Biology subjects

Merila, J.

Publications and source records attributed to Merila, J..

17 recordsLinked to original sources

bioRxiv2026

Demography and selection shape gene loss in freshwater sticklebacks - A pangenomic perspective

The extent of within-species variation in genome assembly size, and the relative contributions of neutral vs. adaptive processes to it, remains poorly understood. We assembled the pangenome for the nine-spined stickleback (Pungitius pungitius) from whole-genome resequencing data obtained from range-wide sampling of 1,478 individuals across 47 populations. Our analysis recovered approximately 234.15 Mb of novel sequence and identified 11,151 protein-coding genes annotated in non-reference-represented regions, which accounted for 28.8% of all annotated pangenomic genes, corresponding to a 40.6% expansion relative to the 27,450 protein-coding genes annotated in the updated v8 reference genome. The identified presence/absence variation (PAV) genes exhibited a higher incidence of deleterious and non-synonymous mutations than core genes. Freshwater populations with smaller effective population sizes had lost more genes and had smaller assembly sizes relative to larger marine populations. Larger genome sizes of marine populations were primarily associated with higher transposable element content. Across gene categories, patterns of molecular variation were consistent with weaker purifying selection in freshwater populations than in marine populations, while recurrent freshwater-biased loss of a subset of PAV genes suggested that gene loss is not entirely random. Together, these results indicate that demographic history explains the overall pattern of gene loss, whereas negative natural selection may contribute to repeated loss of a subset of genes.

genomics↗

bioRxiv2026

Intra-specific evidence to support the drift-barrier hypothesis of mutation rate evolution

Rates of de novo mutations ({micro}) are highly variable among different taxa but less is known about their variability at the intraspecific level. Using a large data set (n=364 trios) from eight nine-spined stickleback (Pungitius pungitius) populations differing in their effective population sizes (Ne), we tested the prediction of the drift-barrier hypothesis (DBH) that {micro} scales negatively with increasing Ne. Indeed, {micro} was a negative function of Ne, also after correcting for phylogenetic non-independence of populations. While the range of variation in mutation rates across populations spanned more than a 4-fold range ({micro} = 1.60 - 6.99 x 10-9), we discovered one highly mutable family with a five-times higher mutation rate than the population average. Evidence was also found (i) for reduced efficiency of selection in small freshwater populations subject to strong genetic drift, (ii) that maternal age associates positively with {micro}, and shorter generation time elevates per-year mutation rates, (iii) that both replication errors and DNA repair efficiency contributed to {micro}, and that (iv) mutation rate variation has a polygenic basis. In general, the results provide support for the DBH identifying elevated mutation rates in populations subject to strong genetic drift.

genomics↗

bioRxiv2026

Recombination rate and efficiency of linked selection in small and large stickleback populations

Population genetic theory predicts that natural selection will be more efficient in large than small populations because genetic drift reduces the efficiency of selection in small populations. Small populations adapting to new environments can also be expected to evolve higher recombination rates to facilitate adaptation as well as to dissociate and purge harmful mutations. We tested these hypotheses (1) by investigating differences in the strength of association between nucleotide diversity ({pi}) and recombination rate across the genomes of nine-spined sticklebacks (Pungitius pungitius) from four small freshwater (mean Ne {approx} 2 578) and four large marine (mean Ne = 86 742) populations, as well as (2) by comparing recombination rates between small and large populations using population specific linkage maps. We found the predicted positive correlation of{pi} with recombination rate from all but the smallest freshwater populations, suggesting prevalent linked selection even after accounting for variation in GC/CpG content, and gene density. Mean recombination rates did not differ between freshwater and marine populations, except that the smallest Ne freshwater population exhibited significantly elevated recombination rate. GWAS analyses suggested a polygenic basis for recombination rates. These results suggest an important role for linked selection in reducing{pi} in low recombination regions especially in large populations. Moreover, as predicted by theory, at least one of the small freshwater populations appears to have evolved a higher recombination rate than its marine ancestors.

evolutionary biology↗

bioRxiv2024

Rate of de novo mutations in the three-spined stickleback

Being a fundamentally important genetic parameter and evolutionary force, estimates of germline mutation rates have many uses in evolutionary biology. However, accurate estimates of de novo mutation (DNM) rates are still relatively scarce even for extensively studied evolutionary biology models. We estimated DNM rates for the three-spined stickleback (Gasterosteus aculeatus), the supermodel of ecology and evolutionary biology. Using a large number of family trios sequenced to depth of 45x coverage, we identified 115 unique mutations genome wide and estimated the DNM rate at {micro} = 5.05 x 10-9/bp/gen without any detectable sex bias. The localised DNM rate was found to be positively correlated with recombination rate supporting the notion that recombination is a mutagenic process. Comparison of {micro} and genomic characteristics to those of the related nine-spined stickleback (Pungitius pungitius) revealed a high degree of similarity suggesting that despite 17.5 million years of independent evolution, the mutational processes in the two species appear to have been conserved.

evolutionary biology↗

bioRxiv2024

SLRfinder: a method to detect candidate sex-linked regions with linkage disequilibrium clustering

Despite their critical roles in genetic sex determination, sex chromosomes remain unknown in many non-model organisms. In contrast to conserved sex chromosomes in mammals and birds, studies of fish, amphibians, and reptiles have found highly labile sex chromosomes with newly evolved sex-linked regions (SLRs). These labile sex chromosomes are important for understanding early sex chromosome evolution but are difficult to identify due to the lack of Y/W degeneration and SLRs limited to small genomic regions. Here we present SLRfinder, a method to identify candidate SLRs and labile sex chromosomes using linkage disequilibrium (LD) clustering, patterns of heterozygosity, and genetic divergence. SLRfinder does not rely on specific sequencing methods or reference genomes and does not require phenotypic sexes which may be unknown from population sampling, although sex information can be incorporated to provide additional inference on candidate SLRs. We tested SLRfinder using various published datasets and compared it to SATC, a method that identifies sex chromosomes based on the depth of coverage and also does not require phenotypic sex. Results show that SATC works better on conserved sex chromosomes (e.g., in African leopards), whereas SLRfinder outperforms SATC in analyzing labile sex chromosomes (e.g., in nine-spined sticklebacks and chum salmon). Since SLRfinder primarily relies on LD clusters, it is expected to be most sensitive to the SLRs harboring structural variants (e.g., inversion) due to strongly reduced recombination rates in heterozygotes. SLRfinder provides a novel and complementary approach for identifying SLRs and uncovering additional sex chromosome diversity in nature.

genomics↗

bioRxiv2023

Secondary contact, introgressive hybridization and genome stabilization in sticklebacks

Advances in genomic studies have revealed that hybridization in nature is pervasive and raised questions about the dynamics of different genetic and evolutionary factors following the initial hybridization event. While recent research has proposed that the genomic outcomes of hybridization might be predictable to some extent, many uncertainties remain. With comprehensive whole-genome sequence data, we investigated the genetic introgression between two divergent lineages of nine-spined sticklebacks (Pungitius pungitius) in the Baltic Sea. We found that the intensity and direction of selection on the introgressed variation varied across different genomic elements: while functionally important regions had experienced reduced rates of introgression, promoter regions showed enrichment. Despite the general trend of negative selection, we identified specific genomic regions that were enriched for introgressed variants and within these regions, we detected footprints of selection, indicating adaptive introgression. We found the selection against the functional changes to be strongest in the vicinity of the secondary contact zone and weaken as a function of distance from the initial contact. Altogether, the results suggest that the stabilization of introgressed variation in the genomes is a complex, multi-stage process involving both negative and positive selection. In spite of the predominance of negative selection against introgressed variants, we also found evidence for adaptive introgression variants likely associated with adaptation to Baltic Sea environmental conditions.

genomics↗

bioRxiv2023

Estimating recent and historical effective population size of marine and freshwater sticklebacks

Effective population size (Ne) is a quantity of central importance in evolutionary biology and population genetics, but often notoriously challenging to estimate. Analyses of Ne are further complicated by the many interpretations of the concept and the alternative approaches to quantify Ne utilising different properties of the data. However, the alternative methods are also informative over different time scales, suggesting that a combination of approaches should allow piecing together the entire continuum of Ne, spanning from the recent to more distant past. To test this in practice, we inferred the Ne continuum for 45 populations of nine-spined sticklebacks (Pungitius pungitius) using whole-genome data with both LD- and coalescent-based methods. Our results show that marine populations exhibit the highest Ne values in contemporary, recent, and historical times, followed by coastal and freshwater populations. They also demonstrate the impact of both recent and historical gene flow on Ne estimates and show that simple summary statistics are informative in comprehending the events in the very recent past and aid in more accurate estimation of NeC, the contemporary Ne, as well as in reconstruction and interpretation of recent demographic histories. Although our sample size for large populations is limited, we found that GONE can provide reasonable Ne estimates. However, due to challenges in detecting subtle genetic drift in large populations, these estimates may represent the lower bound of Ne. Finally, we show that combining GONE and CurrentNe2, both sensitive to population structure, with MSMC2 provides a meaningful interpretation of Ne dynamics over time.

genomics↗

bioRxiv2023

De novo mutation rates in sticklebacks

Mutation rate is a fundamental parameter in population genetics. Apart from being an important scaling parameter for demographic and phylogenetic inference, it allows one to understand at what rate new genetic diversity is generated and what is the expected level of genetic diversity in a population at equilibrium. However, except for well-established model organisms, accurate estimates of de novo mutation rates are available for a very limited number of organisms from the wild. We estimated mutation rates ({micro}) in two marine populations of the nine-spined stickleback (Pungitius pungitius) with the aid of several 2- and 3-generational family pedigrees, deep (>50x) whole genome re-sequencing and a high-quality reference genome. After stringent filtering, we discovered 295 germline mutations from 106 offspring translating to {micro} = 4.64 x 10-9 and {micro} = 4.08 x 10-9 per base, per generation, in the two populations, respectively. Twenty percent of the mutations were shared by full-sibs showing that the level of parental mosaicism was relatively high. Since the estimated {micro} was 3.2 times smaller than the commonly used substitution rate, recalibration with {micro} led to substantial increase in estimated divergence times between different stickleback species. Our estimates of de novo mutation rate should provide a useful resource for research focused on fish population genetics and that of sticklebacks in particular.

genomics↗

bioRxiv2023

Determinants of genetic diversity in sticklebacks

Understanding what determines species and population differences in levels of genetic diversity has important implications for our understanding of evolution, as well as for the conservation and management of wild populations. Previous comparative studies have emphasized the roles of linked selection, life-history trait variation and genomic properties, rather than pure demography, as important determinants of genetic diversity. However, these findings are based on coarse estimates across a range of highly diverged taxa, and it is unclear how well they represent the processes within individual species. We assessed genome-wide genetic diversity ({pi}) in 45 nine-spined stickleback (Pungitius pungitius) populations and found that{pi} varied 15-fold among populations ({pi}min{approx}0.00015,{pi} max{approx}0.0023) whereas estimates of recent effective population sizes varied 122-fold. Analysis of inbreeding coefficients (FROH) estimated from runs of homozygosity revealed strong negative association between{pi} and FROH. Genetic diversity was also negatively correlated with mean body size and longevity, but these associations were not statistically significant after controlling for demographic effects (FROH). The results give strong support for the view that populations demographic features, rather than life history differences, are the chief determinants of genetic diversity in the wild.

evolutionary biology↗

bioRxiv2021

Allopatric origin of sympatric whitefish morphs with insights on the genetic basis of their reproductive isolation

The European whitefish (Coregonus lavaretus) species complex is a classic example of recent adaptive radiation. Here we examine a whitefish population introduced to northern Finnish Lake Tsahkal in late 1960s, where three divergent morphs (viz. littoral, pelagic and profundal feeders) were found ten generations after. Using demographic modelling based on genomic data we show that whitefish morphs evolved during a phase of strict isolation, refuting a rapid symmetric speciation scenario. The lake is now an artificial hybrid zone between morphs originated in allopatry. Despite their current syntopy, clear genetic differentiation remains between two of the three morphs. Using admixture mapping three quantitative trait loci associated with gonad weight variation, a proxy for sexual maturity and spawning time, were identified. We suggest that ecological adaptations in spawning time evolved in allopatry are currently maintaining partial reproductive isolation in the absence of other barriers to gene flow.

evolutionary biology↗

bioRxiv2021

Detailed phylogeographic analysis of sticklebacks exposes challenges in genetic studies of admixed populations

Introgressive hybridization is an important process in evolution but challenging to identify, undermining the efforts to understand its role and significance. On the other hand, many analytical methods assume direct descent from a single common ancestor, and admixture among populations can violate their assumptions and lead to seriously biased results. A detailed analysis of 888 whole genome sequences of nine-spined sticklebacks (Pungitius pungitius) revealed a complex pattern of population ancestry involving multiple waves of gene flow and introgression across northern Europe. The two recognized lineages were found to have drastically different histories and their secondary contact zone was wider than anticipated, displaying a smooth gradient of foreign ancestry with some curious deviations from the expected pattern. Interestingly, the freshwater isolates provided peeks into the past and helped to understand the intermediate states of evolutionary processes. Our analyses and findings paint a detailed picture of the complex colonization history of northern Europe and provide back-drop against which introgression and its role in evolution can be investigated. However, they also expose the challenges in analyses of admixed populations and demonstrate how hidden admixture and colonization history misleads the estimation of admixture proportions and population split times.

genomics↗

bioRxiv2021

Age-dependent genetic architecture underlines similar heritability of body size in sticklebacks

Heritable variation in traits under natural selection is a prerequisite for evolutionary response. While it is recognised that trait heritability may vary spatially and temporally depending under which environmental conditions traits are expressed, less is known about the possibility that genetic variance contributing to the expected selection response in a given trait may vary at different stages of ontogeny. Specifically, whether different loci underlie the expression of a trait throughout development - thus providing an additional source of variation for selection to act on - is unclear. Here we show that the heritability (h2) of body size, an important life history trait, remains constant across ontogeny in a stickleback fish. Nevertheless, both analyses of quantitative trait loci (QTL) and genetic correlations across ages show that different chromosomes/loci contribute to this heritability in different ontogenic time-points. This suggests that body size can respond to selection at different stages of ontogeny but that this response is determined by different loci at different points of development. Hence, this illustrates the notion that diverse genetic architectures may underline similar (expected) phenotypic outcomes, and that similar selection pressures may lead to genetically heterogeneous responses depending on what life stage selection is acting on.

evolutionary biology↗

bioRxiv2021

Dissecting the genetic architecture of quantitative traits using genome-wide identity-by-descent sharing among full-sibs

Additive and dominance genetic variances underlying the expression of quantitative traits are important quantities for predicting short-term responses to selection, but they are notoriously challenging to estimate in most non-model wild populations. Specifically, large-sized or panmictic populations may be characterized by low variance in genetic relatedness among individuals which in turn, can prevent accurate estimation of quantitative genetic parameters. We used estimates of genome-wide identity-by-descent (IBD) sharing from autosomal SNP loci to estimate quantitative genetic parameters for ecologically important traits in nine-spined sticklebacks (Pungitius pungitius) from a large, outbred population. Using empirical and simulated datasets, with varying sample sizes and pedigree complexity, we assessed the performance of different crossing schemes in estimating additive genetic variance and heritability for all traits. We found that low variance in relatedness characteristic of wild outbred populations with high migration rate can impair the estimation of quantitative genetic parameters and bias heritability estimates downwards. On the other hand, the use of a half-sib/full-sib design allowed precise estimation of genetic variance components, and revealed significant additive variance and heritability for all measured traits, with negligible dominance contributions. Genome-partitioning and QTL mapping analyses revealed that most traits had a polygenic basis and were controlled by genes at multiple chromosomes. Furthermore, different QTL contributed to variation in the same traits in different populations suggesting heterogenous underpinnings of parallel evolution at the phenotypic level. Our results provide important guidelines for future studies aimed at estimating adaptive potential in the wild, particularly for those conducted in outbred large-sized populations.

evolutionary biology↗

bioRxiv2021

Population structure limits parallel evolution

Population genetic theory predicts that small effective population sizes (Ne) and restricted gene flow limit the potential for local adaptation. In particular, the probability of evolving similar phenotypes based on shared genetic mechanisms (i.e. parallel evolution), is expected to be reduced. We tested these predictions in a comparative genomic study of two ecologically similar and geographically co-distributed stickleback species (viz. Gasterosteus aculeatus and Pungitius pungitius). We found that P. pungitius harbours less genetic diversity and exhibits higher levels of genetic differentiation and isolation-by-distance than G. aculeatus. Conversely, G. aculeatus exhibits a stronger degree of genetic parallelism across freshwater populations than P. pungitius: 2996 vs. 379 SNPs located within 26 vs nine genomic regions show evidence of selection in multiple freshwater populations of G. aculeatus and P. pungitius, respectively. Most regions involved in parallel evolution in G. aculeatus showed increased levels of divergence, suggestive of selection on ancient haplotypes. In contrast, regions involved in freshwater adaptation in P. pungitius were younger, and often associated with reduced diversity. In accordance with theory, the results suggest that connectivity and genetic drift play crucial roles in determining the levels and geographic distribution of standing genetic variation, providing evidence that population subdivision limits local adaptation and therefore also the likelihood of parallel evolution.

evolutionary biology↗

bioRxiv2020

The rise of the three-spined stickleback: eco-evolutionary consequences of a mesopredator release

Declines of large predatory fish due to overexploitation are restructuring food webs across the globe. It is now becoming evident that restoring these altered food webs requires addressing not only ecological processes, but evolutionary ones as well, because human-induced rapid evolution may in turn affect ecological dynamics. In the central Baltic Sea, abundances of the mesopredatory fish, the three-spined stickleback (Gasterosteus aculeatus), have increased dramatically during the past decades. Time-series data covering 22 years show that this increase coincides with a decline in the number of juvenile perch (Perca fluviatilis), the most abundant predator of stickleback along the coast. We studied the interaction between evolutionary and ecological effects of this mesopredator take-over, by surveying the armour plate morphology of stickleback and the structure of the associated food web. First, we investigated the distribution of different stickleback phenotypes depending on predator abundances and benthic production; and described the stomach content of the stickleback phenotypes using metabarcoding. Second, we explored differences in the relation between different trophic levels and benthic production, between bays where the relative abundance of fish was dominated by stickleback or not; and compared this to previous cage-experiments to support causality of detected correlations. We found two distinct lateral armour plate phenotypes of stickleback, incompletely and completely plated. The proportion of incompletely plated individuals increased with increasing benthic production and decreasing abundances of adult perch. Stomach content analyses showed that the completely plated individuals had a stronger preference for invertebrate herbivores (amphipods) than the incompletely plated ones. In addition, predator dominance interacted with ecosystem production to determine food web structure and the propagation of a trophic cascade: with increasing production, biomass accumulated on the first (macroalgae) and third (stickleback) trophic levels in stickleback-dominated bays, but on the second trophic level (invertebrate herbivores) in perch-dominated bays. Since armour plates are defence structures favoured by natural selection in the presence of fish predators, the phenotype distribution suggest that a novel low-predation regime favours sticklebacks with less armour. Our results indicate that an interaction between evolutionary and ecological effects of the stickleback take-over has the potential to affect food web dynamics.

ecology↗

bioRxiv2020

Convergent genetic architecture underlies parallel pelvic reduction in genetically highly structured stickleback species

Repeated and independent adaptation to specific environmental conditions from standing genetic variation is common. However, if genetic variation is limited, the evolution of similar locally adapted traits may be restricted to genetically different and potentially less optimal solutions or prevented from happening altogether. Using a quantitative trait locus (QTL) mapping approach, we identified the genomic regions responsible for the repeated pelvic reduction (PR) in three crosses between nine-spined stickleback populations expressing full and reduced pelvic structures. In one cross, PR mapped to linkage group 7 (LG7) containing the gene Pitx1, known to control pelvic reduction also in the three-spined stickleback. In the two other crosses, PR was polygenic and attributed to ten novel QTL, of which 90% were unique to specific crosses. When screening the genomes from 27 different populations for deletions in the Pitx1 regulatory element, these were only found in the population in which PR mapped to LG7, even though the morphological data indicated large effect QTL for PR in several other populations as well. Consistent with the available theory and simulations parameterised on empirical data, we hypothesise that the observed variability in genetic architecture of PR is due to heterogeneity in the spatial distribution of standing genetic variation caused by >2x stronger population structuring among freshwater populations and >10x stronger genetic isolation by distance in the sea in nine-spined sticklebacks as compared to three-spined sticklebacks.

evolutionary biology↗

bioRxiv2019

Genome sequencing of the nine-spined stickleback (Pungitius pungitius) provides insights into chromosome evolution.

The Gasterostidae fish family hosts several species that are important models for eco-evolutionary, genetic and genomic research. In particular, a wealth of genetic and genomic data have been generated for the three-spined stickleback (Gasterosteus aculeatus), the ecologys supermodel, while the genomic resources for the nine-spined stickleback (Pungitius pungitius) have remained relatively scarce. Here, we report a high-quality chromosome-level genome assembly of P. pungitius consisting of 5,303 contigs (N50 = 1.2 Mbp) with a total size of 521 Mbp. These contigs were mapped to 21 linkage groups using a high-density linkage map, yielding a final assembly with 98.5% BUSCO completeness. A total of 25,062 protein-coding genes were annotated, and ca. 23% of the assembly was found to consist of repetitive elements. A comprehensive analysis of repetitive elements uncovered centromeric-specific tandem repeats and provided insights into the evolution of retrotransposons. A multigene phylogenetic analysis inferred a divergence time of about 26 million years (MYA) between nine- and three-spined sticklebacks, which is far older than the commonly assumed estimate of 13 MYA. Compared to the three-spined stickleback, we identified an additional duplication of several genes in the hemoglobin cluster. Sequencing data from populations adapted to different environments indicated potential copy number variations in hemoglobin genes. Furthermore, genome-wide synteny comparisons between three- and nine-spined sticklebacks identified chromosomal rearrangements underlying the karyotypic differences between the two species. The high-quality chromosome-scale assembly of the nine-spined stickleback genome obtained with long-read sequencing technology provides a crucial resource for comparative and population genomic investigations of stickleback fishes and teleosts.

genomics↗