Temperature-dependent oxygen limitation and the rise of Bergmann's rule in species with aquatic respiration

Rollinson, Njal; Rowe, Locke

doi:10.1111/evo.13458

Cited by 38 publications

(36 citation statements)

References 75 publications

(179 reference statements)

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“…However, the oxygen hypothesis leads to the prediction that organisms relying on diffusive uptake should be particularly sensitive to temperature stress, regardless of food abundance (Rollinson & Rowe, 2018), a pattern that we did not observe in our experiments. System-specific variation in the relative degree of response in each of these variables might help to explain some of the conflicting results seen in the published literature on the effect of warming on mean adult body size (Atkinson et al, 2006;Audzijonyte et al, 2017;Kooijman & Kooijman, 2010;Rollinson & Rowe, 2018;Vidal, 1980). System-specific variation in the relative degree of response in each of these variables might help to explain some of the conflicting results seen in the published literature on the effect of warming on mean adult body size (Atkinson et al, 2006;Audzijonyte et al, 2017;Kooijman & Kooijman, 2010;Rollinson & Rowe, 2018;Vidal, 1980).…”

Section: Discussioncontrasting

confidence: 64%

Food availability modulates temperature‐dependent effects on growth, reproduction, and survival in Daphnia magna

Betini

Wang

Avgar

et al. 2019

Ecology and Evolution

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Reduced body size and accelerated life cycle due to warming are considered major ecological responses to climate change with fitness costs at the individual level. Surprisingly, we know little about how relevant ecological factors can alter these life history trade‐offs and their consequences for individual fitness. Here, we show that food modulates temperature‐dependent effects on body size in the water flea Daphnia magna and interacts with temperature to affect life history parameters. We exposed 412 individuals to a factorial manipulation of food abundance and temperature, tracked each reproductive event, and took daily measurements of body size from each individual. High temperature caused a reduction in maximum body size in both food treatments, but this effect was mediated by food abundance, such that low food conditions resulted in a reduction of 20% in maximum body size, compared with a reduction of 4% under high food conditions. High temperature resulted in an accelerated life cycle, with pronounced fitness cost at low levels of food where only a few individuals produced a clutch. These results suggest that the mechanisms affecting the trade‐off between fast growth and final body size are food‐dependent, and that the combination of low levels of food and high temperature could potentially threaten viability of ectotherms.

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Section: Discussioncontrasting

confidence: 64%

Food availability modulates temperature‐dependent effects on growth, reproduction, and survival in Daphnia magna

Betini

Wang

Avgar

et al. 2019

Ecology and Evolution

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“…Data on egg diameter, clutch size, adult snout‐to‐vent length (SVL), and reproductive mode of frogs and salamanders were compiled by Rollinson and Rowe (,b). For frogs, we converted SVL to weight (g) using family‐specific conversions, or when family‐level conversions were not available, conversions by lifestyle (arboreal, terrestrial, and aquatic), all provided by Santini et al.…”

Section: Methodsmentioning

confidence: 99%

“…(). Data on adult weight of paedomorphic species were collected from Rollinson and Rowe (), and we otherwise converted SVL to weight using family‐specific conversions in Santini et al. ().…”

Section: Methodsmentioning

confidence: 99%

“…When family‐level conversions were missing from Santini et al. (), we followed Rollinson and Rowe () where adult weight of species in Hynobiidae and Dicamptodonidae was estimated from the Ambystomatidae conversion factor, and Rhyacotritonidae was estimated from the Plethodontidae conversion factor. Mean egg diameter data were converted to weight assuming eggs are spherical and that volume and weight are equivalent (Einum and Fleming ), such that egg weight (g) = (4/3) × π × r 3 , where π = 3.14 and r is the radius in centimeter.…”

Section: Methodsmentioning

confidence: 99%

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Density‐dependent offspring interactions do not explain macroevolutionary scaling of adult size and offspring size

2019

Self Cite

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Most life forms exhibit a correlated evolution of adult size (AS) and size at independence (SI), giving rise to AS–SI scaling relationships. Theory suggests that scaling arises because relatively large adults have relatively high reproductive output, resulting in strong density‐dependent competition in early life, where large size at independence provides a competitive advantage to juveniles. The primary goal of our study is to test this density hypothesis, using large datasets that span the vertebrate tree of life (fishes, amphibians, reptiles, birds, and mammals). Our secondary goal is to motivate new hypotheses for AS–SI scaling by exploring how subtle variation in life‐histories among closely related species is associated with variation in scaling. Our phylogenetically informed comparisons do not support the density hypothesis. Instead, exploration of AS–SI scaling among life‐history variants suggests that steeper AS–SI scaling slopes are associated with evolutionary increases in size at independence. We suggest that a positive association between size at independence and juvenile growth rate may represent an important mechanism underlying AS–SI scaling, a mechanism that has been underappreciated by theorists. If faster juvenile growth is a consequence of evolutionary increases in size at independence, this may help offset the cost of delayed maturation, leading to steeper AS–SI scaling slopes.

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“…This mechanism was linked to the body size adjustment to temperature by Atkinson et al (2006). The hypothesis on the oxygen-driven size-to-temperature response has been positively verified both indirectly (Berner et al, 2007; Harrison et al, 2010; Rollinson and Rowe, 2018a; Rollinson and Rowe, 2018b; Santilli and Rollinson, 2018; Verberk and Atkinson, 2013) and directly (Czarnoleski et al, 2015; Frazier et al, 2001; Hoefnagel and Verberk, 2015). However, results relating this pattern directly to organismal fitness are scarce (Prokosch et al, 2019; Walczyńska et al, 2015a), while such a reference is the only way that enables reliable conclusions on the evolutionary meaning of TSR.…”

Section: Introductionmentioning

confidence: 81%

Aerobic scope does matter in temperature-size rule, but only under optimal conditions

Walczyńska

Łabęcka

Sobczyk

2020

Preprint

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3 1 exposure to hypoxia, (iii) this response enables us to keep the wide scope for aerobic 3 2 performance, and (iv) it prevents the decrease in fitness. We conducted our tests on three clones 3 3 of the rotifer Lecane inermis with different thermal preferences. These clones were exposed to 3 4 three experimental regimes: mild hypoxia, severe hypoxia driven by a too high temperature, and 3 5 severe hypoxia driven by an inadequate oxygen concentration. The results showed that our 3 6 causative reasoning was generally correct, but only under mildly hypoxic conditions. In more 3 7 stressful environments, rotifers had clone-and condition-specific responses, which in fact were 3 8 equally successful in terms of the levels of fitness. Our results join for the first time all factors 3 9 connecting the cause and effect in the temperature-size rule. They indicate the importance of the 4 0conditions under which it should be tested. The most important messages from this study was that 4 1 (i) a decrease in the body size was one of but not the only option for preventing fitness reduction 4 2 under hypoxia, and (ii) such a response to higher temperature fuelled the aerobic scope in clone-4 3 specific, thermally optimal conditions. 4 4 4 5 4 6 4 7 4 8 4 9 7 1 2018; Verberk and Atkinson, 2013) and directly (Czarnoleski et al., 2015; Frazier et al., 2001; 7 2 Hoefnagel and Verberk, 2015). However, results relating this pattern directly to organismal 7 3 fitness are scarce (Prokosch et al., 2019; Walczyńska et al., 2015a), while such a reference is the 7 4only way that enables reliable conclusions on the evolutionary meaning of TSR. 7 5In this study, we linked the hypothesized proximate and ultimate mechanisms behind the 7 6 phenotypically driven size decrease with increasing temperature for the case of the rotifer Lecane 7 7inermis. We aimed to thoroughly test the logic of the reasoning behind hypoxia driving body size 7 8shrinkage to prevent the reduction in fitness. Because the TSR has been empirically confirmed to 7 9 be condition-sensitive and to be performed only in an optimal thermal range (Walczyńska et al., 8 0 4 2016), we conducted our tests under optimal and suboptimal conditions; the latter was further 8 1 diversified between hypoxia driven by stress-inducing high temperatures or by the stress-8 2 inducing low oxygen levels. This distinction enabled inference on the possible border conditions 8 3 for TSR performance, linking the hypothesized proximate and ultimate factors with fitness. 8 4We examined the aerobic scope, our hypothesized ultimate mechanism, by estimating the specific 8 5 dynamic action (SDA). This measure refers to the increasing metabolic expenditures in animals 8 6 and is associated with ingestion, digestion, assimilation and absorption of food (McCue, 2006; 8 7 Secor, 2009), when the increasing oxygen consumption was mostly associated with the 8 8 biochemical transformation of food and the synthesis of the new proteins (Jordan and Steffensen, 8 92007). In practice, it was estimated as a difference in...

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Temperature-dependent oxygen limitation and the rise of Bergmann's rule in species with aquatic respiration

Cited by 38 publications

References 75 publications

Food availability modulates temperature‐dependent effects on growth, reproduction, and survival in Daphnia magna

Food availability modulates temperature‐dependent effects on growth, reproduction, and survival in Daphnia magna

Density‐dependent offspring interactions do not explain macroevolutionary scaling of adult size and offspring size

Aerobic scope does matter in temperature-size rule, but only under optimal conditions

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