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Identifying candidate genes affecting developmental time in Drosophila melanogaster: pervasive pleiotropy and gene-by-environment interaction.

Mensch J, Lavagnino N, Carreira VP, Massaldi A, Hasson E, Fanara JJ - BMC Dev. Biol. (2008)

Bottom Line: Plastic reaction norms were found for a large number of developmental time candidate genes.We also demonstrate that many developmental time genes have pleiotropic effects on several adult traits and that the action of most of them is sensitive to temperature during development.Taken together, our results stress the need to take into account the effect of environmental variation and the dynamics of gene interactions on the genetic architecture of this complex life-history trait.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina. jmensch@ege.fcen.uba.ar

ABSTRACT

Background: Understanding the genetic architecture of ecologically relevant adaptive traits requires the contribution of developmental and evolutionary biology. The time to reach the age of reproduction is a complex life history trait commonly known as developmental time. In particular, in holometabolous insects that occupy ephemeral habitats, like fruit flies, the impact of developmental time on fitness is further exaggerated. The present work is one of the first systematic studies of the genetic basis of developmental time, in which we also evaluate the impact of environmental variation on the expression of the trait.

Results: We analyzed 179 co-isogenic single P[GT1]-element insertion lines of Drosophila melanogaster to identify novel genes affecting developmental time in flies reared at 25 degrees C. Sixty percent of the lines showed a heterochronic phenotype, suggesting that a large number of genes affect this trait. Mutant lines for the genes Merlin and Karl showed the most extreme phenotypes exhibiting a developmental time reduction and increase, respectively, of over 2 days and 4 days relative to the control (a co-isogenic P-element insertion free line). In addition, a subset of 42 lines selected at random from the initial set of 179 lines was screened at 17 degrees C. Interestingly, the gene-by-environment interaction accounted for 52% of total phenotypic variance. Plastic reaction norms were found for a large number of developmental time candidate genes.

Conclusion: We identified components of several integrated time-dependent pathways affecting egg-to-adult developmental time in Drosophila. At the same time, we also show that many heterochronic phenotypes may arise from changes in genes involved in several developmental mechanisms that do not explicitly control the timing of specific events. We also demonstrate that many developmental time genes have pleiotropic effects on several adult traits and that the action of most of them is sensitive to temperature during development. Taken together, our results stress the need to take into account the effect of environmental variation and the dynamics of gene interactions on the genetic architecture of this complex life-history trait.

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Reaction norms of 45 P[GT1] insertion lines tested at 17°C and 25°C. Values are shown as the deviation of the insert line mean from contemporaneous control line.
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Figure 2: Reaction norms of 45 P[GT1] insertion lines tested at 17°C and 25°C. Values are shown as the deviation of the insert line mean from contemporaneous control line.

Mentions: Growth and development of ectotherms are determined in part by their thermal environment [22,23]. In particular, temperature during ontogeny exerts a strong influence shaping the evolution of larval traits [24,47,48]. In fact, phenotypic responses result of adaptation to different thermal environments and/or may be an unavoidable consequence of the effect of temperature on the organism's physiology during development [49]. In this context, the pattern of phenotypic effects of P-element insertion lines reared at different developmental temperatures would provide new insights in the study of phenotypic evolution of larval traits. The ANOVA showed that differences among lines and between thermal treatments were significant (Table 3). More importantly, our screen revealed that the line-by-sex and the line-by-temperature interactions were also highly significant, indicating that the behavior of each line depended on the temperature at which it was reared and the sex. However, there was a large difference in the magnitude of these genotype-by-environment interactions. The former accounts for only 1% of the total phenotypic variance (a percentage similar to that obtained in the 25°C assay) while the line-by-temperature interaction explained 52% of the variation. Moreover, note that in the general assay, the percentage of total phenotypic variance explained by differences among lines was 84%, whereas in our assays of phenotypic plasticity this percentage dropped to 30%. It may be argued that part of the effect was obscured by the high value of the line-by-temperature interaction term. This observation opens an excellent opportunity for studying the genetic basis of phenotypic plasticity of developmental time. Thus, we decided to analyze whether the significant line-by-temperature interaction can be explained by changes in magnitude of among-line variance across thermal treatments or changes in the rank order among lines, i.e. a cross-temperature genetic correlation lower than unity. Our results showed that about half of the interaction variance can be explained by a greater among-line variance observed at 17°C than 25°C and the other half by temperature-specific effects on DT of the lines (Figure 2).


Identifying candidate genes affecting developmental time in Drosophila melanogaster: pervasive pleiotropy and gene-by-environment interaction.

Mensch J, Lavagnino N, Carreira VP, Massaldi A, Hasson E, Fanara JJ - BMC Dev. Biol. (2008)

Reaction norms of 45 P[GT1] insertion lines tested at 17°C and 25°C. Values are shown as the deviation of the insert line mean from contemporaneous control line.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2519079&req=5

Figure 2: Reaction norms of 45 P[GT1] insertion lines tested at 17°C and 25°C. Values are shown as the deviation of the insert line mean from contemporaneous control line.
Mentions: Growth and development of ectotherms are determined in part by their thermal environment [22,23]. In particular, temperature during ontogeny exerts a strong influence shaping the evolution of larval traits [24,47,48]. In fact, phenotypic responses result of adaptation to different thermal environments and/or may be an unavoidable consequence of the effect of temperature on the organism's physiology during development [49]. In this context, the pattern of phenotypic effects of P-element insertion lines reared at different developmental temperatures would provide new insights in the study of phenotypic evolution of larval traits. The ANOVA showed that differences among lines and between thermal treatments were significant (Table 3). More importantly, our screen revealed that the line-by-sex and the line-by-temperature interactions were also highly significant, indicating that the behavior of each line depended on the temperature at which it was reared and the sex. However, there was a large difference in the magnitude of these genotype-by-environment interactions. The former accounts for only 1% of the total phenotypic variance (a percentage similar to that obtained in the 25°C assay) while the line-by-temperature interaction explained 52% of the variation. Moreover, note that in the general assay, the percentage of total phenotypic variance explained by differences among lines was 84%, whereas in our assays of phenotypic plasticity this percentage dropped to 30%. It may be argued that part of the effect was obscured by the high value of the line-by-temperature interaction term. This observation opens an excellent opportunity for studying the genetic basis of phenotypic plasticity of developmental time. Thus, we decided to analyze whether the significant line-by-temperature interaction can be explained by changes in magnitude of among-line variance across thermal treatments or changes in the rank order among lines, i.e. a cross-temperature genetic correlation lower than unity. Our results showed that about half of the interaction variance can be explained by a greater among-line variance observed at 17°C than 25°C and the other half by temperature-specific effects on DT of the lines (Figure 2).

Bottom Line: Plastic reaction norms were found for a large number of developmental time candidate genes.We also demonstrate that many developmental time genes have pleiotropic effects on several adult traits and that the action of most of them is sensitive to temperature during development.Taken together, our results stress the need to take into account the effect of environmental variation and the dynamics of gene interactions on the genetic architecture of this complex life-history trait.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina. jmensch@ege.fcen.uba.ar

ABSTRACT

Background: Understanding the genetic architecture of ecologically relevant adaptive traits requires the contribution of developmental and evolutionary biology. The time to reach the age of reproduction is a complex life history trait commonly known as developmental time. In particular, in holometabolous insects that occupy ephemeral habitats, like fruit flies, the impact of developmental time on fitness is further exaggerated. The present work is one of the first systematic studies of the genetic basis of developmental time, in which we also evaluate the impact of environmental variation on the expression of the trait.

Results: We analyzed 179 co-isogenic single P[GT1]-element insertion lines of Drosophila melanogaster to identify novel genes affecting developmental time in flies reared at 25 degrees C. Sixty percent of the lines showed a heterochronic phenotype, suggesting that a large number of genes affect this trait. Mutant lines for the genes Merlin and Karl showed the most extreme phenotypes exhibiting a developmental time reduction and increase, respectively, of over 2 days and 4 days relative to the control (a co-isogenic P-element insertion free line). In addition, a subset of 42 lines selected at random from the initial set of 179 lines was screened at 17 degrees C. Interestingly, the gene-by-environment interaction accounted for 52% of total phenotypic variance. Plastic reaction norms were found for a large number of developmental time candidate genes.

Conclusion: We identified components of several integrated time-dependent pathways affecting egg-to-adult developmental time in Drosophila. At the same time, we also show that many heterochronic phenotypes may arise from changes in genes involved in several developmental mechanisms that do not explicitly control the timing of specific events. We also demonstrate that many developmental time genes have pleiotropic effects on several adult traits and that the action of most of them is sensitive to temperature during development. Taken together, our results stress the need to take into account the effect of environmental variation and the dynamics of gene interactions on the genetic architecture of this complex life-history trait.

Show MeSH