Helminths, such as the cestode Schistocephalus solidus, are well known to suppress immunity of their host (threespine stickleback, Gasterosteus aculeatus), potentially facilitating other parasite species. Yet, hosts can evolve a more robust immune response (as seen in some stickleback populations), potentially turning facilitation into inhibition. Using wild-caught stickleback from 20 populations with non-zero S. solidus prevalence, we tested an a priori hypothesis that S. solidus infection facilitates infection by other parasites. Consistent with this hypothesis, individuals with S. solidus infections have 18.6% higher richness of other parasites compared to S. solidus-uninfected individuals from the same lakes. This facilitation-like trend is stronger in lakes where S. solidus is particularly successful but is reversed in lakes with sparse and smaller cestodes (indicative of stronger host immunity). These results suggest that a geographic mosaic of host–parasite co-evolution might lead to a mosaic of between-parasite facilitation/inhibition effects.

Populations can be granted conservation status because they harbour a set of unique traits, evolutionary histories, or ecological roles. Such populations are often isolated and specialised and, as such, can be particularly vulnerable to environmental disturbances. Even if distinct populations survive and adapt to severe disturbances, they could show changes in the very traits that made them distinct in the first place. Here, we leverage a natural ‘experiment’ involving an unarmoured population of threespine stickleback (Gasterosteus aculeatus) in Rouge Lake (Haida Gwaii, BC)—a population listed as Special Concern under the Canadian Species at Risk Act. In 2015, Rouge Lake nearly dried up during a severe drought event; yet the stickleback population appeared to have fully recovered its abundance in subsequent years. Using phenotypic measurements, we assessed the extent to which evolution in this population was impacted by the drought. We document important shifts in several phenotypic traits, with the largest occurring in precisely the trait that made the population distinct and prompted its original conservation designation. Specifically, fish with no lateral plates (i.e., ‘unarmoured’) made up 51% of the population before the drought but only 13% after the drought. This shift held (13%–16% unarmoured) over the 4 years of our post‐drought monitoring. Field observations support a strong demographic bottleneck, which we suggest might have been coupled with a shift in the selective regime. These findings underscore how populations of conservation concern are not only at risk of extinction; they are also at risk of losing the characteristics that make them unique. These dynamics highlight the need for policies to consider a population's evolutionary potential and develop more flexible approaches than simply considering single‐timepoint assessments of diversity.

Understanding the genetics of adaptation is a central focus in evolutionary biology. Here, we use a population genomics approach to examine striking parallel morphological divergences of parapatric stream–lake ecotypes of threespine stickleback fish in three watersheds on the Haida Gwaii archipelago, western Canada. Genome-wide variation at greater than 1000 single nucleotide polymorphism loci indicate separate origin of giant lake and small-bodied stream fish within each watershed (mean FST between watersheds = 0.244 and within = 0.114). Genome scans within watersheds identified a total of 21 genomic regions that are highly differentiated between ecotypes and are probably subject to directional selection. Most outliers were watershed-specific, but genomic regions undergoing parallel genetic changes in multiple watersheds were also identified. Interestingly, several of the stream–lake outlier regions match those previously identified in marine–freshwater and benthic–limnetic genome scans, indicating reuse of the same genetic loci in different adaptive scenarios. We also identified multiple new outlier loci, which may contribute to unique aspects of differentiation in stream–lake environments. Overall, our data emphasize the important role of ecological boundaries in driving both local and broadly occurring parallel genetic changes during adaptation.

Genetic divergence between populations is shaped by a combination of drift, migration, and selection, yielding patterns of isolation-by-distance (IBD) and isolation-by-environment (IBE). Unfortunately, IBD and IBE may be confounded when comparing divergence across habitat boundaries. For instance, parapatric lake and stream threespine stickleback (Gasterosteus aculeatus) may have diverged due to selection against migrants (IBE), or mere spatial separation (IBD). To quantitatively partition the strength of IBE and IBD, we used recently developed population genetic software (BEDASSLE) to analyze partial genomic data from three lake-stream clines on Vancouver Island. We find support for IBD within each of three outlet streams (unlike prior studies of lake-stream stickleback). In addition, we find evidence for IBE (controlling for geographic distance): the genetic effect of habitat is equivalent to geographic separation of ~1.9 km of IBD. Remarkably, of our three lake-stream pairs, IBE is strongest where migration between habitats is easiest. Such microgeographic genetic divergence would require exceptionally strong divergent selection, which multiple experiments have failed to detect. Instead, we propose that nonrandom dispersal (e.g., habitat choice) contributes to IBE. Supporting this conclusion, we show that the few migrants between habitats are a nonrandom subset of the phenotype distribution of the source population.

A major goal of evolutionary biology is to identify the genotypes and phenotypes that underlie adaptation to divergent environments. Stickleback fish, including the threespine stickleback (Gasterosteus aculeatus) and the ninespine stickleback (Pungitius pungitius), have been at the forefront of research to uncover the genetic and molecular architecture that underlies phenotypic diversity and adaptation. A wealth of quantitative trait locus (QTL) mapping studies in sticklebacks have provided insight into long-standing questions about the distribution of effect sizes during adaptation as well as the role of genetic linkage in facilitating adaptation. These QTL mapping studies have also provided a basis for the identification of the genes that underlie phenotypic diversity. These data have revealed that mutations in regulatory elements play an important role in the evolution of phenotypic diversity in sticklebacks. Genetic and molecular studies in sticklebacks have also led to new insights on the genetic basis of repeated evolution and suggest that the same loci are involved about half of the time when the same phenotypes evolve independently. When the same locus is involved, selection on standing variation and repeated mutation of the same genes have both contributed to the evolution of similar phenotypes in independent populations. This article is part of the themed issue ‘Evo-devo in the genomics era, and the origins of morphological diversity’.

Background Heteromorphic sex chromosomes have evolved repeatedly across diverse species. Suppression of recombination between X and Y chromosomes leads to degeneration of the Y chromosome. The progression of degeneration is not well understood, as complete sequence assemblies of heteromorphic Y chromosomes have only been generated across a handful of taxa with highly degenerate sex chromosomes. Here, we describe the assembly of the threespine stickleback ( Gasterosteus aculeatus ) Y chromosome, which is less than 26 million years old and at an intermediate stage of degeneration. Our previous work identified that the non-recombining region between the X and the Y spans approximately 17.5 Mb on the X chromosome. Results We combine long-read sequencing with a Hi-C-based proximity guided assembly to generate a 15.87 Mb assembly of the Y chromosome. Our assembly is concordant with cytogenetic maps and Sanger sequences of over 90 Y chromosome BAC clones. We find three evolutionary strata on the Y chromosome, consistent with the three inversions identified by our previous cytogenetic analyses. The threespine stickleback Y shows convergence with more degenerate sex chromosomes in the retention of haploinsufficient genes and the accumulation of genes with testis-biased expression, many of which are recent duplicates. However, we find no evidence for large amplicons identified in other sex chromosome systems. We also report an excellent candidate for the master sex-determination gene: a translocated copy of Amh ( Amhy ). Conclusions Together, our work shows that the evolutionary forces shaping sex chromosomes can cause relatively rapid changes in the overall genetic architecture of Y chromosomes.

We investigated the feeding of the dominant small pelagic fish—herring Clupea harengus membras and three-spined stickleback Gasterosteus aculeatus —in the Gulf of Riga (Baltic Sea) in the summers of 1999–2014. The share of empty stomachs, stomach fullness and taxonomic composition of fish diet was analysed. On average, large herring had the highest (19%) and small herring the lowest (6%) share of empty stomachs. Small (<1 mm) cladoceran Bosmina spp. was the most important prey for three-spined stickleback; preying on small (<1.5 mm) copepod Eurytemora affinis was the most efficient for small herring, while Bosmina spp. and E. affinis were equally important for the large herring, followed by the large (mean body length <2.0 mm) non-indigenous cladoceran Cercopagis pengoi . The number of prey taxa per stomach exhibited significant differences between the fish groups studied; the highest mean value was recorded for small herring and the lowest for three-spined stickleback (2.1 and 1.4 taxa, respectively). Although present, the fish group-specific spatial dynamics in feeding parameters (share of empty stomachs and feeding intensity) were weak compared to the observed interannual variation.

Developmental genetic studies of evolved differences in morphology have led to the hypothesis that cis -regulatory changes often underlie morphological evolution. However, because most of these studies focus on evolved loss of traits, the genetic architecture and possible association with cis -regulatory changes of gain traits are less understood. Here we show that a derived benthic freshwater stickleback population has evolved an approximate twofold gain in ventral pharyngeal tooth number compared with their ancestral marine counterparts. Comparing laboratory-reared developmental time courses of a low-toothed marine population and this high-toothed benthic population reveals that increases in tooth number and tooth plate area and decreases in tooth spacing arise at late juvenile stages. Genome-wide linkage mapping identifies largely separate sets of quantitative trait loci affecting different aspects of dental patterning. One large-effect quantitative trait locus controlling tooth number fine-maps to a genomic region containing an excellent candidate gene, Bone morphogenetic protein 6 ( Bmp6 ). Stickleback Bmp6 is expressed in developing teeth, and no coding changes are found between the high- and low-toothed populations. However, quantitative allele-specific expression assays of Bmp6 in developing teeth in F1 hybrids show that cis -regulatory changes have elevated the relative expression level of the freshwater benthic Bmp6 allele at late, but not early, stages of stickleback development. Collectively, our data support a model where a late-acting cis -regulatory up-regulation of Bmp6 expression underlies a significant increase in tooth number in derived benthic sticklebacks. Significance How body pattern evolves in nature remains largely unknown. Although recent progress has been made on the molecular basis of losing morphological features during adaptation to new environments (regressive evolution), there are few well worked out examples of how morphological features may be gained in natural species (constructive evolution). Here we use genetic crosses to study how threespine stickleback fish have increased their tooth number in a new freshwater environment. Genetic mapping and gene expression experiments suggest regulatory changes have occurred in the gene for a bone morphogenetic signaling molecule, leading to increased expression in the freshwater fish that have more teeth. Our studies suggest that changes in gene regulation may underlie both gain and loss traits during vertebrate evolution.