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Reichard, M.

Publications and source records attributed to Reichard, M..

13 recordsLinked to original sources

Heterogeneous evolution of effective recombination landscapes across percomorph fishes

Recombination shapes allelic combinations across the genome and plays a central role in adaptation and speciation. While recombination rates are known to vary and evolve, how recombination landscapes diverge between populations and which processes drive this divergence remains poorly understood. Here, we use the Population Recombination Divergence Index (PRDI) to quantify divergence in effective recombination landscapes between seven pairs of populations and species from four percomorph fish lineages (cichlids, sticklebacks, killifish, and clownfish). While accounting for stochasticity and confounders of linkage disequilibrium (LD) -based recombination rate estimates, we find that recombination landscapes diverged substantially in all comparisons. This divergence generally increases with genetic differentiation and divergence time, but the amount of PRDI accumulated per unit of genetic divergence (FST), net nucleotide divergence (da), or divergence time varies markedly among population and species pairs. Comparisons across systems suggest that PRDI accumulation tends to be faster (per unit of FST, da, or divergence time) in pairs with higher inferred gene flow. We also introduce a local version of PRDI (_l) to better characterize genomic heterogeneity in effective recombination divergence. We find that higher inferred gene flow between populations tends to be associated with stronger intragenomic correlation between local FST and _l. Finally, we propose a conceptual framework for investigating how divergent selection and gene flow may interact to shape effective recombination landscape divergence. Our work highlights the heterogeneous dynamics of effective recombination landscape evolution, and motivates further theoretical and empirical efforts to integrate recombination landscape evolution into studies of adaptation and speciation.

evolutionary biology↗

Sperm attraction by female reproductive fluid in a fish with an unconventional fertilisation strategy

Active sperm guidance towards the eggs is necessary for gametes to meet within the fertilisation window and is usually achieved through the action of female reproductive fluids (FRF hereafter) on sperm flagellar movement. However, it remains unknown whether FRF retains this function in species with unusual fertilisation strategies. Such examples include systems where gametes are released within confined microhabitats characterised by flow-driven physical processes that could facilitate sperm-egg encounters, hence selection on active sperm guidance may be relaxed. Alternatively, sperm attraction could be maintained by pleiotropic effects of genes involved in other reproductive functions of FRF. Here we tested whether FRF of species with unusual modes of fertilisation retain sperm attractant properties using the bitterling, a small cyprinid fish that parasitises freshwater mussels. Bitterling deposit sperm and eggs inside the mussel gills and gamete interactions are facilitated by the water current generated by mussel respiration. Using a recently developed sperm selection chamber and the European bitterling, we find that more sperm accumulate in the FRF channel compared to the water control. Moreover, European bitterling sperm showed no preference for conspecific FRF over that of a distantly related Asian bitterling FRF. Our results suggest that bitterling FRF resembles that of species with conventional fertilisation modes, implying that it could mediate sperm selection and cryptic female choice. We discuss alternative evolutionary scenarios underlying the persistence of sperm attractant properties of bitterling FRF despite the shift to a physically mediated fertilisation environment.

evolutionary biology↗

Rapid evolution in response to biological invasion: variation in resistance and survival of the European bitterling fish across a gradient of Sinanodonta woodiana expansion

Biological invasions impose new selective pressures on native species, prompting rapid evolutionary responses. We examined how the parasitic larvae (glochidia) of the invasive East Asian mussel Sinanodonta woodiana affect European bitterling fish (Rhodeus amarus) populations with different histories of exposure to the parasite (none, 15 years, or 40+ years). Glochidia parasitise fish fins and gills, and bitterling are especially vulnerable to parasitism due to their spawning association with mussels. We found the lowest glochidia load in bitterling from populations with the longest association with S. woodiana. While infection reduced swimming capacity proportionally to parasite load, this effect was not population-specific. However, post-infection mortality was highest in naive and lowest in long-associated populations, indicating evolved tolerance. No long-term effects on survival, growth, condition, or reproduction were observed, suggesting fitness costs are concentrated shortly after infection. These results show that novel host-parasite interactions during invasions can drive rapid adaptive change, emphasising the need to consider evolutionary dynamics in invasion management.

evolutionary biology↗

Sex chromosome turnover in African annual killifishes of the genus Nothobranchius

Sex chromosomes of teleost fishes often have low levels of differentiation and undergo frequent turnovers. Annual Nothobranchius killifishes comprise representatives with male-heterogametic XY or X1X2Y sex chromosome systems, scattered across their phylogeny, nested within species lacking cytologically detectable sex chromosomes. They thus provide a suitable system to study sex chromosome evolution and turnover. Here, we combined molecular cytogenetics and genomic analyses to examine several multiple sex chromosome systems in Nothobranchius spp. and their outgroup Fundulosoma thierryi. We used fluorescence in situ hybridization with three sex chromosome-specific painting probes and bacterial artificial chromosomes (BAC) bearing eight orthologues of genes found to be repeatedly co-opted as master sex determining (MSD) genes in fishes. Our results suggest at least four independent origins of sex chromosomes in the genus Nothobranchius. The synteny block carrying amhr2 gene was shared by X1X2Y systems of N. brieni, N. guentheri and N. lourensi, but the autosomal additions and the overall neo-Y chromosome structure differed among these species. On the other hand, gdf6 gene was localized to neo-Y of F. thierryi. None of the mapped MSD gene candidates seems to determine sex in N. ditte. We further sequenced genomes of F. thierryi female and N. guentheri male by long-read platforms and performed analyses of male and female Pool-seq data and coverage to delimit their non-recombining regions, determine degree of their differentiation, and thus complement the cytogenetic data in assessing potential MSD genes. We found low level of sex chromosomes differentiation in F. thierryi. In N. guentheri, however, we identified two distinct evolutionary strata on neo-Y. The amhr2 gene resides in the younger stratum and has low allelic variation, which questions its role in sex determination.

evolutionary biology↗

Conserved satellite DNA motif and lack of interstitial telomeric sites in highly rearranged African Nothobranchius killifish karyotypes

Repetitive DNA may have significant impact on genome evolution. African annual killifishes of the genus Nothobranchius (Teleostei: Nothobranchiidae), which has adapted to temporary water pools in African savannahs, possess genomes with high repeat content. They are also characterized by rapid karyotype and sex chromosome evolution but the role of genome repeats in these processes remains largely unknown. Here, we analyzed the distribution of telomeric (TTAGGG)n repeat and Nfu-SatC satellite DNA (isolated formerly from N. furzeri) by fluorescence in situ hybridization in representatives across the Nothobranchius phylogeny (15 species), and with Fundulosoma thierryi as an outgroup. All analyzed taxa shared the presence of Nfu-SatC repeat but with diverse organization and distribution on chromosomes (from small clusters scattered genome-wide, to large localized accumulations, or a combined pattern). Nfu-SatC landscape was similar in conspecific populations of N. guentheri and N. melanospilus but slightly-to-moderately differed between populations of N. pienaari, and between closely related N. kuhntae and N. orthonotus. Inter-individual variability in Nfu-SatC patterns was found in N. orthonotus and N. krysanovi, including distinct segments present often in heterozygous condition. We revealed mostly no sex-linked patterns of studied repeats distribution in any of the sampled species including those with known sex chromosomes. Only in N. brieni (having an X1X2Y multiple sex chromosome system), Nfu-SatC probe covered substantial portion of the Y chromosome, similarly as formerly found in N. furzeri and N. kadleci (XY sex chromosomes), sister species not closely related to N. brieni. All studied species further shared patterns of telomeric FISH, with expected signals at the ends of all chromosomes and no additional interstitial telomeric sites. In summary, we revealed i) the presence of conserved satDNA class in Nothobranchius clade (a rare pattern among ray-finned fishes), ii) independent trajectories of Nothobranchius sex chromosome diferentiation, with recurrent and convergent accumulation of Nfu-SatC on the Y chromosome in some species, and iii) genus-wide shared propensity to loss of telomeric repeats during the mechanism of interchromosomal rearrangements. Collectively, our findings advance our understanding of genome structure, mechanisms of karyotype reshuffling and sex chromosome differentiation in Nothobranchius killifishes from the genus-wide perspective.

genetics↗

Fast centromeric repeat turnover provides a glimpse into satellite DNA evolution in Nothobranchius annual killifishes

Satellite DNA (satDNA) is rapidly evolving class of tandem repeats with some motifs being involved in centromere organization and function. Rapid co-evolution of centromeric satDNA and associated proteins has been mostly attributed to the so-called centromere drive. To identify repeats associated with centromeric regions and test for the role of meiotic drive in their evolution, we investigated satDNA across Southern and Coastal clades of African annual killifishes of the genus Nothobranchius. C-banding showed expansion of (peri)centromeric heterochromatin regions in the Southern-clade killifishes. Molecular cytogenetic and bioinformatic analyses further revealed that two previously identified satellites, Nfu-SatA and Nfu-SatB, are associated with centromeres only in one lineage of the Southern clade. Nfu-SatB was, however, detected outside centromeres also in other members of the Coastal clade, which is consistent with the "library" hypothesis of satDNA evolution. We also identified a novel satDNA, Cl-36, associated with (peri)centromeres in N. foerschi, N. guentheri and N. rubripinnis from the Coastal clade. Our findings could be explained by centromere drive shaping karyotype change and centromeric repeat turnover in Nothobranchius species with possible reversal of spindle polarity within the Southern clade.

genetics↗

Reduced wound healing and angiogenesis in aged zebrafish and turquoise killifish.

Impaired wound healing is associated with aging and has significant effects on human health on an individual level, but also the whole health care sector. Deficient angiogenesis appears to be involved in the process, but the underlying biology is still poorly understood. This is at least partially being explained by complexity and costs in using mammalian aging models. To understand aging-related vascular biology of impaired wound healing, we have utilized zebrafish and turquoise killifish fin regeneration models. The regeneration of caudal fin after resection was significantly reduced in old individuals in both species. Age-related changes in angiogenesis, vascular density and expression levels of angiogenesis biomarker VEGF-A were observed. Furthermore, anti-angiogenic drug, vascular endothelial growth factor receptor blocking inhibitor SU5416 reduced regeneration indicating a key role for angiogenesis in the regeneration of aging caudal fin despite aging-related changes in vasculature. Taken together, our data indicates that these fish models are suitable for studying aging-related decline in wound healing and associated alterations in aging vasculature.

developmental biology↗

Sex chromosome differentiation via changes in the Y chromosome repeat landscape in African annual killifishes Nothobranchius furzeri and N. kadleci

Repetitive DNA represents an important driver of sex chromosome differentiation. Yet, repetitive sequences tend to be misrepresented or overlooked in genomic studies. We analysed repetitive DNA landscape of sex chromosomes in several populations of a turquoise killifish Nothobranchius furzeri and its sister species N. kadleci (Teleostei: Nothobranchiidae), representatives of African annual killifishes with high rate of karyotype and sex chromosome evolution. We combined bioinformatic analyses of repeatome with molecular cytogenetic techniques such as comparative genomic hybridization, fluorescence in situ hybridization with satellite sequences, genes for ribosomal RNAs (rDNA) and bacterial artificial chromosomes (BACs) and immunostaining of SYCP3 and MLH1 proteins, which marked lateral elements of synaptonemal complexes and recombination sites, respectively. We revealed that N. furzeri and N. kadleci share the XY sex chromosome system, which is thus much older than previously assumed. Sex chromosomes are mostly heteromorphic as evidenced by distinct distribution of satellite DNAs and major rDNA. Yet, the heteromorphic XY sex chromosomes pair almost exclusively regularly in meiosis, which implies synaptic adjustment. Physical mapping of BACs identified inversions on Y chromosomes of the N. kadleci populations, akin to the pattern previously reported in N. furzeri. Yet, repetitive DNA landscape of X and Y sex chromosomes either diverged in parallel in populations of both species or it evolved in their common ancestor and thus predates the inversions. The observed differentiation via repeat repatterning thus cannot be explained by the classical sexually antagonistic model. Rather, we hypothesized that relaxed meiotic drive and recombination reduced by neutral processes could drive changes in repeatome and secondary inversions could be maintained by sexually antagonistic regulatory effects resulting from early evolution of dosage compensation. Author summaryEarly differentiation of sex chromosomes is not yet satisfactorily understood despite intensive research effort. Homomorphic sex chromosomes and their rapid turnover are common in teleost fishes, which makes them excellent models for studying evolution of nascent sex chromosomes. We investigated sex chromosomes in several populations of two sister species of African annual killifishes, Nothobranchius furzeri and N. kadleci, particularly their repetitive landscape, which was misrepresented in previous genomic studies. Combination of cytogenetic and genomic approaches revealed that both species share heteromorphic XY sex chromosome system. The N. furzeri XY sex chromosomes thus evolved earlier than previously expected. In N. kadleci, Y-linked inversions analogous to those reported in N. furzeri were detected. Changes in repetitive DNA distribution on sex chromosomes are either convergent or occurred in a common ancestor of both species, prior to the inversion events. The observed sex chromosome differentiation on repetitive DNA level thus cannot be reconciled with the classical theoretical model of sex chromosome evolution driven by sexually antagonistic selection. We invoke alternative explanations such as relaxed meiotic drive and recombination reduced by neutral processes, and we hypothesize that secondary inversions could be maintained by early evolution of dosage compensation resulting in sexually antagonistic regulatory effects.

evolutionary biology↗

Environment and sex control lifespan and telomere length in wild-derived African killifish

Telomere length is correlated positively with longevity at the individual level, but negatively when compared across species. Here, we tested the association between lifespan and telomere length in African annual killifish. We analyzed telomere length in 18 Nothobranchius strains derived from diverse habitats and measured the laboratory lifespan of 14 strains of N. furzeri and N. kadleci. We found that males had shorter telomeres than females. The longest telomeres were recorded in strains derived from dry region where male lifespans were shortest. At the individual level, we detected a weak negative association between rapid juvenile growth and shorter telomeres in early adulthood. Overall, average telomere length was a good descriptor of telomere length distribution. However, within-individual telomere length spread was not related to any pattern. This substantial variation in telomere length between strains from different environments provides killifish as powerful tool to understand the evolutionarily adaptive value of telomere length.

evolutionary biology↗

The sources of sex differences in aging in annual fishes

Sex differences in lifespan and aging are widespread among animals, with males usually the shorter-lived sex. Despite extensive research interest, it is unclear how lifespan differences between the sexes are modulated by genetic, environmental and social factors. We combined comparative data from natural populations of annual killifishes with experimental results on replicated captive populations, showing that females consistently outlived males in the wild. This sex-specific survival difference persisted in social environment only in two most aggressive species, and ceased completely when social and physical contacts were prevented. Demographically, neither an earlier start nor faster rate of aging accounted for shorter male lifespans, but increased baseline mortality and the lack of mortality deceleration in the oldest age shortened male lifespan. The sexes did not differ in any measure of functional aging we recorded. Overall, we demonstrate that sex differences in lifespan and aging may be ameliorated by modulating social and environmental conditions.

evolutionary biology↗

Intra-Species Differences in Population Size shape Life History and Genome Evolution

The evolutionary forces shaping life history trait divergence within species are largely unknown. Killifish (oviparous Cyprinodontiformes) evolved an annual life cycle as an exceptional adaptation to life in arid savannah environments characterized by seasonal water availability. The turquoise killifish (Nothobranchius furzeri) is the shortest-lived vertebrate known to science and displays differences in lifespan among wild populations, representing an ideal natural experiment in the evolution and diversification of life history. Here, by combining genome sequencing and population genetics, we investigate the evolutionary forces shaping lifespan among turquoise killifish populations. We generate an improved reference assembly for the turquoise killifish genome, trace the evolutionary origin of the sex chromosome, and identify genes under strong positive and purifying selection, as well as those evolving neutrally. We find that the shortest-lived turquoise killifish populations, which dwell in fragmented and isolated habitats at the outer margin of the geographical range of the species, are characterized by small effective population size and accumulate throughout the genome several small to large-effect deleterious mutations due to genetic drift. The genes most affected by drift in the shortest-lived turquoise killifish populations are involved in the WNT signalling pathway, neurodegenerative disorders, cancer and the mTOR pathway. As the populations under stronger genetic drift are the shortest-lived ones, we propose that limited population size due to habitat fragmentation and repeated population bottlenecks, by causing the genome-wide accumulation of deleterious mutations, cumulatively contribute to the short adult lifespan in turquoise killifish populations.

evolutionary biology↗

Performance of Turquoise killifish, model organism in aging, on commercial pelleted diet: a step towards husbandry standardization

Dietary alteration is one of the most universally effective aging interventions, making its standardization a fundamental need for model organisms in aging. Here we address the current lack of standardized formulated diet for Turquoise Killifish Nothobranchius furzeri - a promising model organism. We first demonstrated that N. furzeri can be fully weaned onto a standardized commercially available pelleted diet as the sole nutrition when kept in social tanks. We then compared nine somatic and six reproductive parameters between fish fed a typical laboratory diet - frozen chironomid larvae (bloodworms) and fish fed solely on BioMar pellets. Killifish readily consumed the pellets. Although fish consumed 7.5 times less food mass in the form of pellets than bloodworms, they had comparable somatic and reproductive performance. There was no difference between diet groups in body size, specific growth rate, condition or extent of hepatocellular vacuolation. Fish fed a pelleted diet had higher juvenile body mass and more visceral fat. Pellet-fed males had lower liver mass and possessed a lipid type of hepatocellular vacuolation instead of the prevailing glycogen-like vacuolation in the bloodworm-fed group. No significant effect was found on reproductive parameters. The negligible differences between dietary groups and good acceptance of pellets indicates their suitability as a useful starting point for diet standardization (and potential manipulation) in Nothobranchius furzeri.

physiology↗

Regulation of Life Span by the Gut Microbiota in The Short-Lived African Turquoise Killifish

Gut bacteria occupy the interface between the organism and the external environment, contributing to homeostasis and disease. Yet, the causal role of the gut microbiota during host aging is largely unexplored. Here, using the African turquoise killifish (Nothobranchius furzeri), a naturally short-lived vertebrate, we show that the gut microbiota plays a key role in modulating vertebrate life span. Recolonizing the gut of middle-age individuals with bacteria from young donors resulted in life span extension and delayed behavioral decline. This intervention prevented the decrease in microbial diversity associated with host aging and maintained a young-like gut bacterial community, characterized by overrepresentation of the key genera Exiguobacterium, Planococcus, Propionigenium and Psychrobacter. Our findings demonstrate that the natural microbial gut community of young individuals can causally induce long-lasting beneficial systemic effects that lead to life span extension in a vertebrate model.

genomics↗