Does geographic variation in thermal tolerance in Daphnia represent trade-offs or conditional neutrality?

Coggins, Bret L.; Pearson, A. C.; Yampolsky, Lev Y.

doi:10.1016/j.jtherbio.2021.102934

Cited by 11 publications

(13 citation statements)

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“…5B). This is consistent with the clone effect on membrane properties reported in Martin-Creuzburg et al ( 2019) and the persistent positive correlation between heat tolerance and life-history traits observed in Coggins et al (2021). Whatever nature these among-clones differences may have, they do not correlate with lifespan (the "good" and the "bad" clones are present among both short-and long-lived ones) and correlate with heat tolerance in a manner independent from purely dietary differences.…”

Section: Discussionsupporting

confidence: 92%

Dietary polyunsaturated fatty acids affect longevity, heat tolerance, lipid peroxidation and mitochondrial membrane potential in Daphnia.

Yampolsky

Moore

Martin‐Creuzburg

2022

Preprint

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The dietary supply with polyunsaturated fatty acids (PUFA) crucially affects animals’ performance at different temperatures. However, the underlying physiological mechanisms are still insufficiently understood. Here, we analyzed lifespan and heat tolerance of four genotypes of Daphnia magna reared on either the green alga Scenedesmus obliquus that lacks long-chain (>C18) PUFA, or a the heterokont alga Nannochloropsis limnetica that contains C20 PUFA, both either at saturating and near-starvation levels. A significant genotype-by-diet interaction in lifespan was observed at saturating diets, the C20 PUFA-rich diet eliminating differences in lifespan among genotypes observed on the PUFA-deficient diet. Corrected for body length, acute heat tolerance was higher at low than at high food concentration, except for the youngest ages. Genotypes differed significantly in heat tolerance, but there was no genotype-by-diet interactions. As predicted, the C20 PUFA-rich diet resulted in higher lipid peroxidation (LPO) and a lower mitochondrial membrane potential (ΔΨm) and LPO levels averaged across clones and rearing conditions were inversely related to acute heat tolerance. Yet, heat tolerance was higher on the PUFA-rich diet than on the PUFA-deficient diet, particularly in older Daphnia , indicating that the C20 PUFA-rich diet allowed Daphnia to compensate for higher LPO. In contrast, Daphnia with intermediate levels of ΔΨm showed the lowest heat tolerance. Neither LPO nor ΔΨm explained the diet effects on lifespan. We hypothesize that antioxidants present in the PUFA-rich diet may have enabled higher heat tolerance of Daphnia despite higher LPO and may also explain the lifespan expansion of otherwise short-lived genotypes.

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Section: Discussionsupporting

confidence: 92%

Dietary polyunsaturated fatty acids affect longevity, heat tolerance, lipid peroxidation and mitochondrial membrane potential in Daphnia.

Yampolsky

Moore

Martin‐Creuzburg

2022

Preprint

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“…It is reasonable to assume that Daphnia originating from these habitats have been under a stronger selection favoring hypoxia adaptation than those originating from more permanent water bodies. Previous studies (Anderson et al, 2022;Coggins et al, 2021) indicated that the two clones from the intermittent habitats had lower lifespan and higher propensity for sexual reproduction than the two clones from more permanent water bodies, so we anticipated differences in lifespan effects of hypoxia. Indeed, post hoc, it was discovered that many of the physiological and transcriptional effects differ between the clones from intermittent, hypoxia-prone habitats, and those originating from more permanent, hypoxia-free habitats, thus indicating local adaptation.…”

Section: Ecophysiologymentioning

confidence: 95%

The interplay between prior selection, mild intermittent exposure, and acute severe exposure in phenotypic and transcriptional response to hypoxia

Ekwudo

Malek

Anderson

et al. 2022

Ecology and Evolution

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Hypoxia has profound and diverse effects on aerobic organisms, disrupting oxidative phosphorylation and activating several protective pathways. Predictions have been made that exposure to mild intermittent hypoxia may be protective against more severe exposure and may extend lifespan. Here we report the lifespan effects of chronic, mild, intermittent hypoxia, and short‐term survival in acute severe hypoxia in four clones of Daphnia magna originating from either permanent or intermittent habitats. We test the hypothesis that acclimation to chronic mild intermittent hypoxia can extend lifespan through activation of antioxidant and stress‐tolerance pathways and increase survival in acute severe hypoxia through activation of oxygen transport and storage proteins and adjustment to carbohydrate metabolism. Unexpectedly, we show that chronic hypoxia extended the lifespan in the two clones originating from intermittent habitats but had the opposite effect in the two clones from permanent habitats, which also showed lower tolerance to acute hypoxia. Exposure to chronic hypoxia did not protect against acute hypoxia; to the contrary, Daphnia from the chronic hypoxia treatment had lower acute hypoxia tolerance than normoxic controls. Few transcripts changed their abundance in response to the chronic hypoxia treatment in any of the clones. After 12 h of acute hypoxia treatment, the transcriptional response was more pronounced, with numerous protein‐coding genes with functionality in oxygen transport, mitochondrial and respiratory metabolism, and gluconeogenesis, showing upregulation. While clones from intermittent habitats showed somewhat stronger differential expression in response to acute hypoxia than those from permanent habitats, contrary to predictions, there were no significant hypoxia‐by‐habitat of origin or chronic‐by‐acute treatment interactions. GO enrichment analysis revealed a possible hypoxia tolerance role by accelerating the molting cycle and regulating neuron survival through upregulation of cuticular proteins and neurotrophins, respectively.

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“…Daphnia magna clones used in this study (Supplementary Table 1) have been obtained from Basel University Daphnia stock collection in Basel, Switzerland. They are a subset of clones that have been previously characterized for a number of life-history traits (Coggins et al, 2021b) and were chosen to represent a range of clone-specific life expectancies. Stocks are maintained in the lab at 20 °C in 200 mL jars with COMBO water (Kilham et al 1998), 10 adults per jar and fed a diet of Scenedesmus acutus at the concentration of 100,000 cells per mL per day or 2x10 6 cells/Daphnia/day.…”

Section: Origin and Maintenance Of Clonesmentioning

confidence: 99%

Inverse Lansing Effect: Maternal Age and Provisioning Affecting Daughters’ Longevity and Male Offspring Production

Anderson

Malek

Jonas-Closs

et al. 2022

The American Naturalist

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Maternal age effects on life history of offspring has been demonstrated in a variety of organisms, more often than not offspring of older mothers having lower life expectancy (Lansing effect). However, there is no consensus on how general this phenomenon is and what are the genetic and epigenetic mechanisms behind it. We tested the predictions of Lansing effect in several Daphnia magna clones in and observed a significant genotype-by-maternal age interaction, indicating clone-specific magnitude and direction of the effect of maternal age on daughters' longevity. We then repeated this experiment with more detailed life-history and offspring provisioning data focusing on 2 clones with contrasting life-histories. One of these clones demonstrating the inverse Lansing effect, with daughters of older mothers living longer than those of young mothers. Individuals from a single-generation maternal age reversal treatment showed intermediate lifespan. We also report genotype-specific, ambidirectional, and largely fecundity-independent effects of maternal age on daughters' propensity to produce male offspring, with daughters of older mothers showing higher male production than daughters of younger mothers in the least male-producing clone and vise versa. We tested whether both effects can be explained by either lipid provisioning of embryos by mothers of different age, or by properties of mitochondria transmitted by mothers of different age to their offspring, using rhodamine-123 assay of mitochondrial membrane potential as a measure of mitochondria quality. We show that once lipid provisioning is accounted for, the effects of maternal age on lifespan and male production disappear and that the effect of lipid provisioning itself is clone-dependent, confirming that maternal provisioning sets daughters life history parameters. In the clone showing the inverse Lansing effect we demonstrated that, contrary to the predictions, neonates produced by older mothers were characterized by higher mitochondrial membrane potential in neural tissues than their counterparts born to younger mothers. We conclude that, in at least some genotypes, a reverse Lansing effect is possible, and hypothesize that it may be a result of lower lipid provisioning creating calorically restricted environment during embryonic development.

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Does geographic variation in thermal tolerance in Daphnia represent trade-offs or conditional neutrality?

Cited by 11 publications

References 61 publications

Dietary polyunsaturated fatty acids affect longevity, heat tolerance, lipid peroxidation and mitochondrial membrane potential in Daphnia.

Dietary polyunsaturated fatty acids affect longevity, heat tolerance, lipid peroxidation and mitochondrial membrane potential in Daphnia.

The interplay between prior selection, mild intermittent exposure, and acute severe exposure in phenotypic and transcriptional response to hypoxia

Inverse Lansing Effect: Maternal Age and Provisioning Affecting Daughters’ Longevity and Male Offspring Production

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