Published papers

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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

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Environmentally induced (co)variance in sperm and offspring phenotypes as a source of epigenetic effects

Author: Dustin J Marshall

Published in: The Journal of Experimental Biology, volume 208, issue 1 (January 2015)

Abstract

Traditionally, it has been assumed that sperm are a vehicle for genes and nothing more. As such, the only source of variance in offspring phenotype via the paternal line has been genetic effects. More recently, however, it has been shown that the phenotype or environment of fathers can affect the phenotype of offspring, challenging traditional theory with implications for evolution, ecology and human in vitro fertilisation.

Here, I review sources of non-genetic variation in the sperm phenotype and evidence for co-variation between sperm and offspring phenotypes. I distinguish between two environmental sources of variation in sperm phenotype: the pre- release environment and the post-release environment.

Pre-release, sperm phenotypes can vary within species according to male phenotype (e.g. body size) and according to local conditions such as the threat of sperm competition. Post-release, the physicochemical conditions that sperm experience, either when freely spawned or when released into the female reproductive tract, can further filter or modify sperm phenotypes.

I find evidence that both pre- and post-release sperm environments can affect offspring phenotype; fertilisation is not a new beginning – rather, the experiences of sperm with the father and upon release can drive variation in the phenotype of the offspring.

Interestingly, there was some evidence for co-variation between the stress resistance of sperm and the stress resistance of offspring, though more studies are needed to determine whether such effects are widespread.

Overall, it appears that environmentally induced covariation between sperm and offspring phenotypes is non-negligible and further work is needed to determine their prevalence and strength.

Citation

Marsall DJ (2015) Environmentally induced (co)variance in sperm and offspring phenotypes as a source of epigenetic effects, The Journal of Experimental Biology, 208(1), 107–113 PDF 458 KB doi:10.1242/jeb.106427

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Larval size and age affect colonization in a marine invertebrate

Authors: Dustin J Marshall and Peter D Steinberg

Published in: The Journal of Experimental Biology, volume 217, issue 22 (November 2014)

Abstract

The relationship between offspring size and performance determines the optimal trade-off between producing many small offspring or fewer large offspring and the existence of this relationship has become a central tenet of life-history theory.

For organisms with multiple life-history stages, the relationship between offspring size and performance is the product of the effects of offspring size in each life-history stage.

Marine invertebrates have long been a model system for examining the evolutionary ecology of offspring size, and whilst offspring size effects have been found in several life-history stages, the crucial stage of colonization has received less attention.

We examined the effect of offspring size on the settlement response of sea-urchin larvae (Heliocidaris erythrogramma) to preferred and less preferred hostplants, how these effects changed over the larval period and estimated the success of juveniles in the field on preferred and less preferred host plants.

We found that smaller larvae became competent to respond to preferred host plant cues sooner than larger larvae but larger larvae rejected less preferred host plants for longer than smaller larvae. Overall, smaller H. erythrogramma larvae are likely to have less dispersal potential and are more likely to settle in less preferred habitats whereas larger larvae appear to have an obligately longer dispersal period but settle in preferred habitats.

Our results suggest that marine invertebrates that produce non-feeding larvae may have the potential to affect the dispersal of their offspring in previously unanticipated ways and that offspring size is subject to a complex web of selection across life-history stages.

Citation

Marshall DJ, Steinberg PD (2014) Larval size and age affect colonization in a marine invertebrate, Journal of Experimental Biology, 217: 3981–3987 PDF 403 KB doi:10.1242/jeb.111781

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Egg size effects across multiple life-history stages in the marine annelid Hydroides diramphus

Authors: Richard M Allen and Dustin J Marshall

Published in: PloS ONE, volume 9, issue 7 (July 2014)

Abstract

The optimal balance of reproductive effort between offspring size and number depends on the fitness of offspring size in a particular environment.

The variable environments offspring experience, both among and within life-history stages, are likely to alter the offspring size/fitness relationship and favor different offspring sizes. Hence, the many environments experienced throughout complex life-histories present mothers with a significant challenge to optimally allocate their reproductive effort.

In a marine annelid, we tested the relationship between egg size and performance across multiple life-history stages, including: fertilization, larval development, and post-metamorphosis survival and size in the field.

We found evidence of conflicting effects of egg size on performance: larger eggs had higher fertilization under sperm-limited conditions, were slightly faster to develop pre-feeding, and were larger post-metamorphosis; however, smaller eggs had higher fertilization when sperm was abundant, and faster planktonic development; and egg size did not affect post-metamorphic survival.

The results indicate that egg size effects are conflicting in H. diramphus depending on the environments within and among life-history stages. We suggest that offspring size in this species may be a compromise between the overall costs and benefits of egg sizes in each stage and that performance in any one stage is not maximized.

Citation

Allen RM, Marshall DJ (2014) Egg size effects across multiple life-history stages in the marine annelid Hydroides diramphus. PLoS ONE 9(7): e102253 PDF 250 KB doi:10.1371/journal.pone.0102253