Phenotypic links among life-history stages are complex and context-dependent in a marine invertebrate: interactions among offspring size, larval nutrition and postmetamorphic density

Authors: Richard M Allen and Dustin J Marshall

Published in: Functional Ecology, volume 27, issue 6 (December 2013)

Abstract

Examples of simple phenotypic relationships, where variation in one stage directly affects phenotypic variation in a subsequent stage, are documented in most taxa. However, environmental variation can mediate these relationships, and because most organisms develop through multiple life-history stages, each stage-dependent environment has the potential to create new phenotypic relationships and interfere with existing relationships.

Despite the likelihood of complex phenotypic interactions among life-history stages, and the potential for these interactions to resonate throughout the life history, there are few tests of the problem and few predictions of how these phenotypic interactions are resolved.

Hydroides diramphus

Hydroides diramphus, a polychaete tube worm found in cosmopolitan benthic marine assemblages. Image by Richard Allen.

Here, we examined the interdependent effects of three sources of phenotypic variation on the performance of a marine tube worm. Sources of phenotypic variation included: offspring size, larval nutrition and juvenile density.

We found highly context-dependent relationships between these factors and postmetamorphic performance. Within the overarching result of context dependence, we found: interactions could negate and reverse relationships; early-stage phenotypes could persist to postmetamorphosis; later, life-history environments could contribute more to recruit phenotypes than early-stages; and late-stage variation can depend on early-stage phenotypes.

Our results demonstrate that while simple phenotypic links among the egg, larval and post-recruitment stages may be common and important contributors to growth and survival, these relationships should be considered in the context of the organism’s life experience. Each phenotypic link among stages can potentially be complex and depend on prior experience, current state and the subsequent environments experienced.

Full paper

Allen R, Marshall DJ (2013) Phenotypic links among life-history stages are complex and context-dependent in a marine invertebrate: interactions among offspring size, larval nutrition, and post-metamorphic density. Functional Ecology, 27(6): 1358–1366 PDFPDF 390 KB doi: 10.1111/1365-2435.12117

Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance

Authors: Angela J Crean, John M Dwyer and Dustin J Marshall

Published in: Ecology, volume 94, issue 11 (November 2013)

Abstract

The ability of females to adaptively influence offspring phenotype via maternal effects is widely acknowledged, but corresponding nongenetic paternal effects remain unexplored. Males can adjust sperm phenotype in response to local conditions, but the transgenerational consequences of this plasticity are unknown.

We manipulated paternal density of a broadcast spawner (Styela plicata, a solitary ascidean) using methods shown previously to alter sperm phenotype in the field, then conducted in vitro fertilizations that excluded maternal effects and estimated offspring performance under natural conditions. Offspring sired by males from low-density experimental populations developed faster and had a higher hatching success than offspring sired by males living in high densities.

In the field, offspring survived relatively better when their environment matched their father’s, raising the possibility that fathers can adaptively influence the phenotype of their offspring according to local conditions.

As the only difference between offspring is whether they were artificially fertilized by sperm from males kept in high- vs. low-density cages, we can unequivocally attribute any differences in offspring performance to an environmentally induced paternal effect.

Males of many species manipulate the phenotype of their sperm in response to sperm competition: our results show this plasticity can influence offspring fitness, potentially in adaptive ways, raising the possibility that adaptive nongenetic paternal effects may be more common than previously thought.

Full paper

Crean AJ, Dwyer JM, Marshall DJ (2013) Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance. Ecology, 94(11): 2575–2582 PDFPDF 493 KB doi:10.1890/13-0184.1

Predicting evolutionary responses to climate change in the sea

Authors: Philip L Munday, Rober R Warner, Keyne Munro, John M Pandolfi and Dustin J Marshall

Published in: Ecology Letters, volume 16, issue 12 (December 2013)

Abstract

An increasing number of short-term experimental studies show significant effects of projected ocean warming and ocean acidification on the performance on marine organisms. Yet, it remains unclear if we can reliably predict the impact of climate change on marine populations and ecosystems, because we lack sufficient understanding of the capacity for marine organisms to adapt to rapid climate change.

In this review, we emphasise why an evolutionary perspective is crucial to understanding climate change impacts in the sea and examine the approaches that may be useful for addressing this challenge.

We first consider what the geological record and present-day analogues of future climate conditions can tell us about the potential for adaptation to climate change. We also examine evidence that phenotypic plasticity may assist marine species to persist in a rapidly changing climate. We then outline the various experimental approaches that can be used to estimate evolutionary potential, focusing on molecular tools, quantitative genetics, and experimental evolution, and we describe the benefits of combining different approaches to gain a deeper understanding of evolutionary potential.

Our goal is to provide a platform for future research addressing the evolutionary potential for marine organisms to cope with climate change.

Full paper

Munday PL, Warner RR, Munro  K, Pandolfi JM, Marshall DJ (2013) Predicting evolutionary responses to climate change in the sea. Ecology Letters,  16: 1488–1500  PDFPDF 371 KB doi:10.1111/ele.12185

Fertilisation is not a new beginning: sperm environment affects offspring developmental success

Authors: Hannah Ritchie and Dustin J Marshall

Published in: The Journal of Experimental Biology, volume 216 (August 2013)

Abstract

For organisms with complex life histories, the direction and magnitude of phenotypic links among life-history stages can have important ecological and evolutionary effects.

While the phenotypic links between mothers and offspring, as well as between larvae and adults, are well recognised, the links between sperm phenotype and offspring phenotype have been less well explored.

Here, we used a split-clutch / split-ejaculate design to examine whether the environment that sperm experience affects the subsequent performance of larvae in the broadcast spawning marine invertebrate Galeolaria gemineoa. The environment that sperm experienced affected the developmental success of larvae sired by these sperm; larvae sired by sperm that experienced low salinities had poorer developmental success than larvae sired by sperm that experienced a normal salinity.

When we explored the interactive effects of the sperm environment and the larval environment with an orthogonal design, we found an interaction; when sperm and larvae experienced the same environment, performance was generally higher than when the sperm and larval environments differed. These effects could be due to selection on specific sperm phenotypes, phenotypic modification of the sperm or both.

Together, our results challenge the traditional notion that sperm are merely transporters of genetic material; instead, significant covariance between sperm and offspring phenotypes exists. Our study adds to a growing list that demonstrates that fertilisation does have a homogenising effect on the phenotype of the zygote, and that events before fertilisation during the gamete phase can carry through to affect performance in later life-history stages.

Full paper

Ritchie H, Marshall DJ (2013) Fertilisation is not a new beginning: sperm environment affects offspring developmental success. The Journal of Experimental Biology, 216 (16), 3104–3109  PDFPDF 254 KB doi:10.1242/jeb.087221

Estimating physiological tolerances: a comparison of traditional approaches to nonlinear regression techniques

Authors: Dustin J Marshall, Michael Bode and Craig R White

Published in: The Journal of Experimental Biology, volume 216 (June 2013)

Abstract

Traditionally, physiologists have estimated the ability of organisms to withstand lower partial pressures of oxygen by estimating the partial pressure at which oxygen consumption begins to decrease (known as the critical PO2 or Pc). For almost 30 years, the principal way in which Pc has been estimated has been via piecewise ʻbroken stickʼ regression (BSR). BSR was a useful approach when more sophisticated analyses were less available, but BSR makes a number of unsupported assumptions about the underlying form of the relationship between the rate of oxygen consumption and oxygen availability. The BSR approach also distils a range of values into a single point with no estimate of error.

In accordance with more general calls to fit functions to continuous data, we propose the use of nonlinear regression (NLR) to fit various curvilinear functions to oxygen consumption data in order to estimate Pc. Importantly, our approach is back-compatible so that estimates using traditional methods in earlier studies can be compared with data estimates from our technique. When we compared the performance of our approach relative to the traditional BSR approach for real world and simulated data, we found that under realistic circumstances, NLR was more accurate and provided more powerful hypothesis tests.

We recommend that future studies make use of NLR to estimate Pc, and also suggest that this approach might be more appropriate for a range of physiological studies that use BSR currently.

Full paper

Marshall DJ, Bode M, White CR (2013) Estimating physiological tolerances – a comparison of traditional approaches to nonlinear regression techniques. The Journal of Experimental Biology, 216 (12), 2176–2182 PDFPDF 562 KB doi:10.1242/jeb.085712

The maintenance of sperm variability: context-dependent selection on sperm morphology in a broadcast spawning invertebrate

Authors: Darren W Johnson, Keyne Monro, and Dustin J Marshall

Published in: Evolution, volume 67, issue 5 (May 2013)

Abstract

Why are sperm so variable despite having a singular, critical function and an intimate relationship with fitness?

A key to under-standing the evolution of sperm morphology is identifying which traits enable sperm to be successful fertilizers. Several sperm traits (e.g., tail length, overall size) are implicated in sperm performance, but the benefits of these traits are likely to be highly con- text dependent.

Here, we examined phenotypic selection on sperm morphology of a broadcast spawning tube worm (Galeolaria gemineoa). We conducted laboratory experiments to measure the relationship between average sperm morphology and relative fertilization success across a range of sperm environments that were designed to approximate the range of sperm concentrations and ages encountered by eggs in nature.

We found that the strength and form of multivariate selection varied substantially across our environmental gradients. Sperm with long tails and small heads were favored in high-concentration environments, whereas sperm with long heads were favored at low concentrations and old ages.

We suggest variation in the local fertilization environment and resulting differences in selection can preserve variability in sperm morphology both within and among males.

Full paper

Johnson D, Monro K, Marshall DJ (2013) The maintenance of sperm variability: context-dependent selection on sperm morphology in a broadcast spawning invertebrate. Evolution, 67-5: 1383–1395 PDF PDF 889 KB doi:10.1111/evo.12022

Competition in benthic marine invertebrates: the unrecognised role of exploitative competition for oxygen

Authors: Nick Ferguson, Craig R White and Dustin J Marshall

Published in: Ecology, volume 94, issue 1 (January 2013) doi: 10.1890/12-0795.1

Abstract

Competition is a ubiquitous structuring force across systems, but different fields emphasize the role of different types of competition.

In benthic marine environments, where some of the classic examples of competition were described, there is a strong emphasis on interference competition: marine invertebrates are assumed to compete fiercely for the limiting resource of space. Much of our understanding of the dynamics of this system is based on this assumption, yet empirical studies often find that increases in density can reduce performance despite free space being available. Furthermore, the assumption that space is the exclusively limiting resource raises paradoxes regarding species coexistence in this system.

Here, we measure the availability of oxygen in the field and in the laboratory, as well as the tolerance of resident species to low-oxygen conditions.

We show that oxygen can be the primary limiting resource in some instances, and that exploitative competition for this resource is very likely among benthic marine invertebrates. Furthermore, growth form (and the associated risk of oxygen limitation) covaries with the ability to withstand oxygen-poor conditions across a wide range of taxa.

Oxygen availability at very small scales may influence the distribution and abundance of sessile marine invertebrates more than is currently appreciated. Furthermore, competition for multiple resources (space and oxygen) and trade-offs in competitive ability for each may promote coexistence in this system.

Full paper

Ferguson N, White CR, Marshall DJ (2013) Competition in benthic marine invertebrates: the unrecognised role of exploitative competition for oxygen. Ecology, 94(1) 126–135 PDFPDF 311 KB 311 doi: 10.1890/12-0795.1

Costs of dispersal alter optimal offspring size in patchy habitats: combining theory and data for a marine invertebrate

Authors: Scott C Burgess, Michael Bode and Dustin J Marshall

Published in: Functional Ecology doi: 10.1111/1365-2435.12080

Abstract

Much of the theory on offspring size focuses on the effects of habitat quality on the relationship between offspring size and fitness. Habitat spacing may be another important factor that affects selection on offspring size when offspring disperse prior to colonization and accrue deferred costs that are mediated by offspring size.

We developed a theoretical model, based on a well-known optimality model, of how selection on offspring size changes with dispersal distance. The model assumes that offspring fitness depends on both offspring size and dispersal duration and that dispersal time and distance are positively related. Such assumptions are based on thousands of marine invertebrate species with non-feeding larvae, but our model also applies more generally to any organism where offspring size modifies the energetic costs of dispersal, and there is a positive relationship between dispersal duration and distance.

Our model predicts that, even when habitat quality does not vary, more isolated habitats may favour the production of fewer, larger offspring if smaller offspring incur greater deferred costs of dispersal. We then empirically demonstrate that offspring size and dispersal duration have interactive effects on post-settlement survival in a marine invertebrate (Bugula neritina), and such size-dependent deferred costs of dispersal are of a magnitude sufficient enough to potentially favour larger offspring in isolated habitats.

Together, our results indicate that the spatial pattern of suitable habitat could impose very different selective regimes on offspring size compared with the effects of habitat quality. Furthermore, our predictions contrast to those predicted for seed size and dispersal in plants, where the production of smaller, more numerous seeds is often a more efficient way for mothers to access distant, suitable habitat.

Full paper

Burgess SC, Bode M, Marshall DJ (2013) Costs of dispersal alter optimal offspring size in patchy habitats: combining theory and data for a marine invertebrate. Functional Ecology PDFPDF 329 KB doi: 10.1111/1365-2435.12080

Interspecific competition alters non-linear selection on offspring size in the field

Authors: Dustin J Marshall and Keyne Monro

Published in: Evolution, volume 67, issue 2 (February 2013) doi: 10.1111/j.1558-5646.2012.01749.x

Abstract

Offspring size is one of the most important life-history traits with consequences for both the ecology and evolution of most organisms. Surprisingly, formal estimates of selection on offspring size are rare, and the degree to which selection (particularly nonlinear selection) varies among environments remains poorly explored.

We estimate linear and nonlinear selection on offspring size, module size, and senescence rate for a sessile marine invertebrate in the field under three different intensities of interspecific competition. The intensity of competition strongly modified the strength and form of selection acting on offspring size.

We found evidence for differences in nonlinear selection across the three environments.

Our results suggest that the fitness returns of a given offspring size depend simultaneously on their environmental context, and on the context of other offspring traits. Offspring size effects can be more pervasive with regards to their influence on the fitness returns of other traits than previously recognized, and we suggest that the evolution of offspring size cannot be understood in isolation from other traits.

Overall, variability in the form and strength of selection on offspring size in nature may reduce the efficacy of selection on offspring size and maintain variation in this trait.

Full paper

Marshall DJ, Monro K (2013) Interspecific competition alters nonlinear selection on offspring size in the field. Evolution, 67-2: 328–337 PDFPDF 291 KB doi: 10.1111/j.1558-5646.2012.01749.x

Two PhD positions available: the ecology and/or evolutionary biology of sessile marine invertebrates (closed)

Update: applications are now closed.

Two fully-funded PhD stipends are available to students interested in working on the evolutionary ecology of sessile marine invertebrates in Dr Dustin Marshall’s Marine Evolutionary Ecology Group (MEEG). The specifics of the project will be a joint collaboration between student and supervisor.

The stipends include all course fees plus approximately $25,000 AUD per annum tax-free (the equivalent of approximately $33,000 AUD before tax) with no teaching requirements for 3.5 years (the length of a PhD in Australia).

I can guarantee funding of project costs and research support including the costs of attending at least one conference per year.

Project start dates can be any time in 2013.

Interested students should send their CVs, a brief statement of their interests and the contact details of two referees to dustin.marshall@monash.edu.

To be eligible, applicants must have completed at least one year of post-graduate research in ecology or evolution.

Preference will be given to those with strong quantitative skills and publications in international journals.

Applications close Monday 21 January 2013. Update: applications are now closed.