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1.
Nat Rev Genet ; 21(12): 754-768, 2020 12.
Artículo en Inglés | MEDLINE | ID: mdl-32860017

RESUMEN

Studies in diverse biological systems have indicated that host-parasite co-evolution is responsible for the extraordinary genetic diversity seen in some genomic regions, such as major histocompatibility (MHC) genes in jawed vertebrates and resistance genes in plants. This diversity is believed to evolve under balancing selection on hosts by parasites. However, the mechanisms that link the genomic signatures in these regions to the underlying co-evolutionary process are only slowly emerging. We still lack a clear picture of the co-evolutionary concepts and of the genetic basis of the co-evolving phenotypic traits in the interacting antagonists. Emerging genomic tools that provide new options for identifying underlying genes will contribute to a fuller understanding of the co-evolutionary process.


Asunto(s)
Coevolución Biológica/genética , Interacciones Huésped-Parásitos/genética , Animales , Genoma , Humanos , Modelos Genéticos , Parásitos/genética
2.
PLoS Genet ; 19(2): e1010570, 2023 02.
Artículo en Inglés | MEDLINE | ID: mdl-36730161

RESUMEN

Specific interactions of host and parasite genotypes can lead to balancing selection, maintaining genetic diversity within populations. In order to understand the drivers of such specific coevolution, it is necessary to identify the molecular underpinnings of these genotypic interactions. Here, we investigate the genetic basis of resistance in the crustacean host, Daphnia magna, to attachment and subsequent infection by the bacterial parasite, Pasteuria ramosa. We discover a single locus with Mendelian segregation (3:1 ratio) with resistance being dominant, which we call the F locus. We use QTL analysis and fine mapping to localize the F locus to a 28.8-kb region in the host genome, adjacent to a known resistance supergene. We compare the 28.8-kb region in the two QTL parents to identify differences between host genotypes that are resistant versus susceptible to attachment and infection by the parasite. We identify 13 genes in the region, from which we highlight eight biological candidates for the F locus, based on presence/absence polymorphisms and differential gene expression. The top candidates include a fucosyltransferase gene that is only present in one of the two QTL parents, as well as several Cladoceran-specific genes belonging to a large family that is represented in multiple locations of the host genome. Fucosyltransferases have been linked to resistance in previous studies of Daphnia-Pasteuria and other host-parasite systems, suggesting that P. ramosa spore attachment could be mediated by changes in glycan structures on D. magna cuticle proteins. The Cladoceran-specific candidate genes suggest a resistance strategy that relies on gene duplication. Our results add a new locus to a growing genetic model of resistance in the D. magna-P. ramosa system. The identified candidate genes will be used in future functional genetic studies, with the ultimate aim to test for cycles of allele frequencies in natural populations.


Asunto(s)
Daphnia , Resistencia a la Enfermedad , Interacciones Huésped-Patógeno , Pasteuria , Animales , Daphnia/genética , Daphnia/microbiología , Genoma , Genotipo , Interacciones Huésped-Patógeno/genética , Modelos Biológicos , Pasteuria/genética , Polimorfismo Genético , Resistencia a la Enfermedad/genética
3.
Mol Biol Evol ; 41(7)2024 Jul 03.
Artículo en Inglés | MEDLINE | ID: mdl-38935572

RESUMEN

Two important characteristics of metapopulations are extinction-(re)colonization dynamics and gene flow between subpopulations. These processes can cause strong shifts in genome-wide allele frequencies that are generally not observed in "classical" (large, stable, and panmictic) populations. Subpopulations founded by one or a few individuals, the so-called propagule model, are initially expected to show intermediate allele frequencies at polymorphic sites until natural selection and genetic drift drive allele frequencies toward a mutation-selection-drift equilibrium characterized by a negative exponential-like distribution of the site frequency spectrum. We followed changes in site frequency spectrum distribution in a natural metapopulation of the cyclically parthenogenetic pond-dwelling microcrustacean Daphnia magna using biannual pool-seq samples collected over a 5-yr period from 118 ponds occupied by subpopulations of known age. As expected under the propagule model, site frequency spectra in newly founded subpopulations trended toward intermediate allele frequencies and shifted toward right-skewed distributions as the populations aged. Immigration and subsequent hybrid vigor altered this dynamic. We show that the analysis of site frequency spectrum dynamics is a powerful approach to understand evolution in metapopulations. It allowed us to disentangle evolutionary processes occurring in a natural metapopulation, where many subpopulations evolve in parallel. Thereby, stochastic processes like founder and immigration events lead to a pattern of subpopulation divergence, while genetic drift leads to converging site frequency spectrum distributions in the persisting subpopulations. The observed processes are well explained by the propagule model and highlight that metapopulations evolve differently from classical populations.


Asunto(s)
Daphnia , Frecuencia de los Genes , Flujo Genético , Selección Genética , Animales , Daphnia/genética , Flujo Génico , Modelos Genéticos , Genética de Población/métodos , Dinámica Poblacional , Genoma , Evolución Biológica , Evolución Molecular
4.
Mol Biol Evol ; 40(7)2023 Jul 05.
Artículo en Inglés | MEDLINE | ID: mdl-37326294

RESUMEN

Understanding the genomic basis of infectious disease is a fundamental objective in co-evolutionary theory with relevance to healthcare, agriculture, and epidemiology. Models of host-parasite co-evolution often assume that infection requires specific combinations of host and parasite genotypes. Co-evolving host and parasite loci are, therefore, expected to show associations that reflect an underlying infection/resistance allele matrix, yet little evidence for such genome-to-genome interactions has been observed among natural populations. We conducted a study to search for this genomic signature across 258 linked host (Daphnia magna) and parasite (Pasteuria ramosa) genomes. Our results show a clear signal of genomic association between multiple epistatically interacting loci in the host genome, and a family of genes encoding for collagen-like protein in the parasite genome. These findings are supported by laboratory-based infection trials, which show strong correspondence between phenotype and genotype at the identified loci. Our study provides clear genomic evidence of antagonistic co-evolution among wild populations.


Asunto(s)
Parásitos , Animales , Parásitos/genética , Interacciones Huésped-Patógeno/genética , Genoma , Genotipo , Genómica , Daphnia/genética , Interacciones Huésped-Parásitos/genética
5.
Mol Biol Evol ; 40(1)2023 01 04.
Artículo en Inglés | MEDLINE | ID: mdl-36625177

RESUMEN

Recent advances in long-read sequencing technology have allowed for single-molecule sequencing of entire mitochondrial genomes, opening the door for direct investigation of the mitochondrial genome architecture and recombination. We used PacBio sequencing to reassemble mitochondrial genomes from two species of New Zealand freshwater snails, Potamopyrgus antipodarum and Potamopyrgus estuarinus. These assemblies revealed a ∼1.7 kb structure within the mitochondrial genomes of both species that was previously undetected by an assembly of short reads and likely corresponding to a large noncoding region commonly present in the mitochondrial genomes. The overall architecture of these Potamopyrgus mitochondrial genomes is reminiscent of the chloroplast genomes of land plants, harboring a large single-copy (LSC) region and a small single-copy (SSC) region separated by a pair of inverted repeats (IRa and IRb). Individual sequencing reads that spanned across the Potamopyrgus IRa-SSC-IRb structure revealed the occurrence of a "flip-flop" recombination. We also detected evidence for two distinct IR haplotypes and recombination between them in wild-caught P. estuarinus, as well as extensive intermolecular recombination between single-nucleotide polymorphisms in the LSC region. The chloroplast-like architecture and repeat-mediated mitochondrial recombination we describe here raise fundamental questions regarding the origins and commonness of inverted repeats in cytoplasmic genomes and their role in mitochondrial genome evolution.


Asunto(s)
Genoma del Cloroplasto , Genoma Mitocondrial , Animales , Análisis de Secuencia de ADN , Recombinación Genética , Cloroplastos , Filogenia
6.
Mol Biol Evol ; 39(12)2022 12 05.
Artículo en Inglés | MEDLINE | ID: mdl-36472514

RESUMEN

The dynamics of extinction and (re)colonization in habitat patches are characterizing features of dynamic metapopulations, causing them to evolve differently than large, stable populations. The propagule model, which assumes genetic bottlenecks during colonization, posits that newly founded subpopulations have low genetic diversity and are genetically highly differentiated from each other. Immigration may then increase diversity and decrease differentiation between subpopulations. Thus, older and/or less isolated subpopulations are expected to have higher genetic diversity and less genetic differentiation. We tested this theory using whole-genome pool-sequencing to characterize nucleotide diversity and differentiation in 60 subpopulations of a natural metapopulation of the cyclical parthenogen Daphnia magna. For comparison, we characterized diversity in a single, large, and stable D. magna population. We found reduced (synonymous) genomic diversity, a proxy for effective population size, weak purifying selection, and low rates of adaptive evolution in the metapopulation compared with the large, stable population. These differences suggest that genetic bottlenecks during colonization reduce effective population sizes, which leads to strong genetic drift and reduced selection efficacy in the metapopulation. Consistent with the propagule model, we found lower diversity and increased differentiation in younger and also in more isolated subpopulations. Our study sheds light on the genomic consequences of extinction-(re)colonization dynamics to an unprecedented degree, giving strong support for the propagule model. We demonstrate that the metapopulation evolves differently from a large, stable population and that evolution is largely driven by genetic drift.


Asunto(s)
Ecosistema , Flujo Genético , Animales , Dinámica Poblacional , Daphnia/genética , Densidad de Población , Variación Genética
7.
Mol Biol Evol ; 39(3)2022 03 02.
Artículo en Inglés | MEDLINE | ID: mdl-35244177

RESUMEN

Daphnia are well-established ecological and evolutionary models, and the interaction between D. magna and its microparasites is widely considered a paragon of the host-parasite coevolutionary process. Like other well-studied arthropods such as Drosophila melanogaster and Anopheles gambiae, D. magna is a small, widespread, and abundant species that is therefore expected to display a large long-term population size and high rates of adaptive protein evolution. However, unlike these other species, D. magna is cyclically asexual and lives in a highly structured environment (ponds and lakes) with moderate levels of dispersal, both of which are predicted to impact upon long-term effective population size and adaptive protein evolution. To investigate patterns of adaptive protein fixation, we produced the complete coding genomes of 36 D. magna clones sampled from across the European range (Western Palaearctic), along with draft sequences for the close relatives D. similis and D. lumholtzi, used as outgroups. We analyzed genome-wide patterns of adaptive fixation, with a particular focus on genes that have an a priori expectation of high rates, such as those likely to mediate immune responses, RNA interference against viruses and transposable elements, and those with a strongly male-biased expression pattern. We find that, as expected, D. magna displays high levels of diversity and that this is highly structured among populations. However, compared with Drosophila, we find that D. magna proteins appear to have a high proportion of weakly deleterious variants and do not show evidence of pervasive adaptive fixation across its entire range. This is true of the genome as a whole, and also of putative 'arms race' genes that often show elevated levels of adaptive substitution in other species. In addition to the likely impact of extensive, and previously documented, local adaptation, we speculate that these findings may reflect reduced efficacy of selection associated with cyclical asexual reproduction.


Asunto(s)
Daphnia , Drosophila melanogaster , Animales , Elementos Transponibles de ADN/genética , Daphnia/genética , Drosophila melanogaster/genética , Genómica , Masculino , Reproducción Asexuada
8.
Syst Biol ; 71(4): 777-787, 2022 06 16.
Artículo en Inglés | MEDLINE | ID: mdl-34850935

RESUMEN

Although phylogeny estimation is notoriously difficult in radiations that occurred several hundred million years ago, phylogenomic approaches offer new ways to examine relationships among ancient lineages and evaluate hypotheses that are key to evolutionary biology. Here, we reconstruct the deep-rooted relationships of one of the oldest living arthropod clades, the branchiopod crustaceans, using a kaleidoscopic approach. We use concatenation and coalescent tree-building methods to analyze a large multigene data set at the nucleotide and amino acid level and examine gene tree versus species tree discordance. We unequivocally resolve long-debated relationships among extant orders of the Cladocera, the waterfleas, an ecologically relevant zooplankton group in global aquatic and marine ecosystems that is famous for its model systems in ecology and evolution. To build the data set, we assembled eight de novo genomes of key taxa including representatives of all extant cladoceran orders and suborders. Our phylogenetic analysis focused on a BUSCO-based set of 823 conserved single-copy orthologs shared among 23 representative taxa spanning all living branchiopod orders, including 11 cladoceran families. Our analysis supports the monophyly of the Cladocera and reveals remarkable homoplasy in their body plans. We found large phylogenetic distances between lineages with similar ecological specializations, indicating independent evolution in major body plans, such as in the pelagic predatory orders Haplopoda and Onychopoda (the "Gymnomera"). In addition, we assessed rapid cladogenesis by estimating relative timings of divergence in major lineages using reliable fossil-calibrated priors on eight nodes in the branchiopod tree, suggesting a Paleozoic origin around 325 Ma for the cladoceran ancestor and an ancient rapid radiation around 252 Ma at the Perm/Triassic boundary. These findings raise new questions about the roles of homoplasy and rapid radiation in the diversification of the cladocerans and help examine trait evolution from a genomic perspective in a functionally well understood, ancient arthropod group. [Cladocera; Daphnia; evolution; homoplasy; molecular clock; phylogenomics; systematics; waterfleas.].


Asunto(s)
Ecosistema , Genoma , Evolución Biológica , Evolución Molecular , Fósiles , Especiación Genética , Filogenia
9.
Mol Biol Evol ; 38(11): 4918-4933, 2021 10 27.
Artículo en Inglés | MEDLINE | ID: mdl-34289047

RESUMEN

The link between long-term host-parasite coevolution and genetic diversity is key to understanding genetic epidemiology and the evolution of resistance. The model of Red Queen host-parasite coevolution posits that high genetic diversity is maintained when rare host resistance variants have a selective advantage, which is believed to be the mechanistic basis for the extraordinarily high levels of diversity at disease-related genes such as the major histocompatibility complex in jawed vertebrates and R-genes in plants. The parasites that drive long-term coevolution are, however, often elusive. Here we present evidence for long-term balancing selection at the phenotypic (variation in resistance) and genomic (resistance locus) level in a particular host-parasite system: the planktonic crustacean Daphnia magna and the bacterium Pasteuria ramosa. The host shows widespread polymorphisms for pathogen resistance regardless of geographic distance, even though there is a clear genome-wide pattern of isolation by distance at other sites. In the genomic region of a previously identified resistance supergene, we observed consistent molecular signals of balancing selection, including higher genetic diversity, older coalescence times, and lower differentiation between populations, which set this region apart from the rest of the genome. We propose that specific long-term coevolution by negative-frequency-dependent selection drives this elevated diversity at the host's resistance loci on an intercontinental scale and provide an example of a direct link between the host's resistance to a virulent pathogen and the large-scale diversity of its underlying genes.


Asunto(s)
Daphnia , Genoma , Animales , Daphnia/genética , Daphnia/microbiología , Interacciones Huésped-Parásitos/genética , Polimorfismo Genético
10.
Mol Biol Evol ; 38(9): 3581-3592, 2021 08 23.
Artículo en Inglés | MEDLINE | ID: mdl-33885820

RESUMEN

How does asexual reproduction influence genome evolution? Although is it clear that genomic structural variation is common and important in natural populations, we know very little about how one of the most fundamental of eukaryotic traits-mode of genomic inheritance-influences genome structure. We address this question with the New Zealand freshwater snail Potamopyrgus antipodarum, which features multiple separately derived obligately asexual lineages that coexist and compete with otherwise similar sexual lineages. We used whole-genome sequencing reads from a diverse set of sexual and asexual individuals to analyze genomic abundance of a critically important gene family, rDNA (the genes encoding rRNAs), that is notable for dynamic and variable copy number. Our genomic survey of rDNA in P. antipodarum revealed two striking results. First, the core histone and 5S rRNA genes occur between tandem copies of the 18S-5.8S-28S gene cluster, a unique architecture for these crucial gene families. Second, asexual P. antipodarum harbor dramatically more rDNA-histone copies than sexuals, which we validated through molecular and cytogenetic analysis. The repeated expansion of this genomic region in asexual P. antipodarum lineages following distinct transitions to asexuality represents a dramatic genome structural change associated with asexual reproduction-with potential functional consequences related to the loss of sexual reproduction.


Asunto(s)
Genoma , Histonas , Animales , Genómica , Histonas/genética , Humanos , Reproducción Asexuada/genética , Caracoles/genética
11.
Mol Ecol ; 31(9): 2528-2544, 2022 05.
Artículo en Inglés | MEDLINE | ID: mdl-35253310

RESUMEN

Analysing variation in a species' genomic diversity can provide insights into its historical demography, biogeography and population structure, and thus its ecology and evolution. Although such studies are rarely undertaken for parasites, they can be highly revealing because of the parasite's co-evolutionary relationships with hosts. Modes of reproduction and transmission are thought to be strong determinants of genomic diversity for parasites and vary widely among microsporidia (fungal-related intracellular parasites), which are known to have high intraspecific genetic diversity and interspecific variation in genome architecture. Here we explore genomic variation in the microsporidium Hamiltosporidium, a parasite of the freshwater crustacean Daphnia magna, looking especially at which factors contribute to nucleotide variation. Genomic samples from 18 Eurasian populations and a new, long-read-based reference genome were used to determine the roles that reproduction mode, transmission mode and geography play in determining population structure and demographic history. We demonstrate two main Hamiltosporidium tvaerminnensis lineages and a pattern of isolation-by-distance, but note an absence of congruence between these two parasite lineages and the two Eurasian host lineages. We suggest a comparatively recent parasite spread through Northern Eurasian host populations after a change from vertical to mixed-mode transmission and the loss of sexual reproduction. While gaining knowledge about the ecology and evolution of this focal parasite, we also identify common features that shape variation in genomic diversity for many parasites, such as distinct modes of reproduction and the intertwining of host-parasite demographies.


Asunto(s)
Parásitos , Animales , Daphnia/genética , Daphnia/parasitología , Demografía , Genómica
12.
J Eukaryot Microbiol ; 69(3): e12902, 2022 05.
Artículo en Inglés | MEDLINE | ID: mdl-35279911

RESUMEN

Speciation is a complex and continuous process that makes the delineation of species boundaries a challenging task in particular in species with little morphological differentiation, such as parasites. In this case, the use of genomic data is often necessary, such as for the intracellular Microsporidian parasites. Here, we characterize the genome of a gut parasite of the cladoceran Daphnia longispina (isolate FI-F-10), which we propose as a new species within the genus Ordospora: Ordospora pajunii sp. nov (Ordosporidae). FI-F-10 closest relative, Ordospora colligata is only found in D. magna. Both microsporidian species share several morphological features. Although it is not possible to estimate divergence times for Microsporidia due to the lack of fossil records and accelerated evolutionary rates, we base our proposal on the phylogenomic and genomic distances between both microsporidian lineages. The phylogenomic reconstruction shows that FI-F-10 forms an early diverging branch basal to the cluster that contains all known O. colligata strains. Whole-genome comparisons show that FI-F-10 presents a greater divergence at the sequence level than observed among O. colligata strains, and its genomic average nucleotide identity (ANI) values against O. colligata are beyond the intraspecific range previously established for yeast and prokaryotes. Our data confirm that the ANI metrics are useful for fine genetic divergence calibration across Microsporidia taxa. In combination with phylogenetic and ecological data, genome-based metrics provide a powerful approach to delimitate species boundaries.


Asunto(s)
Microsporidios , Parásitos , Animales , Daphnia/genética , Daphnia/parasitología , Genómica , Microsporidios/genética , Filogenia
13.
Mol Biol Evol ; 37(12): 3439-3452, 2020 12 16.
Artículo en Inglés | MEDLINE | ID: mdl-32658956

RESUMEN

Knowledge of the genetic architecture of pathogen infectivity and host resistance is essential for a mechanistic understanding of coevolutionary processes, yet the genetic basis of these interacting traits remains unknown for most host-pathogen systems. We used a comparative genomic approach to explore the genetic basis of infectivity in Pasteuria ramosa, a Gram-positive bacterial pathogen of planktonic crustaceans that has been established as a model for studies of Red Queen host-pathogen coevolution. We sequenced the genomes of a geographically, phenotypically, and genetically diverse collection of P. ramosa strains and performed a genome-wide association study to identify genetic correlates of infection phenotype. We found multiple polymorphisms within a single gene, Pcl7, that correlate perfectly with one common and widespread infection phenotype. We then confirmed this perfect association via Sanger sequencing in a large and diverse sample set of P. ramosa clones. Pcl7 codes for a collagen-like protein, a class of adhesion proteins known or suspected to be involved in the infection mechanisms of a number of important bacterial pathogens. Consistent with expectations under Red Queen coevolution, sequence variation of Pcl7 shows evidence of balancing selection, including extraordinarily high diversity and absence of geographic structure. Based on structural homology with a collagen-like protein of Bacillus anthracis, we propose a hypothesis for the structure of Pcl7 and the physical location of the phenotype-associated polymorphisms. Our results offer strong evidence for a gene governing infectivity and provide a molecular basis for further study of Red Queen dynamics in this model host-pathogen system.


Asunto(s)
Coevolución Biológica , Interacciones Huésped-Patógeno/genética , Pasteuria/genética , Proteínas Bacterianas/química , Genes Bacterianos , Estudio de Asociación del Genoma Completo , Glicosilación , Pasteuria/patogenicidad , Polimorfismo de Nucleótido Simple , Estructura Cuaternaria de Proteína
14.
Mol Biol Evol ; 37(11): 3258-3266, 2020 11 01.
Artículo en Inglés | MEDLINE | ID: mdl-32520985

RESUMEN

The rate and spectrum of spontaneous mutations are critical parameters in basic and applied biology because they dictate the pace and character of genetic variation introduced into populations, which is a prerequisite for evolution. We use a mutation-accumulation approach to estimate mutation parameters from whole-genome sequence data from multiple genotypes from multiple populations of Daphnia magna, an ecological and evolutionary model system. We report extremely high base substitution mutation rates (µ-n,bs = 8.96 × 10-9/bp/generation [95% CI: 6.66-11.97 × 10-9/bp/generation] in the nuclear genome and µ-m,bs = 8.7 × 10-7/bp/generation [95% CI: 4.40-15.12 × 10-7/bp/generation] in the mtDNA), the highest of any eukaryote examined using this approach. Levels of intraspecific variation based on the range of estimates from the nine genotypes collected from three populations (Finland, Germany, and Israel) span 1 and 3 orders of magnitude, respectively, resulting in up to a ∼300-fold difference in rates among genomic partitions within the same lineage. In contrast, mutation spectra exhibit very consistent patterns across genotypes and populations, suggesting the mechanisms underlying the mutational process may be similar, even when the rates at which they occur differ. We discuss the implications of high levels of intraspecific variation in rates, the importance of estimating gene conversion rates using a mutation-accumulation approach, and the interacting factors influencing the evolution of mutation parameters. Our findings deepen our knowledge about mutation and provide both challenges to and support for current theories aimed at explaining the evolution of the mutation rate, as a trait, across taxa.


Asunto(s)
Daphnia/genética , Tasa de Mutación , Animales , Acumulación de Mutaciones , Secuenciación Completa del Genoma
15.
Mol Ecol ; 30(15): 3660-3676, 2021 08.
Artículo en Inglés | MEDLINE | ID: mdl-34038012

RESUMEN

Host-parasite coevolution is ubiquitous, shaping genetic and phenotypic diversity and the evolutionary trajectory of interacting species. With the advances of high throughput sequencing technologies applicable to model and non-model organisms alike, it is now feasible to study in greater detail (a) the genetic underpinnings of coevolution, (b) the speed and type of dynamics at coevolving loci, and (c) the genomic consequences of coevolution. This review focuses on three recently developed approaches that leverage information from host and parasite full genome data simultaneously to pinpoint coevolving loci and draw inference on the coevolutionary history. First, co-genome-wide association study (co-GWAS) methods allow pinpointing the loci underlying host-parasite interactions. These methods focus on detecting associations between genetic variants and the outcome of experimental infection tests or on correlations between genomes of naturally infected hosts and their infecting parasites. Second, extensions to population genomics methods can detect genes under coevolution and infer the coevolutionary history, such as fitness costs. Third, correlations between host and parasite population size in time are indicative of coevolution, and polymorphism levels across independent spatially distributed populations of hosts and parasites can reveal coevolutionary loci and infer coevolutionary history. We describe the principles of these three approaches and discuss their advantages and limitations based on coevolutionary theory. We present recommendations for their application to various host (prokaryotes, fungi, plants, and animals) and parasite (viruses, bacteria, fungi, and macroparasites) species. We conclude by pointing out methodological and theoretical gaps to be filled to extract maximum information from full genome data and thereby to shed light on the molecular underpinnings of coevolution.


Asunto(s)
Parásitos , Animales , Evolución Biológica , Estudio de Asociación del Genoma Completo , Genómica , Interacciones Huésped-Parásitos/genética , Parásitos/genética
16.
J Evol Biol ; 34(5): 792-802, 2021 05.
Artículo en Inglés | MEDLINE | ID: mdl-33704857

RESUMEN

Inbreeding refers to the fusion of related individuals' gametes, with self-fertilization (selfing) being an extreme form of inbreeding-involving gametes produced by the same individual. Selfing is expected to reduce heterozygosity by an average of 50% in one generation; however, little is known about the empirical variation on a genome level surrounding this figure and the factors that affect variation. We selfed genotypes of the cyclic parthenogen Daphnia magna and analysed whole genomes of mothers and selfed offspring, observing the predicted 50% heterozygosity reduction on average. We also saw substantial variation around this value and significant differences among mother-offspring pairs. Crossover analysis confirmed the known trend of recombination occurring more often towards the telomeres. This effect was shown, through simulations, to increase the variance of heterozygosity reduction compared to when a uniform distribution of crossovers was used. Similarly, we simulated inbred line production after several generations of selfing and we observed higher variance in achieved homozygosity when we consider a higher recombination rate towards the telomeres. Our empirical and simulation study highlights that the expected mean values of heterozygosity reduction show remarkable variation, which can help understand, for example, differences among inbred individuals.


Asunto(s)
Daphnia/genética , Pérdida de Heterocigocidad , Modelos Genéticos , Partenogénesis/genética , Autofecundación/genética , Animales , Intercambio Genético , Genoma
17.
Mol Biol Evol ; 36(7): 1551-1564, 2019 07 01.
Artículo en Inglés | MEDLINE | ID: mdl-31173134

RESUMEN

Genetic sex determination (GSD) can evolve from environmental sex determination (ESD) via an intermediate state in which both coexist in the same population. Such mixed populations are found in the crustacean Daphnia magna, where non-male producers (NMP, genetically determined females) coexist with male producers (MP), in which male production is environmentally inducible and can also artificially be triggered by exposure to juvenile hormone. This makes Daphnia magna a rare model species for the study of evolutionary transitions from ESD to GSD. Although the chromosomal location of the NMP-determining mutation has been mapped, the actual genes and pathways involved in the evolution of GSD from ESD remain unknown. Here, we present a transcriptomic analysis of MP and NMP females under control (female producing) and under hormone exposure conditions. We found ∼100 differentially expressed genes between MP and NMP under control conditions. Genes in the NMP-determining chromosome region were especially likely to show such constitutive expression differences. Hormone exposure led to expression changes of an additional ∼100 (MP) to ∼600 (NMP) genes, with an almost systematic upregulation of those genes in NMP. These observations suggest that the NMP phenotype is not determined by a simple "loss-of-function" mutation. Rather, homeostasis of female offspring production under hormone exposure appears to be an active state, tightly regulated by complex mechanisms involving many genes. In a broader view, this illustrates that the evolution of GSD, while potentially initiated by a single mutation, likely leads to secondary integration involving many genes and pathways.


Asunto(s)
Evolución Biológica , Daphnia/genética , Expresión Génica , Procesos de Determinación del Sexo , Animales , Femenino , Perfilación de la Expresión Génica , Hormonas , Masculino
18.
Heredity (Edinb) ; 125(4): 173-183, 2020 10.
Artículo en Inglés | MEDLINE | ID: mdl-32561843

RESUMEN

To understand the mechanisms of antagonistic coevolution, it is crucial to identify the genetics of parasite resistance. In the Daphnia magna-Pasteuria ramosa host-parasite system, the most important step of the infection process is the one in which P. ramosa spores attach to the host's foregut. A matching-allele model (MAM) describes the host-parasite genetic interactions underlying attachment success. Here we describe a new P. ramosa genotype, P15, which, unlike previously studied genotypes, attaches to the host's hindgut, not to its foregut. Host resistance to P15 attachment shows great diversity across natural populations. In contrast to P. ramosa genotypes that use foregut attachment, P15 shows some quantitative variation in attachment success and does not always lead to successful infections, suggesting that hindgut attachment represents a less-efficient infection mechanism than foregut attachment. Using a Quantitative Trait Locus (QTL) approach, we detect two significant QTLs in the host genome: one that co-localizes with the previously described D. magna PR locus of resistance to foregut attachment, and a second, major QTL located in an unlinked genomic region. We find no evidence of epistasis. Fine mapping reveals a genomic region, the D locus, of ~13 kb. The discovery of a second P. ramosa attachment site and of a novel host-resistance locus increases the complexity of this system, with implications for both for the coevolutionary dynamics (e.g., Red Queen and the role of recombination), and for the evolution and epidemiology of the infection process.


Asunto(s)
Infecciones Bacterianas , Daphnia/genética , Resistencia a la Enfermedad/genética , Pasteuria , Animales , Daphnia/microbiología , Interacciones Huésped-Patógeno/genética , Pasteuria/genética , Sitios de Carácter Cuantitativo
19.
PLoS Genet ; 13(2): e1006596, 2017 02.
Artículo en Inglés | MEDLINE | ID: mdl-28222092

RESUMEN

Negative frequency-dependent selection (NFDS) is an evolutionary mechanism suggested to govern host-parasite coevolution and the maintenance of genetic diversity at host resistance loci, such as the vertebrate MHC and R-genes in plants. Matching-allele interactions of hosts and parasites that prevent the emergence of host and parasite genotypes that are universally resistant and infective are a genetic mechanism predicted to underpin NFDS. The underlying genetics of matching-allele interactions are unknown even in host-parasite systems with empirical support for coevolution by NFDS, as is the case for the planktonic crustacean Daphnia magna and the bacterial pathogen Pasteuria ramosa. We fine-map one locus associated with D. magna resistance to P. ramosa and genetically characterize two haplotypes of the Pasteuria resistance (PR-) locus using de novo genome and transcriptome sequencing. Sequence comparison of PR-locus haplotypes finds dramatic structural polymorphisms between PR-locus haplotypes including a large portion of each haplotype being composed of non-homologous sequences resulting in haplotypes differing in size by 66 kb. The high divergence of PR-locus haplotypes suggest a history of multiple, diverse and repeated instances of structural mutation events and restricted recombination. Annotation of the haplotypes reveals striking differences in gene content. In particular, a group of glycosyltransferase genes that is present in the susceptible but absent in the resistant haplotype. Moreover, in natural populations, we find that the PR-locus polymorphism is associated with variation in resistance to different P. ramosa genotypes, pointing to the PR-locus polymorphism as being responsible for the matching-allele interactions that have been previously described for this system. Our results conclusively identify a genetic basis for the matching-allele interaction observed in a coevolving host-parasite system and provide a first insight into its molecular basis.


Asunto(s)
Daphnia/genética , Interacciones Huésped-Parásitos/genética , Pasteuria/genética , Selección Genética/genética , Alelos , Animales , Daphnia/microbiología , Evolución Molecular , Variación Genética , Genotipo , Haplotipos/genética , Pasteuria/patogenicidad , Polimorfismo Genético
20.
Mol Ecol ; 28(21): 4770-4785, 2019 11.
Artículo en Inglés | MEDLINE | ID: mdl-31591747

RESUMEN

Parasite-mediated selection varying across time and space in metapopulations is expected to result in host local adaptation and the maintenance of genetic diversity in disease-related traits. However, nonadaptive processes like migration and extinction-(re)colonization dynamics might interfere with adaptive evolution. Understanding how adaptive and nonadaptive processes interact to shape genetic variability in life-history and disease-related traits can provide important insights into their evolution in subdivided populations. Here we investigate signatures of spatially fluctuating, parasite-mediated selection in a natural metapopulation of Daphnia magna. Host genotypes from infected and uninfected populations were genotyped at microsatellite markers, and phenotyped for life-history and disease traits in common garden experiments. Combining phenotypic and genotypic data a QST -FST -like analysis was conducted to test for signatures of parasite mediated selection. We observed high variation within and among populations for phenotypic traits, but neither an indication of host local adaptation nor a cost of resistance. Infected populations have a higher gene diversity (Hs) than uninfected populations and Hs is strongly positively correlated with fitness. These results suggest a strong parasite effect on reducing population level inbreeding. We discuss how stochastic processes related to frequent extinction-(re)colonization dynamics as well as host and parasite migration impede the evolution of resistance in the infected populations. We suggest that the genetic and phenotypic patterns of variation are a product of dynamic changes in the host gene pool caused by the interaction of colonization bottlenecks, inbreeding, immigration, hybrid vigor, rare host genotype advantage and parasitism. Our study highlights the effect of the parasite in ameliorating the negative fitness consequences caused by the high drift load in this metapopulation.


Asunto(s)
Daphnia/genética , Parásitos/genética , Animales , Variación Genética , Genotipo , Vigor Híbrido/genética , Endogamia/métodos , Repeticiones de Microsatélite/genética , Dinámica Poblacional
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