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, 8 (1), 273

The Genetic Basis of Natural Variation in a Phoretic Behavior

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The Genetic Basis of Natural Variation in a Phoretic Behavior

Daehan Lee et al. Nat Commun.

Abstract

Phoresy is a widespread form of commensalism that facilitates dispersal of one species through an association with a more mobile second species. Dauer larvae of the nematode Caenorhabditis elegans exhibit a phoretic behavior called nictation, which could enable interactions with animals such as isopods or snails. Here, we show that natural C. elegans isolates differ in nictation. We use quantitative behavioral assays and linkage mapping to identify a genetic locus (nict-1) that mediates the phoretic interaction with terrestrial isopods. The nict-1 locus contains a Piwi-interacting small RNA (piRNA) cluster; we observe that the Piwi Argonaute PRG-1 is involved in the regulation of nictation. Additionally, this locus underlies a trade-off between offspring production and dispersal. Variation in the nict-1 locus contributes directly to differences in association between nematodes and terrestrial isopods in a laboratory assay. In summary, the piRNA-rich nict-1 locus could define a novel mechanism underlying phoretic interactions.Nematodes use a characteristic set of movements, called nictation, to hitchhike on more mobile animals. Here, Lee et al. identify a genetic locus in the nematode Caenorhabditis elegans that underlies nictation and contributes to successful hitchhiking, but at expense of reduced offspring production.

Conflict of interest statement

The authors declare no competing financial interests.

Figures

Fig. 1
Fig. 1
C. elegans differences in a phoretic behavior map to chromosome IV. a The mean nictation fractions of 12 divergent wild isolates are shown (from left, CB4856 (blue), EG4725, ED3017, JT11398, N2 (orange), JU258, JU775, DL238, LKC34, CX11314, MY16, and MY23). Twenty-four replicates of CB4856 and three replicates of all other strains were measured to calculate the means. Error bars are standard deviations. b A histogram of the normalized nictation fractions of 186 N2xCB4856 recombinant inbred advanced intercross lines (RIAILs) is shown. c Linkage-mapping results of normalized nictation fraction are shown with genomic position (Mb) on the x-axis and logarithm of odds (LOD) score on the y-axis. The tick marks on the x-axis denote every 5 Mb. Each chromosome is in its own box labeled on top. The gray line is the LOD threshold for 5% genome-wide error rate obtained by permuting the phenotype data and mapping 1000 times. The red triangle denotes the peak QTL marker. d Tukey box plots of N2 (orange) and CB4856 (blue) are shown with data points plotted behind. The horizontal line in the middle of the box is the median, and the box denotes the 25th to 75th quantiles of the data. The vertical line represents the 1.5 interquartile range
Fig. 2
Fig. 2
Variation in 21U piRNAs underlies nictation differences. a Genotypes of near isogenic lines (NILs) represented by orange (N2) and blue (CB4856) colored bars are shown. Strain labels are to the right. Solid vertical lines denote the confidence interval from the genetic mapping experiment. Dotted lines denote the narrowed genetic interval. b The mean nictation fractions of N2 (orange), CB4856 (blue), and NILs are shown as horizontal bars. Error bars are standard deviations. The number of biological replicates for each strain range from 17 to 49. c Genomic features of NIL-narrowed 73 kb nict-1 QTL interval are shown. Protein-coding genes (top) are colored orange (higher expression in the N2 nict-1 strain), blue (higher expression in CB4856 nict-1 strain), or gray (no expression difference between the nict-1 genotypes). The blue dot denotes a predicted functional effect in Y105C5A.1272. The locations of piRNAs and other genomics features (tRNAs, snoRNAs, etc.) are shown in gray in the middle and bottom rows. d Tukey box plots of normalized nictation fractions of N2 (orange), LJ1203 (nict-1 CB4856 > N2, blue), ECA586 (prg-1(ean28) in the N2 genetic background, gray), CB4856 (blue), LJ1213 (nict-1 N2 > CB4856, orange), ECA584 (prg-1(ean30) in the CB4856 genetic background, gray) are shown with data points plotted behind. The horizontal line is the median, and the box denotes the 25th to 75th quantiles of the data. The vertical line represents the 1.5 interquartile range. All strains were scored in 21 biological replicates, except for strain ECA584 where 19 biological replicates were scored. Each biological replicate was composed of three technical replicates
Fig. 3
Fig. 3
The nict-1 QTL controls a fitness trade-off and species dispersal on isopods. a Brood sizes of N2, CB4856, LJ1203 (nict-1 CB4856 > N2), and LJ1213 (nict-1 N2 > CB4856) are shown as Tukey box plots colored based on the nict-1 genotype. The horizontal line is the median, and the box denotes the 25th to 75th quantiles of the data. The vertical line represents the 1.5 interquartile range. All four strains were scored in 30 biological replicates, except for LJ1213 where only 29 biological replicates were scored. b The mean N2 nict-1 QTL allele frequencies before (origin) and after (destination) transmission competition assays are plotted. Error bars are standard deviations. c The experimental scheme of the transmission competition assay is shown. Transmission competition assay chambers contain two nematode culture plates. The “origin” plate contained a mixture of dauer animals from the CB4856 and LJ1213 (nict-1 N2 > CB4856) strains and was covered with medical gauze to facilitate nictation. The “destination” plate was placed 1–2 cm away with no nematodes on this plate. Terrestrial isopods were added to the chamber and allowed to roam freely for 24 h. Nematodes depend on the isopods for transfer to the “destination” plate from the “origin” plate because no transfer was observed without isopods presence. Eleven different biological replicates were scored

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