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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’.

During the study of parasites of ninespine stickleback Pungitius pungitius (L., 1758), a resident in the Volga basin, we have found intestinal nematodes, Pseudocapillaria tomentosa (Dujardin, 1843) Lomakin et Trofimenko, 1982 and Rhabdochona denudata (Dujardin, 1845) Railliet, 1916. Both species are recorded for the first time in the parasite fauna of the host in the European part of Russia. Data on the occurrence and intensity of fish invasion by worms are presented.

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.

Abstract Chromosomal fusions are hypothesized to facilitate adaptation to divergent environments, both by bringing together previously unlinked adaptive alleles and by creating regions of low recombination that facilitate the linkage of adaptive alleles; but, there is little empirical evidence to support this hypothesis. Here, we address this knowledge gap by studying threespine stickleback (Gasterosteus aculeatus), in which ancestral marine fish have repeatedly adapted to freshwater across the northern hemisphere. By comparing the threespine and ninespine stickleback (Pungitius pungitius) genomes to a de novo assembly of the fourspine stickleback (Apeltes quadracus) and an outgroup species, we find two chromosomal fusion events involving the same chromosomes have occurred independently in the threespine and ninespine stickleback lineages. On the fused chromosomes in threespine stickleback, we find an enrichment of quantitative trait loci underlying traits that contribute to marine versus freshwater adaptation. By comparing whole-genome sequences of freshwater and marine threespine stickleback populations, we also find an enrichment of regions under divergent selection on these two fused chromosomes. There is elevated genetic diversity within regions under selection in the freshwater population, consistent with a simulation study showing that gene flow can increase diversity in genomic regions associated with local adaptation and our demographic models showing gene flow between the marine and freshwater populations. Integrating our results with previous studies, we propose that these fusions created regions of low recombination that enabled the formation of adaptative clusters, thereby facilitating freshwater adaptation in the face of recurrent gene flow between marine and freshwater threespine sticklebacks.

The genomic consequences of prolonged population decline and isolation are increasingly recognized, but quantitative assessments of mutation loads have been limited by low population-level replication in individual studies. Moreover, how inbreeding and purifying selection shape the genomic landscape of deleterious variation remains poorly understood. We evaluated the abundance and frequency of putative deleterious mutations, characterized the landscape of deleterious variation, and measured the efficacy of purifying selection in 17 wild nine-spined stickleback (Pungitius pungitius) populations covering varying levels of inbreeding (FROH = 0.015 to 0.912) and histories of isolation. We found significantly more deleterious homozygous mutations and a greater frequency of mildly deleterious variants in long-term small, isolated, and inbred populations than in larger outbred populations. Deleterious homozygotes were enriched in runs of homozygosity regions across all study populations, but the extent of enrichment was more pronounced in larger outbred populations than in small inbred populations. Historical effective population sizes serve as an indicator of the strength of purifying selection for mildly deleterious alleles but not for strongly deleterious alleles. The results demonstrate that the accumulation and purging of deleterious variants can occur simultaneously and that a large fraction of segregating strongly deleterious variants are recessive lethals. These findings, which are based on analyses of highly replicated samples of populations, suggest that the level of inbreeding is a good predictor of realized loads of deleterious mutations and that the genomic consequences of prolonged isolation in small populations are predictable.

The Asian cyprinid Pseudorasbora parva is considered to be a major threat to native fish communities and listed as an invasive alien species of European Union concern. Our study aims to gain evidence-based knowledge on the impact of both P. parva and its parasite Sphaerothecum destruens on native fish populations by analysing fish assemblages and body condition of individuals of native fish species in floodplain water bodies that were invaded and uninvaded by P. parva. We explored the use of environmental DNA (eDNA) techniques to detect S. destruens. Prevalence of S. destruens in native fish species was assessed. Fish samplings showed significantly negative correlations between the abundance of P. parva and the native Leucaspius delineatus, and Pungitius pungitius and three biodiversity indices of the fish assemblages (Simpson’s diversity index, Shannon–Wiener index and evenness). Contrastingly, the abundances of the native Gasterosteus aculeatus and P. parva were positively related. In nearly all isolated water bodies with P. parva, this species is outnumbering native fish species. No effect of P. parva presence was found on body condition of native fish species. Sphaerothecum destruens was demonstrated to occur in both P. parva and G. aculeatus. Gasterosteus aculeatus is suggested to be an asymptomatic carrier that can aid the further spread of S. destruens. Analysis of eDNA proved to be a promising method for early detection of S. destruens, here showing that S. destruens presence coincided with P. parva presence. The ongoing invasion of both P. parva and S. destruens is predicted to pose a significant risk to native fish communities.

Recent discoveries of sex chromosome diversity across the tree of life have challenged the canonical model of conserved sex chromosome evolution and evoked new theories on labile sex chromosomes that maintain less differentiation and undergo frequent turnover. However, theories of labile sex chromosome evolution lack direct empirical support due to the paucity of case studies demonstrating ongoing sex chromosome turnover in nature. Two divergent lineages (viz. WL & EL) of nine-spined sticklebacks (Pungitius pungitius) with different sex chromosomes (linkage group [LG] 12 in the EL, unknown in the WL) hybridize in a natural secondary contact zone in the Baltic Sea, providing an opportunity to study ongoing turnover between coexisting sex chromosomes. In this study, we first identify an 80 kbp genomic region on LG3 as the sex-determining region (SDR) using whole-genome resequencing data of family crosses of a WL population. We then verify this region as the SDR in most other WL populations and demonstrate a potentially ongoing sex chromosome turnover in admixed marine populations where the evolutionarily younger and homomorphic LG3 sex chromosome replaces the older and heteromorphic LG12 sex chromosome. The results provide a rare glimpse of sex chromosome turnover in the wild and indicate the possible existence of additional yet undiscovered sex chromosome diversity in Pungitius sticklebacks.

The influence of environmental complexity on brain development has been demonstrated in a number of taxa, but the potential influence of social environment on neural architecture remains largely unexplored. We investigated experimentally the influence of social environment on the development of different brain parts in geographically and genetically isolated and ecologically divergent populations of nine-spined sticklebacks (Pungitius pungitius). Fish from two marine and two pond populations were reared in the laboratory from eggs to adulthood either individually or in groups. Group-reared pond fish developed relatively smaller brains than those reared individually, but no such difference was found in marine fish. Group-reared fish from both pond and marine populations developed larger tecta optica and smaller bulbi olfactorii than individually reared fish. The fact that the social environment effect on brain size differed between marine and pond origin fish is in agreement with the previous research, showing that pond fish pay a high developmental cost from grouping while marine fish do not. Our results demonstrate that social environment has strong effects on the development of the stickleback brain, and on the brain's sensory neural centres in particular. The potential adaptive significance of the observed brain-size plasticity is discussed.

Adaptation in the wild often involves standing genetic variation (SGV), which allows rapid responses to selection on ecological timescales. However, we still know little about how the evolutionary histories and genomic distributions of SGV influence local adaptation in natural populations. Here, we address this knowledge gap using the threespine stickleback fish (Gasterosteus aculeatus) as a model. We extend restriction site‐associated DNA sequencing (RAD‐seq) to produce phased haplotypes approaching 700 base pairs (bp) in length at each of over 50,000 loci across the stickleback genome. Parallel adaptation in two geographically isolated freshwater pond populations consistently involved fixation of haplotypes that are identical‐by‐descent. In these same genomic regions, sequence divergence between marine and freshwater stickleback, as measured by dXY, reaches tenfold higher than background levels and genomic variation is structured into distinct marine and freshwater haplogroups. By combining this dataset with a de novo genome assembly of a related species, the ninespine stickleback (Pungitius pungitius), we find that this habitat‐associated divergent variation averages six million years old, nearly twice the genome‐wide average. The genomic variation that is involved in recent and rapid local adaptation in stickleback has therefore been evolving throughout the 15‐million‐year history since the two species lineages split. This long history of genomic divergence has maintained large genomic regions of ancient ancestry that include multiple chromosomal inversions and extensive linked variation. These discoveries of ancient genetic variation spread broadly across the genome in stickleback demonstrate how selection on ecological timescales is a result of genome evolution over geological timescales, and vice versa.

Despite longstanding interest in parallel evolution, little is known about the genes that control similar traits in different lineages of vertebrates. Pelvic reduction in stickleback fish (family Gasterosteidae) provides a striking example of parallel evolution in a genetically tractable system. Previous studies suggest that cis-acting regulatory changes at the Pitxl locus control pelvic reduction in a population of threespine sticklebacks (Gasterosteus aculeatus). In this study, progeny from intergeneric crosses between pelvicreduced threespine and ninespine (Pungitius pungitius) sticklebacks also showed severe pelvic reduction, implicating a similar genetic origin for this trait in both genera. Comparative sequencing studies in complete and pelvic-reduced Pungitius revealed no differences in the Pitxl coding sequences, but Pitxl expression was absent from the prospective pelvic region of larvae from pelvicreduced parents. A much more phylogenetically distant example of pelvic reduction, loss of hindlimbs in manatees, shows a similar left-right size bias that is a morphological signature of Pitxlmediated pelvic reduction in both sticklebacks and mice. These multiple lines of evidence suggest that changes in Pitxl may represent a key mechanism of morphological evolution in multiple populations, species, and genera of sticklebacks, as well as in distantly related vertebrate lineages.