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In the course of global climate change, central Europe is experiencing more frequent and prolonged periods of drought. The drought years 2018 and 2019 affected European beeches (Fagus sylvatica L.) differently: even in the same stand, drought damaged trees neighboured healthy trees, suggesting that the genotype rather than the environment was responsible for this conspicuous pattern. We used this natural experiment to study the genomic basis of drought resistance with Pool-GWAS. Contrasting the extreme phenotypes identified 106 significantly associated SNPs throughout the genome. Most annotated genes with associated SNPs (>70%) were previously implicated in the drought reaction of plants. Non-synonymous substitutions led either to a functional amino acid exchange or premature termination. A SNP-assay with 70 loci allowed predicting drought phenotype in 98.6% of a validation sample of 92 trees. Drought resistance in European beech is a moderately polygenic trait that should respond well to natural selection, selective management, and breeding.
The gradual heterogeneity of climatic factors pose varying selection pressures across geographic distances that leave signatures of clinal variation in the genome. Separating signatures of clinal adaptation from signatures of other evolutionary forces, such as demographic processes, genetic drift, and adaptation to non-clinal conditions of the immediate local environment is a major challenge. Here, we examine climate adaptation in five natural populations of the harlequin fly Chironomus riparius sampled along a climatic gradient across Europe. Our study integrates experimental data, individual genome resequencing, Pool-Seq data, and population genetic modelling. Common-garden experiments revealed a positive correlation of population growth rates corresponding to the population origin along the climate gradient, suggesting thermal adaptation on the phenotypic level. Based on a population genomic analysis, we derived empirical estimates of historical demography and migration. We used an FST outlier approach to infer positive selection across the climate gradient, in combination with an environmental association analysis. In total we identified 162 candidate genes as genomic basis of climate adaptation. Enriched functions among these candidate genes involved the apoptotic process and molecular response to heat, as well as functions identified in other studies of climate adaptation in other insects. Our results show that local climate conditions impose strong selection pressures and lead to genomic adaptation despite strong gene flow. Moreover, these results imply that selection to different climatic conditions seems to converge on a functional level, at least between different insect species.
Active transposable elements (TEs) may result in divergent genomic insertion and abundance patterns among conspecific populations. Upon secondary contact, such divergent genetic backgrounds can theoretically give rise to classical Dobzhansky-Muller incompatibilities (DMI), a way how TEs can contribute to the evolution of endogenous genetic barriers and eventually population divergence. We investigated whether differential TE activity created endogenous selection pressures among conspecific populations of the non-biting midge Chironomus riparius, focussing on a Chironomus-specific TE, the minisatellite-like Cla-element, whose activity is associated with speciation in the genus. Using an improved and annotated draft genome for a genomic study with five natural C. riparius populations, we found highly population-specific TE insertion patterns with many private insertions. A highly significant correlation of pairwise population FST from genome-wide SNPs with the FST estimated from TEs suggests drift as the major force driving TE population differentiation. However, the significantly higher Cla-element FST level due to a high proportion of differentially fixed Cla-element insertions indicates that segregating, i.e. heterozygous insertions are selected against. With reciprocal crossing experiments and fluorescent in-situ hybridisation of Cla-elements to polytene chromosomes, we documented phenotypic effects on female fertility and chromosomal mispairings that might be linked to DMI in hybrids. We propose that the inferred negative selection on heterozygous Cla-element insertions causes endogenous genetic barriers and therefore acts as DMI among C. riparius populations. The intrinsic genomic turnover exerted by TEs, thus, may have a direct impact on population divergence that is operationally different from drift and local adaptation.
Bears are iconic mammals with a complex evolutionary history. Natural bear hybrids and studies of few nuclear genes indicate that gene flow among bears may be more common than expected and not limited to the closely related polar and brown bears. Here we present a genome analysis of the bear family with representatives of all living species. Phylogenomic analyses of 869 mega base pairs divided into 18,621 genome fragments yielded a well-resolved coalescent species tree despite signals for extensive gene flow across species. However, genome analyses using three different statistical methods show that gene flow is not limited to closely related species pairs. Strong ancestral gene flow between the Asiatic black bear and the ancestor to polar, brown and American black bear explains numerous uncertainties in reconstructing the bear phylogeny. Gene flow across the bear clade may be mediated by intermediate species such as the geographically wide-spread brown bears leading to massive amounts of phylogenetic conflict. Genome-scale analyses lead to a more complete understanding of complex evolutionary processes. The increasing evidence for extensive inter-specific gene flow, found also in other animal species, necessitates shifting the attention from speciation processes achieving genome-wide reproductive isolation to the selective processes that maintain species divergence in the face of gene flow.
All giraffe (Giraffa) were previously assigned to a single species (G. Camelopardalis) and nine subspecies. However, multi-locus analyses of all subspecies have shown that there are four genetically distinct clades and suggest four giraffe species. This conclusion might not be fully accepted due to limited data and lack of explicit gene flow analyses. Here we present an extended study based on 21 independent nuclear loci from 137 individuals. Explicit gene flow analyses identify less than one migrant per generation, including between the closely related northern and reticulated giraffe. Thus, gene flow analyses and population genetics of the extended dataset confirm four genetically distinct giraffe clades and support four independent giraffe species. The new findings call for a revision of the IUCN classification of giraffe taxonomy. Three of the four species are threatened with extinction, mostly occurring in politically unstable regions, and as such, require the highest conservation support possible.
Phylogenetic analyses of nuclear and mitochondrial genomes have shown that polar bears captured the mitochondrial genome of brown bears some 160,00 years ago. This hybridization event likely led to an extinction of the original polar bear mitochondrial genome. However, parts of the mitochondrial DNA occasionally integrates into the nuclear genome, forming pseudogenes called numts (nuclear mitochondrial integrations). Screening the polar bear genome for numts, we identified only 13 such integrations. Analyses of whole-genome sequences from additional polar bears, brown and American black bears as well as the giant panda indicates that the discovered numts entered the bear lineage before the initial ursid radiation some 14 million years ago. Our findings suggests a low integration rate of numts in the bear lineage and a complete loss of the original polar bear mitochondrial genome.
Species is the fundamental taxonomic unit in biology and its delimitation has implications for conservation. In giraffe (Giraffa spp.), multiple taxonomic classifications have been proposed since the early 1900s.1 However, one species with nine subspecies has been generally accepted,2 likely due to limited in-depth assessments, subspecies hybridizing in captivity,3,4 and anecdotal reports of hybrids in the wild.5 Giraffe taxonomy received new attention after population genetic studies using traditional genetic markers suggested at least four species.6,7 This view has been met with controversy,8 setting the stage for debate.9,10 Genomics is significantly enhancing our understanding of biodiversity and speciation relative to traditional genetic approaches and thus has important implications for species delineation and conservation.11 We present a high-quality de novo genome assembly of the critically endangered Kordofan giraffe (G. camelopardalis antiquorum)12 and a comprehensive whole-genome analysis of 50 giraffe representing all traditionally recognized subspecies. Population structure and phylogenomic analyses support four separately evolving giraffe lineages, which diverged 230–370 ka ago. These lineages underwent distinct demographic histories and show different levels of heterozygosity and inbreeding. Our results strengthen previous findings of limited gene flow and admixture among putative giraffe species6,7,9 and establish a genomic foundation for recognizing four species and seven subspecies, the latter of which should be considered as evolutionary significant units. Achieving a consensus over the number of species and subspecies in giraffe is essential for adequately assessing their threat level and will improve conservation efforts for these iconic taxa.
Background: Understanding the processes that lead to hybridization of wolves and dogs is of scientific and management importance, particularly over large geographical scales, as wolves can disperse great distances. However, a method to efficiently detect hybrids in routine wolf monitoring is lacking. Microsatellites offer only limited resolution due to the low number of markers showing distinctive allele frequencies between wolves and dogs. Moreover, calibration across laboratories is time-consuming and costly. In this study, we selected a panel of 96 ancestry informative markers for wolves and dogs, derived from the Illumina CanineHD Whole-Genome BeadChip (174 K). We designed very short amplicons for genotyping on a microfluidic array, thus making the method suitable also for non-invasively collected samples.
Results: Genotypes based on 93 SNPs from wolves sampled throughout Europe, purebred and non-pedigree dogs, and suspected hybrids showed that the new panel accurately identifies parental individuals, first-generation hybrids and first-generation backcrosses to wolves, while second- and third-generation backcrosses to wolves were identified as advanced hybrids in almost all cases. Our results support the hybrid identity of suspect individuals and the non-hybrid status of individuals regarded as wolves. We also show the adequacy of these markers to assess hybridization at a European-wide scale and the importance of including samples from reference populations.
Conclusions: We showed that the proposed SNP panel is an efficient tool for detecting hybrids up to the third-generation backcrosses to wolves across Europe. Notably, the proposed genotyping method is suitable for a variety of samples, including non-invasive and museum samples, making this panel useful for wolf-dog hybrid assessments and wolf monitoring at both continental and different temporal scales.
Consistent individual differences in behaviour (animal personality) are widespread throughout the Animal Kingdom. This includes variation in risk-taking versus risk-averse behavioural tendencies. Variation in several personality dimensions is associated with distinct fitness consequences and thus, may become a target of natural and/or sexual selection. However, the link between animal personality and mate choice—as a major component of sexual selection—remains understudied. We asked (1) whether females and males of the livebearing fish Poecilia mexicana prefer risk-taking mating partners (directional mating preference), (2) or if their preferences are dependent on the choosing individual’s own personality type (assortative mating). We characterized each test subject for its risk-taking behaviour, assessed as the time to emerge from shelter and enter an unknown area. In dichotomous association preference tests, we offered two potential mating partners that differed in risk-taking behaviour but were matched for other phenotypic traits (body size, shape, and colouration). Females, but not males, exhibited a strong directional preference for risk-taking over risk-averse mating partners. At the same time, the strength of females’ preferences correlated positively with their own risk-taking scores. Our study is the first to demonstrate that a strong overall preference for risk-taking mating partners does not preclude effects of choosing individuals’ own personality type on (subtle) individual variation in mating preferences. More generally, two different preferences functions appear to interact to determine the outcome of individual mate choice decisions.
The plant family Brassicaceae includes some of the most studied hosts of plant microbiomes, targeting microbial diversity, community assembly rules, and effects on host performance. Compared to bacteria, eukaryotes in the brassicaceous microbiome remain understudied, especially under natural settings. Here, we assessed the impact of host identity and age on the assembly of fungal and oomycete root communities, using DNA metabarcoding of roots and associated soil of three annual co-habiting Brassicaceae collected at two time points. Our results showed that fungal communities are more diverse and structured than those of oomycetes. In both cases, plant identity and sampling time had little influence on community variation, whereas root/soil compartment had a strong effect by exerting control on the entry of soil microorganisms into the roots. The enrichment in roots of specific fungi suggests a specialization towards the asymptomatic colonization of plant tissues, which could be relevant to host’s fitness and health.