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.

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 DOI 

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 

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 

Evolutionary consequences of sex-specific selection in variable environments: four simple models reveal diverse evolutionary outcomes

Authors: Tim Connallon, Shefali Sharma, and Colin Olito

Published in: The American Naturalist

The evolutionary trajectories of species with separate sexes depend on the effects of genetic variation on female and male traits as well as the direction and alignment of selection between the sexes.

Classical theory has shown that evolution is equally responsive to selection on females and males, with natural selection increasing the product of the average relative fitness of each sex over time.

This simple rule underlies several important predictions regarding the maintenance of genetic variation, the genetic basis of adaptation, and the dynamics of “sexually antagonistic” alleles. Nevertheless, theories of sex-specific selection overwhelmingly focus on evolution in constant environments, and it remains unclear whether they apply under changing conditions.

We derived four simple models of sex-specific selection in variable environments and explored how conditions of population subdivision, the timing of dispersal, sex differences in dispersal, and the nature of environmental change mediate the evolutionary dynamics of sex-specific adaptation.

We find that these dynamics are acutely sensitive to ecological, demographic, and life-history attributes that vary widely among species, with classical predictions breaking down in contexts of environmental heterogeneity.

The evolutionary rules governing sex-specific adaptation may therefore differ between species, suggesting new avenues for research on the evolution of sexual dimorphism.

Connallon T, Sharma S, Olito C (2018) Evolutionary consequences of sex-specific selection in variable environments: four simple models reveal diverse evolutionary outcomes, The American Naturalist PDF DOI

Research fellow position: marine larval biologist

  • Level A, research-only academic
  • $66,706 to $90,532pa + 9.5% superannuation
  • Full-time, starting late 2018
  • Two-year, fixed-term
  • Monash University Clayton campus

Professor Dustin Marshall is seeking a marine larval biologist, with strong quantitative skills, to explore the ways in which temperature affects the energetics of development in marine invertebrates.  This position will be with the Centre for Geometric Biology within the School of Biological Sciences at Monash University.

As the successful candidate, you will be expected to undertake experiments to determine the relative performance of different larval types across every stage of the life history, but more importantly demonstrate a strong conceptual understanding of relevant life history theory and have a demonstrated track record in producing high quality publications.

Key selection criteria

  1. A doctoral qualification in larval biology
  2. Demonstrated analytical and manuscript preparation skills; including an excellent track record of refereed research publications in high impact journals
  3. Demonstrated experience in empirical research using cutting-edge quantitative approaches
  4. Ability to solve complex problems by using discretion, innovation and the exercise of diagnostic skills and/or expertise
  5. Well-developed planning and organisational skills, with the ability to prioritise multiple tasks and set and meet deadlines
  6. Excellent written communication and verbal communication skills with proven ability to produce clear, succinct reports and documents
  7. A demonstrated awareness of the principles of confidentiality, privacy and information handling
  8. A demonstrated capacity to work in a collegiate manner with other staff in the workplace
  9. Demonstrated computer literacy and proficiency in the production of high level work using software such as Microsoft Office applications and specified University software programs, with the capability and willingness to learn new packages as appropriate.

Enquiries to Professor Dustin Marshall on +61 3 9902 4449

For more information, or to apply, refer to the Monash University website