The origin and maintenance of metabolic allometry in animals

Authors: Craig R White, Dustin J Marshall, Lesley A Alton, Pieter A Arnold, Julian E Beaman, Candice L Bywater, Catriona Condon, Taryn S Crispin, Aidan Janetzki, Elia Pirtle, Hugh S Winwood-Smith, Michael J Angilletta Jr, Stephen F Chenoweth, Craig E Franklin, Lewis G Halsey, Michael R Kearney, Steven J Portugal, and Daniel Ortiz-Barrientos

Published in: Nature Ecology & Evolution

Abstract

Organisms vary widely in size, from microbes weighing 0.1 pg to trees weighing thousands of megagrams — a 1021-fold range similar to the difference in mass between an elephant and the Earth.

Mass has a pervasive influence on biological processes, but the effect is usually non-proportional; for example, a tenfold increase in mass is typically accompanied by just a four- to sevenfold increase in metabolic rate.

Understanding the cause of allometric scaling has been a long-standing problem in biology. Here, we examine the evolution of metabolic allometry in animals by linking microevolutionary processes to macroevolutionary patterns.

We show that the genetic correlation between mass and metabolic rate is strong and positive in insects, birds and mammals.

We then use these data to simulate the macroevolution of mass and metabolic rate, and show that the interspecific relationship between these traits in animals is consistent with evolution under persistent multivariate selection on mass and metabolic rate over long periods of time.

Citation

White CR, Marshall DJ, Alton LA, Arnold PA, Beaman JE, Bywater CL, Condon C, Crispin TS, Janetzki A, Pirtle E, Winwood-Smith HS, Angilletta MJ, Chenoweth SF, Franklin CE, Halsey LG, Kearney MR, Portugal SJ, Ortiz-Barrientos D (2019) The origin and maintenance of metabolic allometry in animals, Nature Ecology & Evolution PDF 8 MB doi:10.1038/s41559-019-0839-9

Influence of food, body size, and fragmentation on metabolic rate in a sessile marine invertebrate

Authors: Lukas Schuster, Craig R White, and Dustin J Marshall

Published in: Invertebrate Biology

Abstract

Metabolic rates vary among individuals according to food availability and phenotype, most notably body size. Disentangling size from other factors (e.g., age, reproductive status) can be difficult in some groups, but modular organisms may provide an opportunity for manipulating size experimentally. While modular organisms are increasingly used to understand metabolic scaling, the potential of feeding to alter metabolic scaling has not been explored in this group.

Here, we perform a series of experiments to examine the drivers of metabolic rate in a modular marine invertebrate, the bryozoan Bugula neritina. We manipulated size and examined metabolic rate in either fed or starved individuals to test for interactions between size manipulation and food availability.

Field collected colonies of unknown age showed isometric metabolic scaling, but those colonies in which size was manipulated showed allometric scaling.

To further disentangle age effects from size effects, we measured metabolic rate of individuals of known age and again found allometric scaling. Metabolic rate strongly depended on access to food: starvation decreased metabolic rate by 20% and feeding increased metabolic rate by 43%.

In comparison to other marine invertebrates, however, the increase in metabolic rate, as well as the duration of the increase (known as specific dynamic action, SDA), were both low. Importantly, neither starvation nor feeding altered the metabolic scaling of our colonies.

Overall, we found that field‐collected individuals showed isometric metabolic scaling, whereas metabolic rate of size‐manipulated colonies scaled allometrically with body size. Thus, metabolic scaling is affected by size manipulation but not feeding in this colonial marine invertebrate.

Citation

Schuster L, White CR, Marshall DJ (2019) Influence of food, body size, and fragmentation on metabolic rate in a sessile marine invertebrate. Invertebrate Biology PDF 1 MB doi:10.1111/ivb.12241

Aquatic life history trajectories are shaped by selection, not oxygen limitation

Authors: Dustin J Marshall and Craig R White

Published in: Trends in Ecology & Evolution

Pauly1 argues that, as espoused in the gill-oxygen limitation theory (GOLT), growth slows as size increases because oxygen supply via the gills is unable to keep up with the oxygen demands of an increasingly large body. Thus, according to GOLT, growth determines the timing of reproduction, and fish reproduce when they become oxygen limited and growth starts to decline. GOLT has been critiqued on physiological grounds2,3 and we agree with those critiques. Large fish are no more oxygen limited than small fish, primarily because their respiratory surface area matches their metabolic demand for oxygen over a large size range…

Citation

Marshall DJ, White CR (2019) Aquatic life history trajectories are shaped by selection, not oxygen limitation, Trends in Ecology & Evolution. PDF 255 KB doi:10.1016/j.tree.2018.12.015

Linking life-history theory and metabolic theory explains the offspring size-temperature relationship

Authors: Amanda K Pettersen, Craig R White, Robert J Bryson‐Richardson, and Dustin J Marshall

Published in: Ecology Letters

Abstract

Temperature often affects maternal investment in offspring. Across and within species, mothers in colder environments generally produce larger offspring than mothers in warmer environments, but the underlying drivers of this relationship remain unresolved.

We formally evaluated the ubiquity of the temperature–offspring size relationship and found strong support for a negative relationship across a wide variety of ectotherms. We then tested an explanation for this relationship that formally links life‐history and metabolic theories. We estimated the costs of development across temperatures using a series of laboratory experiments on model organisms, and a meta‐analysis across 72 species of ectotherms spanning five phyla.

We found that both metabolic and developmental rates increase with temperature, but developmental rate is more temperature sensitive than metabolic rate, such that the overall costs of development decrease with temperature. Hence, within a species’ natural temperature range, development at relatively cooler temperatures requires mothers to produce larger, better provisioned offspring.

Citation

Pettersen AK, White CR, Bryson-Richardson RJ, Marshall DJ (2019) Linking life-history theory and metabolic theory explains the offspring size-temperature relationship, Ecology Letters PDF 556 KB doi:10.1111/ele.13213

Releasing small ejaculates slowly increases per‐gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae)

Authors: Colin Olito and Dustin J Marshall

Published in: Journal of Evolutionary Biology

Abstract

The idea that male reproductive strategies evolve primarily in response to sperm competition is almost axiomatic in evolutionary biology. However, externally fertilizing species, especially broadcast spawners, represent a large and taxonomically diverse group that have long challenged predictions from sperm competition theory – broadcast spawning males often release sperm slowly, with weak resource‐dependent allocation to ejaculates despite massive investment in gonads. One possible explanation for these counter‐intuitive patterns is that male broadcast spawners experience strong natural selection from the external environment during sperm dispersal.

Using a manipulative experiment, we examine how male reproductive success in the absence of sperm competition varies with ejaculate size and rate of sperm release, in the broadcast spawning marine invertebrate Galeolaria caespitosa (Polychaeta: Serpulidae).

We find that the benefits of Fast or Slow sperm release depend strongly on ejaculate size, but also that the per‐gamete fertilization rate decreases precipitously with ejaculate size.

Overall, these results suggest that, if males can facultatively adjust ejaculate size, they should slowly release small amounts of sperm. Recent theory for broadcast spawners predicts that sperm competition can also select for Slow release rates. Taken together, our results and theory suggest that selection often favours Slow ejaculate release rates whether males experience sperm competition or not.

Citation

Olito C, Marshall DJ (2018) Releasing small ejaculates slowly increases per‐gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae), Journal of Evolutionary Biology, PDF 833 KB doi:10.1111/jeb.13403

Have we outgrown the existing models of growth?

Authors: Dustin J Marshall and Craig R White

Published in: Trends in Ecology & Evolution

Theories of growth have a long history in biology. Two major branches of theory (mechanistic and phenomenological) describe the dynamics of growth and explain variation in the size of organisms. Both theory branches usually assume that reproductive output scales proportionately with body size, in other words that reproductive output is isometric.

A meta-analysis of hundreds of marine fishes contradicts this assumption, larger mothers reproduce disproportion- ately more in 95% of species studied, and patterns in other taxa suggest that reproductive hyperallometry is widespread.

We argue here that reproductive hyperallometry represents a profound challenge to mechanistic theories of growth in particular, and that they should be revised accordingly. We suspect that hyperallometric reproduction drives growth trajectories in ways that are largely unanticipated by current theories.

Citation

Marshall DJ, White CR (2018) Have we outgrown the existing models of growth? Trends in Ecology & Evolution PDF 2 MB doi:10.1016/j.tree.2018.10.005

How does parental environment influence the potential for adaptation to global change?

Authors: Evatt Chirgwin, Dustin J Marshall, Carla M Sgrò, and Keyne Monro

Published in: Proceedings of the Royal Society B

Abstract

Parental environments are regularly shown to alter the mean fitness of offspring, but their impacts on the genetic variation for fitness, which predicts adaptive capacity and is also measured on offspring, are unclear. Consequently, how parental environments mediate adaptation to environmental stressors, like those accompanying global change, is largely unknown.

Here, using an ecologically important marine tubeworm in a quantitative-genetic breeding design, we tested how parental exposure to projected ocean warming alters the mean survival, and genetic variation for survival, of offspring during their most vulnerable life stage under current and projected temperatures.

Offspring survival was higher when parent and offspring temperatures matched. Across offspring temperatures, parental exposure to warming altered the distribution of additive genetic variance for survival, making it covary across current and projected temperatures in a way that may aid adaptation to future warming. Parental exposure to warming also amplified nonadditive genetic variance for survival, suggesting that compatibilities between parental genomes may grow increasingly important under future warming.

Our study shows that parental environments potentially have broader-ranging effects on adaptive capacity than currently appreciated, not only mitigating the negative impacts of global change but also reshaping the raw fuel for evolutionary responses to it.

Citation

Chirgwin E, Marshall DJ, Sgrò CM, Monro K (2018) How does parental environment influence the potential for adaptation to global change?, Proceedings of the Royal Society B, PDF 556 KB doi:10.1098/rspb.2018.1374

Global environmental drivers of marine fish egg size

Authors: Diego R Barneche, Scott C Burgess, and Dustin J Marshall

Published in: Global Ecology and Biogeography, volume 27, issue 8 (August 2018)

Abstract

Aim: To test long‐standing theory on the role of environmental conditions (both mean and predictability) in shaping global patterns in the egg sizes of marine fishes.

Location: Global (50° S to 50° N).

Time period: 1880 to 2015.

Major taxa studied: Marine fish.

Methods: We compiled the largest geo‐located dataset of marine fish egg size (diameter) to date (n = 1,078 observations; 192 studies; 288 species; 242 localities). We decomposed sea surface temperature (SST) and chlorophyll‐a time series into mean and predictability (seasonality and colour of environmental noise – i.e. how predictable the environment is between consecutive time steps), and used these as predictors of egg size in a Bayesian phylogenetic hierarchical model. We test four specific hypotheses based on the classic discussion by Rass (1941), as well as contemporary life‐history theory, and the conceptual model of Winemiller and Rose (1992).

Results: Both environmental mean and predictability correlated with egg size. Our parsimonious model indicated that egg size decreases by c. 2.0‐fold moving from 1 to 30 °C. Environments that were more seasonal with respect to temperature were associated with larger eggs. Increasing mean chlorophyll‐a, from 0.1 to 1 mg/m3, was associated with a c. 1.3‐fold decrease in egg size. Lower chlorophyll‐a seasonality and reddened noise were also associated with larger egg sizes – aseasonal but more temporally autocorrelated resource regimes favoured larger eggs.

Main conclusions: Our findings support results from Rass (1941) and some predictions from Winemiller and Rose (1992). The effects of environmental means and predictability on marine fish egg size are largely consistent with those observed in marine invertebrates with feeding larvae, suggesting that there are important commonalities in how ectotherm egg size responds to environmental change. Our results further suggest that anthropogenically mediated changes in the environment will have profound effects on the distribution of marine life histories.

Citation

Barneche DR, Burgess SC, Marshall DJ (2018) Global environmental drivers of marine fish egg size, Global Ecology and Biogeography, PDF 9 MB doi:10.1111/geb.12748

Resources mediate selection on module longevity in the field

Authors: Karin Svanfeldt, Keyne Monro, and Dustin J Marshall

Published in: Evolutionary Biology

Abstract

The life histories of modular organisms are complicated, where selection and optimization can occur at both organismal and modular levels.

At a modular level, growth, reproduction and death can occur in one module, independently of others. Across modular groups, there are no formal investigations of selection on module longevity.

We used two field experiments to test whether selection acts on module longevity in a sessile marine invertebrate and whether selection varies across successional gradients and resource regimes.

We found that selection does act on module longevity and that the strength of selection varies with environmental conditions. In environments where interspecific competition is high, selection favours colonies with longer zooid (module) longevity for colonies that initially received high levels of maternal investment. In environments where food availability is high and flow rate is low, selection also favours colonies with longer zooid longevity.

These patterns of selection provide partial support for module longevity theory developed for plants. Nevertheless, that selection on module longevity is so context‐dependent suggests that variation in module longevity is likely to be maintained in this system.

Citation

Svanfeldt K, Monro K, Marshall DJ (2018) Resources mediate selection on module longevity in the field, Journal of Evolutionary Biology, PDF 350 KB doi:10.1111/jeb.13362

Do larger individuals cope with resource fluctuations better? An artificial selection approach

Authors: Martino E Malerba, Maria M Palacios, and Dustin J Marshall

Published in: Proceedings of the Royal Society B

Abstract

Size determines the rate at which organisms acquire and use resources but it is unclear what size should be favoured under unpredictable resource regimes.

Some theories claim smaller organisms can grow faster following a resource pulse, whereas others argue larger species can accumulate more resources and maintain growth for longer periods between resource pulses. Testing these theories has relied on interspecific comparisons, which tend to confound body size with other life-history traits.

As a more direct approach, we used 280 generations of artificial selection to evolve a 10-fold difference in mean body size between small- and large-selected phytoplankton lineages of Dunaliella tertiolecta, while controlling for biotic and abiotic variables. We then quantified how body size affected the ability of this species to grow at nutrient-replete conditions and following periods of nitrogen or phosphorous deprivation.

Overall, smaller cells showed slower growth, lower storage capacity and poorer recovery from phosphorous depletion, as predicted by the ‘fasting endurance hypothesis’. However, recovery from nitrogen limitation was independent of size—a finding unanticipated by current theories.

Phytoplankton species are responsible for much of the global carbon fixation and projected trends of cell size decline could reduce primary productivity by lowering the ability of a cell to store resources.

Citation

Malerba ME, Palacios MM, Marshall DJ (2018) Do larger individuals cope with resource fluctuations better? An artificial selection approach, Proceedings of the Royal Society B, PDF 2 MB doi:10.1098/rspb.2018.1347