Adaptive and non-adaptive divergence in a common landscape

Raeymaekers, Joost; Chaturvedi, Anurag; Hablützel, Pascal I.; Verdonck, Io; Hellemans, Bart; Maes, Grégory E.; Meester, Luc De; Volckaert, Filip

doi:10.1038/s41467-017-00256-6

Cited by 56 publications

(84 citation statements)

References 75 publications

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“…Shared outliers and/or correlated differentiation are then often interpreted as indication that divergent natural selection has targeted the same genes in multiple population pairs, and hence as evidence of parallel evolution at the molecular level. However, such analyses are frequently performed with low physical marker resolution (recent examples: Egger, Roesti, Böhne, Roth, & Salzburger, ; Perreault‐Payette et al., ; Ravinet et al., ; Raeymaekers et al., ; Rougemont et al., ; Stuart et al., ; Trucchi, Frajman, Haverkamp, Schönswetter, & Paun, ). Consequently, single markers are highly unlikely to coincide with polymorphisms under direct selection.…”

Section: Resultsmentioning

confidence: 99%

Meta‐analysis of chromosome‐scale crossover rate variation in eukaryotes and its significance to evolutionary genomics

et al. 2018

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Understanding the distribution of crossovers along chromosomes is crucial to evolutionary genomics because the crossover rate determines how strongly a genome region is influenced by natural selection on linked sites. Nevertheless, generalities in the chromosome-scale distribution of crossovers have not been investigated formally. We fill this gap by synthesizing joint information on genetic and physical maps across 62 animal, plant and fungal species. Our quantitative analysis reveals a strong and taxonomically widespread reduction of the crossover rate in the centre of chromosomes relative to their peripheries. We demonstrate that this pattern is poorly explained by the position of the centromere, but find that the magnitude of the relative reduction in the crossover rate in chromosome centres increases with chromosome length. That is, long chromosomes often display a dramatically low crossover rate in their centre, whereas short chromosomes exhibit a relatively homogeneous crossover rate. This observation is compatible with a model in which crossover is initiated from the chromosome tips, an idea with preliminary support from mechanistic investigations of meiotic recombination. Consequently, we show that organisms achieve a higher genome-wide crossover rate by evolving smaller chromosomes. Summarizing theory and providing empirical examples, we finally highlight that taxonomically widespread and systematic heterogeneity in crossover rate along chromosomes generates predictable broad-scale trends in genetic diversity and population differentiation by modifying the impact of natural selection among regions within a genome. We conclude by emphasizing that chromosome-scale heterogeneity in crossover rate should urgently be incorporated into analytical tools in evolutionary genomics, and in the interpretation of resulting patterns.

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Section: Resultsmentioning

confidence: 99%

Meta‐analysis of chromosome‐scale crossover rate variation in eukaryotes and its significance to evolutionary genomics

et al. 2018

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“…Most previous studies of phenotypic and genomic parallelism have made deductions based on comparisons involving multiple species (Conte et al., ; Raeymaekers et al., ), have focused on detecting if parallelism is a general feature within single species or species complexes (Bradbury et al., ; Gagnaire et al., ; Losos, ; Ravinet et al., ; Terekhanova et al., ) or have focused on detecting the genetic architecture and possible genomic parallelism associated with individual traits (Chan et al., ; Colosimo et al., ; Cooley, Modliszewski, Rommel, & Willis, ; Laurent et al., ). Here, we took a different approach and made use of the presence of separate systems within a single species showing contrasting patterns of parallelism.…”

Section: Discussionmentioning

confidence: 99%

“…Most previous studies of phenotypic and genomic parallelism have made deductions based on comparisons involving multiple species (Conte et al, 2012;Raeymaekers et al, 2017), have focused on detecting if parallelism is a general feature within single species or species complexes (Bradbury et al, 2010;Gagnaire et al, 2013;Losos, 2009;Ravinet et al, 2016;Terekhanova et al, 2014) showing contrasting patterns of parallelism. This allowed for adding different aspects to our understanding of the dynamics of parallelism than could have been obtained from analysing each system on its own.…”

Section: Discussionmentioning

confidence: 99%

Genomic parallelism and lack thereof in contrasting systems of three‐spined sticklebacks

et al. 2018

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Parallel evolution and the extent to which it involves gene reuse have attracted much interest. Whereas it has theoretically been predicted under which circumstances gene reuse is expected, empirical studies that directly compare systems showing high and low parallelism are rare. Three-spined stickleback (Gasterosteus aculeatus), where freshwater populations have been independently founded by ancestral marine populations, represent prime examples of phenotypic and genomic parallelism, but cases exist where parallelism is low. Based on RAD (restriction site associated DNA) sequencing, we analysed SNPs and chromosome inversions in populations in Denmark and Greenland showing low and high parallelism, respectively. We identified parallelism across freshwater populations in Greenland at genomic regions previously identified to be associated with marine-freshwater divergence. These same markers also separated Danish marine and freshwater sticklebacks, albeit to a weaker extent. Hence, parallelism was not absent in Denmark but possibly constrained by spatially and temporally varying selection. Divergence time estimates found one Danish freshwater population to be much older than the others. It also deviated strongly with respect to parallelism and may represent earlier postglacial colonization based on a different pool of standing variation and eliciting different adaptive responses to freshwater conditions. These findings provide empirical support to previous suggestions that the time since replicate populations had access to a common pool of standing variation is a major factor determining gene reuse. At last, based on the observed parallelism in the Greenlandic system we discuss the predictability of adaptive responses in newly established populations.

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“…The nine-spined stickleback (Pungitius pungitius Linnaeus, 1758), suggested to have diverged from the three-spined stickleback at least 13 million years ago ), is the next most frequently utilized model species from the Gasterostidae family. It has recently gained recognition as an especially interesting model system for comparative investigations of adaptive evolution (e.g (Shapiro et al 2006;Shikano et al 2013;Raeymaekers et al 2017)), sex chromosome evolution (e.g (Natri et al 2019)) and study of adaptive divergence in the face of strong genetic drift (Merilä 2013;Karhunen et al 2014). Although the nine-and three-spined sticklebacks share nearly identical circumpolar distribution ranges (Wootton 1984), the former shows a far greater degree of genetic population structuring than the latter (Shikano et al 2010;DeFaveri et al 2011).…”

Section: Introductionmentioning

confidence: 99%

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

Varadharajan

Rastas

Löytynoja

et al. 2019

Preprint

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The Gasterostidae fish family hosts several species that are important models for ecoevolutionary, genetic and genomic research. In particular, a wealth of genetic and genomic data have been generated for the three-spined stickleback (Gasterosteus aculeatus), the 'ecology's 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 521Mbp. 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.

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Adaptive and non-adaptive divergence in a common landscape

Cited by 56 publications

References 75 publications

Meta‐analysis of chromosome‐scale crossover rate variation in eukaryotes and its significance to evolutionary genomics

Meta‐analysis of chromosome‐scale crossover rate variation in eukaryotes and its significance to evolutionary genomics

Genomic parallelism and lack thereof in contrasting systems of three‐spined sticklebacks

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

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