Why does offspring size affect performance? Integrating metabolic scaling with life-history theory

Authors: Amanda K Pettersen, Craig R White and Dustin J Marshall

Published in: Proceedings of the Royal Society B, volume 282, issue 1819 (November 2015)


Within species, larger offspring typically out-perform smaller offspring. While the relationship between offspring size and performance is ubiquitous, the cause of this relationship remains elusive.

By linking metabolic and life-history theory, we provide a general explanation for why larger offspring perform better than smaller offspring. Using high-throughput respirometry arrays, we link metabolic rate to offspring size in two species of marine bryozoan.

We found that metabolism scales allometrically with offspring size in both species: while larger offspring use absolutely more energy than smaller offspring, larger offspring use proportionally less of their maternally derived energy throughout the dependent, non-feeding phase. The increased metabolic efficiency of larger offspring while dependent on maternal investment may explain offspring size effects—larger offspring reach nutritional independence (feed for themselves) with a higher proportion of energy relative to structure than smaller offspring.

These findings offer a potentially universal explanation for why larger offspring tend to perform better than smaller offspring but studies on other taxa are needed.


Pettersen AK, White CR, Marshall DJ (2015) Why does offspring size affect performance? Integrating metabolic scaling with life-history theory. Proceedings of the Royal Society B, 282: 20151946. PDF 771 KB LINK doi:10.1098/rspb.2015.1946

Eggs with larger accessory structures are more likely to be fertilized in both low and high sperm concentrations in Styela plicate (Ascidiaceae)

Authors: Angela J Crean and Dustin J Marshall

Published in: Marine Biology, volume 162, issue 11 (November 2015)


The evolution of egg size has been intensively studied due to its influence on both fecundity and offspring performance. In marine broadcast spawners, egg size influences the probability of sperm–egg collision, and therefore, egg size can also in influence fertilization success, depending on the local concentration of sperm.

Many broadcast-spawning species have egg accessory structures that are thought to be a cheap means of altering egg size, but their influence on fertilization remains controversial.

To determine the relative influences of ovicell size and follicle cell size on fertilization success in the ascidian Styela plicata, the size distribution of eggs that were not successfully fertilized in both high and low sperm concentrations was compared to that of unfertilized controls.

At high sperm concentrations, a greater proportion of eggs with smaller ovicells were fertilized, resulting in smaller larvae hatching from this treatment. Eggs with a large follicle cell area relative to ovicell area were preferentially fertilized in both high and low sperm concentration treatments.

Hence, follicle cells do not eliminate selection on ovicell size at fertilization in S. plicata. Furthermore, follicle cells appear to increase fertilization success across a range of sperm concentrations by performing different functions in each environment — increasing the target size of eggs in low-sperm concentrations and presumably reducing polyspermy in high sperm concentrations.


Crean AJ, Marshall DJ (2015) Eggs with larger accessory structures are more likely to be fertilized in both low and high sperm concentrations in Styela plicata (Ascidiaceae). Marine Biology, 162:2251–2256 PDF 318 KB doi:10.1007/s00227-015-2755-0

Evolutionary consequences of fertilization mode for reproductive phenology and asynchrony

Authors: Colin Olito, Michael Bode and Dustin J Marshall

Published in: Marine Ecology Progress Series, volume 537


Reproductive phenology is a crucial life-history trait that is influenced by both environmental and frequency-dependent effects. The fitness benefits of any phenology strategy will depend strongly on other aspects of the life history: one of the most fundamental ways life histories can differ is fertilization mode. Despite the strong potential for fertilization mode to alter selection on phenology, explorations into how these 2 fundamental life-history traits interact are lacking.

We explore theoretically how frequency-dependent effects and fertilization mode influence the evolution of asynchronous reproduction, and the evolutionary stable strategy (ESS) for a population in which individuals’ mean and variance in phenology are evolvable traits.

We find that when males compete for fertilizations, perfect reproductive synchrony with optimal environmental conditions is never an optimal evolutionary strategy, and asynchronous reproduction is an inevitable consequence of frequency-dependent selection. Fertilization mode qualitatively alters frequency-dependent selection on the variance in phenology, as well as the prevalence of sexual conflict over reproductive timing.

Our results contrast with traditional hypotheses that have primarily considered asynchronous reproduction as an adaptive bet-hedging strategy in stochastic environments, and provide a much-needed explanation for the emerging picture of reproductive asynchrony observed in many systems.


Olito C, Bode M, Marshall DJ (2015) Evolutionary consequences of fertilization mode for reproductive phenology and asynchrony. Marine Ecology Progress Series, 537: 23–38 PDF 491 KB doi: 10.3354/meps11453


The biogeography of fertilization mode in the sea

Authors: Keyne Monro and Dustin J Marshall

Published in: Global Ecology and Biogeography, volume 24, issue 12 (December 2015)


Knowledge of the biogeography of life histories is central to understanding and predicting the impacts of global change on key functional traits that shape species distributions and transcend taxonomic boundaries. Whether species are internal or external fertilizers is a fundamental aspect of reproductive diversity in the sea, and has profound ecological and evolutionary consequences. However, geographic variation in this trait and the factors that potentially drive it (e.g. transitions in associated life-history traits, ecological conditions that favour one mode over the other or the evolutionary history of species) remain poorly characterized.

We collated life-history data (modes of fertilization and development), geographic data and biophysical data (sea-surface temperatures and food availability) for 1532 marine species spanning 17 invertebrate phyla. We used standard and phylogenetic logistic regressions to evaluate latitudinal gradients in fertilization mode, plus their interactions with development (transitions from planktonic to aplanktonic development, or from feeding to non-feeding larvae) and taxonomy. We also explored the dependence of fertilization mode on biophysical variables to understand how ecology potentially contributes to geographic variation in this trait.

Fertilization mode often varies predictably with latitude, but the exact nature of this relationship depends on developmental mode and the phylum under consideration. Some commonalities were evident, however, with the likelihood of internal fertilization declining at higher latitudes for Annelida and Echinodermata with aplanktonic development, but increasing at higher latitudes for Cnidaria and Porifera with non-feeding, planktonic larvae. Synergistic effects of temperature and food availability may potentially shape some of these patterns.

There are latitudinal gradients in fertilization mode in the sea. The variation among phyla and developmental modes, however, is a complexity that is unexplained by existing theory. Combined effects of recent adaptation and deeper phylogenetic history have probably shaped this systematic variation in the reproductive ecology of marine organisms.


Monro K, Marshall DJ (2015) The biogeography of fertilization mode in the sea. Global Ecology and Biogeography, 24: 1499–1509 PDF 534 KB doi: 10.1111/geb.12358

Two PhD positions available: the ecology and/or evolutionary biology of sessile marine invertebrates

Two fully-funded PhD stipends are available to students interested in working on the evolutionary ecology of sessile marine invertebrates in Prof Dustin Marshall’s Marine Evolutionary Ecology Group (MEEG). The specifics of the project will joint collaboration between student and supervisor.

The stipends include all course fees plus ~$26,288 AUD per annum tax-free (the equivalent of approx. $33,000 before tax) with no teaching requirements for 3.5 years (the length of a PhD in Australia).

Guaranteed funding of project costs and research support, including the costs of attending at least one conference per year, is included

Project start dates can be any time in 2016.

To be eligible, applicants must have completed at least one year of post-graduate research in ecology and/or evolution.

Preference will be given to those with strong quantitative skills and publications in international journals.

Interested students should send a CV, brief statement of interests and contact details of two referees to dustin.marshall@monash.edu

Applications are now closed. 

Transgenerational plasticity and environmental stress: do paternal effects act as a conduit or a buffer?

Authors: Annie S Guillaume, Keyne Monro and Dustin J Marshall


For most organisms, early life-history stages are the most sensitive to environmental stress and so transgenerational phenotypic plasticity, whereby the parental environment and off-spring environment interact to alter the phenotype of the offspring, is viewed as key to promoting
persistence in the face of environmental change. While there has been long-standing interest in the role of transgenerational plasticity via the maternal line (traditionally the field of maternal effects), increasingly it appears that paternal effects can also play a role.

Despite the emerging role of paternal effects in studies of global change, key knowledge gaps remain: first, whether paternal effects act to increase or decrease offspring performance remains largely unexplored; second, the relative roles of maternal and paternal effects are rarely disentangled; and third, the role of environmental variation, a key determinant of the
benefits of transgenerational plasticity, has not been explored with regard to paternal effects.

Here, we explore all three issues using the marine tubeworm Galeolaria caespitosa, an important habitat-forming species in southern Australia.

We found that both paternal and maternal experiences affected key stages of offspring performance (fertilization and larval development) and, surprisingly, paternal effects were often stronger than maternal effects. Furthermore, we found that paternal effects often reduced off-spring performance, especially when environments varied compared with when environments were stable.

Our results suggest that, while transgenerational plasticity may play an important role in modifying the impacts of global change, these effects are not uniformly positive. Importantly, paternal effects can be as strong, or stronger, than maternal effects and environmental variability
strongly alters the impacts of paternal effects.


Guillaume AS, Monro K, Marshall DJ (2015) Transgenerational plasticity and environmental stress: do paternal effects act as a conduit or a buffer?, Functional Ecology PDF 397 KB doi:10.1111/1365-2435.12604

Avoiding low-oxygen environments: oxytaxis as a mechanism of habitat selection in a marine invertebrate

Authors: Marcelo E Lagos, Craig R White and Dustin J Marshall

Published in: Marine Ecology Progress Series, volume 540 (November 2015)


Oxygen-poor habitats are increasingly common in aquatic environments. Human activities are accelerating the spread of oxygen-poor environments, yet the way in which larvae avoid low-oxygen conditions remains poorly resolved.

For organisms with a sessile or sedentary adult phase, habitat selection is crucial, and many organisms show sophisticated responses to various habitat cues during colonization.

Whether oxygen availability serves as such a cue is unknown, yet increasingly, it seems that oxygen is an essential limiting resource in some systems.

In a series of experiments, we manipulated oxygen levels during dispersal and colonization in larvae of the model marine invertebrate Bugula neritina in the laboratory.

We found that, in the presence of lower oxygen levels, larvae reduce the time spent in habitat exploration and that they delay settlement. We also found that larvae avoid hypoxic water (positive oxytaxis) — the first such demonstration for marine larvae. All of these behaviors may decrease the likelihood of colonizing low-oxygen habitats in nature.

Our results suggest that marine invertebrate larvae, in this species at least, can use oxygen availability as an initial cue for habitat selection but that additional factors (e.g. biofilms) determine settlement patterns.


Lagos ME, White CR, Marshall DJ (2015) voiding low-oxygen environments: oxytaxis as a mechanism of habitat selection in a marine invertebrate, Marine Ecology Progress Series, 540 99–107 PDF (332 KB) doi:10.3354/meps11509

Revealing hidden evolutionary capacity to cope with global change

Authors: Evatt Chirgwin, Keyne Monro, Carla M Sgró And Dustin J Marshall

Published in: Global Change Biology, volume 21, issue 9 (September 2015)


The extent to which global change will impact the long-term persistence of species depends on their evolutionary potential to adapt to future conditions.

While the number of studies that estimate the standing levels of adaptive genetic variation in populations under predicted global change scenarios is growing all the time, few studies have considered multiple environments simultaneously and even fewer have considered evolutionary potential in multi- variate context.

Because conditions will not be constant, adaptation to climate change is fundamentally a multivariate process so viewing genetic variances and covariances over multivariate space will always be more informative than relying on bivariate genetic correlations between traits. A multivariate approach to understanding the evolutionary capacity to cope with global change is necessary to avoid misestimating adaptive genetic variation in the dimensions in which selection will act.

We assessed the evolutionary capacity of the larval stage of the marine polychaete Galeolaria caespitosa to adapt to warmer water temperatures. Galeolaria is an important habitat-forming species in Australia, and its earlier life-history stages tend to be more susceptible to stress. We used a powerful quantitative genetics design that assessed the impacts of three temperatures on subsequent survival across over 30,000 embryos across 204 unique families.

We found adaptive genetic variation in the two cooler temperatures in our study, but none in the warmest temperature. Based on these results, we would have concluded that this species has very little capacity to evolve to the warmest temperature. However, when we explored genetic variation in multivariate space, we found evidence that larval survival has the potential to evolve even in the warmest temperatures via correlated responses to selection across thermal environments.

Future studies should take a multivariate approach to estimating evolutionary capacity to cope with global change lest they misestimate a species’ true adaptive potential.


Chirgwin E, Monro K, Sgró CM, Marshall DJ (2015) Revealing hidden evolutionary capacity to cope with global change. Global Change Biology, 21: 3356–3366. PDF 230 KB doi: 10.1111/gcb.12929


Lecturer positions x3 (Centre for Geometric Biology)

  • Level B academic
  • Up to 120K including 17% super
  • Full time, ongoing
  • Monash University Clayton campus
  • Applications are now closed

Prof Dustin Marshall is seeking to appoint dynamic individuals wishing to pursue academic careers in ecology, microbial evolutionary ecology or quantitative community ecology as a Lecturer (level B, equivalent to the US system’s tenure-track Assistant Professor) on a continuing basis.

  • Lecturer in Quantitative Community Ecology
  • Lecturer in Ecology
  • Lecturer in Empirical Microbiology

These three positions represent an exciting opportunity to develop a world-class program of research alongside a group of leading researchers in ecology, evolution and physiology, as part of an exciting new initiative at the Monash University School of Biological Science’s Centre for Geometric Biology.

Succesful applicants will:

  • have an outstanding track record of excellence in research
  • have a demonstrated ability to obtain external research funds
  • have developed and delivered teaching materials
  • have excellent written and verbal communication skills
  • be innovative in and develop/lead successful research programs in ecology or microbial ecology or community ecology
  • be proactive in building funded research collaborations including with appropriate external partners
  • excel in teaching activities at the undergraduate level and in post-graduate supervision.

Applications must address of the key selection criteria outlined in the position description.

Enquiries to Professor Dustin Marshall, Director of the Centre for Geometric Biology, on +61 3 9902 4449 or Professor Steven Chown, Head of the School of Biological Sciences on +61 3 9905 5650.

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

Research Fellow position (Centre for Geometric Biology)

  • Level A, research-only academic
  • Up to $96K including 17% superannuation
  • Full-time
  • Two-year, fixed-term
  • Monash University Clayton campus
  • Applications are now closed

Prof Dustin Marshall is seeking an experienced phytoplankton biologist to explore the dynamics of biological systems, specifically how size and shape affect the ways resources move through populations and communities.

As a postdoctoral researcher, you will explore how phytoplankton populations and communities change their function as they change in size and shape, using empirical approaches. The research will be conducted in collaboration with Professor Dustin Marshall as part of the Centre for Geometric Biology at Monash University.

As the successful candidate, you will be expected to conduct empirical research in fundamental ecology or the design and analysis of experiments in phytoplankton systems. You will further be expected to maintain consistently high research output in the form of quality publications, supervision of students, development and submission of grant proposals to external funding agencies, contribute more generally to communicating the research activities of the group, and participation in appropriate career development activities.

Key selection criteria

  1. PhD in phytoplankton biology.
  2. Demonstrated experience in conducting empirical research using cutting-edge quantitative approaches.
  3. Demonstrated ability to undertake outstanding research; with a high quality research publication record in recognised journals;
  4. Ability to solve problems by using discretion, innovation and the exercise of high level diagnostic skills within areas of functional responsibility or professional expertise;
  5. Excellent written communication and verbal communication skills with proven ability to effectively analyse information and produce clear, succinct reports and documents which requires interaction with others.
  6. Demonstrated planning and organisational skills, with the ability to prioritise multiple tasks and set and meet deadlines.
  7. Demonstrated awareness of the principles of confidentiality, privacy and information handling.
  8. Demonstrated ability to effectively work independently and in a multidisciplinary team to make a contribution to research and scholarship.
  9. Experience of, or willingness to work on biological scaling (desirable).
  10. A demonstrated understanding of questions in fundamental ecology and/or evolution (desirable).

Enquiries to Professor Dustin Marshall on +61 3 9902 4449

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