Limits...
Highly polygenic variation in environmental perception determines dauer larvae formation in growing populations of Caenorhabditis elegans.

Green JW, Stastna JJ, Orbidans HE, Harvey SC - PLoS ONE (2014)

Bottom Line: We also show that food patch size affects both the ability to detect QTLs and estimates of effect size, and demonstrate that an allele of nath-10 affects dauer larvae formation in growing populations.These data indicate that QTLs affecting the number of dauer larvae at food exhaustion in growing populations of C. elegans are highly reproducible, and that nearly all can be explained by variation affecting dauer larvae formation in response to defined amounts of pheromone.This suggests that most variation in dauer larvae formation in growing populations is a consequence of variation in the perception of the food and pheromone environment (i.e. chemosensory variation) and in the integration of these cues.

View Article: PubMed Central - PubMed

Affiliation: Biomolecular Research Group, School of Human and Life Sciences, Canterbury Christ Church University, Canterbury, United Kingdom.

ABSTRACT

Background: Determining how complex traits are genetically controlled is a requirement if we are to predict how they evolve and how they might respond to selection. This requires understanding how distinct, and often more simple, life history traits interact and change in response to environmental conditions. In order to begin addressing such issues, we have been analyzing the formation of the developmentally arrested dauer larvae of Caenorhabditis elegans under different conditions.

Results: We find that 18 of 22 previously identified quantitative trait loci (QTLs) affecting dauer larvae formation in growing populations, assayed by determining the number of dauer larvae present at food patch exhaustion, can be recovered under various environmental conditions. We also show that food patch size affects both the ability to detect QTLs and estimates of effect size, and demonstrate that an allele of nath-10 affects dauer larvae formation in growing populations. To investigate the component traits that affect dauer larvae formation in growing populations we map, using the same introgression lines, QTLs that affect dauer larvae formation in response to defined amounts of pheromone. This identifies 36 QTLs, again demonstrating the highly polygenic nature of the genetic variation underlying dauer larvae formation.

Conclusions: These data indicate that QTLs affecting the number of dauer larvae at food exhaustion in growing populations of C. elegans are highly reproducible, and that nearly all can be explained by variation affecting dauer larvae formation in response to defined amounts of pheromone. This suggests that most variation in dauer larvae formation in growing populations is a consequence of variation in the perception of the food and pheromone environment (i.e. chemosensory variation) and in the integration of these cues.

Show MeSH

Related in: MedlinePlus

Variation surrounding nath-10 affects the number of dauer larvae at food exhaustion in growing populations.Box and whisker plots showing number of dauer larvae (top panels) and the population size (bottom panels) at exhaustion of 100 µl of 20% w/v food in two assays (left and right columns) in N2 and in JU1648, JU2041 and JU2047, lines with very fine introgressions of the nath-10(haw6805) allele in an N2 genetic background. The nath-10(haw6805) allele is the only common difference that distinguishes JU2041, JU2047, and JU1648 from N2, and JU2041 contains only two known alleles that differ from N2, nath-10(haw6805) and mfP19 (see [19] for further details). Asterisks indicate significant difference to N2 within that assay (p<0.05, post hoc testing by Fisher’s Least Significant Difference).
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4231163&req=5

pone-0112830-g003: Variation surrounding nath-10 affects the number of dauer larvae at food exhaustion in growing populations.Box and whisker plots showing number of dauer larvae (top panels) and the population size (bottom panels) at exhaustion of 100 µl of 20% w/v food in two assays (left and right columns) in N2 and in JU1648, JU2041 and JU2047, lines with very fine introgressions of the nath-10(haw6805) allele in an N2 genetic background. The nath-10(haw6805) allele is the only common difference that distinguishes JU2041, JU2047, and JU1648 from N2, and JU2041 contains only two known alleles that differ from N2, nath-10(haw6805) and mfP19 (see [19] for further details). Asterisks indicate significant difference to N2 within that assay (p<0.05, post hoc testing by Fisher’s Least Significant Difference).

Mentions: Given that a laboratory derived allele of npr-1 affects dauer larvae development in growing populations [28], we investigated if other alleles that have arisen during the time N2 has spent in culture in the laboratory (see Table S3 in [30]) could affect this trait. Comparison of the QTL limits to candidate laboratory alleles with non-synonymous amino acid substitutions (see Table S3 in [30]) revealed candidate genes for QTLs gp2 (nath-10, identified in [30] as F55A12.8, and gld-2), gp10 (K10D2.1, K04G7.1 and F56C9.11), gp15 (pept-1, identified in [30] as opt-1) and gp21 (C46C11.4 and F39C12.1, with this QTL also containing npr-1). As variation at nath-10 has been shown to affect age at maturity, brood size, and egg-laying speed [31], traits that might be expected to affect the properties of growing populations, this polymorphism was further investigated. No evidence was identified to link the polymorphisms in other genes to either reproductive or dauer development traits, so these were not further investigated here. Analysis of data from lines that vary at nath-10 indicated that population size at food exhaustion was lower in lines carrying the nath-10(haw6805) allele, but did not differ between isolates in either assay (Figure 3: F3,32 = 0.85, p = 0.48, F3,31 = 1.27, p = 0.30 for assays 1 and 2, respectively). In contrast, the number of dauer larvae at food exhaustion differed between lines in both assays (Figure 3: F3,32 = 4.96, p = 0.006, F3,31 = 3.64, p = 0.02 for assays 1 and 2, respectively), with more dauer larvae observed in N2 than all other lines in assay 1 and more than JU2041 and JU2047 in assay 2 (Fisher’s LSD). This indicates that variation in the region of nath-10 affects dauer larvae formation in growing populations. As the nath-10(haw6805) allele is the only common difference distinguishing JU2041, JU2047, and JU1648 from N2, and JU2041 contains only two known alleles that differ from N2, nath-10(haw6805) and mfP19[19], the most parsimonious explanation is that the differences observed here are a consequence of variation at nath-10.


Highly polygenic variation in environmental perception determines dauer larvae formation in growing populations of Caenorhabditis elegans.

Green JW, Stastna JJ, Orbidans HE, Harvey SC - PLoS ONE (2014)

Variation surrounding nath-10 affects the number of dauer larvae at food exhaustion in growing populations.Box and whisker plots showing number of dauer larvae (top panels) and the population size (bottom panels) at exhaustion of 100 µl of 20% w/v food in two assays (left and right columns) in N2 and in JU1648, JU2041 and JU2047, lines with very fine introgressions of the nath-10(haw6805) allele in an N2 genetic background. The nath-10(haw6805) allele is the only common difference that distinguishes JU2041, JU2047, and JU1648 from N2, and JU2041 contains only two known alleles that differ from N2, nath-10(haw6805) and mfP19 (see [19] for further details). Asterisks indicate significant difference to N2 within that assay (p<0.05, post hoc testing by Fisher’s Least Significant Difference).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4231163&req=5

pone-0112830-g003: Variation surrounding nath-10 affects the number of dauer larvae at food exhaustion in growing populations.Box and whisker plots showing number of dauer larvae (top panels) and the population size (bottom panels) at exhaustion of 100 µl of 20% w/v food in two assays (left and right columns) in N2 and in JU1648, JU2041 and JU2047, lines with very fine introgressions of the nath-10(haw6805) allele in an N2 genetic background. The nath-10(haw6805) allele is the only common difference that distinguishes JU2041, JU2047, and JU1648 from N2, and JU2041 contains only two known alleles that differ from N2, nath-10(haw6805) and mfP19 (see [19] for further details). Asterisks indicate significant difference to N2 within that assay (p<0.05, post hoc testing by Fisher’s Least Significant Difference).
Mentions: Given that a laboratory derived allele of npr-1 affects dauer larvae development in growing populations [28], we investigated if other alleles that have arisen during the time N2 has spent in culture in the laboratory (see Table S3 in [30]) could affect this trait. Comparison of the QTL limits to candidate laboratory alleles with non-synonymous amino acid substitutions (see Table S3 in [30]) revealed candidate genes for QTLs gp2 (nath-10, identified in [30] as F55A12.8, and gld-2), gp10 (K10D2.1, K04G7.1 and F56C9.11), gp15 (pept-1, identified in [30] as opt-1) and gp21 (C46C11.4 and F39C12.1, with this QTL also containing npr-1). As variation at nath-10 has been shown to affect age at maturity, brood size, and egg-laying speed [31], traits that might be expected to affect the properties of growing populations, this polymorphism was further investigated. No evidence was identified to link the polymorphisms in other genes to either reproductive or dauer development traits, so these were not further investigated here. Analysis of data from lines that vary at nath-10 indicated that population size at food exhaustion was lower in lines carrying the nath-10(haw6805) allele, but did not differ between isolates in either assay (Figure 3: F3,32 = 0.85, p = 0.48, F3,31 = 1.27, p = 0.30 for assays 1 and 2, respectively). In contrast, the number of dauer larvae at food exhaustion differed between lines in both assays (Figure 3: F3,32 = 4.96, p = 0.006, F3,31 = 3.64, p = 0.02 for assays 1 and 2, respectively), with more dauer larvae observed in N2 than all other lines in assay 1 and more than JU2041 and JU2047 in assay 2 (Fisher’s LSD). This indicates that variation in the region of nath-10 affects dauer larvae formation in growing populations. As the nath-10(haw6805) allele is the only common difference distinguishing JU2041, JU2047, and JU1648 from N2, and JU2041 contains only two known alleles that differ from N2, nath-10(haw6805) and mfP19[19], the most parsimonious explanation is that the differences observed here are a consequence of variation at nath-10.

Bottom Line: We also show that food patch size affects both the ability to detect QTLs and estimates of effect size, and demonstrate that an allele of nath-10 affects dauer larvae formation in growing populations.These data indicate that QTLs affecting the number of dauer larvae at food exhaustion in growing populations of C. elegans are highly reproducible, and that nearly all can be explained by variation affecting dauer larvae formation in response to defined amounts of pheromone.This suggests that most variation in dauer larvae formation in growing populations is a consequence of variation in the perception of the food and pheromone environment (i.e. chemosensory variation) and in the integration of these cues.

View Article: PubMed Central - PubMed

Affiliation: Biomolecular Research Group, School of Human and Life Sciences, Canterbury Christ Church University, Canterbury, United Kingdom.

ABSTRACT

Background: Determining how complex traits are genetically controlled is a requirement if we are to predict how they evolve and how they might respond to selection. This requires understanding how distinct, and often more simple, life history traits interact and change in response to environmental conditions. In order to begin addressing such issues, we have been analyzing the formation of the developmentally arrested dauer larvae of Caenorhabditis elegans under different conditions.

Results: We find that 18 of 22 previously identified quantitative trait loci (QTLs) affecting dauer larvae formation in growing populations, assayed by determining the number of dauer larvae present at food patch exhaustion, can be recovered under various environmental conditions. We also show that food patch size affects both the ability to detect QTLs and estimates of effect size, and demonstrate that an allele of nath-10 affects dauer larvae formation in growing populations. To investigate the component traits that affect dauer larvae formation in growing populations we map, using the same introgression lines, QTLs that affect dauer larvae formation in response to defined amounts of pheromone. This identifies 36 QTLs, again demonstrating the highly polygenic nature of the genetic variation underlying dauer larvae formation.

Conclusions: These data indicate that QTLs affecting the number of dauer larvae at food exhaustion in growing populations of C. elegans are highly reproducible, and that nearly all can be explained by variation affecting dauer larvae formation in response to defined amounts of pheromone. This suggests that most variation in dauer larvae formation in growing populations is a consequence of variation in the perception of the food and pheromone environment (i.e. chemosensory variation) and in the integration of these cues.

Show MeSH
Related in: MedlinePlus