Chromosomal Analysis of Heat-Shock Tolerance in Drosophila melanogaster Evolving at Different Temperatures in the Laboratory

Cavicchi, Sandro; Guerra, Daniela; Torre, Vittoria La; Huey, Raymond B.

doi:10.2307/2410321

Cited by 68 publications

(100 citation statements)

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“…Inbreeding effects on CT max tend to be minor across Drosophila species (40), whereas the impact of laboratory adaptation is less certain (41,42). Nevertheless, in our opinion these confounding effects will be minor relative to heat resistance variation found between species.…”

Section: Discussionmentioning

confidence: 68%

Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically

Kellermann

Overgaard

Hoffmann

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

478

560

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Upper thermal limits vary less than lower limits among related species of terrestrial ectotherms. This pattern may reflect weak or uniform selection on upper limits, or alternatively tight evolutionary constraints. We investigated this issue in 94 Drosophila species from diverse climates and reared in a common environment to control for plastic effects that may confound species comparisons. We found substantial variation in upper thermal limits among species, negatively correlated with annual precipitation at the central point of their distribution and also with the interaction between precipitation and maximum temperature, showing that heat resistance is an important determinant of Drosophila species distributions. Species from hot and relatively dry regions had higher resistance, whereas resistance was uncorrelated with temperature in wetter regions. Using a suite of analyses we showed that phylogenetic signal in heat resistance reflects phylogenetic inertia rather than common selection pressures. Current species distributions are therefore more likely to reflect environmental sorting of lineages rather than local adaptation. Similar to previous studies, thermal safety margins were small at low latitudes, with safety margins smallest for species occupying both humid and dry tropical environments. Thus, species from a range of environments are likely to be at risk owing to climate change. Together these findings suggest that this group of insects is unlikely to buffer global change effects through marked evolutionary changes, highlighting the importance of facilitating range shifts for maintaining biodiversity.niche conservatism | stress resistance | thermal adaptation | evolutionary history | space T emperatures are expected to rise across the globe over the coming decades and centuries (1), and many studies suggest the potential for range shifts/reductions in many species (2). When assessing the likely impact of temperature changes on species survival, an implicit assumption is that the thermal environment shapes resistance to temperature extremes and thus dictates species range limits. Nevertheless, few studies have directly tested for such links between physiological upper thermal limits of ectothermic species and temperature conditions within their geographic range (3, 4). A related, little-investigated key point for predicting species range responses to climate change is whether upper thermal limits are modifiable through plastic and/or evolutionary responses (5, 6). Ideally, evolutionary and plastic responses within and across generations, including short-term hardening and acclimation, should be separated, as through a common garden approach whereby species are kept under controlled laboratory conditions (7,8). Without controlling for plastic responses, it is not possible to distinguish adaptive evolutionary responses, and species may erroneously seem close to their upper thermal thresholds (9-12), biasing extinction risk estimates.Furthermore, by examining the evolution of upper thermal limits (heat re...

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Section: Discussionmentioning

confidence: 68%

Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically

Kellermann

Overgaard

Hoffmann

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

478

560

View full text Add to dashboard Cite

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“…Third, female Drosophila spp. do not always have higher heat resistance (Quintana and Prevosti 1990a,b;Loescheke and Krebs 1994;Cavicchi et al 1995). Fourth, selection for increased knock-down temperature has not altered body size (Huey and Gilchrist, unpubl.…”

Section: Discussionmentioning

confidence: 99%

WITHIN‐ AND BETWEEN‐GENERATION EFFECTS OF TEMPERATURE ON THE MORPHOLOGY AND PHYSIOLOGY OF DROSOPHILA MELANOGASTER

1996

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Abstract,-We investigated the effects of developmental and parental temperatures on several physiological and morphological traits of adult Drosophila melanogaster. Flies for the parental generation were raised at either low or moderate temperature (18°C or 25°C) and then mated in the four possible sex-by-parental temperature crosses. Their offspring were raised at either 18°C or 25°C and then scored as adults for morphological (dry body mass, wing size, and abdominal melanization [females only]), physiological (knock-down temperature, and thermal dependence of walking speed), and life history (egg size) traits. The experiment was replicated, and the factorial design allows us to determine whether and how paternal, maternal, and developmental temperatures (as well as offspring sex) influence the various traits. Sex and developmental temperature had major effects on all traits. Females had larger bodies and wings, higher knock-down temperatures, and slower speeds (but similar shaped performance curves) than males, Development at 2YC (versus at 18°C) increased knock-down temperature, increased maximal speed and thermal performance breadth, decreased the optimal temperature for walking, decreased body mass and wing size, reduced abdominal melanization, and reduced egg size. Parental temperatures influenced a few traits, but the effects were generally small relative to those of sex or developmental temperature. Flies whose mother had been raised at 25°C (versus at 18°C) had slightly higher knock-down temperature and smaller body mass. Flies whose father had been raised at 25°C had relatively longer wings. The effects of paternal, maternal, and developmental temperatures sometimes differed in direction. The existence of significant within-and between-generation effects suggests that comparative studies need to standardize thermal environments for at least two generations, that attempts to estimate "field" heritabilities may be unreliable for some traits, and that predictions of short-term evolutionary responses to selection will be difficult. The magnitude and nature of nongenetic effects on an organism's phenotype (phenotypic plasticity, norms of reaction, acclimation) have recently received considerable attention. Such nongenetic effects are relevant not only to functional biologists studying how organisms work (Somero 1995), but also to evolutionary biologists studying the dynamics of phenotypic evolution (Kirkpatrick and Lande 1989;Stearns 1989). The magnitude of phenotypic plasticity is genetically variable and can respond to selection (Gebhardt and Stearns 1988; Scheiner and Lyman 1991). However, marked phenotypic plasticity complicates attempts to predict responses to selection (Via and Lande 1985;Kirkpatrick and Lande 1989).Most studies of phenotypic plasticity have focused on the phenotypic effects of environmental factors within an individual's lifetime. For example, many studies report on the consequences of developmental regimes (temperature, food regime, or crowding) on adult size, life span, physiologic...

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“…Clones and siblings of five organismal groups, including Coelenterata, Arthropoda, Echinodermata and Amphibia, which showed greater heat tolerance initially, acquired less of an increase in tolerance after acclimation to higher temperatures (Ushakov et al, 1977); strains and populations of Drosophila that were found or raised in warmer thermal habitats or temperatures during laboratory selection showed not only higher heat tolerance but also a limited short-term capacity to increase tolerance to greater heat stress, e.g. heat-hardening (Cavicchi et al, 1995;Hoffmann et al, 2003;Zatsepina et al, 2001); and more heat-tolerant porcelain crabs of the genus Petrolisthes show a lower capacity to acclimate the upper thermal limits of cardiac function (Stillman, 2003). To date, no other cellular mechanism has been proposed to explain this relationship.…”

Section: Phenotypic Plasticity and Heat Tolerancementioning

confidence: 99%

“…This suggests that species with the highest heat tolerance may have a relatively lower capacity to further adjust the stress response to warmer acclimation temperatures. If so, this limit to acclimation capacity of Hsp expression could explain the limited ability of more heat-tolerant organisms to increase tolerance to even greater heat stress (Cavicchi et al, 1995;Hoffmann et al, 2003;Stillman, 2003;Ushakov et al, 1977;Zatsepina et al, 2001).…”

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confidence: 99%

Two-dimensional gel analysis of the heat-shock response in marine snails(genusTegula): interspecific variation in protein expression and acclimation ability

Tomanek

2005

Journal of Experimental Biology

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SUMMARY The degree to which temperature acclimation modifies the acute synthesis of the entire heat-shock protein (Hsp) complement is still unknown, but it may constitute an important mechanism for understanding the differences in acclimation ability among closely related ectothermic species that occupy widely varying thermal environments. In general, eurythermal (heat-tolerant)species modify physiological function in response to an increase in acclimation temperature to a greater extent than stenothermal (heat-sensitive)species. In the present work I used 35S-labelled amino acids and two-dimensional gel electrophoresis to test this assumption for how acclimation affects acute Hsp expression (referred to as phenotypic plasticity) in two heat-sensitive, low-intertidal to subtidal zone turban snails, Tegula brunnea and T. montereyi, in comparison to a heat-tolerant, mid- to low-intertidal zone congener, T. funebralis. I was able (i) to detect the synthesis of over 30 proteins in gill tissue,primarily in the 70 kDa range, in response to an increase in temperature(13°C, 24°C, 27°C and 30°C), (ii) to assess the effect of acclimation (13°C vs 22°C) on acute Hsp synthesis, and (iii)to compare this effect among the three Tegula congeners. After increasing acclimation temperature from 13°C to 22°C, synthesis of the most highly expressed Hsps decreased more in T. brunnea and T. montereyi than in T. funebralis. Two highly expressed proteins of molecular mass 71 and 74 kDa, however, were also synthesized constitutively at 13°C and changed with increasing acclimation temperature in all three species. Although similar in phenotypic plasticity, T. brunnea and T. montereyi synthesized either a 76 or a 72 kDa cluster of proteins,respectively, and differed in how acclimation affected the acute synthesis of several 77 kDa proteins. Thus, in Tegula, the effect of acclimation on Hsp expression is (i) Hsp-specific, (ii) dependent on a protein's expression pattern (constitutive and inducible vs only inducible),(iii) and is actually limited in the more eurythermal mid- to low-intertidal congener. These results contradict the general assumption that greater heat tolerance correlates with an increased ability to modify physiological function in response to acclimation.

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Chromosomal Analysis of Heat-Shock Tolerance in Drosophila melanogaster Evolving at Different Temperatures in the Laboratory

Cited by 68 publications

References 0 publications

Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically

Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically

WITHIN‐ AND BETWEEN‐GENERATION EFFECTS OF TEMPERATURE ON THE MORPHOLOGY AND PHYSIOLOGY OF DROSOPHILA MELANOGASTER

Two-dimensional gel analysis of the heat-shock response in marine snails(genusTegula): interspecific variation in protein expression and acclimation ability

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