Physical and physiological impacts of ocean warming alter phenotypic selection on sperm morphology

Authors: Evatt Chirgwin, Dustin J Marshall, and Keyne Monro

Published in: Functional Ecology


Global warming may threaten fertility, which is a key component of individual fitness and vital for population persistence. For males, fertility relies on the ability of sperm to collide and fuse with eggs; consequently, sperm morphology is predicted to be a prime target of selection owing to its effects on male function.

In aquatic environments, warming will expose gametes of external fertilizers to the physiological effects of higher temperature and the physical effects of lower viscosity. However, the consequences of either effect for fertility, and for selection acting on sperm traits to maintain fertility, are poorly understood.

Here, we test how independent changes in water temperature and viscosity alter male fertility and selection on sperm morphology in an externally fertilizing marine tubeworm. To create five fertilization environments, we manipulate temperature to reflect current-day conditions (16.5 °C), projected near-term warming (21 °C) and projected long-term warming (25 °C), then adjust two more environments at 21 °C and 25 °C to the viscosity of environments at 16.5 °C and 21 °C, respectively. We then use a split-ejaculate design to measure the fertility of focal males, and selection on their sperm, in each environment.

Projected changes in temperature and viscosity act independently to reduce male fertility, but act jointly to alter selection on sperm morphology. Specifically, environments resulting from projected warming alter selection on the sperm midpiece in ways that suggest shifts in the energetic challenges of functioning under stressful conditions. Selection also targets sperm head dimensions and tail length, irrespective of environment.

We provide the first evidence that projected changes in ocean temperature and viscosity will not only impact the fertility of marine external fertilizers, but expose their gametes to novel selection pressures that may drive them to adapt in response if gamete phenotypes are sufficiently heritable.

Chirgwin E, Marshall DJ, Monro K (2019) Physical and physiological impacts of ocean warming alter phenotypic selection on sperm morphology. Functional Ecology PDF DOI

Research fellow position: marine larval biologist

  • Level A, research-only academic
  • $68,040 – $92,343 pa (plus 9.5% employer superannuation)
  • Full-time, starting early 2020
  • One year, fixed term with the possibility of extension to a second year
  • Monash University Clayton campus

Professor Dustin Marshall is seeking an experienced ecologist / evolutionary biologist, who specialises in microalgal biology with a strong empirical background, to explore the ways in which size affects the structure and function of marine phytoplankton. 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 maintain the Centre’s evolved lines of the microalgae Dunaliella and use these evolved microalgae to undertake experiments that test ecological and evolutionary theories. You will also have a strong quantitative background and have a demonstrated track record in producing high-quality publications.

Key selection criteria

  1. A doctoral qualification in empirical ecology / evolutionary biology using microalgae as a model species.
  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. Strong leadership, organisational and project management skills.
  5. Ability to work collaboratively with others

Enquiries to Professor Dustin Marshall on +61 3 9902 4449

Applications close Thursday 5 December 2019.

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

Size and density mediate transitions between competition and facilitation

Authors: Hayley Cameron, Tim Coulson, and Dustin J Marshall

Published in: Ecology Letters


Species simultaneously compete with and facilitate one another. Size can mediate transitions along this competition–facilitation continuum, but the consequences for demography are unclear.

We orthogonally manipulated the size of a focal species, and the size and density of a heterospecific neighbour, in the field using a model marine system. We then parameterised a size‐structured population model with our experimental data.

We found that heterospecific size and density interactively altered the population dynamics of the focal species. Size determined whether heterospecifics facilitated (when small) or competed with (when large) the focal species, while density strengthened these interactions.

Such size‐mediated interactions also altered the pace of the focal’s life history. We provide the first demonstration that size and density mediate competition and facilitation from a population dynamical perspective. We suspect such effects are ubiquitous, but currently underappreciated.

We reiterate classic cautions against inferences about competitive hierarchies made in the absence of size‐specific data.

Cameron H, Coulson T, Marshall DJ (2019) Size and density mediate transitions between competition and facilitation. Ecology Letters PDF DOI

Can competitive asymmetries maintain offspring size variation? A manipulative field test

Authors: Hayley Cameron and Dustin J Marshall

Published in: Evolution


Offspring sizes vary within populations but the reasons are unclear. Game‐theoretic models predict that selection will maintain offspring‐size variation when large offspring are superior competitors (i.e., competition is asymmetric), but small offspring are superior colonizers. Empirical tests are equivocal, however, and typically rely on interspecific comparisons, whereas explicit intraspecific tests are rare.

In a field study, we test whether offspring size affects competitive asymmetries using the sessile marine invertebrate, Bugula neritina. Surprisingly, we show that offspring size determines whether interactions are competitive or facilitative — large neighbors strongly facilitated small offspring, but also strongly competed with large offspring. These findings contradict the assumptions of classic theory — that is, large offspring were not superior competitors. Instead, smaller offspring actually benefit from interactions with large offspring— suggesting that asymmetric facilitation, rather than asymmetric competition, operates in our system.

We argue that facilitation of small offspring may be more widespread than currently appreciated, and may maintain variation in offspring size via negative frequency‐dependent selection.

Offspring size theory has classically viewed offspring interactions through the lens of competition alone, yet our results and those of others suggest that theory should accommodate positive interactions in explorations of offspring‐size variation.

Cameron H, Marshall DJ (2019) Can competitive asymmetries maintain offspring size variation? A manipulative field test. Evolution PDF DOI

The outsized trophic footprint of marine urbanization

Authors: Martino E Malerba, Craig R White, and Dustin J Marshall

Published in: Frontiers in Ecology and the Environment


Artificial structures are proliferating along coastlines worldwide, creating new habitat for heterotrophic filter feeders. The energy demand of this heterotrophic biomass is likely to be substantial, but is largely unquantified.

Combining in situ surveys, laboratory assays, and information obtained from geographic information systems, we estimated the energy demands of sessile invertebrates found on marine artificial structures worldwide.

At least 950,000 metric tons of heterotrophic biomass are associated with commercial ports around the world, emitting over 600 metric tons of carbon dioxide into the atmosphere and consuming 5 million megajoules of energy per day.

We propose the concept of a trophic “footprint” of marine urbanization, in which every square meter of artificial structure can negate the primary production of up to 130 square meters of surrounding coastal waters; collectively, these structures not only act as energy sinks and carbon sources, but also potentially reduce the productivity of coastal food webs.

Malerba ME, White CR, Marshall DJ (2019) The outsized trophic footprint of marine urbanization. Frontiers in Ecology and the Environment PDF DOI

Underestimating the benefits of marine protected areas for the replenishment of fished populations

Authors: Dustin J Marshall, Steven Gaines, Robert Warner, Diego R Barneche, and Michael Bode

Published in: Frontiers in Ecology and the Environment


Marine protected areas (MPAs) are important tools for managing marine ecosystems. MPAs are expected to replenish nearby exploited populations through the natural dispersal of young, but the models that make these predictions rely on assumptions that have recently been demonstrated to be incorrect for most species of fish.

A meta‐analysis showed that fish reproductive output scales “hyperallometrically” with fish mass, such that larger fish produce more offspring per unit body mass than smaller fish. Because fish are often larger inside MPAs, they should exhibit disproportionately higher reproductive output as compared to fish outside of MPAs.

We explore the consequences of hyperallometric reproduction for a range of species for population replenishment and the productivity of exploited species.

We show that the reproductive contribution of fish inside MPAs has been systematically underestimated and that fisheries yields can be enhanced by the establishment of reservoirs of larger, highly fecund fish.

Marshall DJ, Gaines S, Warner R, Barneche DR, Bode M (2019) Underestimating the benefits of marine protected areas for the replenishment of fished populations. Frontiers in Ecology and the Environment PDF DOI

Size‐abundance rules? Evolution changes scaling relationships between size, metabolism and demography

Authors: Martino E Malerba and Dustin J Marshall

Published in: Ecology Letters


Body size often strongly covaries with demography across species. Metabolism has long been invoked as the driver of these patterns, but tests of causal links between size, metabolism and demography within a species are exceedingly rare.

We used 400 generations of artificial selection to evolve a 2,427% size difference in the microalga Dunaliella tertiolecta. We repeatedly measured size, energy fluxes and demography across the evolved lineages. Then, we used standard metabolic theory to generate predictions of how size and demography should covary based on the scaling of energy fluxes that we measured.

The size dependency of energy remained relatively consistent in time, but metabolic theory failed to predict demographic rates, which varied unpredictably in strength and even sign across generations.

Classic theory holds that size affects demography via metabolism – our results suggest that both metabolism and size act separately to drive demography and that among‐species patterns may not predict within‐species processes.

Malerba ME, Marshall DJ (2019) Size-abundance rules? Evolution changes scaling relationships between size, metabolism and demography. Ecology Letters PDF DOI

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


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


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


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