Cast away in the Adriatic: Low degree of parallel genetic differentiation in three‐spined sticklebacks

Dahms, Carolin; Kemppainen, Petri; Zanella, L. N.; Zanella, Davor; Carosi, Antonella; Merilä, Juha; Momigliano, Paolo

doi:10.1111/mec.16295

Cited by 9 publications

(9 citation statements)

References 113 publications

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“…The TreeMix analysis was then run as per Dahms et al (2022). Briefly, 500 TreeMix bootstrap replicates were created using a SNP block size of 100 for estimating the covariance matrix without migration events.…”

Section: Methodsmentioning

confidence: 99%

“…First, a list of sites with quality control (-uniqueOnly 1, -remove_bads 1, -minQ 20, -minMapQ 20, -SNP_pval 1e-6), a minor allele frequency of 0.05 (-minMaf 0.05) and allowing for 50% missingness (-minInd 64) was used to calculate minor allele frequencies for each population, which were filtered further for 20% missingness and combined into a final data set of 11,896 sites. The TreeMix analysis was then run as per Dahms et al (2022). Briefly, 500 TreeMix bootstrap replicates were created using a SNP block size of 100 for estimating the covariance matrix without migration events.…”

Section: Phylogenetic Analysesmentioning

confidence: 99%

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Rapid intralacustrine evolution of an invasive pelagic three-spined stickleback (Gasterosteus aculeatus) ecotype in Lake Constance

Dahms

Roch²,

Elmer

et al. 2022

Preprint

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The rapid invasion of the pelagic zone in Lake Constance by three-spined sticklebacks (Gasterosteus aculeatus) since 2012 and their subsequent drastic population growth has had stark ecosystem-wide effects, such as food-web shifts and declines in native biodiversity, including commercially important fish species. Yet, the origin of this invasive pelagic ecotype remains unclear. This study aims to determine if the pelagic ecotype arose in situ from the existing littoral population or following external colonisation, identify potential phenotypic differences between individuals from different habitats, and assess genomic signals of selection. Integrating RAD-sequencing of Lake Constance individuals and whole-genome sequence data for European outgroup populations, this study shows that the pelagic Lake Constance population likely arose recently within the lake from the littoral population, with only weak genome-wide differentiation between individuals from different habitats. This is further supported by minimal differences in meristic and morphometric traits, with shape differences only found between pelagic/inflow sticklebacks and littoral sticklebacks. Using genome scans, we identified multiple outlier loci between littoral and pelagic ecotypes across the genome, potentially suggesting early signs of sympatric speciation despite high connectivity. Furthermore, increased differentiation between pelagic and littoral sticklebacks for body shape-associated loci and the overlap of outlier loci with quantitative trait loci for ecologically relevant traits points toward a driving role of selection in this pelagic invasion. This study provides an important example of rapid ecological diversification from standing genetic variation and a rare case of littoral-pelagic ecotype divergence under high gene flow in a large oligotrophic lake. Ultimately, the results of this study will have major implications for the management of the invasive pelagic ecotype, and the entire stickleback population as a whole.

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Section: Methodsmentioning

confidence: 99%

Section: Phylogenetic Analysesmentioning

confidence: 99%

Rapid intralacustrine evolution of an invasive pelagic three-spined stickleback (Gasterosteus aculeatus) ecotype in Lake Constance

Dahms

Roch²,

Elmer

et al. 2022

Preprint

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“…One set of factors that may help explain these broadscale differences is that effective population size and genetic structure are generally higher, and gene flow is lower, in anadromous species such as shad, and those in freshwater, compared with stickleback, whitefish, herring, and snails (Waples, 1998 ). Indeed, at higher geographic scales (Fang et al, 2020 , 2021 ; Magalhaes et al, 2021 ; Roberts Kingman et al, 2021 ), and when N E or genetic diversity is limited due to historical factors (Dahms et al, 2022 ), parallelism in stickleback is more moderate than at the regional or local scales.…”

Section: Discussionmentioning

confidence: 99%

The genetics of adaptation in freshwater Eurasian shad (Alosa)

Sabatino

Pereira

Carneiro

et al. 2022

Ecology and Evolution

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Studying the genetics of phenotypic convergence can yield important insights into adaptive evolution. Here, we conducted a comparative genomic study of four lineages (species and subspecies) of anadromous shad ( Alosa ) that have independently evolved life cycles entirely completed in freshwater. Three naturally diverged ( A . fallax lacustris , A . f . killarnensis , and A . macedonica ), and the fourth ( A . alosa ) was artificially landlocked during the last century. To conduct this analysis, we assembled and annotated a draft of the A . alosa genome and generated whole‐genome sequencing for 16 anadromous and freshwater populations of shad. Widespread evidence for parallel genetic changes in freshwater populations within lineages was found. In freshwater A . alosa , which have only been diverging for tens of generations, this shows that parallel adaptive evolution can rapidly occur. However, parallel genetic changes across lineages were comparatively rare. The degree of genetic parallelism was not strongly related to the number of shared polymorphisms between lineages, thus suggesting that other factors such as divergence among ancestral populations or environmental variation may influence genetic parallelism across these lineages. These overall patterns were exemplified by genetic differentiation involving a paralog of ATPase ‐ α1 that appears to be under selection in just two of the more distantly related lineages studied, A . f . lacustris and A . alosa . Our findings provide insights into the genetic architecture of adaptation and parallel evolution along a continuum of population divergence.

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“…In fact, studies of sticklebacks have so far resorted to using the substitution rates between three- ( Gasterosteus aculeatus ) and nine-spined stickleback (Guo et al 2013) and an estimate of divergence time as proxy of µ (e.g. Liu et al 2018; Ravinet et al 2018; Varadharjan et al 2019; Yamasaki et al 2020; Dahms et al 2022; Feng et al 2022).…”

Section: Introductionmentioning

confidence: 99%

De novomutation rates in sticklebacks

Zhang

Reid

Sands

et al. 2023

Preprint

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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 (mu) 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 mu = 4.64 x 10 to the -9 and mu = 4.08 x 10 to the -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 mu was 3.2 times smaller than the commonly used substitution rate, recalibration with mu 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.

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Cast away in the Adriatic: Low degree of parallel genetic differentiation in three‐spined sticklebacks

Cited by 9 publications

References 113 publications

Rapid intralacustrine evolution of an invasive pelagic three-spined stickleback (Gasterosteus aculeatus) ecotype in Lake Constance

Rapid intralacustrine evolution of an invasive pelagic three-spined stickleback (Gasterosteus aculeatus) ecotype in Lake Constance

The genetics of adaptation in freshwater Eurasian shad (Alosa)

De novomutation rates in sticklebacks

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