Does thermoregulatory behavior maximize reproductive fitness of natural isolates of Caenorhabditis elegans?
- Jennifer L Anderson†1,
- Lori Albergotti†1, 4,
- Barbara Ellebracht2,
- Raymond B Huey3 and
- Patrick C Phillips1Email author
© Anderson et al; licensee BioMed Central Ltd. 2011
Received: 21 April 2011
Accepted: 6 June 2011
Published: 6 June 2011
A central premise of physiological ecology is that an animal's preferred body temperature should correspond closely with the temperature maximizing performance and Darwinian fitness. Testing this co-adaptational hypothesis has been problematic for several reasons. First, reproductive fitness is the appropriate measure, but is difficult to measure in most animals. Second, no single fitness measure applies to all demographic situations, complicating interpretations. Here we test the co-adaptation hypothesis by studying an organism (Caenorhabditis elegans) in which both fitness and thermal preference can be reliably measured.
We find that natural isolates of C. elegans display a range of mean thermal preferences and also vary in their thermal sensitivities for fitness. Hot-seeking isolates CB4854 and CB4857 prefer temperatures that favor population growth rate (r), whereas the cold-seeking isolate CB4856 prefers temperatures that favor Lifetime Reproductive Success (LRS).
Correlations between fitness and thermal preference in natural isolates of C. elegans are driven primarily by isolate-specific differences in thermal preference. If these differences are the result of natural selection, then this suggests that the appropriate measure of fitness for use in evolutionary ecology studies might differ even within species, depending on the unique ecological and evolutionary history of each population.
How organisms respond to environmental variation and change, both in the short term via mechanisms such as behavior modulation and in the long term via evolutionary changes in features such as the pattern of reproductive allocation, remains a central question in ecology and evolutionary biology. Temperature variation in particular has profound effects on the physiology, ecology, and fitness of ectotherms [1–5]. Extreme temperatures are injurious and potentially lethal, but even temperatures within lethal limits dramatically change performance and ultimately Darwinian fitness [3, 6, 7]. Even so, most ectotherms are not at the mercy of the thermal environment but rely on behavioral adjustments (, but see ) to regulate body temperatures at usually narrow, species-specific levels. These behaviors are thought to be adaptive in two complementary ways. (i) They help animals avoid extreme temperatures that can be damaging or lethal [10, 11]. (ii) They increase the time spent at physiologically optimal temperatures, thus enhancing overall physiological performance and survival in nature [10, 12–17]. For these reasons, thermal preferences are widely assumed to maximize Darwinian fitness .
According to the co-adaptational hypothesis, population mean fitness would be maximized if all individuals in a population thermoregulate perfectly: if so, individuals will prefer and experience only the narrow range of temperatures that results in the highest fitness (but see ). However, organisms - either in laboratory thermal gradients or in nature - at least temporarily occupy a range of temperatures. From the coadaptation hypothesis, it naturally follows that such imperfect thermoregulation will impose a fitness cost or decrement. Regardless of whether distribution of individuals on a thermal gradient is due to underlying variation in preferred temperature or the transient occupation of different temperatures within a range of preferred or non-lethal temperatures, deviations from the optimal fitness temperature should lower population mean fitness, generating a "performance load" on the population (sensu [28, 29]). Thus a corollary to the thermal coadaptation hypothesis is that natural selection should act to decrease the performance load of a population under environmental conditions in which variation in performance has its largest effect on overall fitness.
A complication in testing the relationship between thermal preference and Darwinian fitness is that the appropriate measure of fitness differs depending on the specific demographic context of the population involved. Fitness is commonly estimated either as reproductive output, Ro [or its individual level equivalent Lifetime Reproductive Success (LRS), the total number of offspring produced during a female's lifetime] or as the intrinsic rate of population increase (r), which is influenced both by offspring number and reproductive timing. Because r is strongly and inversely related to generation time , which decreases with temperature in ectotherms, temperatures that maximize r are generally higher than those that maximize rate-insensitive fitness metrics Ro and LRS (Figure 1B) . Thus, thermal preference behaviors can maximize Ro (or LRS) or r, but not both simultaneously (Figure 1B). The question then becomes which measure of fitness should correspond with thermal preference? Evolutionary ecologists [31–35] have suggested that the relevant fitness measure can be identified using basic demographic information (e.g. knowing whether the population is stable or expanding, or has discrete or overlapping generations). However, these factors are frequently unknown for natural populations, making a priori identification of the appropriate fitness metric impossible.
Here we study thermal coadaptation in Caenorhabditis elegans. These nematodes are very small (~1 mm as adults) and are easily maintained in the laboratory . Consequently, the distribution and T p of large numbers of individuals can be determined on controlled thermal gradients. Moreover, fitness (e.g. [37–41]) - and specifically the thermal dependence of fitness [42–44] - can also be repeatedly and reliably estimated in C. elegans. Although the demographic status of these worms is unknown, both LRS and r are readily estimable in this system: thus we can examine the relationship between thermal preference and both fitness metrics. Accordingly, we determined the T p and the thermal dependence of both fitness measures for eight natural isolates of C. elegans and then explored whether T p corresponds with temperatures that maximize fitness.
Thermal preference and fitness assays
Geographic origin of C.elegans natural isolates used in this study.
Altadena, CA, USA
Palo Alto, CA, USA
Claremont, CA, USA
Fibeiro Frio, Madeira
Le Blanc, France
Thermal preference was assayed as previously described . Briefly, age-synchronized populations of final larval stage worms (L4), reared at 20°C, were applied to thermal gels [NGM-lite in plastic frames (10.2 × 17.5 × 0.5 cm) seeded with E. coli strain OP50] on stable linear thermal gradients (10.5°C - 29°C) at a starting point corresponding to 24°C. The positions of individual worms were scored after one hour. The temperature chosen by each individual was then estimated from its position on the thermal gradient using a linear model that relates gradient position to temperature. Results were analyzed using analysis of variance (ANOVA) with isolate as the main effect and replicate as a random nested effect. Standard errors were calculated from the model, with replicate as the unit of sampling variation, using a least-square means approach. Differences in thermal preferences among isolates were evaluated using Tukey's HSD, α = 0.05. All analyses were performed in JMP 4.0 (SAS Institute, Cary, NC, USA).
Fitness (LRS and r) was assayed at seven temperatures (10°C, 12°C, 14°C, 15°C, 20°C, 23°C, and 25°C) in four isolates (CB4854, CB4856, CB4857, PX174) with extreme thermal preferences. Subpopulations of each isolate were allowed to acclimate to the assay temperature for at least two generations prior to use in fitness assays. Individual L4 hermaphrodites, reared from eggs laid by 30 adults within a 3-h period, were transferred to individual Petri dishes (35 × 15 mm) containing NGM-lite seeded with OP50 and incubated at the assay temperature. Reproductively active individuals were subsequently transferred to new dishes at 24-hour intervals. At the highest temperatures worms were transferred more frequently to prevent offspring overcrowding. Offspring produced during each 24-h period were counted at maturity. LRS was calculated as total lifetime fecundity at each temperature and r was calculated from, ∑e -rx l x m x = 1 where l x is age specific survivorship to day x, and m x is the fecundity at day x . Results were analyzed using a full factorial ANOVA with isolate and temperature as main effects (data from 25°C were excluded from this analysis because PX174 did not reproduce at this temperature). The isolate-specific effects of temperature on fitness were analyzed using ANOVA with isolate as the main effect at each temperature. Differences among isolates were evaluated using LSMeans Contrasts and Tukey's HSD.
Correspondence between thermal preference and fitness
To determine the correspondence between preference and the two fitness metrics, each isolate's preference for a given temperature, as indicated by the fraction of worms positioned at that temperature (10°C, 12°C, 14°C, 15°C, 20°C, 23°C, and 25°C; ± 0.5) on the thermal gradient was correlated with the fitness estimate associated with each of the seven assayed temperatures. If thermoregulation is effective, then the fraction of worms found at a given temperature will correlate positively and strongly with the fitness at that temperature. This approach takes advantage of information from the shape of each isolate's thermal preference distribution and fitness performance curve (i.e. the convolution of the distributions). Note that this is a within-isolate preference-performance measure, as opposed to a between-isolate measure, such as the correlation between Tp and T max among isolates.
Consequences of thermal preference on average fitness
To determine the average expected fitness (w exp ) of worms in a thermal gradient for each isolate, we estimated fitness at temperatures from 9°C - 29°C via linear interpolation of measured values and integrated these data over the isolate-specific thermal preference frequency distribution. The integral was approximated by summing the product of the temperature-specific fitness measures and the proportion of total individuals displaying a preference to that temperature. To quantify the deficit in fitness between the maximum fitness possible (w max , if individuals thermoregulate perfectly) and the expected average fitness (based on the actual distribution of Tp), we calculated the Performance Load as PL = (w max - w exp )/w max . PL measures the proportional reduction in fitness of the average individual in a isolate given the thermal preference distribution of that isolate relative to the maximum observed fitness. PL ranges from 0 to 1 where 0 means that all individuals achieve equal, thus maximum, fitness and 1 means that all but one individual has zero fitness.
Thermal preferences in C. elegansnatural isolates
Temperature dependent fitness
The thermal sensitivities of LRS and r vary by isolate (effect of isolate: LRS F 3, 341 = 6.63, p = 0.0002; r F 3, 341 = 27.23, p < 0.0001; isolate x temperature interaction: LRS F 15, 341 = 4.97, p < 0.0001; r F 15, 341 = 18.36, p < 0.0001; see also Additional file 2: Fig. S2 and Additional file 3: Fig. S3) but nonetheless show some similarities among isolates. Generally, r increases with temperature up to about 23°C before declining steeply for all isolates (Figure 3). LRS increases sharply from 10°C to 12°C, remains relatively high between 12°C and 20°C (except in CB4857), but then declines rapidly at higher temperatures (Figure 3). CB4857 is unique in that it produces fewer offspring at 14°C and 15°C than all other isolates (LSMeans Contrast: 14°C F 1, 62 = 19.00, p < 0.001; 15°C F 1, 45 = 13.53, p < 0.001). Overall, C. elegans natural isolates are able to maximize LRS, but not r, over a broad range of temperatures (Figure 3). In other words, r is more thermally sensitive than is LRS.
Performance cost of imperfect thermoregulation
Average expected fitness for each isolate calculated by integrating temperature-dependent fitness measures over the observed thermal preference distributions ("Obs.") compared to the maximum fitness expected is all individuals chose the single best temperature ("Max.")
Many ectotherms use behavioral adjustments (e.g. in habitat choice, posture, and timing of activity) to regulate body temperatures within preferred ranges [8, 12, 49–52] thereby avoiding damaging and lethal temperatures as well as maximizing time spent at or near physiologically optimal temperatures. The classical co-adaptational hypothesis [12, 18, 21] predicts that thermal preferences should be centered at or near temperatures that maximize fitness (but see ). Moreover, evolutionary shifts in thermal preferences should drive compensatory shifts in the thermal sensitivity of fitness and vice versa [18, 21]. In this study, we assayed thermal preference and Darwinian fitness in natural isolates of C. elegans to test this coadaptational hypothesis.
Does thermoregulatory behavior maximize fitness in the isolates of C. elegans studied here? We find that preferred temperatures do correspond with temperatures maximizing fitness, but that the relationship between thermal preference and different aspects of fitness varies among natural isolates of C. elegans (Figures 3, 4). Intraspecific variation in thermal preference-fitness relationships is not predicted by the classical preference-fitness coadaptation hypothesis. Whereas the coadaptation hypothesis predicts that differences in T p among populations should be accompanied by corresponding shifts in T max (Figure 1A), in our data, fitness curves are not systematically shifted such that T p consistently corresponds with Tmax of either r or LRS. Rather, the isolate with the coolest T p favors LRS, while the two isolates preferring a warmer T p (CB4854 and CB4857) favor r. Under these circumstances it is not surprising that isolates with high Tp maximize r rather than LRS and vice versa due to the negative relationship between generation time and temperature (Figure 1B) [3, 7]. We find that correlations between fitness and thermal preference are driven primarily by isolate-specific differences in thermal preference, but the effects of temperature on fitness also vary among isolates. This is most clearly seen in temperature-dependent reproductive rates among isolates, in which cold-seeking CB4856 strongly outperforms hot-seeking CB4857 at cold temperatures and vice versa (Figure 5). Some of the differentiation among isolates may be facilitated by the largely self-fertilizing mode of reproduction in C. elegans, which tends to increase linkage disequilibrium across the genome [53, 54]. There are obviously too few isolates here to definitely define new temperature-fitness rules within this species, but these data strongly suggest that preference-fitness relationships are more complicated than predicted by the classical coadaptation hypothesis.
The optimization of different aspects of fitness under different ecological and/or demographic conditions is predicted by life history theory [32, 33, 35]. Specifically, total offspring production, R o or LRS, should be optimized in stable populations where population size is regulated by density-dependent factors, whereas the intrinsic rate of increase, r, should be optimized in density-independent populations where natural selection should favor early reproduction [32, 33, 35, 55]. Therefore, if the coadaptation hypothesis is indeed correct, different components of fitness (e.g. total reproduction versus rate of reproduction) might have been under selection in different isolates of C. elegans. The specific structure of these predictions is likely to benefit from more detailed models of the relationship between metabolism and population dynamics (e.g. ).
It is almost certainly true, however, that the evolution of thermal preference-fitness relationships is also influenced by interacting genetic, genomic, physiological, ecological, and environmental factors. For example, important life history traits and genetic correlations between these traits (e.g. age at maturity, egg number, and egg size, and the genetic control of phenotypic plasticity) are temperature-dependent in C. elegans [43, 56–58]. Moreover, soil nematodes live in highly dynamic thermal environments [59–61]; and nematode community structure is both complex  and strongly influenced by temperature [62–65]. Additionally, the impact of temperature on performance may differ depending on physiological context and resource availability . In any case, the fact that Performance Loads are fairly high in all C. elegans isolates (Table 2) suggests that T p is not strongly optimized in this species, and possibly reflects the effects of complex ecological, environmental, and genetic interactions on the evolution of thermal preference-fitness relationships. Thus, while we are able to robustly measure the effect of temperature of various components of fitness in the laboratory environment, true fitness in nature awaits measurement in the field.
Although the effects of temperature on fitness vary among isolates of C. elegans (Figures 3, S2, S3) (see also [44, 67]), this species can generally be described as a "Jack of all temperatures"  in terms of LRS. The isolates studied here produce large numbers of offspring (≥ 75% of maximal production) over up to 64% (CB4854) of their reproductive temperature range (9°C to 26°C, herein). Caenorhabditis briggsae, an androdioecious sister species to C. elegans, has similarly high offspring production (≥ 75% of maximal production) over 63% of its reproductive temperature range . However, C. briggsae reproduces at a warmer range of temperatures than C. elegans (14°C to 30°C; ).
The thermal sensitivity of reproductive output in C. briggsae appears to vary with latitude; isolates of tropical origin produce more offspring at high temperatures than do isolates from temperate regions . This pattern is not evident in C. elegans; the lowest latitude isolate we studied (CB4856) does not produce more offspring at high temperatures than do other isolates. There is some evidence, however, that thermal preference varies with latitude in C. elegans (r 2 = 0.60, p = 0.11); this suggestive result is entirely driven by CB4856. To date, too few isolates of C. elegans and of C. briggsae from geographically diverse, well-characterized collections (i.e. known microclimate and elevation) have been characterized for both thermal preference and temperature dependent fitness to define relationships among thermal preference, fitness, and latitude, or other ecologically relevant clines.
Thermal preference behavior has been studied in C. elegans for more than 30 years  and has led to advances in the fields of genetics [71–76], neuroscience [77–80], and the study of memory and learning [74, 78, 81]. Even so, findings from many of these studies are somewhat problematic because seemingly conflicting results have been obtained by different laboratories, apparently driven in part by sensitivity to environmental conditions such as nutritional state and cultivation temperature (e.g. [45, 74, 82]). Thermal gradient steepness can also influence thermal preference behavior in some isolates . The standard laboratory strain N2 only displays typical thermal preference behaviors on gradients < 1°C/cm, whereas natural isolates of C. elegans, such as those assayed here, are less sensitive to gradient steepness . Here, we assayed thermal preference in eight isolates of C. elegans, under identical experimental conditions. Thus, our data clearly illustrate that thermal preference behavior varies significantly among natural isolates in C. elegans (see also [45, 83]). Environment-dependent and isolate-specific variation in thermal preference behavior might be informative from an evolutionary perspective because a behavior with such important effects on fitness might be fine tuned to be sensitive to a number of possible environmental cues. In fact, it would be surprising if we did not find variation in this important behavior given the large potential fitness effects of thermal preference behavior and the fact that C. elegans populations are found around the world in different climates. Using genetic differentiation among natural isolates as means of probing this system  should help to distinguish evolutionary signal from noise [45, 83]. However, our results show that interpretation of natural variation, and probably any variation in this trait, must be performed in the context of the ecological causes and consequences of that variation.
Most studies of the coadaptation of thermal preference and fitness have examined only performance traits and not Darwinian fitness per se. Here we show that thermal preferences can indeed correspond with temperatures maximizing Darwinian fitness in C. elegans, but not as predicted by the coadaptation hypothesis. We find that the relationship between thermal preference and fitness varies among isolates such that isolates that prefer relatively warm temperatures, CB4854 and CB4857, maximize the timing of offspring production (r) and the isolate that prefers a cooler temperature, CB4856, maximizes offspring number (LRS). Thus, we demonstrate that preference-fitness relationships can be more complex that predicted by current theory. Our results also demonstrate that the choice of fitness measure can have a large effect on the interpretation of the coadaptedness of thermal preference and fitness: had we measured only r, for instance, we would have concluded that thermal preferences were not correlated with fitness. Finally, despite the tight correlations between thermal preference and specific measures of fitness, the isolates examined here still demonstrate substantial performance loads caused by imprecision of individual preference behavior. Coupling this individual variation with other known external environmental drivers such as rearing temperature (e.g. [70, 83]) and potential unknown temperature correlates such as predation risk and inter-specific competition suggests that co-adaptation of Tp and thermal sensitivity of fitness is likely to depend on overall interactions involving ecology, environmental experience, behavior and fitness.
We thank Christina Cooke for lab assistance and Van Savage and three anonymous reviewers for helpful input on the manuscript. This work was supported by the National Science Foundation (IBN-0416205 to PCP and IOB-011684 to RBH) and National Institutes of Health (5F32HD055057 to JLA), and by materials support from the Reliance Steel and Aluminum Co.
- Fry FEJ: Effects of the environment on animal activity. Univ Toronto Stud, Biol Ser no 55. 1947, 68: 1-62.
- Bennett AF: The thermal dependence of lizard behaviour. Anim Behav. 1980, 28: 752-762. 10.1016/S0003-3472(80)80135-7.View Article
- Huey RB, Berrigan D: Temperature, demography, and ectotherm fitness. Am Nat. 2001, 158: 204-210. 10.1086/321314.View ArticlePubMed
- Angilletta MJ: Thermal Adaptation: A Theoretical and Empirical Synthesis. 2009, Oxford: Oxford University PressView Article
- Dell AI, Pawar S, Savage VM: Systematic variation in the temperature dependence of physiological and ecological traits. Proc Natl Acad Sci USA. 2011
- Martin TL, Huey RB: Why "suboptimal" is optimal: Jensen's inequality and ectotherm thermal preferences. Am Nat. 2008, 171: E102-E118. 10.1086/527502.View ArticlePubMed
- Savage VM, Gillooly JF, Brown JH, West GB, Charnov EL: Effects of body size and temperature on population growth. Am Nat. 2004, 163: 429-441. 10.1086/381872.View ArticlePubMed
- Stevenson RD: The relative importance of behavioral and physiological adjustments controlling body-temperature in terrestrial ectotherms. Am Nat. 1985, 126: 362-386. 10.1086/284423.View Article
- Heinrich B: The Hot-blooded Insects: Strategies and Mechanisms of Thermoregulation. 1993, Cambridge, MA: Harvard University PressView Article
- Kingsolver JG, Watt WB: Thermoregulatory strategies in Colias butterflies: Thermal stress and the limits to adaptation in temporally varying environments. Am Nat. 1983, 121: 32-55. 10.1086/284038.View Article
- Grant BW, Dunham AW: Thermally imposed time constraints on the activity of desert lizard Sceloporus merriami. Ecology. 1988, 69: 167-176. 10.2307/1943171.View Article
- Cowles RB, Bogert CM: A preliminary study of the thermal requirements of desert reptiles. Bull Am Mus Nat Hist. 1944, 83: 261-296.
- Christian KA, Tracy CR: The effect of the thermal environment on the ability of hatchling Galapagos land iguanas to avoid predation during dispersal. Oecologia. 1981, 49: 218-223. 10.1007/BF00349191.View Article
- Huey RB: Natural variation in body temperature and physiological performance in a lizard. Advances in Herpetology and Evolutionary Biology: Essays in Honor of Ernest E. Williams. Edited by: Rhodin AGJ, Miyata K. 1983, Cambridge, MA: Museum of Comparative Zoology, 484-490.
- Waldschmidt S, Tracy CR: Interactions between a lizard and its thermal environment: Implications for sprint performance and space utilization in the lizard Uta stansburiana. Ecology. 1983, 64: 476-484. 10.2307/1939967.View Article
- Hertz PE, Huey RB, Stevenson RD: Evaluating temperature regulation by field-active ectotherms: The fallacy of the inappropriate question. Am Nat. 1993, 142: 796-818. 10.1086/285573.View ArticlePubMed
- Huey RB, Hertz PE, Sinervo B: Behavioral drive versus behavioral inertia in evolution: A null model approach. Am Nat. 2003, 161: 357-366. 10.1086/346135.View ArticlePubMed
- Huey RB, Bennett AF: Phylogenetic studies of coadaptation: Preferred temperatures versus optimal performance temperatures of lizards. Evolution. 1987, 41: 1098-1115. 10.2307/2409194.View Article
- Beitinger TL, Fitzpatrick LC: Physiological and ecological correlates of preferred temperature in fish. Am Zool. 1979, 19: 319-329.View Article
- Bennett AF: Evolution of the control of body temperature: Is warmer better?. Comparative Physiology: Life in Water and on Land. Edited by: Dejours P, Taylor CR, Weibel ER. 1987, Padova: Liviana Press, 421-431.
- Angilletta MJ, Bennett AF, Guderley H, Navas CA, Seebacher F, Wilson RS: Coadaptation: A unifying principle in evolutionary thermal biology. Physiol Biochem Zool. 2006, 79: 282-294. 10.1086/499990.View ArticlePubMed
- Licht PE, Dawson WR, Shoemaker VH, Main AR: Observations on the thermal relations of Western Australian lizards. Copeia. 1966, 97-110.
- Dawson WR: On the physiological significance of the preferred body temperatures of reptiles. Perspectives of Biophysical Ecology. Edited by: Gates DM, Schmerl R. 1975, New York: Springer-Verlag, 443-473.View Article
- Angilletta MJ, Hill T, Robson MA: Is physiological performance optimized by thermoregulatory behavior?: A case study of the eastern fence lizard, Sceloporus undulatus. J Therm Biol. 2002, 27: 199-204. 10.1016/S0306-4565(01)00084-5.View Article
- Bartholomew GA: Interaction of physiology and behavior under natural conditions. The Galápagos. Edited by: Bowman RI. 1966, Berkeley: University of California Press, 39-45.
- Huey RB, Stevenson RD: Integrating thermal physiology and ecology of ectotherms: A discussion of approaches. Am Zool. 1979, 19: 357-366.View Article
- Arnold SJ: Morphology, performance and fitness. Am Zool. 1983, 23: 347-361.View Article
- Haldane JBS: The effect of variation of fitness. Am Nat. 1937, 71: 337-349. 10.1086/280722.View Article
- Crow JF: Genetic loads and the cost of natural selection. Mathematical Topics in Population Genetics. Edited by: Kojima K. 1970, Berlin: Springer-Verlag, 128-177.View Article
- Cole LC: The population consequences of life history phenomena. Q Rev Biol. 1954, 29: 103-137. 10.1086/400074.View ArticlePubMed
- Travis J, Henrich S: Some problems in estimating the intensity of selection through fertility differences in natural and experimental populations. Evolution. 1986, 40: 786-790. 10.2307/2408463.View Article
- Roff DA: The Evolution of Life Histories: Theory and Analysis. 1992, New York: Chapman & Hall
- Stearns SC: The Evolution of Life Histories. 1992, Oxford: Oxford University Press
- Kozlowski J: Measuring fitness in life-history studies. Trends Ecol Evol. 1993, 8: 84-85. 10.1016/0169-5347(93)90056-U.View ArticlePubMed
- Charlesworth B: Evolution in Age-structured Populations. 1994, Cambridge: Cambridge University Press, 2View Article
- Stiernagle T: Maintenance of C. elegans. C. elegans: A practical approach. Edited by: Hope I. 1999, Oxford: Oxford University Press, 51-67.
- Hodgkin J, Barnes TM: More is not better: Brood size and population growth in a self-fertilizing nematode. Proc R Soc Lond B Biol Sci. 1991, 246: 19-24. 10.1098/rspb.1991.0119.View Article
- Keightley PD, Caballero A: Genomic mutation rates for lifetime reproductive output and lifespan in Caenorhabditis elegans. Proc Natl Acad Sci USA. 1997, 94: 3823-3827. 10.1073/pnas.94.8.3823.View ArticlePubMedPubMed Central
- Vassilieva LL, Lynch M: The rate of spontaneous mutation for life-history traits in Caenorhabditis elegans. Genetics. 1999, 151: 119-129.PubMedPubMed Central
- Estes S, Ajie BC, Lynch M, Phillips PC: Spontaneous mutational correlations for life-history, morphological and behavioral characters in Caenorhabditis elegans. Genetics. 2005, 170: 645-653. 10.1534/genetics.104.040022.View ArticlePubMedPubMed Central
- Baer CF, Phillips N, Ostrow D, Avalos A, Blanton D, Boggs A, Keller T, Levy L, Mezerhane E: Cumulative effects of spontaneous mutations for fitness in Caenorhabditis: Role of genotype, environment and stress. Genetics. 2006, 174: 1387-1395. 10.1534/genetics.106.061200.View ArticlePubMedPubMed Central
- Byerly L, Cassada RC, Russell RL: The life cycle of the nematode Caenorhabditis elegans: I. Wild-type growth and reproduction. Dev Biol. 1976, 51: 23-33. 10.1016/0012-1606(76)90119-6.View ArticlePubMed
- Gutteling EW, Riksen JAG, Bakker J, Kammenga JE: Mapping phenotypic plasticity and genotype-environment interactions affecting life-history traits in Caenorhabditis elegans. Heredity. 2007, 98: 28-37. 10.1038/sj.hdy.6800894.View ArticlePubMed
- Harvey SC, Viney ME: Thermal variation reveals natural variation between isolates of Caenorhabditis elegans. J Exp Zool B Mol Dev Evol. 2007, 308B: 409-416. 10.1002/jez.b.21161.View Article
- Anderson JL, Albergotti L, Proulx S, Peden C, Huey RB, Phillips PC: Thermal preference of Caenorhabditis elegans: A null model and empirical tests. J Exp Biol. 2007, 210: 3107-3116. 10.1242/jeb.007351.View ArticlePubMed
- McGrath PT, Rockman MV, Zimmer M, Jang H, Macosko EZ, Kruglyak L, Bargmann CI: Quantitative mapping of a digenic behavioral trait implicates globin variation in C. elegans sensory behaviors. Neuron. 2009, 61: 692-699. 10.1016/j.neuron.2009.02.012.View ArticlePubMedPubMed Central
- Weber KP, De S, Kozarewa I, Turner DJ, Babu MM, de Bono M: Whole genome sequencing highlights genetic changes associated with laboratory domestication of C. elegans. PLoS ONE. 2010, 5: e13922-10.1371/journal.pone.0013922.View ArticlePubMedPubMed Central
- Gaertner BE, Phillips PC: Caenorhabditis elegans as a platform for molecular quantitative genetics and the systems biology of natural variation. Genet Res. 2010, 92: 331-348. 10.1017/S0016672310000601.View Article
- Heath JE: Temperature regulation and diurnal activity in horned lizards. Univ Calif Publ Zool. 1965, 64: 97-136.
- Huey RB, Pianka ER, Hoffman J: Seasonal variation in thermoregulatory behavior and body temperature of diurnal Kalahari lizards. Ecology. 1977, 58: 1066-1075. 10.2307/1936926.View Article
- Christian K, Tracy CR, Porter WP: Seasonal shifts in body temperature and use of microhabitats by Galapagos land iguanas (Conolophus pallidus). Ecology. 1983, 64: 463-468. 10.2307/1939965.View Article
- Kingsolver JG: Evolution and coadaptation of thermoregulatory behavior and wing pigmentation pattern in Pierid butterflies. Evolution. 1987, 41: 472-490. 10.2307/2409250.View Article
- Cutter AD: Nucleotide polymorphism and linkage disequilibrium in wild populations of the partial selfer Caenorhabditis elegans. Genetics. 2006, 172: 171-184.View ArticlePubMedPubMed Central
- Rockman MV, Kruglyak L: Recombinational landscape and population genomics of Caenorhabditis elegans. PLoS Genet. 2009, 5: e1000419-10.1371/journal.pgen.1000419.View ArticlePubMedPubMed Central
- Fisher RA: The genetical theory of natural selection. 1930, Oxford: Clarendon PressView Article
- Gutteling EW, Doroszuk A, Riksen JAG, Prokop Z, Reszka J, Kammenga JE: Environmental influence on the genetic correlations between life-history traits in Caenorhabditis elegans. Heredity. 2007, 98: 206-213. 10.1038/sj.hdy.6800929.View ArticlePubMed
- Voorhies V: Bergmann size clines: A simple explanation for their occurrence in ectotherms. Evolution. 1996, 50: 1259-1264. 10.2307/2410666.View Article
- Kammenga JE, Doroszuk A, Riksen JAG, Hazendonk E, Spiridon L, Petrescu AJ, Tijsterman M, Plasterk RHA, Bakker J: A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3. PLoS Genet: e34. 2007
- Anderson RV, Coleman DC: Nematode temperature responses: A niche dimension in populations of bacterial-feeding nematodes. J Nematol. 1982, 14: 69-76.PubMedPubMed Central
- Feder ME: Necrotic fruit: A novel model system for thermal ecologists. J Therm Biol. 1997, 22: 1-9. 10.1016/S0306-4565(96)00028-9.View Article
- Jones JS, Coyne JA, Partridge L: Estimation of the thermal niche of Drosophila melanogaster using a temperature-sensitive mutation. Am Nat. 1987, 130: 83-90. 10.1086/284699.View Article
- Freckman DW, Virginia RA: Low-diversity Antarctic soil nematode communities: Distribution and response to disturbance. Ecology. 1997, 78: 363-369. 10.1890/0012-9658(1997)078[0363:LDASNC]2.0.CO;2.View Article
- Ruess L, Michelsen A, Jonasson S: Simulated climate change in subarctic soils: Responses in nematode species composition and dominance structure. Nematology. 1999, 1: 513-526. 10.1163/156854199508513.View Article
- Hoschitz M, Kaufmann R: Soil nematode communities of Alpine summits-site differentiation and microclimatic influences. Pedobiologia. 2004, 48: 313-320. 10.1016/j.pedobi.2004.03.004.View Article
- Pen-Mouratov S, He XL, Steinberger Y: Spatial distribution and trophic diversity of nematode populations under Acacia raddiana along a temperature gradient in the Negev Desert ecosystem. J Arid Environ. 2004, 56: 339-355. 10.1016/S0140-1963(03)00058-2.View Article
- Brett JR: Energetic responses of salmon to temperature. A study of some thermal relations in physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerka). Am Zool. 1971, 11 (1): 99-113.View Article
- Kader NA, Côté MG: Isolation, identification and characterization of some strains of Caenorhabditis elegans (Maupas, 1900) from Quebec. Fund Appl Nematol. 1996, 19: 381-389.
- Huey RB, Hertz PE: Is a Jack-of-all-temperatures a master of none?. Evolution. 1984, 38: 441-444. 10.2307/2408502.View Article
- Prasad A, Croydon-Sugarman MJ, Murray RL, Cutter AD: Temperature-dependent fecundity associates with latitude in Caenorhabditis briggsae. Evolution. 2010, 65: 52-63.View ArticlePubMed
- Hedgecock EM, Russell RL: Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA. 1975, 72: 4061-4065. 10.1073/pnas.72.10.4061.View ArticlePubMedPubMed Central
- Cassata G, Kagoshima H, Andachi Y, Kohara Y, Durrenberger MB, Hall DH, Burglin TR: The LIM homeobox gene ceh-14 confers thermosensory function to the AFD neurons in Caenorhabditis elegans. Neuron. 2000, 25: 587-597. 10.1016/S0896-6273(00)81062-4.View ArticlePubMed
- Colosimo ME, Brown A, Mukhopadhyay S, Gabel C, Lanjuin AE, Samuel ADT, Sengupta P: Identification of thermosensory and olfactory neuron-specific genes via expression profiling of single neuron types. Curr Biol. 2004, 14: 2245-2251. 10.1016/j.cub.2004.12.030.View ArticlePubMed
- Satterlee JS, Ryu WS, Sengupta P: The CMK-1 CaMKI and the TAX-4 cyclic nucleotide-gated channel regulate thermosensory neuron gene expression and function in C. elegans. Curr Biol. 2004, 14: 62-68. 10.1016/j.cub.2003.12.030.View ArticlePubMed
- Mohri A, Kodama E, Kimura KD, Koike M, Mizuno T, Mori I: Genetic control of temperature preference in the nematode Caenorhabditis elegans. Genetics. 2005, 169: 1437-1450.View ArticlePubMedPubMed Central
- Inada H, Ito H, Satterlee J, Sengupta P, Matsumoto K, Mori I: Identification of guanylyl cyclases that function in thermosensory neurons of Caenorhabditis elegans. Genetics. 2006, 172: 2239-2252.View ArticlePubMedPubMed Central
- Tanizawa Y, Kuhara A, Inada H, Kodama E, Mizuno T, Mori I: Inositol monophosphatase regulates localization of synaptic components and behavior in the mature nervous system of C. elegans. Genes Dev. 2006, 20: 3296-3310. 10.1101/gad.1497806.View ArticlePubMedPubMed Central
- Mori I, Ohshima Y: Neural regulation of thermotaxis in Caenorhabditis elegans. Nature. 1995, 376: 344-348. 10.1038/376344a0.View ArticlePubMed
- Samuel ADT, Silva RA, Murthy VN: Synaptic activity of the AFD neuron in Caenorhabditis elegans correlates with thermotactic memory. J Neurosci. 2003, 23: 373-376.PubMed
- Zariwala HA, Miller AC, Faumont S, Lockery SR: Step response analysis of thermotaxis in Caenorhabditis elegans. J Neurosci. 2003, 23: 4369-4377.PubMed
- Clark DA, Biron D, Sengupta P, Samuel ADT: The AFD sensory neurons encode multiple functions underlying thermotactic behavior in Caenorhabditis elegans. J Neurosci. 2006, 26: 7444-7451. 10.1523/JNEUROSCI.1137-06.2006.View ArticlePubMed
- Kodama E, Kuhara A, Mohri-Shiomi A, Kimura KD, Okumura M, Tomioka M, Iino Y, Mori I: Insulin-like signaling and the neural circuit for integrative behavior in C. elegans. Genes Dev. 2006, 20: 2955-2960. 10.1101/gad.1479906.View ArticlePubMedPubMed Central
- Ito H, Inada H, Mori I: Quantitative analysis of thermotaxis in the nematode Caenorhabditis elegans. J Neurosci Methods. 2006, 154: 45-52. 10.1016/j.jneumeth.2005.11.011.View ArticlePubMed
- Jurado P, Kodama E, Tanizawa Y, Mori I: Distinct thermal migration behaviors in response to different thermal gradients in Caenorhabditis elegans. Genes Brain Behav. 2010, 9: 120-127. 10.1111/j.1601-183X.2009.00549.x.View ArticlePubMed
- Kammenga JE, Phillips PC, De Bono M, Doroszuk A: Beyond induced mutants: Using worms to study natural variation in genetic pathways. Trends Genet. 2008, 24: 178-185. 10.1016/j.tig.2008.01.001.View ArticlePubMed
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.