Identifying the presence and magnitude of population genetic structure remains a major consideration in evolutionary biology as doing so allows one to understand the demographic history of a species as well as make predictions of how the evolutionary process will proceed. Next-generation sequencing methods allow us to reconsider previous ideas and conclusions concerning the distribution of genetic variation, and what this distribution implies about a given species evolutionary history. A previous phylogeographic study of the crustacean Daphnia magna suggested that, despite strong genetic differentiation among populations at a local scale, the species shows only moderate genetic structure across its European range, with a spatially patchy occurrence of individual lineages. We apply RAD sequencing to a sample of D. magna collected across a wide swath of the species' Eurasian range and analyse the data using principle component analysis (PCA) of genetic variation and Procrustes analytical approaches, to quantify spatial genetic structure. We find remarkable consistency between the first two PCA axes and the geographic coordinates of individual sampling points, suggesting that, on a continent-wide scale, genetic differentiation is driven to a large extent by geographic distance. The observed pattern is consistent with unimpeded (i.e. no barriers, landscape or otherwise) migration at large spatial scales, despite the fragmented and patchy nature of favourable habitats at local scales. With high-resolution genetic data similar patterns may be uncovered for other species with wide geographic distributions, allowing an increased understanding of how genetic drift and selection have shaped their evolutionary history.
The breeding systems of many organisms are cryptic and difficult to investigate with observational data, yet they have profound effects on a species' ecology, evolution, and genome organization. Genomic approaches offer a novel, indirect way to investigate breeding systems, specifically by studying the transmission of genetic information from parents to offspring. Here we exemplify this method through an assessment of self-fertilization vs. automictic parthenogenesis in Daphnia magna. Self-fertilization reduces heterozygosity by 50% compared to the parents, but under automixis, whereby two haploid products from a single meiosis fuse, the expected heterozygosity reduction depends on whether the two meiotic products are separated during meiosis I or II (i.e., central vs. terminal fusion). Reviewing the existing literature and incorporating recombination interference, we derive an interchromosomal and an intrachromosomal prediction of how to distinguish various forms of automixis from self-fertilization using offspring heterozygosity data. We then test these predictions using RAD-sequencing data on presumed automictic diapause offspring of so-called nonmale producing strains and compare them with "self-fertilized" offspring produced by within-clone mating. The results unequivocally show that these offspring were produced by automixis, mostly, but not exclusively, through terminal fusion. However, the results also show that this conclusion was only possible owing to genome-wide heterozygosity data, with phenotypic data as well as data from microsatellite markers yielding inconclusive or even misleading results. Our study thus demonstrates how to use the power of genomic approaches for elucidating breeding systems, and it provides the first demonstration of automictic parthenogenesis in Daphnia.KEYWORDS genome-wide heterozygosity; breeding system; inbreeding; automixis; tychoparthenogenesis; Daphnia magna; nonmale producers W HILE humans and most other mammals reproduce exclusively by sexual reproduction with sexes being determined by the well-known XY sex-chromosome system, the breeding systems of many other organisms, including many pests and parasites, remain unknown (Bell 1982;Normark 2003). The breeding system sensu lato, (including details of meiosis, e.g., recombination patterns and syngamy, e.g., levels of inbreeding, as well as their variants, e.g., modified meiosis in parthenogens) represents a key for understanding the biology of a species and has profound effects on its ecology, evolution, and genomics. Yet investigating breeding systems is often far from straightforward: Many species cannot easily be cultured and bred in the laboratory and observations of breeding behavior in nature are difficult. Even in species than can be bred in the laboratory, parts of the breeding system may be cryptic and not directly observable.The advent of high-throughput genotyping methods opens an alternative possibility that can be used on a much larger array of species: indirect inference of the breeding system usi...
BackgroundRecombination rate is an essential parameter for many genetic analyses. Recombination rates are highly variable across species, populations, individuals and different genomic regions. Due to the profound influence that recombination can have on intraspecific diversity and interspecific divergence, characterization of recombination rate variation emerges as a key resource for population genomic studies and emphasises the importance of high-density genetic maps as tools for studying genome biology. Here we present such a high-density genetic map for Daphnia magna, and analyse patterns of recombination rate across the genome.ResultsA F2 intercross panel was genotyped by Restriction-site Associated DNA sequencing to construct the third-generation linkage map of D. magna. The resulting high-density map included 4037 markers covering 813 scaffolds and contigs that sum up to 77 % of the currently available genome draft sequence (v2.4) and 55 % of the estimated genome size (238 Mb). Total genetic length of the map presented here is 1614.5 cM and the genome-wide recombination rate is estimated to 6.78 cM/Mb. Merging genetic and physical information we consistently found that recombination rate estimates are high towards the peripheral parts of the chromosomes, while chromosome centres, harbouring centromeres in D. magna, show very low recombination rate estimates.ConclusionsDue to its high-density, the third-generation linkage map for D. magna can be coupled with the draft genome assembly, providing an essential tool for genome investigation in this model organism. Thus, our linkage map can be used for the on-going improvements of the genome assembly, but more importantly, it has enabled us to characterize variation in recombination rate across the genome of D. magna for the first time. These new insights can provide a valuable assistance in future studies of the genome evolution, mapping of quantitative traits and population genetic studies.Electronic supplementary materialThe online version of this article (doi:10.1186/s12863-016-0445-7) contains supplementary material, which is available to authorized users.
1 Sex chromosomes can evolve during the evolution of genetic sex determination (GSD) 2 from environmental sex determination (ESD). Despite theoretical attention, early mechanisms 3 involved in the transition from ESD to GSD have yet to be studied in nature. No mixed ESD-4 GSD animal species have been reported, except for some species of Daphnia, small freshwater 5 crustaceans in which sex is usually determined solely by the environment, but in which a 6 dominant female sex-determining locus is present in some populations. This locus follows 7Mendelian single-locus inheritance, but has otherwise not been characterized genetically. We 8 now show that the sex-determining genomic region maps to the same low-recombining peri-9 centromeric region of linkage group 3 (LG3) in three highly divergent populations of D. magna, 10 and spans 3.6 Mb. Despite low levels of recombination, the associated region contains signs of 11 historical recombination, suggesting a role for selection acting on several genes thereby 12 maintaining linkage disequilibrium among the 36 associated SNPs. The region carries numerous 13 genes involved in sex differentiation in other taxa, including transformer2 and sox9. Taken 14 together, the region determining the NMP phenotype shows characteristics of a sex-related 15 supergene, suggesting that LG3 is potentially an incipient W chromosome despite the lack of 16 significant additional restriction of recombination between Z and W. The occurrence of the 17 female-determining locus in a pre-existing low recombining region illustrates one possible form 18 of recombination suppression in sex chromosomes. D. magna is a promising model for studying 19 the evolutionary transitions from ESD to GSD and early sex chromosome evolution. 20 animal groups (Ohno 1967;Pokorná and Kratochvíl 2016). Although transition from ESD to 44 GSD may be gradual, involving shifting genotype-specific thresholds for male vs. female 45 development under fluctuating environmental conditions (Van Dooren and Leimar 2003), a 46 scenario similar to that of the transition from hermaphroditism to separate sexes is also plausible: 47Supplementary Material S1). In all three crosses, the fully linked markers mapped between cM 129 positions 87.8 cM and 94.0 cM of LG3 in the reference genetic map. This region also contains 130 the centromere (at 90.8 cM). We call this region the "NMP region" (Fig. 2). A Marey map of 131LG3 (Dukič et al. in press) shows that the NMP-region corresponds to a large (~3 Mb) non-132 recombining region around the centromere (Fig. 2). Non-recombining regions around the 133 centromeres are found on all linkage groups of D. magna, and are not a sign of reduced 134
Sex chromosomes can evolve during the evolution of genetic sex determination (GSD) from environmental sex determination (ESD). Despite theoretical attention, early mechanisms involved in the transition from ESD to GSD have yet to be studied in nature. No mixed ESD-GSD animal species have been reported, except for some species of Daphnia, small freshwater crustaceans in which sex is usually determined solely by the environment, but in which a dominant female sex-determining locus is present in some populations. This locus follows Mendelian single-locus inheritance, but has otherwise not been characterized genetically. We now show that the sex-determining genomic region maps to the same low-recombining peri-centromeric region of linkage group 3 (LG3) in three highly divergent populations of D. magna, and spans 3.6 Mb. Despite low levels of recombination, the associated region contains signs of historical recombination, suggesting a role for selection acting on several genes thereby maintaining linkage disequilibrium among the 36 associated SNPs. The region carries numerous genes involved in sex differentiation in other taxa, including transformer2 and sox9. Taken together, the region determining the genetic females shows characteristics of a sex-related supergene, suggesting that LG3 is potentially an incipient W chromosome despite the lack of significant additional restriction of recombination between Z and W. The occurrence of the female-determining locus in a pre-existing low recombining region illustrates one possible form of recombination suppression in sex chromosomes. D. magna is a promising model for studying the evolutionary transitions from ESD to GSD and early sex chromosome evolution.
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