An SNP-based second-generation genetic map of Daphnia magna and its application to QTL analysis of phenotypic traits

Routtu, Jarkko; Hall, Matthew D.; Albere, Brian; Beisel, Christian; Bergeron, R. Daniel; Chaturvedi, Anurag; Choi, Jeong-Hyeon; Colbourne, John K.; Meester, Luc De; Stephens, Melissa; Stelzer, Claus‐Peter; Solorzano, Eleanne; Thomas, W. Kelley; Pfrender, Michael E.; Ebert, Dieter

doi:10.1186/1471-2164-15-1033

Cited by 54 publications

(105 citation statements)

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“…The total genetic map distance of the new map is 1451 Kosambi cM, slightly greater than that of the D. arenata map (1206 cM) and similar to D. magna (1483 cM; Routtu et al 2014). This map anchors to chromosomes 187 scaffolds (131.9 Mbp), in comparison to 73 anchored scaffolds (73.9 Mb) from the D. arenata map.…”

Section: Discussionmentioning

confidence: 88%

“…Furthermore, the new map provides much refined estimates of the recombination rate between markers (0.87 vs.7 cM), allowing the mapping of 90% of the D. pulex genome to on average ,1 cM to the nearest genetic marker. This intermarker distance is also smaller than that in the SNP-based D. magna genetic map (1.13 cM; Routtu et al 2014). Therefore, this map provides a framework to examine the role of recombination rate in shaping the various aspects of the genomic architecture of Daphnia genome such as patterns of nucleotide substitution and codon usage, which to date have not been explored in detail.…”

Section: Discussionmentioning

confidence: 89%

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A Male-Specific Genetic Map of the MicrocrustaceanDaphnia pulexBased on Single-Sperm Whole-Genome Sequencing

Ackerman

Long

et al. 2015

Genetics

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Genetic linkage maps are critical for assembling draft genomes to a meaningful chromosome level and for deciphering the genomic underpinnings of biological traits. The estimates of recombination rates derived from genetic maps also play an important role in understanding multiple aspects of genomic evolution such as nucleotide substitution patterns and accumulation of deleterious mutations. In this study, we developed a high-throughput experimental approach that combines fluorescence-activated cell sorting, whole-genome amplification, and shortread sequencing to construct a genetic map using single-sperm cells. Furthermore, a computational algorithm was developed to analyze singlesperm whole-genome sequencing data for map construction. These methods allowed us to rapidly build a male-specific genetic map for the freshwater microcrustacean Daphnia pulex, which shows significant improvements compared to a previous map. With a total of mapped 1672 haplotype blocks and an average intermarker distance of 0.87 cM, this map spans a total genetic distance of 1451 Kosambi cM and comprises 90% of the resolved regions in the current Daphnia reference assembly. The map also reveals the mistaken mapping of seven scaffolds in the reference assembly onto chromosome II by a previous microsatellite map based on F 2 crosses. Our approach can be easily applied to many other organisms and holds great promise for unveiling the intragenomic and intraspecific variation in the recombination rates.KEYWORDS meiosis; fluorescence-activated cell sorting; single cell; whole-genome amplification C ONSTRUCTING a genetic linkage map that encompasses as much genomic sequence as possible is critical for current endeavors of de novo genomic assembly (e.g., Kawakami et al. 2014; International Cassava Genetic Map Consortium (ICGMC) 2015) and for deciphering the genomic underpinnings of the biological traits in the species of interest (Lynch and Walsh 1998). Genetic maps can be utilized in several ways to help achieve these goals. At the very least, a linkage map with an adequate number of genetic markers can serve as the backbone for orienting and assembling segments of DNA (i.e., scaffolds) into chromosomes. The developed genetic markers can also be used in QTL association mapping and genomic-scanning efforts to investigate genetic loci underlying ecological tolerance, adaptation, and disease. Furthermore, a linkage map provides genome-wide estimates of the meiotic recombination rate, which plays a significant role in the distribution of genetic diversity (Nachman 2001), rate of adaptation (Bachtrog and Charlesworth 2002), accumulation of deleterious mutations (Hussin et al. 2015), and nucleotide substitution (Duret and Arndt 2008).Currently, the most common approach for constructing a genetic linkage map is based on genotyping a large number of molecular markers (e.g., SNPs, microsatellites) from a large number of offspring (usually on the order of hundreds) derived from various kinds of crossing schemes (e.g., backcrosses, F 2 s, reco...

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Section: Discussionmentioning

confidence: 88%

Section: Discussionmentioning

confidence: 89%

A Male-Specific Genetic Map of the MicrocrustaceanDaphnia pulexBased on Single-Sperm Whole-Genome Sequencing

Ackerman

Long

et al. 2015

Genetics

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“…The values of the phototactic index (De Meester, , ) of some of the F2 clones from the same F2 panel used in the present study were retrieved from the data set published by Routtu et al . (). Briefly, the authors quantified the phototactic behaviour of the clones by counting the proportion of animals occupying the upper (U; 12 cm), middle (M; 10 cm) or lower (L; 3 cm) compartments of a 25‐cm‐high glass column illuminated from above.…”

Section: Methodsmentioning

confidence: 99%

Ecological genetics of sediment browsing behaviour in a planktonic crustacean

Arbore

Andras

Routtu

et al. 2016

J of Evolutionary Biology

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Zooplankton can display complex habitat selection behaviours that influence the way they interact with their environments. Some species, although primarily pelagic, can exploit sediment-borne particles as a food source or use sediments as a refuge from pelagic predation. However, this strategy may increase the exposure to other risks such as benthic predation and infection from sediment-borne parasite transmission stages. The evolution of habitat selection behaviour in these species is thus expected to be influenced by multiple and possibly contrasting selective forces. Here, we study the browsing behaviour of the water flea Daphnia magna on bottom sediments. First, we demonstrated genetic variation for sediment browsing among D. magna genotypes from natural populations sampled across a broad geographic range. Next, we used an F2 recombinant panel to perform a QTL analysis and identified three regions in the D. magna genome contributing to variation in browsing behaviour. We also analysed the correlation between our data and previously published data on the phototactic behaviour of genotypes from the same F2 panel. Clonal means of the two behavioral traits were not correlated, suggesting that they may evolve independently. Browsing behaviour is likely to be a relevant component of habitat selection in D. magna, and its study may help to incorporate the interactions with the sediment into eco-evolutionary models of this key freshwater species.

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Section: Microsatellite Genotypes Of Offspring From Cultures Containimentioning

confidence: 99%

“…It ranged from 0.24 to 0.67 among linkage groups and from 0.40 to 0.73 among individuals (Table S3). The relatively high variation among individuals and linkage groups was expected because only few recombination events occur per meiosis and chromosome (Routtu et al 2010(Routtu et al , 2014, so that many linked markers show identical inheritance patterns.As a control, RAD sequencing was also carried out on 27 offspring of the RM1-18 MP clone. Average genome-wide heterozygosity among these offspring was 0.60 (N = 1610 loci), varying among linkage groups between 0.46 and 0.71 (Table S3).…”

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Uncovering Cryptic Asexuality in Daphnia magna by RAD Sequencing

et al. 2015

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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...

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An SNP-based second-generation genetic map of Daphnia magna and its application to QTL analysis of phenotypic traits

Cited by 54 publications

References 56 publications

A Male-Specific Genetic Map of the MicrocrustaceanDaphnia pulexBased on Single-Sperm Whole-Genome Sequencing

A Male-Specific Genetic Map of the MicrocrustaceanDaphnia pulexBased on Single-Sperm Whole-Genome Sequencing

Ecological genetics of sediment browsing behaviour in a planktonic crustacean

Uncovering Cryptic Asexuality in Daphnia magna by RAD Sequencing

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