Conspecific chemical cues drive density-dependent metabolic suppression independently of resource intake

Authors: Melanie K Lovass, Dustin J Marshall, and Giulia Ghedini

Published in: Journal of Experimental Biology

Abstract

Within species, individuals of the same size can vary substantially in their metabolic rate. One source of variation in metabolism is conspecific density – individuals in denser populations may have lower metabolism than those in sparser populations. However, the mechanisms through which conspecifics drive metabolic suppression remain unclear.

While food competition is a potential driver, other density-mediated factors could act independently or in combination to drive metabolic suppression but these drivers have rarely been investigated.

We used sessile marine invertebrates to test how food availability interacts with oxygen availability, water flow and chemical cues to affect metabolism.

We show that conspecific chemical cues induce metabolic suppression independently of food and this metabolic reduction is associated with the downregulation of physiological processes rather than feeding activity.

Conspecific cues should be considered when predicting metabolic variation and competitive outcomes as they are an important, but underexplored, source of variation in metabolic traits.

Lovass MK, Marshall DJ, Ghedini G (2020) Conspecific chemical cues drive density-dependent metabolic suppression independently of resource intake. The Journal of Experimental Biology PDF DOI

How to estimate community energy flux? A comparison of approaches reveals that size-abundance trade-offs alter the scaling of community energy flux

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

Published in: Proceedings of the Royal Society B: Biological Sciences

Abstract

Size and metabolism are highly correlated, so that community energy flux might be predicted from size distributions alone. However, the accuracy of predictions based on interspecific energy–size relationships relative to approaches not based on size distributions is unknown.

We compare six approaches to predict energy flux in phytoplankton communities across succession: assuming a constant energy use among species (per cell or unit biomass), using energy–size interspecific scaling relationships and species-specific rates (both with or without accounting for density effects).

Except for the per cell approach, all others explained some variation in energy flux but their accuracy varied considerably. Surprisingly, the best approach overall was based on mean biomass-specific rates, followed by the most complex (species-specific rates with density).

We show that biomass-specific rates alone predict community energy flux because the allometric scaling of energy use with size measured for species in isolation does not reflect the isometric scaling of these species in communities. We also find energy equivalence throughout succession, even when communities are not at carrying capacity.

Finally, we discuss that species assembly can alter energy–size relationships, and that metabolic suppression in response to density might drive the allometry of community energy flux as biomass accumulates.

Ghedini G, Malerba ME, Marshall DJ (2020) How to estimate community energy flux? A comparison of approaches reveals that size-abundance trade-offs alter the scaling of community energy flux. Proceedings of the Royal Society B: Biological Sciences PDF DOI

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

‘Oh, the places you’ll go.’ How far can marine larvae travel?

While travel restrictions have become part of the new normal for people all around the world, a recent study has found that the distance travelled by marine larvae is dictated by both biological and physical constraints.

Marine invertebrates face many challenges when it comes to reproduction. Sperm and sometimes eggs are released into the water where they must meet-up to allow fertilisation to take place. These fertilised embryos develop into larvae and remain in the water column until they find a suitable spot to settle. The amount of time they spend in the water column and the distances they travel can be vastly different for different species.

It is not easy to measure how far larvae travel in real-time so, instead, biologists often use genetic information to work out the relatedness of populations as a proxy for dispersal distance. An alternative approach gathers data on larval characteristics to estimate the time spent in the plankton and so the potential for dispersal.

Mariana Noriega and Dustin Marshall from the Centre for Geometric Biology have been working with colleagues from the United States to examine existing data to help them grasp how larval dispersal distance changes on a global scale. Recent exploration of this question has focused on the role of latitude (or temperature) on larval development, developmental mode (feeding or non-feeding larvae), maternal investment into egg size and hydrodynamics. Often these factors are considered separately rather than all together.

Here’s what we know. Higher temperatures speed up larval development so larvae in the tropics may spend less time in the plankton and disperse less far. But to complicate things, larvae in the tropics are more likely to be feeding larvae which means they tend to spend more time in the plankton than their non-feeding counterparts. Plus, mothers in cooler climes tend to invest more energy into their eggs which for non-feeding larvae means more time in the plankton for those that live at higher latitudes.

Mariana and her colleagues were particularly interested in understanding whether these life-history traits that change with latitude will combine with ocean current information to support their prediction that dispersal distances are shorter in the tropics.

The team have looked at data from 766 marine invertebrate species and classified the larvae into feeding or non-feeding. They extracted data on egg size and the time spent in the plankton, plus the latitude and longitude of the recorded observation.

They were then able to use statistical models to estimate planktonic duration at different latitudes by incorporating their data on development mode and egg size. Having the location of the record also enabled Mariana and the team to estimate local current speeds using the publicly available Mercator-Ocean modelling system. Finally, the expected planktonic duration for the ‘average larvae’ was then multiplied by current speed at each location to estimate dispersal potential.

To the team’s surprise, they didn’t find that dispersal distances were shorter in the tropics.

Instead, they found that the faster surface current speeds in the tropics overcame the effects of temperature on larval development time. So, even though larvae spend less time in the plankton they still have the potential to disperse further than the team predicted due to the faster current speeds.

In fact, the team found that larvae travel further at high and low latitudes, that is, the tropics and the poles. Dispersal distances were shortest in temperate regions where the time spent in the plankton is intermediate and current speeds are slower.

Planktonic duration (PD, days) across latitudes. Planktonic duration was estimated for both feeding and non-feeding larvae and then the potential time spent in the plankton was calculated using data for larval development times and egg size (a proxy measure for reserves available for the larvae). Grey circles show the distribution of studies from which data were obtained. The size of circle corresponds to the number of studies (n) at each location; n ranges from 1 to 33.

Predicted dispersal distance. These predictions incorporate both the biological data of the previous figure with current speeds and demonstrate that dispersal distance is actually shorter in temperate regions, (the dark blue areas), in contrast to the research team’s expectations.

Species richness is greater in the tropics but it seems as if this pattern is not driven by larval dispersal as has been previously suggested. If species richness were driven purely by dispersal distance, this study suggests we would find similar species richness at high latitudes and in the tropics, yet this is not the case.

Understanding patterns in larval dispersal is essential for understanding patterns in marine biodiversity and managing our marine systems. Without this, we will struggle to adequately design marine protected areas, effectively manage biological invasions and predict the consequences of climate change.

This research was published in the journal Nature Ecology & Evolution.

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

The effect of ambient oxygen on the thermal performance of a cockroach, Nauphoeta cinerea

Authors: Emily J Lombardi, Candice L Bywater, and Craig R White

Published in: Journal of Experimental Biology

Abstract

The oxygen and capacity-limited thermal tolerance (OCLTT) hypothesis proposes that the thermal tolerance of an animal is shaped by its capacity to deliver oxygen in relation to oxygen demand. Studies testing this hypothesis have largely focused on measuring short-term performance responses in animals under acute exposure to critical thermal maximums. The OCLTT hypothesis, however, emphasises the importance of sustained animal performance over acute tolerance.

The present study tested the effect of chronic hypoxia and hyperoxia during development on moderate to long-term performance indicators at temperatures spanning the optimal temperature for growth in the speckled cockroach, Nauphoeta cinerea.

In contrast to the predictions of the OCLTT hypothesis, development under hypoxia did not significantly reduce growth rate or running performance, and development under hyperoxia did not significantly increase growth rate or running performance. The effects of developmental temperature and oxygen on tracheal morphology and metabolic rate were also not consistent with OCLTT predictions, suggesting that oxygen delivery capacity is not the primary driver shaping thermal tolerance in this species.

Collectively, these findings suggest that the OCLTT hypothesis does not explain moderate to long-term thermal performance in N. cinerea, which raises further questions about the generality of the hypothesis.

Lombardi EJ, Bywater CL, White CR (2020) The effect of ambient oxygen on the thermal performance of a cockroach, Nauphoeta cinerea. Journal of Experimental Biology 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 PDF DOI

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

Abstract

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

When does diet matter? The roles of larval and adult nutrition in regulating adult size traits

Authors: Gonçalo M Poças, Alexander E Crosbie, and Christen K Mirth

In press in: Journal of Insect Physiology (preprint)

Abstract

Adult body size is determined by the quality and quantity of nutrients available to animals. In insects, nutrition affects adult size primarily during the nymphal or larval stages. However, measures of adult size like body weight are likely to also change with adult nutrition.

In this study, we sought to the roles of nutrition throughout the life cycle on adult body weight and the size of two appendages, the wing and the femur, in the fruit fly Drosophila melanogaster.

We manipulated nutrition in two ways: by varying the protein to carbohydrate content of the diet, called macronutrient restriction, and by changing the caloric density of the diet, termed caloric restriction. We employed a fully factorial design to manipulate both the larval and adult diets for both diet types.

We found that manipulating the larval diet had greater impacts on all measures of adult size. Further, macronutrient restriction was more detrimental to adult size than caloric restriction. For adult body weight, a rich adult diet mitigated the negative effects of poor larval nutrition for both types of diets. In contrast, small wing and femur size caused by poor larval diet could not be increased with the adult diet.

Taken together, these results suggest that appendage size is fixed by the larval diet, while those related to body composition remain sensitive to adult diet. Further, our studies provide a foundation for understanding how the nutritional environment of juveniles affects how adults respond to diet.

Poças GM, Crosbie AE, Mirth CK (2019) When does diet matter? The roles of larval and adult nutrition in regulating adult size traits. Journal of Insect Physiology PDF DOI