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.

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 DOI

Should we care if models are phenomenological or mechanistic?

Authors: Craig R White and Dustin J Marshall

Published in: Trends in Ecology & Evolution

Abstract

A recent meta-analysis of published data demonstrated that reproductive output increases disproportionately with size in fish.

Building on this observation, we hypothesised that growth slows as animals increase in size because of an increasing allocation of energy to reproduction, and we demonstrated that this hypothesis is plausible by fitting a simple model of energy allocation to growth, reproduction, and maintenance to weight-for-age data for a selection of fish species.

The fit of our model to growth data was indistinguishable from that of the well-known models of Pütter, von Bertallanfy, and the ontogenetic growth model (OGM) proposed by West and colleagues. However, these and other existing models of growth (e.g., dynamic energy budget (DEB) theory) fail to predict hyperallometric reproduction, and we therefore suggested that this disconnect between theory and data requires the revision of existing theory.

White CR, Marshall DJ (2019) Should we care if models are phenomenological or mechanistic? Trends in Ecology & Evolution PDF DOI 

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…

Marshall DJ, White CR (2019) Aquatic life history trajectories are shaped by selection, not oxygen limitation, Trends in Ecology & Evolution. PDF DOI

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.

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 DOI

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.

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 DOI

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.

Marshall DJ, White CR (2018) Have we outgrown the existing models of growth? Trends in Ecology & Evolution PDF DOI

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