Authors: Tess Laidlaw, Tobias E Hector, Carla M. Sgrò, and Matthew D Hall
Published in: Ecology and Evolution
The climate is warming at an unprecedented rate, pushing many species toward and beyond the upper temperatures at which they can survive. Global change is also leading to dramatic shifts in the distribution of pathogens. As a result, upper thermal limits and susceptibility to infection should be key determinants of whether populations continue to persist, or instead go extinct. Within a population, however, individuals vary in both their resistance to both heat stress and infection, and their contributions to vital growth rates. No more so is this true than for males and females. Each sex often varies in their response to pathogen exposure, thermal tolerances, and particularly their influence on population growth, owing to the higher parental investment that females typically make in their offspring. To date, the interplay between host sex, infection, and upper thermal limits has been neglected.
Here, we explore the response of male and female Daphnia to bacterial infection and static heat stress.
We find that female Daphnia, when uninfected, are much more resistant to static heat stress than males, but that infection negates any advantage that females are afforded. We discuss how the capacity of a population to cope with multiple stressors may be underestimated unless both sexes are considered simultaneously.
Laidlaw T, Hector TE, Sgrò CM, Hall MD (2020) Pathogen exposure reduces sexual dimorphism in a host’s upper thermal limits. Ecology and EvolutionPDFDOI
Authors: Martino E Malerba, Dustin J Marshall, Maria M Palacios, John A Raven, and John Beardall
Published in:New Phytologist
Cell size influences the rate at which phytoplankton assimilate dissolved inorganic carbon (DIC), but it is unclear whether volume‐specific carbon uptake should be greater in smaller or larger cells. On the one hand, Fick’s Law predicts smaller cells to have a superior diffusive CO2 supply. On the other, larger cells may have greater scope to invest metabolic energy to upregulate active transport per unit area through CO2‐concentrating mechanisms (CCMs).
Previous studies have focused on among‐species comparisons, which complicates disentangling the role of cell size from other covarying traits. In this study, we investigated the DIC assimilation of the green alga Dunaliella tertiolecta after using artificial selection to evolve a 9.3‐fold difference in cell volume. We compared CO2affinity, external carbonic anhydrase (CAext), isotopic signatures (δ13C) and growth among size‐selected lineages.
Evolving cells to larger sizes led to an upregulation of CCMs that improved the DIC uptake of this species, with higher CO2 affinity, higher CAext and higher δ13C. Larger cells also achieved faster growth and higher maximum biovolume densities.
We showed that evolutionary shifts in cell size can alter the efficiency of DIC uptake systems to influence the fitness of a phytoplankton species.
Malerba ME, Marshall DJ, Palacios MM, Raven JA, Beardall J (2020) Cell size influences inorganic carbon acquisition in artificially selected phytoplankton. New PhytologistPDFDOI
Global change will alter the distribution of organisms around the planet. Dustin Marshall and Mariana Álvarez-Noriega found rising ocean temperatures will impact early life stages of marine invertebrates and change the patterns in the distribution of species that we see today. In particular, species in which mothers invest heavily in offspring will be the biggest losers. These species occur predominantly at the poles.
In terrestrial environments seeds often disperse in the wind, with shape and size affecting how far they travel. It turns out much the same happens in the ocean but currents rather than wind carry marine larvae to their new homes. Larvae able to feed spend much longer in the water column meaning these species have far greater dispersal capabilities.
As with plants, dispersal is crucial to the survival of marine populations. Arriving larvae can seed new areas, re-seed vulnerable populations, and provide genetic variation for subsequent generations in far-flung regions. There is a downside: if temperature affects dispersal, it will also shape how species are affected by global warming.
Not all marine species use the same reproductive or life-history strategies which can mean differences in dispersal distances from centimetres to hundreds of kilometres for different species. Interestingly, there is a well-recognised relationship between latitude (or temperature) and reproductive strategy.
Species at higher latitudes (nearer the poles) tend to invest more heavily in their offspring and produce non-feeding larvae or bypass the larval stage altogether. This means these species don’t disperse very far. In contrast, tropical species tend to put little effort into provisioning their offspring and produce larvae that can feed. As a result, these larvae can spend a lot more time in the plankton and can be dispersed vast distances.
Dustin and Mariana wanted to know how these dispersal relationships might change as global temperatures change. To address this question, they revisited the database of marine invertebrates classified into feeding / development types from a previous study. They established relationships between temperature and development mode so they could then explore how predicted temperatures for 2100 would change patterns in distributions.
So, how will global warming affect these relationships? We know species’ in warmer waters are more likely to produce large numbers of feeding larvae able to remain in the water column for weeks at a time. As waters warm, these species are well placed to extend their range.
In contrast, species based in cooler waters tend to invest heavily in individual offspring, meaning that they develop quicker and settle closer to their parents. This reproductive strategy means that such species are more vulnerable to rapid global change as moving to new areas will, of necessity, be step-wise and slow.
Species at the poles will therefore be the biggest losers because not only will their lower dispersal lifestyles mean they will be slow to access cooler waters but also the options are limited; there is nowhere to go.
Authors: Dustin J Marshall and Mariana Álvarez-Noriega
Published in:Philosophical Transactions of the Royal Society B: Biological Sciences
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 SciencesPDFDOI
An enduring concept in ecology is that space is the resource most in demand for communities living on hard substrates such as rocky shores and pier pilings. We have seen before how these communities can be extremely dense and diverse with little or no unoccupied space. But is space the whole story? These communities also need food and oxygen. How do such dense assemblages of animals manage to extract enough food to allow them to co-exist?
Belinda Comerford, Mariana Álvarez-Noriega, and Dustin Marshall have found different species of filter-feeders tend to consume one species of phytoplankton much more than others when offered a selection. They noticed studies looking at the role food plays in structuring filter-feeding communities tend to consider phytoplankton as a uniform resource. This makes no allowance for differences in size, shape or chemical make-up of the different algal species.
Belinda, Mariana and Dustin suspected that different species of filter-feeders will consume different components of the phytoplankton, reducing competition for food and allowing for the dense and diverse communities that we see in nature. So, they set about testing how different species of filter feeder consumed a mix of three different phytoplankton species that varied in size and shape and chemical make-up.
They used 11 different species of invertebrate filter-feeding animals and offered them a mix of the three phytoplankton species. They measured the concentrations of each phytoplankton species in the animal chambers one minute and one hour after adding equal volumes of each species to the chambers. They also had control chambers that contained no animals which enabled them to estimate how much of the algae settled out to the bottom during the experimental period.
While most of the animals ingested all three phytoplankton species they did so at different rates. The encrusting bryozoan Watersiporasubtorquata consumed the largest algal species at a much greater rate than it did the other two species while the sponge Syconspp. favoured the smallest algal species. Some species such as the sea squirt Ciona intestinalis appear to be generalists, consuming all three algal species at the same rate.
It seems that Belinda, Mariana and Dustin might be right. Thinking of phytoplankton as a homogenous resource underestimates the potential for reducing competition between filter-feeding species. If, instead of competing for a ‘common pool’ of phytoplankton, filter feeders target specific subsections then the diverse and densely packed communities that we see are more readily explained.
Published in:Proceedings of the Royal Society B: Biological Sciences
Females and males carry nearly identical genomes, which can constrain the evolution of sexual dimorphism and generate conditions that are favourable for maintaining sexually antagonistic (SA) polymorphisms, in which alleles beneficial for one sex are deleterious for the other.
An influential theoretical prediction, by Rice (Rice 1984 Evolution), is that the X chromosome should be a ‘hot spot’ (i.e. enriched) for SA polymorphisms. While important caveats to Rice’s theoretical prediction have since been highlighted (e.g. by Fry 2010 Evolution), several empirical studies appear to support it.
Here, we show that current tests of Rice′s theory—most of which are based on quantitative genetic measures of fitness (co)variance—are frequently biased towards detecting X-linked effects. We show that X-linked genes tend to contribute disproportionately to quantitative genetic patterns of SA fitness variation whether or not the X is enriched for SA polymorphisms.
Population genomic approaches for detecting SA loci, including genome-wide association study of fitness and analyses of intersexual FST, are similarly biased towards detecting X-linked effects. In the light of our models, we critically re-evaluate empirical evidence for Rice′s theory and discuss prospects for empirically testing it.
Ruzicka F, Connallon T (2020) Is the X chromosome a hot spot for sexually antagonistic polymorphisms? Biases in current empirical tests of classical theory. Proceedings of the Royal Society B: Biological SciencesPDFDOI
Authors: Belinda Comerford, Mariana Álvarez-Noriega, and Dustin J Marshall
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. PDFDOI
Authors: Alexander N Gangur, and Dustin J Marshall
Published in:Marine Ecology Progress Series
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 SeriesPDFDOI
Authors: Melanie K Lovass, Dustin J Marshall, and Giulia Ghedini
Published in:Journal of Experimental Biology
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. The Journal of Experimental BiologyPDFDOI
Authors: Giulia Ghedini, Martino E Malerba, and Dustin J Marshall
Published in:Proceedings of the Royal Society B: Biological Sciences
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 SciencesPDFDOI