Parallel adaptive evolution
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Parallel adaptive radiations have arisen following the colonization of islands by lizards and lakes by fishes. In these classic examples, parallel adaptive radiation is a response to the ecological opportunities afforded by the colonization of novel ecosystems and similar adaptive landscapes that favour the evolution of similar suites of ecomorphs, despite independent evolutionary histories. Here, we demonstrate that parallel adaptive radiations of cichlid fishes arose in South American rivers. Speciation-assembled communities of pike cichlids (Crenicichla) have independently diversified into similar suites of novel ecomorphs in the Uruguay and Paraná Rivers, including crevice feeders, periphyton grazers and molluscivores. There were bursts in phenotypic evolution associated with the colonization of each river and the subsequent expansion of morphospace following the evolution of the ecomorphs. These riverine clades demonstrate that characteristics emblematic of textbook parallel adaptive radiations of island- and lake-dwelling assemblages are feasible evolutionary outcomes even in labile ecosystems such as rivers.
- Klíčová slova
- Crenicichla, cichlid, convergence, diversification, parallel evolution, species flock,
- MeSH
- biologická adaptace genetika MeSH
- biologická evoluce * MeSH
- cichlidy anatomie a histologie genetika MeSH
- ekosystém MeSH
- fenotyp MeSH
- fylogeneze MeSH
- jednonukleotidový polymorfismus genetika MeSH
- jezera MeSH
- ostrovy MeSH
- řeky * MeSH
- sekvenování celého genomu MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- Geografické názvy
- ostrovy MeSH
- Uruguay MeSH
Parallel evolution is common in nature and provides one of the most compelling examples of rapid environmental adaptation. In contrast to the recent burst of studies addressing genomic basis of parallel evolution, integrative studies linking genomic and phenotypic parallelism are scarce. Edaphic islands of toxic serpentine soils provide ideal systems for studying rapid parallel adaptation in plants, imposing strong, spatially replicated selection on recently diverged populations. We leveraged threefold independent serpentine adaptation of Arabidopsis arenosa and combined reciprocal transplants, ion uptake phenotyping, and available genome-wide polymorphisms to test if parallelism is manifested to a similar extent at both genomic and phenotypic levels. We found pervasive phenotypic parallelism in functional traits yet with varying magnitude of fitness differences that was congruent with neutral genetic differentiation between populations. Limited costs of serpentine adaptation suggest absence of soil-driven trade-offs. On the other hand, the genomic parallelism at the gene level was significant, although relatively minor. Therefore, the similarly modified phenotypes, for example, of ion uptake arose possibly by selection on different loci in similar functional pathways. In summary, we bring evidence for the important role of genetic redundancy in rapid adaptation involving traits with polygenic architecture.
- Klíčová slova
- Adaptation, Arabidopsis, genetic redundancy, natural selection, parallel evolution, reciprocal transplant,
- MeSH
- Arabidopsis * genetika MeSH
- fenotyp MeSH
- fyziologická adaptace genetika MeSH
- genomika MeSH
- půda MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- půda MeSH
Parallel adaptation provides valuable insight into the predictability of evolutionary change through replicated natural experiments. A steadily increasing number of studies have demonstrated genomic parallelism, yet the magnitude of this parallelism varies depending on whether populations, species, or genera are compared. This led us to hypothesize that the magnitude of genomic parallelism scales with genetic divergence between lineages, but whether this is the case and the underlying evolutionary processes remain unknown. Here, we resequenced seven parallel lineages of two Arabidopsis species, which repeatedly adapted to challenging alpine environments. By combining genome-wide divergence scans with model-based approaches, we detected a suite of 151 genes that show parallel signatures of positive selection associated with alpine colonization, involved in response to cold, high radiation, short season, herbivores, and pathogens. We complemented these parallel candidates with published gene lists from five additional alpine Brassicaceae and tested our hypothesis on a broad scale spanning ∼0.02 to 18 My of divergence. Indeed, we found quantitatively variable genomic parallelism whose extent significantly decreased with increasing divergence between the compared lineages. We further modeled parallel evolution over the Arabidopsis candidate genes and showed that a decreasing probability of repeated selection on the same standing or introgressed alleles drives the observed pattern of divergence-dependent parallelism. We therefore conclude that genetic divergence between populations, species, and genera, affecting the pool of shared variants, is an important factor in the predictability of genome evolution.
- Klíčová slova
- Arabidopsis, alpine adaptation, evolution, genomics, parallelism,
- MeSH
- anotace sekvence MeSH
- Arabidopsis klasifikace genetika metabolismus účinky záření MeSH
- biologická evoluce * MeSH
- býložravci fyziologie MeSH
- fyziologická adaptace genetika MeSH
- fyziologický stres MeSH
- genetická variace * MeSH
- genetický drift MeSH
- genom rostlinný * MeSH
- genová introgrese MeSH
- genová ontologie MeSH
- ionizující záření MeSH
- modely genetické MeSH
- nízká teplota MeSH
- rostlinné proteiny genetika metabolismus MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- rostlinné proteiny MeSH
Parallel evolution provides powerful natural experiments for studying repeatability of evolution and genomic basis of adaptation. Well-documented examples from plants are, however, still rare, as are inquiries of mechanisms driving convergence in some traits while divergence in others. Arabidopsis arenosa, a predominantly foothill species with scattered morphologically distinct alpine occurrences is a promising candidate. Yet, the hypothesis of parallelism remained untested. We sampled foothill and alpine populations in all regions known to harbor the alpine ecotype and used SNP genotyping to test for repeated alpine colonization. Then, we combined field surveys and a common garden experiment to quantify phenotypic parallelism. Genetic clustering by region but not elevation and coalescent simulations demonstrated parallel origin of alpine ecotype in four mountain regions. Alpine populations exhibited parallelism in height and floral traits which persisted after two generations in cultivation. In contrast, leaf traits were distinctive only in certain region(s), reflecting a mixture of plasticity and genetically determined non-parallelism. We demonstrate varying degrees and causes of parallelism and non-parallelism across populations and traits within a plant species. Parallel divergence along a sharp elevation gradient makes A. arenosa a promising candidate for studying genomic basis of adaptation.
- Klíčová slova
- Arabidopsis, adaptation, alpine environments, convergence, parallel evolution, phenotypic parallelism,
- Publikační typ
- časopisecké články MeSH
Cuticular hydrocarbons (CHCs) are hydrophobic compounds deposited on the arthropod cuticle that are of functional significance with respect to stress tolerance, social interactions and mating dynamics. We characterized CHC profiles in natural populations of Drosophila melanogaster at five levels: across a latitudinal transect in the eastern United States, as a function of developmental temperature during culture, across seasonal time in replicate years, and as a function of rapid evolution in experimental mesocosms in the field. Furthermore, we also characterized spatial and temporal changes in allele frequencies for SNPs in genes that are associated with the production and chemical profile of CHCs. Our data demonstrate a striking degree of parallelism for clinal and seasonal variation in CHCs in this taxon; CHC profiles also demonstrate significant plasticity in response to rearing temperature, and the observed patterns of plasticity parallel the spatiotemporal patterns observed in nature. We find that these congruent shifts in CHC profiles across time and space are also mirrored by predictable shifts in allele frequencies at SNPs associated with CHC chain length. Finally, we observed rapid and predictable evolution of CHC profiles in experimental mesocosms in the field. Together, these data strongly suggest that CHC profiles respond rapidly and adaptively to environmental parameters that covary with latitude and season, and that this response reflects the process of local adaptation in natural populations of D. melanogaster.
- Klíčová slova
- Drosophila *, cuticular hydrocarbons *, experimental evolution *, spatiotemporal variation *, thermal plasticity *,
- MeSH
- Drosophila melanogaster chemie MeSH
- Drosophila MeSH
- fyziologická adaptace * MeSH
- podnebí MeSH
- uhlovodíky * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- uhlovodíky * MeSH
Urbanization and its urban-heat-island effect (UHI) have expanding footprints worldwide. The UHI means that urban habitats experience a higher mean and more frequent extreme high temperatures than rural habitats, impacting the ontogeny and resilience of urban biodiversity. However, many organisms occupy different microhabitats during different life stages and thus may experience the UHI differently across their development. While evolutionary changes in heat tolerance in line with the UHI have been demonstrated, it is unknown whether such evolutionary responses can vary across development. Here, using common-garden-reared Chiasmia clathrata moths from urban and rural populations from three European countries, we tested for urban evolution of heat shock tolerance in two life stages: larvae and adults. Our results indicate widespread urban evolution of increased heat tolerance in the adult stage only, suggesting that the UHI may be a stronger selective agent in adults. We also found that the difference in heat tolerance between urban and rural populations was similar to the difference between Mid- and North-European regions, suggesting similarity between adaptation to the UHI and natural, latitudinal temperature variation. Our observations incentivize further research to quantify the impact of these UHI adaptations on fitness during urbanization and climate change, and to check whether life-stage-specific adaptations in heat tolerance are typical of other ectothermic species that manage to survive in urbanized settings.
- Klíčová slova
- heat knock‐down time (HKDT), heat tolerance, latitudinal variation, lepidoptera, urban evolution, urban‐heat‐island effect (UHI),
- Publikační typ
- časopisecké články MeSH
BACKGROUND: Understanding the mechanisms and selective forces leading to adaptive radiations and origin of biodiversity is a major goal of evolutionary biology. Acrocephalus warblers are small passerines that underwent an adaptive radiation in the last approximately 10 million years that gave rise to 37 extant species, many of which still hybridize in nature. Acrocephalus warblers have served as model organisms for a wide variety of ecological and behavioral studies, yet our knowledge of mechanisms and selective forces driving their radiation is limited. Here we studied patterns of interspecific gene flow and selection across three European Acrocephalus warblers to get a first insight into mechanisms of radiation of this avian group. RESULTS: We analyzed nucleotide variation at eight nuclear loci in three hybridizing Acrocephalus species with overlapping breeding ranges in Europe. Using an isolation-with-migration model for multiple populations, we found evidence for unidirectional gene flow from A. scirpaceus to A. palustris and from A. palustris to A. dumetorum. Gene flow was higher between genetically more closely related A. scirpaceus and A. palustris than between ecologically more similar A. palustris and A. dumetorum, suggesting that gradual accumulation of intrinsic barriers rather than divergent ecological selection are more efficient in restricting interspecific gene flow in Acrocephalus warblers. Although levels of genetic differentiation between different species pairs were in general not correlated, we found signatures of apparently independent instances of positive selection at the same two Z-linked loci in multiple species. CONCLUSIONS: Our study brings the first evidence that gene flow occurred during Acrocephalus radiation and not only between sister species. Interspecific gene flow could thus be an important source of genetic variation in individual Acrocephalus species and could have accelerated adaptive evolution and speciation rate in this avian group by creating novel genetic combinations and new phenotypes. Independent instances of positive selection at the same loci in multiple species indicate an interesting possibility that the same loci might have contributed to reproductive isolation in several speciation events.
- Klíčová slova
- Acrocephalus warblers, Adaptive radiation, Gene flow, Parallel adaptive evolution, Speciation, Z chromosome,
- MeSH
- biodiverzita MeSH
- biologická evoluce MeSH
- fenotyp MeSH
- genetická variace MeSH
- hybridizace genetická MeSH
- pohlavní chromozomy * MeSH
- reprodukční izolace MeSH
- selekce (genetika) * MeSH
- tok genů * MeSH
- vznik druhů (genetika) MeSH
- zpěvní ptáci genetika MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Evropa MeSH
Viruses rapidly co-evolve with their hosts. The 9 million sequenced SARS-CoV-2 genomes by March 2022 provide a detailed account of viral evolution, showing that all amino acids have been mutated many times. However, only a few became prominent in the viral population. Here, we investigated the emergence of the same mutations in unrelated parallel lineages and the extent of such convergent evolution on the molecular level in the spike (S) protein. We found that during the first phase of the pandemic (until mid 2021, before mass vaccination) 31 mutations evolved independently ≥3-times within separated lineages. These included all the key mutations in SARS-CoV-2 variants of concern (VOC) at that time, indicating their fundamental adaptive advantage. The omicron added many more mutations not frequently seen before, which can be attributed to the synergistic nature of these mutations, which is more difficult to evolve. The great majority (24/31) of S-protein mutations under convergent evolution tightly cluster in three functional domains; N-terminal domain, receptor-binding domain, and Furin cleavage site. Furthermore, among the S-protein receptor-binding motif mutations, ACE2 affinity-improving substitutions are favoured. Next, we determined the mutation space in the S protein that has been covered by SARS-CoV-2. We found that all amino acids that are reachable by single nucleotide changes have been probed multiple times in early 2021. The substitutions requiring two nucleotide changes have recently (late 2021) gained momentum and their numbers are increasing rapidly. These provide a large mutation landscape for SARS-CoV-2 future evolution, on which research should focus now.
- Klíčová slova
- SARS-CoV-2, convergent evolution, mutations, spike (S) protein, virus,
- MeSH
- aminokyseliny MeSH
- glykoprotein S, koronavirus * genetika MeSH
- mutace MeSH
- nukleotidy MeSH
- SARS-CoV-2 * genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- aminokyseliny MeSH
- glykoprotein S, koronavirus * MeSH
- nukleotidy MeSH
- spike protein, SARS-CoV-2 MeSH Prohlížeč
Functional and structural adjustments of plants in response to environmental factors, including those occurring in alpine habitats, can result in transient acclimation, plastic phenotypic adjustments and/or heritable adaptation. To unravel repeatedly selected traits with potential adaptive advantage, we studied parallel (ecotypic) and non-parallel (regional) differentiation in leaf traits in alpine and foothill ecotypes of Arabidopsis arenosa. Leaves of plants from eight alpine and eight foothill populations, representing three independent alpine colonization events in different mountain ranges, were investigated by microscopy techniques after reciprocal transplantation. Most traits clearly differed between the foothill and the alpine ecotype, with plastic adjustments to the local environment. In alpine populations, leaves were thicker, with altered proportions of palisade and spongy parenchyma, and had fewer trichomes, and chloroplasts contained large starch grains with less stacked grana thylakoids compared to foothill populations. Geographical origin had no impact on most traits except for trichome and stomatal density on abaxial leaf surfaces. The strong parallel, heritable ecotypic differentiation in various leaf traits and the absence of regional effects suggests that most of the observed leaf traits are adaptive. These trait shifts may reflect general trends in the adaptation of leaf anatomy associated with the colonization of alpine habitats.
- Klíčová slova
- adaptation, alpine environment, ecotype, leaf anatomy, parallel evolution,
- Publikační typ
- časopisecké články MeSH
Relative contributions of pre-existing vs de novo genomic variation to adaptation are poorly understood, especially in polyploid organisms. We assess this in high resolution using autotetraploid Arabidopsis arenosa, which repeatedly adapted to toxic serpentine soils that exhibit skewed elemental profiles. Leveraging a fivefold replicated serpentine invasion, we assess selection on SNPs and structural variants (TEs) in 78 resequenced individuals and discover significant parallelism in candidate genes involved in ion homeostasis. We further model parallel selection and infer repeated sweeps on a shared pool of variants in nearly all these loci, supporting theoretical expectations. A single striking exception is represented by TWO PORE CHANNEL 1, which exhibits convergent evolution from independent de novo mutations at an identical, otherwise conserved site at the calcium channel selectivity gate. Taken together, this suggests that polyploid populations can rapidly adapt to environmental extremes, calling on both pre-existing variation and novel polymorphisms.
- MeSH
- alely * MeSH
- Arabidopsis účinky léků genetika MeSH
- fyziologická adaptace účinky léků genetika MeSH
- genom rostlinný * MeSH
- jednonukleotidový polymorfismus MeSH
- mutace MeSH
- polyploidie * MeSH
- proteiny huseníčku genetika metabolismus MeSH
- půda chemie MeSH
- sekologanin-tryptaminové alkaloidy metabolismus MeSH
- vápníkové kanály metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- proteiny huseníčku MeSH
- půda MeSH
- sekologanin-tryptaminové alkaloidy MeSH
- serpentine (alkaloid) MeSH Prohlížeč
- TPC1 protein, Arabidopsis MeSH Prohlížeč
- vápníkové kanály MeSH