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1.
Mol Ecol ; 31(3): 811-821, 2022 02.
Article in English | MEDLINE | ID: mdl-34753205

ABSTRACT

Adaptation to derived habitats often occurs from standing genetic variation. The maintenance within ancestral populations of genetic variants favourable in derived habitats is commonly ascribed to long-term antagonism between purifying selection and gene flow resulting from hybridization across habitats. A largely unexplored alternative idea based on quantitative genetic models of polygenic adaptation is that variants favoured in derived habitats are neutral in ancestral populations when their frequency is relatively low. To explore the latter, we first identify genetic variants important to the adaptation of threespine stickleback fish (Gasterosteus aculeatus) to a rare derived habitat-nutrient-depleted acidic lakes-based on whole-genome sequence data. Sequencing marine stickleback from six locations across the Atlantic Ocean then allows us to infer that the frequency of these derived variants in the ancestral habitat is unrelated to the likely opportunity for gene flow of these variants from acidic-adapted populations. This result is consistent with the selective neutrality of derived variants within the ancestor. Our study thus supports an underappreciated explanation for the maintenance of standing genetic variation, and calls for a better understanding of the fitness consequences of adaptive variation across habitats and genomic backgrounds.


Subject(s)
Smegmamorpha , Animals , Gene Flow , Genetic Variation , Genome , Selection, Genetic , Smegmamorpha/genetics
2.
Nat Commun ; 12(1): 4850, 2021 08 11.
Article in English | MEDLINE | ID: mdl-34381033

ABSTRACT

How ecological divergence causes strong reproductive isolation between populations in close geographic contact remains poorly understood at the genomic level. We here study this question in a stickleback fish population pair adapted to contiguous, ecologically different lake and stream habitats. Clinal whole-genome sequence data reveal numerous genome regions (nearly) fixed for alternative alleles over a distance of just a few hundred meters. This strong polygenic adaptive divergence must constitute a genome-wide barrier to gene flow because a steep cline in allele frequencies is observed across the entire genome, and because the cline center closely matches the habitat transition. Simulations confirm that such strong divergence can be maintained by polygenic selection despite high dispersal and small per-locus selection coefficients. Finally, comparing samples from near the habitat transition before and after an unusual ecological perturbation demonstrates the fragility of the balance between gene flow and selection. Overall, our study highlights the efficacy of divergent selection in maintaining reproductive isolation without physical isolation, and the analytical power of studying speciation at a fine eco-geographic and genomic scale.


Subject(s)
Ecosystem , Genome/genetics , Reproductive Isolation , Smegmamorpha/genetics , Adaptation, Physiological/genetics , Animals , Floods , Gene Flow , Genetic Speciation , Genetic Variation , Lakes , Multifactorial Inheritance , Phenotype , Rivers , Selection, Genetic
3.
Sci Rep ; 9(1): 19205, 2019 12 16.
Article in English | MEDLINE | ID: mdl-31844092

ABSTRACT

Most knowledge on biodiversity derives from the study of charismatic macro-organisms, such as birds and trees. However, the diversity of micro-organisms constitutes the majority of all life forms on Earth. Here, we ask if the patterns of richness inferred for macro-organisms are similar for micro-organisms. For this, we barcoded samples of soil, litter and insects from four localities on a west-to-east transect across Amazonia. We quantified richness as Operational Taxonomic Units (OTUs) in those samples using three molecular markers. We then compared OTU richness with species richness of two relatively well-studied organism groups in Amazonia: trees and birds. We find that OTU richness shows a declining west-to-east diversity gradient that is in agreement with the species richness patterns documented here and previously for birds and trees. These results suggest that most taxonomic groups respond to the same overall diversity gradients at large spatial scales. However, our results show a different pattern of richness in relation to habitat types, suggesting that the idiosyncrasies of each taxonomic group and peculiarities of the local environment frequently override large-scale diversity gradients. Our findings caution against using the diversity distribution of one taxonomic group as an indication of patterns of richness across all groups.


Subject(s)
Birds/physiology , Trees/physiology , Animals , Biodiversity , Ecosystem , Geography/methods , Insecta/physiology
4.
Evol Lett ; 3(1): 28-42, 2019 Feb.
Article in English | MEDLINE | ID: mdl-30788140

ABSTRACT

Genomic studies of parallel (or convergent) evolution often compare multiple populations diverged into two ecologically different habitats to search for loci repeatedly involved in adaptation. Because the shared ancestor of these populations is generally unavailable, the source of the alleles at adaptation loci, and the direction in which their frequencies were shifted during evolution, remain elusive. To shed light on these issues, we here use multiple populations of threespine stickleback fish adapted to two different types of derived freshwater habitats-basic and acidic lakes on the island of North Uist, Outer Hebrides, Scotland-and the present-day proxy of their marine ancestor. In a first step, we combine genome-wide pooled sequencing and targeted individual-level sequencing to demonstrate that ecological and phenotypic parallelism in basic-acidic divergence is reflected by genomic parallelism in dozens of genome regions. Exploiting data from the ancestor, we next show that the acidic populations, residing in ecologically more extreme derived habitats, have adapted by accumulating alleles rare in the ancestor, whereas the basic populations have retained alleles common in the ancestor. Genomic responses to selection are thus predictable from the ecological difference of each derived habitat type from the ancestral one. This asymmetric sorting of standing genetic variation at loci important to basic-acidic divergence has further resulted in more numerous selective sweeps in the acidic populations. Finally, our data suggest that the maintenance in marine fish of standing variation important to adaptive basic-acidic differentiation does not require extensive hybridization between the marine and freshwater populations. Overall, our study reveals striking genome-wide determinism in both the loci involved in parallel divergence, and in the direction in which alleles at these loci have been selected.

5.
Mol Ecol ; 27(11): 2477-2497, 2018 06.
Article in English | MEDLINE | ID: mdl-29676042

ABSTRACT

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.


Subject(s)
Chromosomes/genetics , Crossing Over, Genetic/genetics , Eukaryota/genetics , Genetic Variation/genetics , Animals , Biological Evolution , Genome/genetics , Genomics/methods
6.
PLoS One ; 12(10): e0186929, 2017.
Article in English | MEDLINE | ID: mdl-29059215

ABSTRACT

The three-spined stickleback (Gasterosteus aculeatus L., hereafter 'stickleback') is a common mesopredatory fish in marine, coastal and freshwater areas. In large parts of the Baltic Sea, stickleback densities have increased >10-fold during the last decades, and it is now one of the dominating fish species both in terms of biomass and effects on lower trophic levels. Still, relatively little is known about its diet-knowledge which is essential to understand the increasing role sticklebacks play in the ecosystem. Fish diet analyses typically rely on visual identification of stomach contents, a labour-intensive method that is made difficult by prey digestion and requires expert taxonomic knowledge. However, advances in DNA-based metabarcoding methods promise a simultaneous identification of most prey items, even from semi-digested tissue. Here, we studied the diet of stickleback from the western Baltic Sea coast using both DNA metabarcoding and visual analysis of stomach contents. Using the cytochrome oxidase (CO1) marker we identified 120 prey taxa in the diet, belonging to 15 phyla, 83 genera and 84 species. Compared to previous studies, this is an unusually high prey diversity. Chironomids, cladocerans and harpacticoids were dominating prey items. Large sticklebacks were found to feed more on benthic prey, such as amphipods, gastropods and isopods. DNA metabarcoding gave much higher taxonomic resolution (median rank genus) than visual analysis (median rank order), and many taxa identified using barcoding could not have been identified visually. However, a few taxa identified by visual inspection were not revealed by barcoding. In summary, our results suggest that the three-spined stickleback feeds on a wide variety of both pelagic and benthic organisms, indicating that the strong increase in stickleback populations may affect many parts of the Baltic Sea coastal ecosystem.


Subject(s)
DNA Barcoding, Taxonomic , Ecosystem , Smegmamorpha/physiology , Animals , Smegmamorpha/genetics
7.
R Soc Open Sci ; 4(8): 170315, 2017 Aug.
Article in English | MEDLINE | ID: mdl-28878981

ABSTRACT

Precision and reliability of barcode-based biodiversity assessment can be affected at several steps during acquisition and analysis of data. Identification of operational taxonomic units (OTUs) is one of the crucial steps in the process and can be accomplished using several different approaches, namely, alignment-based, probabilistic, tree-based and phylogeny-based. The number of identified sequences in the reference databases affects the precision of identification. This paper compares the identification of marine nematode OTUs using alignment-based, tree-based and phylogeny-based approaches. Because the nematode reference dataset is limited in its taxonomic scope, OTUs can only be assigned to higher taxonomic categories, families. The phylogeny-based approach using the evolutionary placement algorithm provided the largest number of positively assigned OTUs and was least affected by erroneous sequences and limitations of reference data, compared to alignment-based and tree-based approaches.

9.
Methods Mol Biol ; 1452: 197-207, 2016.
Article in English | MEDLINE | ID: mdl-27460379

ABSTRACT

This protocol details the preparation of multiplexed amplicon libraries for metabarcoding (amplicon-based) studies of microscopic marine eukaryotes. Metabarcoding studies, based on the amplification of a taxonomically informative marker from a collection of organisms or an environmental sample, can be performed to analyze biodiversity patterns or predator-prey interactions. For Metazoa, we use the mitochondrial cytochrome oxidase 1 (CO1) or the small ribosomal subunit (SSU) markers. Here, we describe a strategy for the preparation of multiplexed Illumina MiSeq libraries using a dual-PCR approach for the addition of index and adaptor sequences.


Subject(s)
DNA Barcoding, Taxonomic/methods , Polymerase Chain Reaction/methods , Biodiversity , Sequence Analysis, DNA
10.
Methods Mol Biol ; 1452: 209-18, 2016.
Article in English | MEDLINE | ID: mdl-27460380

ABSTRACT

Amplicon-based studies of marine microscopic eukaryotes, also referred to as metabarcoding studies, can be performed to analyze patterns of biodiversity or predator-prey interactions targeting the mitochondrial cytochrome oxidase 1 (CO1) or the small ribosomal subunit (SSU) markers. Because high-throughput sequencing (HTS) Illumina platforms provide millions of reads per run, hundreds of samples may be sequenced simultaneously. This protocol details the preparation of multiplexed amplicon libraries for Illumina MiSeq sequencing. We describe a strategy for sample multiplexing using a combination of tailed PCR primers and ligation of indexed adapters.


Subject(s)
Marine Biology/methods , Electron Transport Complex IV/genetics , Eukaryota/genetics , High-Throughput Nucleotide Sequencing , Ribosome Subunits, Small/genetics , Software , Water Microbiology
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