Published papers

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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)

Abstract

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.

Citation

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

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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)

Abstract

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.

Citation

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

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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

Abstract

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.

Citation

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

 

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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)

Abstract

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.

Citation

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

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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

Abstract

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.

Citation

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

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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)

Abstract

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.

Citation

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

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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)

Abstract

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.

Citation

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

 

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Limiting resources in sessile systems: food enhances diversity and growth of suspension feeders despite available space

Authors: J Robin Svensson and Dustin J Marshall

Published in: Ecology, volume 96, issue 3 (March 2015)

Abstract

Much of our understanding of competition comes from observations in sessile systems, such as rainforests and marine invertebrate communities.

In terrestrial systems, sessile species often compete for multiple limiting resources (i.e., space, light, and nutrients), but in marine systems, space is viewed as the primary or sole limiting resource. Competition theory, on the other hand, suggests that competition for a single limiting resource is unlikely to maintain high species diversity, but manipulative tests of competition for other resources in marine benthic systems are exceedingly rare.

Here, we manipulate the availability of food for a classic system, marine sessile invertebrate communities, and investigate the effects on species diversity, abundance, and composition during early succession as well as on the growth of bryozoan populations in the field.

We found the number of species to be greater, available space to be lower, and the community composition to be different in assemblages subjected to increased food availability compared to controls. Similarly, laboratory-settled bryozoans deployed into the field grew more in the presence of enhanced food.

Our results suggest that food can act as a limiting resource, affecting both diversity and abundance, even when bare space is still available in hard-substratum communities. Consequently, broadening the view of resource limitation beyond solely space may increase our understanding and predictability of marine sessile systems.

Citation

Svensson R, Marshall DJ (2015) Limiting resources in sessile systems: food enhances diversity and growth of suspension feeders despite available space, Ecology, 96(3) 819–827 PDF 836 KB doi:10.1890/14-0665.1

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Non-contact competition in a sessile marine invertebrate: causes and consequences

Authors: Matthew L Thompson, Dustin J Marshall and Keyne Monro

Published in: Marine Ecology Progress Series, volume 522 (March 2015)

Abstract

In marine benthic communities, phenotypic responses to contact competition are
well resolved, but the causes and consequences of non-contact competition remain unclear.

Here, we used the arborescent bryozoan Bugula neritina to firstly identify whether colonies change their phenotype as a result of non-contact competition, and then understand the mechanism behind the changes. Secondly, we determined the phenotypes that change in response to non-contact competition, with focus on changes in the feeding structure, viz. the lophophore. Lastly, we used a reciprocal transplant design to test whether phenotypic responses to non-contact competition reduce its negative effects.

We found that phenotypic responses to non-contact competition were mediated by the biological effects of conspecific neighbours, but were also determined by the physical effects associated with increased density. Further, we found that colonies grown in high
conspecific density environments were smaller (though more elongated for their size) and had smaller lophophores than colonies from low conspecific density treatments. However, we found no evidence that such phenotypic responses constituted adaptive plasticity; instead, individuals that experienced non-contact competition always performed worse than individuals that had not, and the effects of exposure to non-contact competition were additive.

Our study suggests that noncontact competition is an important and persistent process in benthic marine communities, but that phenotypic plasticity, though present, does not buffer individuals from the negative effects of this process.

Citation:

Thompson ML, Marshall DJ, Monro K (2015) Non-contact competition in a sessile marine invertebrate: causes and consequences. Marine Ecology Progress Series, 522:115–125 doi: 10.3354/meps11178

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Deconstructing environmental predictability: seasonality, environmental colour and the biogeography of marine life histories

Authors: Dustin J Marshall and Scott C Burgess

Published in: Ecology Letters, volume 18, issue 2 (February 2015)

Abstract

Environmental predictability is predicted to shape the evolution of life histories. Two key types of environmental predictability, seasonality and environmental colour, may influence life-history evolution independently but formal considerations of both and how they relate to life history are exceedingly rare.

Here, in a global biogeographical analysis of over 800 marine invertebrates, we explore the relationships between both forms of environmental predictability and three fundamental life-history traits: location of larval development (aplanktonic vs. planktonic), larval develop- mental mode (feeding vs. non-feeding) and offspring size.

We found that both dispersal potential and offspring size related to environmental predictability, but the relationships depended on both the environmental factor as well as the type of predictability. Environments that were more seasonal in food availability had a higher prevalence of species with a planktonic larval stage.

Future studies should consider both types of environmental predictability as each can strongly affect life-history evolution.

Citation

Marshall DJ, Burgess SC (2015) Deconstructing environmental predictability: seasonality, environmental color and the biogeography of marine life histories, Ecology Letters, 18, 174–181 PDF 1.2 MB doi:10.1111/ele.12402