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Ecological speciation in European whitefish is driven by a large-gaped predator.

ABSTRACT: Lake-dwelling fish that form species pairs/flocks characterized by body size divergence are important model systems for speciation research. Although several sources of divergent selection have been identified in these systems, their importance for driving the speciation process remains elusive. A major problem is that in retrospect, we cannot distinguish selection pressures that initiated divergence from those acting later in the process. To address this issue, we studied the initial stages of speciation in European whitefish (Coregonus lavaretus) using data from 358 populations of varying age (26-10,000 years). We find that whitefish speciation is driven by a large-growing predator, the northern pike (Esox lucius). Pike initiates divergence by causing a largely plastic differentiation into benthic giants and pelagic dwarfs: ecotypes that will subsequently develop partial reproductive isolation and heritable differences in gill raker number. Using an eco-evolutionary model, we demonstrate how pike's habitat specificity and large gape size are critical for imposing a between-habitat trade-off, causing prey to mature in a safer place or at a safer size. Thereby, we propose a novel mechanism for how predators may cause dwarf/giant speciation in lake-dwelling fish species.

SUBMITTER: Ohlund G

PROVIDER: S-EPMC7293097 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Ecological speciation in European whitefish is driven by a large-gaped predator.

Öhlund Gunnar G Bodin Mats M Nilsson Karin A KA Öhlund Sven-Ola SO Mobley Kenyon B KB Hudson Alan G AG Peedu Mikael M Brännström Åke Å Bartels Pia P Præbel Kim K Hein Catherine L CL Johansson Petter P Englund Göran G

Evolution letters 20200513 3

Lake-dwelling fish that form species pairs/flocks characterized by body size divergence are important model systems for speciation research. Although several sources of divergent selection have been identified in these systems, their importance for driving the speciation process remains elusive. A major problem is that in retrospect, we cannot distinguish selection pressures that initiated divergence from those acting later in the process. To address this issue, we studied the initial stages of ...[more]

PMID: 32547784

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Project description:In bacteria, physiological change may be effected by a single gene acquisition, producing ecological differentiation without genetic isolation. Natural selection acting on such differences can reduce the frequency of genotypes that arise from recombination at these loci. However, gene acquisition can only account for recombination interference in the fraction of the genome that is tightly linked to the integration site. To identify additional loci that contribute to adaptive differences, we examined orthologous genes in species of Enterobacteriaceae to identify significant differences in the degree of codon selection. Significance was assessed using the Adaptive Codon Enrichment metric, which accounts for the variation in codon usage bias that is expected to arise from mutation and drift; large differences in codon usage bias were identified in more genes than would be expected to arise from stochastic processes alone. Genes in the same operon showed parallel differences in codon usage bias, suggesting that changes in the overall levels of gene expression led to changes in the degree of adaptive codon usage. Most significant differences between orthologous operons were found among those involved with specific environmental adaptations, whereas "housekeeping" genes rarely showed significant changes. When considered together, the loci experiencing significant changes in codon selection outnumber potentially adaptive gene acquisition events. The identity of genes under strong codon selection seems to be influenced by the habitat from which the bacteria were isolated. We propose a two-stage model for how adaptation to different selective regimes can drive bacterial speciation. Initially, gene acquisitions catalyze rapid ecological differentiation, which modifies the utilization of genes, thereby changing the strength of codon selection on them. Alleles develop fitness variation by substitution, producing recombination interference at these loci in addition to those flanking acquired genes, allowing sequences to diverge across the entire genome and establishing genetic isolation (i.e., protection from frequent homologous recombination).

Project description:BackgroundSpeciation reversal: the erosion of species differentiation via an increase in introgressive hybridization due to the weakening of previously divergent selection regimes, is thought to be an important, yet poorly understood, driver of biodiversity loss. Our study system, the Alpine whitefish (Coregonus spp.) species complex is a classic example of a recent postglacial adaptive radiation: forming an array of endemic lake flocks, with the independent origination of similar ecotypes among flocks. However, many of the lakes of the Alpine radiation have been seriously impacted by anthropogenic nutrient enrichment, resulting in a collapse in neutral genetic and phenotypic differentiation within the most polluted lakes. Here we investigate the effects of eutrophication on the selective forces that have shaped this radiation, using population genomics. We studied eight sympatric species assemblages belonging to five independent parallel adaptive radiations, and one species pair in secondary contact. We used AFLP markers, and applied FST outlier (BayeScan, Dfdist) and logistic regression analyses (MatSAM), to identify candidate regions for disruptive selection in the genome and their associations with adaptive traits within each lake flock. The number of outlier and adaptive trait associated loci identified per lake were then regressed against two variables (historical phosphorus concentration and contemporary oxygen concentration) representing the strength of eutrophication.ResultsWhilst we identify disruptive selection candidate regions in all lake flocks, we find similar trends, across analysis methods, towards fewer disruptive selection candidate regions and fewer adaptive trait/candidate loci associations in the more polluted lakes.ConclusionsWeakened disruptive selection and a concomitant breakdown in reproductive isolating mechanisms in more polluted lakes has lead to increased gene flow between coexisting Alpine whitefish species. We hypothesize that the resulting higher rates of interspecific recombination reduce either the number or extent of genomic islands of divergence surrounding loci evolving under disruptive natural selection. This produces the negative trend seen in the number of selection candidate loci recovered during genome scans of whitefish species flocks, with increasing levels of anthropogenic eutrophication: as the likelihood decreases that AFLP restriction sites will fall within regions of heightened genomic divergence and therefore be classified as F(ST) outlier loci. This study explores for the first time the potential effects of human-mediated relaxation of disruptive selection on heterogeneous genomic divergence between coexisting species.

Dataset Information

Ecological speciation in European whitefish is driven by a large-gaped predator.

Publications

Ecological speciation in European whitefish is driven by a large-gaped predator.

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