Authors: Dustin J Marshall and Mariana Álvarez-Noriega

Published in: Philosophical Transactions of the Royal Society B: Biological Sciences

Abstract

Global change will alter the distribution of organisms around the planet. While many studies have explored how different species, groups and traits might be re-arranged, few have explored how dispersal is likely to change under future conditions.

Dispersal drives ecological and evolutionary dynamics of populations, determining resilience, persistence and spread. In marine systems, dispersal shows clear biogeographical patterns and is extremely dependent on temperature, so simple projections can be made regarding how dispersal potentials are likely to change owing to global warming under future thermal regimes.

We use two proxies for dispersal — developmental mode and developmental duration. Species with a larval phase are more dispersive than those that lack a larval phase, and species that spend longer developing in the plankton are more dispersive than those that spend less time in the plankton.

Here, we explore how the distribution of different development modes is likely to change based on current distributions. Next, we estimate how the temperature-dependence of development itself depends on the temperature in which the species lives, and use this estimate to project how developmental durations are likely to change in the future.

We find that species with feeding larvae are likely to become more prevalent, extending their distribution poleward at the expense of species with aplanktonic development. We predict that developmental durations are likely to decrease, particularly in high latitudes where durations may decline by more than 90%. Overall, we anticipate significant changes to dispersal in marine environments, with species in the polar seas experiencing the greatest change.

This article is part of the theme issue ‘Integrative research perspectives on marine conservation’.

Marshall DJ, Álvarez-Noriega M (2020) Projecting marine developmental diversity and connectivity in future oceans. Philosophical Transactions of the Royal Society B: Biological Sciences PDF DOI

Authors: Belinda Comerford, Mariana Álvarez-Noriega, and Dustin J Marshall

Published in: Oecologia

Abstract

Coexistence theory predicts that, in general, increases in the number of limiting resources shared among competitors should facilitate coexistence.

Heterotrophic sessile marine invertebrate communities are extremely diverse but traditionally, space was viewed as the sole limiting resource. Recently planktonic food was recognized as an additional limiting resource, but the degree to which planktonic food acts as a single resource or is utilized differentially remains unclear. In other words, whether planktonic food represents a single resource niche or multiple resource niches has not been established.

We estimated the rate at which 11 species of marine invertebrates consumed three phytoplankton species, each different in shape and size.

Rates of consumption varied by a 240-fold difference among the species considered and, while there was overlap in the consumer diets, we found evidence for differential resource usage (i.e. consumption rates of phytoplankton differed among consumers). No consumer ingested all phytoplankton species at equivalent rates, instead most species tended to consume one of the species much more than others.

Our results suggest that utilization of the phytoplankton niche by filter feeders is more subdivided than previously thought, and resource specialization may facilitate coexistence in this system. Our results provide a putative mechanism for why diversity affects community function and invasion in a classic system for studying competition.

Comerford B, Álvarez-Noriega M, Marshall D (2020) Differential resource use in filter-feeding marine invertebrates. Oecologia. PDF DOI

Authors: Alexander N Gangur, and Dustin J Marshall

Published in: Marine Ecology Progress Series

Abstract

Most marine invertebrate larvae either feed or rely on reserves provisioned by parents to fuel development, but facultative feeders can do both.

Food availability and temperature are key environmental drivers of larval performance, but the effects of larval experience on performance later in life are poorly understood in facultative feeders. In particular, the functional relevance of facultative feeding is unclear. One feature to be tested is whether starved larvae can survive to adulthood and reproduce.

We evaluated effects of larval temperature and food abundance on performance in a marine harpacticoid copepod, Tisbe sp. In doing so, we report the first example of facultative feeding across the entire larval stage for a copepod.

In a series of experiments, larvae were reared with ad libitum food or with no food, and at 2 different temperatures (20 vs 24 °C). We found that higher temperatures shortened development time, and larvae reared at higher temperature tended to be smaller. Larval food consistently improved early performance (survival, development rate and size) in larvae, while starvation consistently decreased survival, increased development time and decreased size at metamorphosis. Nonetheless, a small proportion (3–9.5%, or 30–42.7% with antibiotics) of larvae survived to metamorphosis, could recover from a foodless larval environment, reach maturity and successfully reproduce.

We recommend that future studies of facultative feeding consider the impact of larval environments on adult performance and ability to reproduce.

Gangur A, Marshall D (2020) Facultative feeding in a marine copepod: effects of larval food and temperature on performance. Marine Ecology Progress Series PDF DOI

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. Although 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. Journal of Experimental Biology PDF DOI

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

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

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

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 (T_opt).

Our developmental cost theory-derived estimates of T_opt 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

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

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