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

Abstract

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 widely different properties of the data. On the other hand, alternative methods are informative for different time scales such that a set of complementary methods should allow piecing together the entire continuum of Ne from a few generations before the present to the distant past. To test this in practice, we inferred the continuum of Ne for 45 nine-spined stickleback populations (Pungitius pungitius) using whole-genome data. We found that the marine populations had the largest historical and recent Ne, followed by coastal and other freshwater populations. We identified the impact of both recent and historical gene flow on the Ne estimates obtained from different methods and found that simple summary statistics are informative in comprehending the events in the very recent past. Overall, our analyses showed that the coalescence-based trajectories of Ne in the recent past and the LD-based estimates of near-contemporary Ne are incongruent, though in some cases the incongruence might be explained by specific demographic events. Despite still lacking accuracy and resolution for the very recent past, the sequentially Markovian coalescent-based methods seem to provide the most meaningful interpretation of the real-life Ne varying across time.

Secondary contact, introgressive hybridization and genome stabilization in sticklebacks

“…The data were subsetted from the vcf file provided in Feng et al (2023) using BCFtools v.1.7 (Li et al, 2009). Following Feng et al (2022), DEN-NOR (from the North Sea) was used as the WL source population, GBR-GRO (from the UK) as the WL reference population, RUS-LEV (from the White Sea) as the EL source population, and CAN-TEM (from Quebec, Canada) was selected as the outgroup.…”

“…1a and Table S1). In the earlier analyses of this data (Feng et al, 2023), the reads were first mapped to the latest nine-spined stickleback reference genome (Kivikoski et al, 2021) using the Burrows-Wheeler Aligner v.0.7.17 (BWA-MEM algorithm, Li, 2013) and its default parameters. Duplicate reads were marked with SAMtools v.1.7 (Li et al, 2009) and variant calling was performed with the Genome Analysis Toolkit (GATK) v.4.0.1.2 (McKenna et al, 2010) following the GATK Best Practices workflows.…”

“…(b) Map of the sea surface temperature and (c) salinity of the Baltic Sea and its surroundings, adapted from Garcia et al (2019). (d) Demographic history of parental, reference, and admixed populations from 30,000 years ago (kya) to the present, adapted from Feng et al (2023). The blue, green, and red colors indicate the EL parental population RUS-LEV, WL parental population DEN-NOR, and WL reference population GBR-GRO, respectively; the orange and green colors indicate GER-RUE and POL-GDY, the two southern Baltic Sea populations, respectively.…”

“…The nine-spined stickleback ( Pungtitius pungitius ) is a small euryhaline teleost fish that inhabits circumpolar regions of the northern hemisphere. The evolutionary history of nine-spined sticklebacks has been extensively studied (Aldenhoven et al, 2010; Shikano, Ramadevi, et al, 2010; Teacher et al, 2011; Bruneaux et al, 2013; Natri et al, 2019; Guo et al, 2019; Feng et al, 2022, 2023), and in Europe two distinct evolutionary lineages have been identified: the Western European lineage (WL) and the Eastern European lineage (EL). Despite the lineages exhibiting distinct sex determination systems (Natri et al, 2019) and highly differentiated mitochondrial haplotypes (Aldenhoven et al, 2010; Shikano, Shimada, et al, 2010; Guo et al, 2019), they are known to interbreed (Natri et al, 2019) and populations in the Baltic Sea area display a gradient of mixed ancestry (Feng et al, 2022).…”

“…The objective of this study was to investigate the mechanisms influencing the introgression landscape between two evolutionary lineages of nine-spined sticklebacks ( Pungitius pungitius ) after their secondary contact in northern Europe. To this end, we employed whole-genome sequence data from 284 individuals belonging to 13 populations across the Baltic Sea hybrid zone, subsampled from Feng et al (2023). Our analysis aimed to estimate the levels of introgression across various populations and different genomic regions, thereby characterizing the genomic landscape of introgression across the hybrid zone.…”