Genome size affects fitness in the eukaryotic alga Dunaliella tertiolecta

Authors: Martino E Malerba, Giulia Ghedini, and Dustin J Marshall

Published in: Current Biology

Abstract

Genome size is tightly coupled to morphology, ecology, and evolution among species, with one of the best-known patterns being the relationship between cell size and genome size.

Classic theories, such as the ‘selfish DNA hypothesis,’ posit that accumulating redundant DNA has fitness costs but that larger cells can tolerate larger genomes, leading to a positive relationship between cell size and genome size. Yet the evidence for fitness costs associated with relatively larger genomes remains circumstantial.

Here, we estimated the relationships between genome size, cell size, energy fluxes, and fitness across 72 independent lineages in a eukaryotic phytoplankton. Lineages with relatively smaller genomes had higher fitness, in terms of both maximum growth rate and total biovolume reached at carrying capacity, but paradoxically, they also had lower energy fluxes than lineages with relative larger genomes. We then explored the evolutionary trajectories of absolute genome size over 100 generations and across a 10-fold change in cell size.

Despite consistent directional selection across all lineages, genome size decreased by 11% in lineages with absolutely larger genomes but showed little evolution in lineages with absolutely smaller genomes, implying a lower absolute limit in genome size.

Our results suggest that the positive relationship between cell size and genome size in nature may be the product of conflicting evolutionary pressures, on the one hand, to minimize redundant DNA and maximize performance — as theory predicts — but also to maintain a minimum level of essential function.

Malerba ME, Ghedini G, Marshall DJ (2020) Genome size affects fitness in the eukaryotic alga Dunaliella tertiolecta. Current Biology PDF DOI

Global biogeography of marine dispersal potential

Authors: Mariana Álvarez-Noriega, Scott C Burgess, James E Byers, James M Pringle, John P Wares, and Dustin J Marshall

Published in: Nature Ecology & Evolution

Abstract

The distance travelled by marine larvae varies by seven orders of magnitude. Dispersal shapes marine biodiversity, and must be understood if marine systems are to be well managed.

Because warmer temperatures quicken larval development, larval durations might be systematically shorter in the tropics relative to those at high latitudes. Nevertheless, life history and hydro-dynamics also covary with latitude—these also affect dispersal, precluding any clear expectation of how dispersal changes at a global scale.

Here we combine data from the literature encompassing >750 marine organisms from seven phyla with oceanographic data on current speeds, to quantify the overall latitudinal gradient in larval dispersal distance.

We find that planktonic duration increased with latitude, confirming predictions that temperature effects outweigh all others across global scales. However, while tropical species have the shortest planktonic durations, realized dispersal distances were predicted to be greatest in the tropics and at high latitudes, and lowest at mid-latitudes. At high latitudes, greater dispersal distances were driven by moderate current speed and longer planktonic durations. In the tropics, fast currents overwhelmed the effect of short planktonic durations.

Our results contradict previous hypotheses based on biology or physics alone; rather, biology and physics together shape marine dispersal patterns.

Álvarez-Noriega M, Burgess SC, Byers JE, Pringle JM, Wares JP, Marshall DJ (2020) Global biogeography of marine dispersal potential. Nature Ecology & Evolution PDF DOI

Metabolic rate, context-dependent selection, and the competition-colonization trade-off

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

Published in: Evolution Letters

Abstract

Metabolism is linked with the pace-of-life, co-varying with survival, growth, and reproduction. Metabolic rates should therefore be under strong selection and, if heritable, become less variable over time. Yet intraspecific variation in metabolic rates is ubiquitous, even after accounting for body mass and temperature.

Theory predicts variable selection maintains trait variation, but field estimates of how selection on metabolism varies are rare.

We use a model marine invertebrate to estimate selection on metabolic rates in the wild under different competitive environments.

Fitness landscapes varied among environments separated by a few centimetres: interspecific competition selected for higher metabolism, and a faster pace‐of‐life, relative to competition‐free environments.

Populations experience a mosaic of competitive regimes; we find metabolism mediates a competition-colonization trade-off across these regimes. Although high metabolic phenotypes possess greater competitive ability, in the absence of competitors, low metabolic phenotypes are better colonizers.

Spatial heterogeneity and the variable selection on metabolic rates that it generates is likely to maintain variation in metabolic rate, despite strong selection in any single environment.

Pettersen AK, Hall MD, White CR, Marshall DJ (2020) Metabolic rate, context-dependent selection, and the competition-colonization trade-off. Evolution Letters PDF DOI

Developmental cost theory predicts thermal environment and vulnerability to global warming

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

Published in: Nature Ecology & Evolution

Abstract

Metazoans must develop from zygotes to feeding organisms. In doing so, developing offspring consume up to 60% of the energy provided by their parent.

The cost of development depends on two rates: metabolic rate, which determines the rate that energy is used; and developmental rate, which determines the length of the developmental period. Both development and metabolism are highly temperature-dependent such that developmental costs should be sensitive to the local thermal environment.

Here, we develop, parameterize and test developmental cost theory, a physiologically explicit theory that reveals that ectotherms have narrow thermal windows in which developmental costs are minimized (Topt).

Our developmental cost theory-derived estimates of Topt predict the natural thermal environment of 71 species across seven phyla remarkably well (R2⁓0.83).

Developmental cost theory predicts that costs of development are much more sensitive to small changes in temperature than classic measures such as survival. Warming-driven changes to developmental costs are predicted to strongly affect population replenishment and developmental cost theory provides a mechanistic foundation for determining which species are most at risk. Developmental cost theory predicts that tropical aquatic species and most non-nesting terrestrial species are likely to incur the greatest increase in developmental costs from future warming.

Marshall DJ, Pettersen AK, Bode M, White CR (2020) Developmental cost theory predicts thermal environment and vulnerability to global warming. Nature Ecology & Evolution DOI PDF

Community efficiency during succession: a test of MacArthur’s minimization principle in phytoplankton communities

Authors: Giulia Ghedini, Michel Loreau, and Dustin J Marshall

Published in: Ecology

Robert MacArthur’s niche theory makes explicit predictions on how community function should change over time in a competitive community. A key prediction is that succession progressively minimizes the energy wasted by a community, but this minimization is a trade-off between energy losses from unutilised resources and costs of maintenance. By predicting how competition determines community efficiency over time MacArthur’s theory may inform on the impacts of disturbance on community function and invasion risk.

We provide a rare test of this theory using phytoplankton communities, and find that older communities wasted less energy than younger ones but that the reduction in energy wastage was not monotonic over time. While community structure followed consistent and clear trajectories, community function was more idiosyncratic among adjoining successional stages and driven by total community biomass rather than species composition.

Our results suggest that subtle shifts in successional sequence can alter community efficiency and these effects determine community function independently of individual species membership.

We conclude that, at least in phytoplankton communities, general trends in community function are predictable over time accordingly to MacArthur’s theory. Tests of MacArthur’s minimization principle across very different systems should be a priority given the potential of this theory to inform on the functional properties of communities.

Ghedini G, Loreau M, Marshall DJ (2020) Community efficiency during succession: a test of MacArthur’s minimization principle in phytoplankton communities. Ecology PDF DOI

Testing the drivers of the temperature-size covariance using artificial selection

Authors: Martino E Malerba, and Dustin J Marshall

Published in: Evolution

Abstract

Body size often declines with increasing temperature. Although there is ample evidence for this effect to be adaptive, it remains unclear whether size shrinking at warmer temperatures is driven by specific properties of being smaller (e.g., surface to volume ratio) or by traits that are correlated with size (e.g., metabolism, growth).

We used 290 generations (22 months) of artificial selection on a unicellular phytoplankton species to evolve a 13‐fold difference in volume between small‐selected and large‐selected cells and tested their performance at 22 °C (usual temperature), 18 °C (−4), and 26 °C (+4).

Warmer temperatures increased fitness in small‐selected individuals and reduced fitness in large‐selected ones, indicating changes in size alone are sufficient to mediate temperature‐dependent performance.

Our results are incompatible with the often‐cited geometric argument of warmer temperature intensifying resource limitation. Instead, we find evidence that is consistent with larger cells being more vulnerable to reactive oxygen species. By engineering cells of different sizes, our results suggest that smaller‐celled species are pre‐adapted for higher temperatures.

We discuss the potential repercussions for global carbon cycles and the biological pump under climate warming.

Malerba ME, Marshall DJ (2019) Testing the drivers of the temperature-size covariance using artificial selection. Evolution PDF DOI

 

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

Abstract

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

Abstract

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

Abstract

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