Does thermoregulatory behavior maximize reproductive fitness of natural isolates of Caenorhabditis elegans?

Anderson, Jennifer; Albergotti, Lori C.; Ellebracht, Barbara; Huey, Raymond B.; Phillips, Patrick C.

doi:10.1186/1471-2148-11-157

Cited by 55 publications

(71 citation statements)

References 81 publications

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“…The fitness of different wild genetic backgrounds of C. briggsae is affected differentially by rearing temperature in accord with the strong phylogeographic patterning of this species in which genotype, phenotype and geographic distribution all are associated (Prasad et al, 2011). By contrast, C. elegans shows no comparable association between phenotypes and geographic origin, including differences in temperature-dependent fecundity (Hodgkin and Doniach, 1997;Rockman and Kruglyak, 2009;Anderson et al, 2011). In particular, strains from the two most commonly isolated C. briggsae genetic groups suggest a latitudinal divide, and these two groups have been designated as 'temperate' and 'tropical' clades (Cutter et al, 2006).…”

Section: Introductionmentioning

confidence: 90%

Temperature-dependent behaviours are genetically variable in the nematode Caenorhabditis briggsae

Stegeman

Mesquita

Ryu

et al. 2012

Journal of Experimental Biology

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SUMMARY Temperature-dependent behaviours inCaenorhabditis elegans, such as thermotaxis and isothermal tracking, are complex behavioural responses that integrate sensation, foraging and learning, and have driven investigations to discover many essential genetic and neural pathways. The ease of manipulation of the Caenorhabditis model system also has encouraged its application to comparative analyses of phenotypic evolution, particularly contrasts of the classic model C. elegans with C. briggsae. And yet few studies have investigated natural genetic variation in behaviour in any nematode. Here we measure thermotaxis and isothermal tracking behaviour in genetically distinct strains of C. briggsae, further motivated by the latitudinal differentiation in C. briggsae that is associated with temperature-dependent fitness differences in this species. We demonstrate that C. briggsae performs thermotaxis and isothermal tracking largely similar to that of C. elegans, with a tendency to prefer its rearing temperature. Comparisons of these behaviours among strains reveal substantial heritable natural variation within each species that corresponds to three general patterns of behavioural response. However, intraspecific genetic differences in thermal behaviour often exceed interspecific differences. These patterns of temperature-dependent behaviour motivate further development of C. briggsae as a model system for dissecting the genetic underpinnings of complex behavioural traits. Supplementary material available online at

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Section: Introductionmentioning

confidence: 90%

Temperature-dependent behaviours are genetically variable in the nematode Caenorhabditis briggsae

Stegeman

Mesquita

Ryu

et al. 2012

Journal of Experimental Biology

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“…In C. elegans (N2), the spontaneous mutation process does not appear to differ between 18°and 26°, but it does in C. briggsae (C. F. Baer, personal observation). Moreover, small differences in temperature ($1°) can result in large differences in absolute fitness in C. elegans (Anderson et al 2011;C. F. Baer, unpublished results), which suggests that at least some alleles must have very sharp temperature thresholds.…”

Section: Discussionmentioning

confidence: 99%

No Evidence of Elevated Germline Mutation Accumulation Under Oxidative Stress in Caenorhabditis elegans

et al. 2011

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Variation in rates of molecular evolution has been attributed to numerous, interrelated causes, including metabolic rate, body size, and generation time. Speculation concerning the influence of metabolic rate on rates of evolution often invokes the putative mutagenic effects of oxidative stress. To isolate the effects of oxidative stress on the germline from the effects of metabolic rate, generation time, and other factors, we allowed mutations to accumulate under relaxed selection for 125 generations in two strains of the nematode Caenorhabditis elegans, the canonical wild-type strain (N2) and a mutant strain with elevated steady-state oxidative stress (mev-1). Contrary to our expectation, the mutational decline in fitness did not differ between N2 and mev-1. This result suggests that the mutagenic effects of oxidative stress in C. elegans are minor relative to the effects of other types of mutations, such as errors during DNA replication. However, mev-1 MA lines did go extinct more frequently than wild-type lines; some possible explanations for the difference in extinction rate are discussed. Lanfear et al. 2007;and Galtier et al. 2009). Usually, it is supposed that organisms with high metabolic rates have higher rates of mutation, and thus faster rates of evolution, than do organisms with low metabolic rates. There are two (not mutually exclusive) ways by which metabolic rate might affect mutation rate. First, organisms with high metabolic rates have shorter generation times (Savage et al. 2004;Bromham 2009) and thus undergo relatively more rounds of DNA replication per generation (Laird et al. 1969;Ellegren 2007;Nikolaev et al. 2007;Thomas et al. 2010) than do organisms with low metabolic rates. If most mutations occur during DNA replication, a positive relationship between metabolic rate and mutation rate, and thus rates of evolution, is expected. Second, the oxygen-centered free radicals that are by-products of aerobic metabolism (Boveris and Chance 1973;Fridovich 2004) can cause oxidative damage to DNA (Hsie et al.

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“…We demonstrate the importance of accounting for the thermal environment in studies of host–pathogen interactions and highlight that measuring classic fitness measures, LRS and r , within the same experiment can yield novel insights (Huey & Berrigan 2001; Anderson et al . 2011). Most importantly, we hope that these results stimulate further experimental work that directly assesses the importance of this mechanism in thermally variable environments including wild populations where poikilotherms are subject to fluctuating environmental temperatures.…”

Section: Discussionmentioning

confidence: 99%

Cold‐seeking behaviour mitigates reproductive losses from fungal infection in Drosophila

Hunt

Zhong

McClure

et al. 2015

Journal of Animal Ecology

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Summary Animals must tailor their life‐history strategies to suit the prevailing conditions and respond to hazards in the environment. Animals with lethal infections are faced with a difficult choice: to allocate more resources to reproduction and suffer higher mortality or to reduce reproduction with the expectation of enhanced immunity and late‐age reproduction. However, the strategies employed to mediate shifts in life‐history traits are largely unknown.Here, we investigate the temperature preference of the fruit fly, Drosophila melanogaster, during infection with the fungal pathogen, Metarhizium robertsii, and the consequence of temperature preference on life‐history traits.We have measured the temperature preference of fruit flies under different pathogen conditions. We conducted multiple fitness assays of the host and the pathogen under different thermal conditions. From these data, we estimated standard measures of fitness and used age‐specific methodologies to test for the fitness trade‐offs that are thought to underlie differences in life‐history strategy.We found that fungus‐infected fruit flies seek out cooler temperatures, which facilitates an adaptive shift in their life‐history strategy. The colder temperatures preferred by infected animals were detrimental to the pathogen because it increased resistance to infection. But, it did not provide net benefits that were specific to infected animals, as cooler temperatures increased lifetime reproductive success and survival whether or not the animals were infected. Instead, we find that cold‐seeking benefits infected animals by increasing their late‐age reproductive output, at a cost to their early‐age reproductive output. In contrast, naive control flies prefer warmer temperatures that optimize early‐age reproductive, at a cost to reproductive output at late ages.These findings show that infected animals exhibit fundamentally different reproductive strategies than their healthy counterparts. Temperature preference can facilitate shifts in strategy, but not without inevitable trade‐offs.

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Does thermoregulatory behavior maximize reproductive fitness of natural isolates of Caenorhabditis elegans?

Cited by 55 publications

References 81 publications

Temperature-dependent behaviours are genetically variable in the nematode Caenorhabditis briggsae

Temperature-dependent behaviours are genetically variable in the nematode Caenorhabditis briggsae

No Evidence of Elevated Germline Mutation Accumulation Under Oxidative Stress in Caenorhabditis elegans

Cold‐seeking behaviour mitigates reproductive losses from fungal infection in Drosophila

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