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First published online February 12, 2007
Journal of Experimental Biology 210, 750-764 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02695

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Phosphoglucose isomerase genotype affects running speed and heat shock protein expression after exposure to extreme temperatures in a montane willow beetle

Nathan E. Rank^1,2,*, Douglas A. Bruce^1,2, David M. McMillan^2,3,, Colleen Barclay^1,2 and Elizabeth P. Dahlhoff^2,3

¹ Department of Biology, Sonoma State University, Rohnert Park, CA 94928, USA
² University of California, White Mountain Research Station, Bishop, CA 93514, USA
³ Santa Clara University, Santa Clara, CA 95053, USA

View larger version (9K): [in this window] [in a new window]   Fig. 1. Experimental design used to determine effects of exposure to thermal extremes on beetle running speed and Hsp70 expression. After field-collection and initial running speed measurement, beetles were divided into three temperature-treatment groups, each of which was subdivided into two groups. Beetles in first treatment were held at identical or opposite temperatures in the second treatment. Running speed measurements were made immediately after field collection and after two days of consecutive 4 h temperature treatments. Adult sample sizes are shown. Larvae sample sizes were as follows: collection N=240; first treatment: N=80 for each cell; second treatment: N=40 for each cell. Larval heat-treatment temperature was 35°C. Additional details of collection and treatment regime are described in the text. Actual sample sizes used for each analysis are reported in the figure captions.

View larger version (16K): [in this window] [in a new window]   Fig. 2. (A) Effects of body temperature on field running speed for males (N=86, open triangles) and females (N=84, circles; gravid individuals are indicated by dotted circles). Adult running speed was related to beetle Tb in nature for females (broken line: y=–0.29+0.068x; R2=0.31; F1,82=37.1; P<0.0001) and males (solid line: y=–0.22+0.072x; R2=0.28; F1,84=32.3; P<0.0001). (B) Field running speed of males and females mating or not mating in nature. Data are least square means (±s.e.m.) of running speed of N=42 individuals for all treatments but field-mating males (N=44). The sex difference and mating status effect were significant (see Results).

View larger version (9K): [in this window] [in a new window]   Fig. 3. Field running speed of males after being held in the laboratory in either the presence or absence of two females. Data are least square means (±s.e.m.) of running speed for the three predominant phosphoglucose isomerase (PGI) genotypes, reported as a function of mating treatment (open bars, no female, N=37, 48, 4; striped bars, two females, N=39, 32, 14).

View larger version (10K): [in this window] [in a new window]   Fig. 4. Laboratory running speed of field-collected male and female adults of three predominant PGI genotypes. Data shown are least square means (±s.e.m.) of running speed for PGI 1-1, 1-4 and 4-4 genotypes (female, N=98, 92, 20; male, N=100, 88, 29). Statistical analyses were performed using ANOVA and the results are described in the text. See Table S2 in supplemental material for analysis of other polymorphic enzyme genotypes.

View larger version (12K): [in this window] [in a new window]   Fig. 5. Variation among PGI genotypes in the effects of body mass on running speed for field-collected larvae. Data shown are running speeds for PGI 1-1, 1-4 and 4-4 genotypes (N=74, 87, 24, respectively). Running speed was significantly related to body mass for PGI 1-4 and 4-4 (1-4: y=3.45x+0.17; R2=0.05; F1,85=4.9; P=0.03; 4-4: y=10.03x+0.07; R2=0.33; F1,22=10.7; P=0.003), but not 1-1 genotypes (not significant).

View larger version (16K): [in this window] [in a new window]   Fig. 6. Repeatability of laboratory running speed measures for adults and larvae. Data shown are running speeds measured immediately after field collection and after first temperature treatment for beetles of three predominant PGI genotypes (1-1: diamonds; 1-4: circles; 4-4: triangles). Residuals of one-way ANOVA (effects of treatment temperature on running speed) were used as dependent variables in regression analysis, to factor out direct effects of treatment temperature on laboratory running speed. Regression analyses, y=–0.75+0.54x, R2=0.20, F1,368=88.0; P<0.0001 (adults); y=–0.05+0.23x, R2=0.05, F1,179=8.3, P<0.005 (larvae).

View larger version (31K): [in this window] [in a new window]   Fig. 7. Differences among PGI genotypes in effect of first temperature treatment on running speed in adults and larvae. Data are least square means (±s.e.m.) of running speed for PGI 1-1, 1-4 and 4-4 genotypes (adults: –4°C: N=72, 62, 18; 20°C: N=68, 71, 15; 36°C: N=72, 62, 19. Larvae: 20°C: N=31, 41, 6; –4°C: N=28, 32, 14; 35°C: N=29, 34, 10). Statistical analyses of effects of single treatment temperature were performed using ANOVA (adults) and ANCOVA (larvae) and results are described in the text. Additional analyses of effects of other enzyme genotypes are described in Tables S2, S3 in supplementary material.

View larger version (10K): [in this window] [in a new window]   Fig. 8. Differences in adult and larval running speed measured after first and second temperature treatments. Data are least square means (±s.e.m.) of running speed for the three main PGI genotypes, reported as a function of second temperature treatment [–4°C (open bars), 36 or 35°C (shaded bars)]. Sample sizes are as follows. Adults: –4°C second treatment: N=85, 72, 9; 36°C second treatment: N=73, 79, 23. Larvae: –4°C second treatment: N=39, 52, 14; 35°C second treatment: N=48, 48, 15. Statistical analyses of difference in running speed between two temperature treatments were performed using ANOVA (adults) and ANCOVA (larvae) and results are described in the text and in the supplemental tables (supplementary material Tables S4, S5).

View larger version (28K): [in this window] [in a new window]   Fig. 9. Differences between PGI genotypes in effects of two 4 h temperature treatments on Hsp70 expression in adult beetles. Treatment temperatures, in order, are shown in each panel. Data are least square means (±s.e.m.) of Hsp70 expression (ng of Hsp70 per g of thoracic muscle), measured by western blot analysis of PGI 1-1, 1-4 and 4-4 genotypes [left panels (–4°C second treatment): 20°C: N=15, 10, 2; –4°C: N=17, 9, 2; 36°C: N=15, 10, 2. Right panels (36°C second treatment): 20°C: N=10, 18, 3; –4°C: N=15, 9, 2; 36°C: N=15, 11, 1]. Statistical analysis was performed on Hsp70 data using ANOVA (Table 1).

View larger version (8K): [in this window] [in a new window]   Fig. 10. Differences in larval Hsp70 expression after two 4 h laboratory temperature treatments. Data are least square means (±s.e.m.) of Hsp70 expression for the three main PGI genotypes, reported as a function of second temperature treatment (–4°C second treatment: N=21, 26, 6; 35°C second treatment: N=28, 24, 5). Statistical analysis was performed on Hsp70 data using ANOVA (Table 1).